Characterizing the 3D Interactions of the Base-Pair Stems

CHARACTERIZING THE 3D INTERACTIONS OF THE BASE-PAIR STEMS

AND HELICES IN RNA MOLECULES

ZAINAB MOHAMMED HASSAN FADHIL

A thesis submitted to the

The Graduate School- New Brunswick

Rutgers, the state University of New Jersey

In partial fulfillment of the requirements

For the degree of

Master of Science

Graduate Program in Chemistry and Chemical Biology

Written under the direction of

Dr. Wilma K. Olson

And approved By

…………………………………

New Brunswick, New Jersey

October 2017

ABSTRACT OF THE THESIS

CHARACTERIZING THE 3D INTERACTIONS OF THE BASE-PAIR STEMS

AND HELICES IN RNA MOLECULES

By ZAINAB MOHAMMED HASSAN FADHIL

Thesis Director: Wilma K. Olson

Characterizing RNA structure experimentally is a challenging task. Computational methods complement experimental methods. In this thesis, we study, using software tools such as DSSR, Matlab, and Excel, the three-dimensional structures of a group of non-redundant RNA structures. These structures are those identifiers as Leontis and Zirbel at January 2017 [1], and the relevant coordinates for these structures downloaded from the Protein Data Bank (PDB) [2].

Specifically, we find the angles between all pairs of chemically linked double helical stems in each of the RNA structures, the distances between the mid points between all these stems, and the distributions for the calculated angles and distances. Additionally, we separate the above calculations to consider stems within the same helix. A helix is composed of at least two stacked base pairs and these base pairs are not necessarily chemically linked. The third part contains these calculations separated for stems in different helices. Based on these calculations, the stems in the same helix can be classified into two groups. The first group has small angles and mid distance among its stems. The stems all lie in the same direction. In the second group, the angle is large, while the distance is small, which means that the stem directions are opposite to each other. There are different probability density functions that fit closely to the data histograms.

While the details are given in Chapter 3, the fitted probability density functions confirm that the proposed classification methods are correct. Finally, we plot the distribution of stems lengths to find that the lengths interacting stems tend to be of equal lengths and that interacting stems are more likely to be shorter.

iii

Acknowledgements

I would like to express my most sincere gratitude to my adviser Dr. Olson who has supported me throughout my Master study with her patience and knowledge.

Many thanks to my thesis committee Dr. York and Dr. Khare for offering their invaluable insights into my thesis.

I would also like to thank my fellow labmates in Dr. Olson’s group for their support in my research.

Many thanks to the department of Chemistry at Rutgers for accepting me and supporting me throughout these years.

I would like to convey gratitude towards my parents: my father Mohammed and my mother Iman, my sisters Zahraa and Noor, my brothers Mostafa and Ali in Iraq, my kids: Fadhl,

Yusur, and Dur for their unconditional love and support. This would have been impossible without their support.

Finally, many thanks to my husband, Ahmed, for always being on my side.

Table of Contents

Abstract ……………………………………………………………………………………….... ii

Acknowledgements ……………………………………………………………………………. iv

List of Tables ………………………………………………………………………………...... vi

List of Figures …………………………………………………………………………………. vi

Chapter1. Introduction ……………………………………………………………………….. 1

1.1 RNA Chemistry …………………………………………………………………………. 4 1.2 Canonical and Noncanonical base pairs ……………………………………………….... 5 1.3 Secondary structure …………………………………………………………………….. 7 1.3.1Internal Loops and Bulges ……………………………………………………… 7 1.3.2 Hairpin Loops ………………………………………………………………….. 8 1.3.3 Junctions between Double Helical Stems …………………………………….... 8

Chapter2. Material and Methods …………..…………………………………………………. 8

2.1 Obtaining the Dataset……….…………………………………………………………... 11 2.2 Processing the Date with Matlab. ……………………………………………………… 12 2.3 Calculations on the Dataset……...…………………………………………………...... 12 2.4 Dataset Histogram Plots …….……………………………………………………....… 13 2.5 Algorithm 1……..………………………………………………………………………. 14

Chapter3. Results ………….………………………………………………………………….. 16

3.1 Results for All the RNA Structures ……………………………………………………. 16 3.2 Fitting Data to Selected Probability Distributions ……………………………………... 17 3.3 Results for RNA Structures Grouped by Their Coaxial Stack……………...…………. 20 3.4 Stems in the Same Helix………………………………………………………………... 20 3.5 Stems in Different Helix ……….……………………………………………………… 24 3.6 Stems Lengths………………………………………………………………………….. 26

Chapter4. Conclusions …………….………………………………………………………….. 28

Chapter5. References ………….……………………………………………………………… 30

List of Tables

Table 1: shows PDB and number of stem in the non-redundant dataset of RNA structures with resolution 3Å or better which contain two or more stems ……………………………………….. 33

Table 2: Type of RNA structures and the number of nucleotides in each structure in the non- redundant dataset of RNA structures with resolution 3Å or better ………………………………. 41

Table 3: PDB_ID of the RNA structures in structures in the non-redundant dataset of RNA structures with resolution 3Å or better …….……………………………………………….….....50

References ………….....………………………………………………………………...……… 60

List of Figures

Figure 1.1:2P7D (Hairpin Ribozyme, RNA) three-dimensional structure generated with the DSSR, Jmol. This structure contains 4 stems. ……………………….…………………………...………… 3

Figure 1.2: Base pairs found in RNA double helices: Shown are the structures of commonly base pairs. This image takes from [Echols, H. G. (2001) Operators and promoters: the story of molecular biology anits creators, of California Press …………………………………………………………………………………...... 6

Figure 1.3 Secondary elements of RNA structures. This image takes from Nowakowski, J., and Tinoco, I. (1997) RNA structure and stability. In Seminars in Virology, Elsevier…………….. 10

Figure 3.1.a: Histogram showing the distribution of distances in Å between midpoint in stems in the non-redundant dataset of structures with resolution 3Å or better…………………………... 17

Figure 3.1.b: Normalized histogram inter segment and fitted probability density functions in the non-redundant dataset composed of structures with resolution 3Å or better…………………… 18

Figure 3.2: Histogram showing the distribution of angles in the non-redundant dataset of RNA structures with resolution 3Å or better …………………..……………….…………………….. 19

Figure 3.3: A 3D histogram showing the relation between angles and distances between stems in the non-redundant dataset composed of structures with resolution 3Å or better …………….... 20

Figure 3.4.a: Histogram showing the distribution of distances in the non-redundant dataset of RNA structures with resolution 3Å or better …………………………………………………... 21

Figure 3.4.b: Normalized histogram and fitted probability density functions for the non- redundant dataset of structures with resolution 3Å or better ………….……...... …… 22

Figure 3.5 : Histogram showing the distribution of histogram showing the distribution of angles between stems in the same helix in the non-redundant dataset of structures with resolution 3Å or better.……………………………………………….……….………………………………….. 23

Figure 3.6: A 3D histogram showing the relation between angles and distances between stems in same helix in structures in the non-redundant dataset of structures with resolution 3Å or better …………………………………………………………………………………………………... 23

Figure 3.7: Histogram showing the distribution distances between stems in the different helix in tRNA structures in the non-redundant dataset of structures with resolution 3Å or better……… 24

Figure 3.8: Histogram showing the distribution of angles between stems in the different helix in the structures in the non-redundant dataset of structures with resolution 3Å or better………… 25

Figure 3.9: A 3D histogram showing the distribution of angles and distances between stems in the different helix in RNA structures in the non-redundant with resolution 3Å or better……………………………………………………………………………………………. 25

Figure 3.10: Histogram showing the distribution of stems lengths in RNA structures in the non redundant dataset of structures with resolution 3Å or better ………………………………………… 26

Figure 3.11: Histogram showing the distribution of stems lengths in the same helices in RNA structures in the non-redundant dataset of structures with resolution 3Å or better ………………………………………………………………………………………………….. 27

Figure 3.12: Histogram showing the distribution of stems lengths in the different helices in RNA structures in the non-redundant dataset of structures with resolution 3Å or better ………………………………………………………………………………………………….. 27

vii

Chapter 1

Introduction

RNA is defined as a large group of macromolecules involved in many essential cellular processes [3]. The biological functions of these macromolecules depend on the complex secondary and three-dimensional structures that they form. In particular, RNA is a main player in the field of molecular biology because of its role in the transcription and translation of the genetic code, i.e., DNA makes RNA (via transcription) and RNA makes protein (during translation) [4].

There are several types of RNA, and probably more to be discovered. The synthesis of protein involves messenger RNA (mRNA), transfer RNA (tRNA), and ribosomal RNA (rRNA).

These RNA types are independent of each other and perform different tasks. In particular, the transfer RNA selects the amino acids, the messenger RNA directs the order in which the amino acid are sequenced, and the ribosome, which contains ribosomal RNA combined with protein, carries out the attaching process [5].

The main biophysical methods used to find macromolecular structure are: X-ray crystallography, nuclear magnetic resonance (NMR), small-angle X-ray scattering (SAXS), and

Cryo-electron microscopy (Cryo-EM). In general, experimental methods, unfortunately, can be either expensive, time consuming, or not always applicable [3].

Base pairing is one of the most important aspects in RNA 3D model. Hydrogen bonds between spatially contacting residues are formed when the RNA molecule folds. The base pairs determine the secondary structure of the RNA molecule. The dominant base pairs are: canonical

(Watson-Crick A-U and C-G) and wobble (G-U) base pairs [6].

Reddy et al. [7], studied the quantitative relationship between the interactive- packing distance and the residues in the packing interface of proteins. Furthermore, they investigated the interactive packing between the -helix and the -strand ( / u), and between the -helix and the -sheet unit ( / u). They presented their study in terms of the distances between the elements, the dihedral angles between the axes, the number, and nature of residues involved in packing. They observed relationship between the distance and volume dependent function of the residues in the packing interface.

DSSR software is a software package used for analysis, re-building, and visualization of three-dimensional nucleic acid structures. DSSR presents maps of the complex networks of interactions between nucleotide bases in known three-dimensional structures of RNAs, and facilitate the extraction and the recognition of the sequence constraints underlying a fold or three-dimensional motif [8].

In this work, DSSR has been used to identify the axes and end points of stretches of base- paired stems, the names/residue numbers/chain IDs of the nucleotides at the ends of each stem.

DSSR defines a helix to be composed of at least two stacked base pairs and a stem as a helix consisting of only canonical pairs with continuous backbones.

In this thesis, we first use DSSR to get information about individual structures. The information from DSSR contains the orientation of helices/stems, helical-axis, and the end points of the helical-axis named here as point-1 and point-2. After that, we use Matlab software to calculate the angle between all pairs of stems, the distance between midpoints. We classify the

3 dataset that we got depending on whether the stem lies in the same helix or a different helix and stems are in the same direction or opposite direction [9].

Figure 1.1: 2P7D (Hairpin Ribozyme, RNA) three-dimensional structure generated with the DSSR, Jmol [20].

This structure is taken from Torelli, A. T., Krucinska, J., and Wedekind, J. E. (2007) a comparison of vanadate to a 2′–5′ linkage at the active site of a small ribozyme suggests a role for water in transition-state stabilization. RNA (New York, N.Y.) 13, 1052-1070

1.1 RNA Chemistry

Ribonucleic acid (RNA) is a polymeric molecule made by stringing together individual ribonucleotides by adding the -phosphate group of one nucleotide onto the 3'-hydroxyl group of the previous nucleotide. Nucleotides are phosphate esters of a five carbon sugar (D-ribose) in which a nitrogenous base is covalently linked to of the sugar residue [5]. A nitrogenous base is an organic molecule with nitrogen atoms and has the chemical properties of a base. The nitrogenous bases are planar, aromatic, heterocyclic molecules which for the most part are derivatives of two parent compounds, pyrimidine and purine. For RNA, the majority of the purine components are adenine and guanine residues, and the majority of the pyrimidine residues are cytosine and uracil [10].

RNA structure is divided into three fundamental levels of organization: primary, secondary, and tertiary structure. Primary structure is the nucleotide sequence of an RNA that can be obtained, to a first approximation; from the DNA sequence of the gene encoding the RNA. The

DNA sequence often does not reveal its true primary structure, because many biologically active

RNAs are post-transcriptionally modified. The methylation of nucleotide bases and 2'-hydroxyl groups of ribose sugars are examples of these modifications. Also, other modifications can be noticed by forming unusual bases such as pseudo uracil (Y) and dihydrouridine (D), insertion or deletion of nucleotides in messenger RNA, and splicing of internal sequences (introns) from pre- messenger RNA.

The secondary structure of RNA is presented as a two-dimensional representation of its

Watson-Crick base pairs and intervening regions without such contacts. The elements of common secondary structure are: duplex, single-stranded regions, hairpins, bulges, internal

5 loops, and junctions. For example, the secondary structure of transfer RNA (tRNA) is organized into four duplex stems, three hairpin loops and a central junction [11].

The tertiary structure refers how the secondary structure elements are associated through numerous van der Waals contacts, specific hydrogen bonds via the formation of a small number of additional Watson-Crick and/or unusual pairs involving hairpin loops, internal bulges or other features [12].

1.2 Canonical and Noncanonical Base Pairs

RNA molecules can be studied at the secondary structure level, where the building blocks include helical stems and single-stranded regions such as hairpins, internal loops, and junctions.

Stems are formed by complementary canonical Watson-Crick base pairs GC and AU, along with the GU wobble base pair [13].

Frequently, RNA double helices contain non-canonical (non-Watson-Crick) base pairs in addition to conventional Watson-Crick base pairs. The non-Watson-Crick base pairs are important in forming tertiary interactions between remote portions of RNA structures. Also, the non-canonical pairs participate in the formation of structurally specific and evolutionarily conserved regions of RNA structures called RNA motifs [14].

There are different types of noncanonical base pairs. The most common types are the GU wobble, the sheared GA pair, the reverse Hoogsteen pair, and the GA imino pair. Some the most common types of base pairs are shown in Figure 1.2.

Figure 1.2: Base pairs found in RNA double helices: Shown are the structures of commonly base pairs. This

image is taken from [Echols, H. G. (2001) Operators and promoters: the story of molecular biology

anits creators, Uni of California Press].

1.3 Secondary Structure

The secondary structure of RNA is presented as a two-dimensional representation of its

Watson-Crick base pairs and intervening unpaired regions. The elements of common secondary structure are: bulges, internal loops, hairpins, and junctions as shown in Figure 1.3.

1.3.1 Internal Loops and Bulges

Internal loops and bulges are created when the nucleotides that do not have Watson–

Crick complements on the opposite strand are presented in the double-stranded regions. The smallest bulge loop is formed by a single unpaired base on one strand, where the base can be either stacked into the helix or remain outside of it. A bend is usually created in the helix when a single bulge is incorporated into the duplex. An extrahelical residue creates a possible site of interaction with external ligands, because it is exposed to the solvent. However, an extrahelical residue does not necessary cause bending. There are few structural studies available on single

RNA bulges, where it seems that single purines (G and A) stack inside the helix whereas pyrimidines (C and U) are extrahelical [15]. Distinguishing internal loops from bulges is done by checking where Watson–Crick pairing is interrupted. In internal loops, Watson–Crick base pairing is interrupted in both strands, while in bulges the Watson–Crick pairing is continuous on one strand. Non-canonical pairs appear in the smallest internal loops. These loops have two apposed nucleotides that cannot form Watson–Crick pairs. RNA bases have the ability to form hydrogen bonded pairs in other combination. Inside of the loop, the nucleotides form complex structures with non-Watson–Crick pairs, base–sugar, sugar–sugar, and sugar–phosphate hydrogen bonds and extensive stacking interactions. The structure of a particular internal loop is

8 not easily predicted from the sequence. It depends on the number and sequence of the unpaired nucleotides. Internal loops can cause significant bending of the RNA helix and can introduce sites of local flexibility (21) like bulges. The disordered loop regions, frequently, become highly structured upon binding an external ligand, such as a protein that specifically recognizes the loop. Protein–RNA interaction can significantly modify the general conformation of the RNA

(and the protein) [16].

1.3.2 Hairpin Loops

If a single-stranded RNA chain makes a sharp turn and folds back on itself to form

Watson–Crick base pairs leaving some residues unpaired, then this will form a hairpin loop. By this mechanism, a stem-loop structure is formed, which covers the end of the helix. Hairpin loops can be as small as two nucleotides. The formation of base pairs that divide the loop into an internal loop and a smaller hairpin loop leads to very large hairpin loops. Hairpin loops can be flexible and disordered, or they may form rigid and well-defined, three-dimensional structures depending on their sequence and their size. Hairpin loops are important RNA structural elements which provide sites for interactions with proteins and nucleic acids and serve as nucleation sites for RNA folding [17].

1.3.3 Junctions between Double Helical Stems

The global shapes of RNA molecules are often determined from the regions where two or more double-helical stems come together. For example, a three-way junction in the hammerhead ribozyme is responsible for its wish-bone-like structure; and the four-way junction from transfer

RNAs determines their characteristic L-shaped conformation. The junction structure and stability

9 depends on the coaxial stacking of double-helical stems. Helix stacking introduces little bending.

Coaxial stacks provide means for extending existing shorter helices, as well as stabilizing junctions. In general, there are single-stranded regions at stacked helical junctions. These unpaired nucleotides are responsible, among many other functions, for the formation of sites for protein binding (5S rRNA) and RNA self-cleavage on the hammerhead ribozyme. Also, unpaired bases are responsible for stabilizing the junction through the formation of base triples with the junction stems, or they can form metal binding pockets which reduce unfavorable repulsions between negatively charged phosphate groups. The conformations of RNA junctions vary widely, because they depend on the number of stems, and the sizes and sequences of the single- stranded regions in the branch region [18].

Figure 1.3: Secondary elements of RNA structures. This image is taken from Nowakowski, J., and Tinoco, I.

(1997) RNA structure and stability. In Seminars in Virology, Elsevier.

Chapter 2

Materials and Methods

As the number of experimentally solved RNA-containing structure grows, it is becoming increasingly important to characterize the geometric features of the molecules consistently and efficiently. We used the DSSR software package [8] to analyze a group of non-redundant RNA structures defined by X-ray analysis at 3Å or better resolution and calculated the angles and distances between all stems in each structure.

Using files from Protein Data Bank (PDB) [2], I arranged two tables which have information on the structure type as shown in Table [2], and their description as shown in Table

[3].

2.1 Obtaining the Dataset

RNA crystal structures are identified as Leontis and Zirbel at January 2017 [1], as non- redundant and of 3Ao or better resolution and are listed in Table [1].

All structures were downloaded in PDB or PDBx/mmCIF format [2]. For each of group of RNA structures, we used DSSR to collect (i) the number of stems, (ii) the helical-axis of each stem (the helical-axis can be used to quantify the relative orientation between any two stems),

(iii) point-one and point-two (designating the end points in the original coordinate frame of the helical axis of the stem), (iv) names /residue numbers/chain IDs of the nucleotides at the ends of each stem. After that, we saved the information in a CSV file. Finally, we filtered the RNA structures according to the number of stems. This means that we considered only the RNA structures that have two or more stems.

2.2 Processing the Dataset with Matlab

We used Matlab version 2016 B to write our code. This code helps us to retain some information from CSV files (the output from DSSR) including:

- The number of the stem as show in Table [1] in Appendix A.

- The names/residue numbers/chain IDs of the nucleotides at the ends of each stem.

- The number of nucleotides and type of RNA as show in Table [2] in Appendix A.

We then calculated the midpoint, angle and distance between all pairs of stems in the RNA structure and saved the information in an Excel file.

2.3 Calculations on the Dataset

The information from DSSR contains the helical/stem-axis and its corresponding normalized helical axis vector. This vector is used to measure the orientation between any two straight helical/stems [9]. The end points of the helical/stem-axis named as point-1 and point-2 are used to calculate midpoint. We use point-1 and point-2 of the first stem to calculate midpoint-1 as shown in equation (2.1). Similarly, we find midpoint-2 for the second stem as shown in equation (2.2). After that, we calculate the distance between midpoint-1 and midpoint-2 as shown in equation (2.3).

2.1,

2.2,

2.3,

The helical-axis is used to calculate the angle; first we calculate dot product between axis1 and axis2 as in equation (2.4), then angle in degrees using equation (2.5).

2.4,

2.5

2.4 Dataset Histogram Plots

We created a table in Excel that contains the measurements that we need. These measurements are the distances between all pairs of stems in each RNA structure and the angles between the axes of the pairs of stems. From this information, we calculated the maximum, the minimum, the standard deviation, and the average of all the distances and angles.

We created two (2D) histogram plots, where the first histogram is for the distribution of the distances as shown in Figure [3.1]. In the second histogram plot, we showed the distribution of the angles, in degrees, which is shown in Figure [3.2].To get a more general view, we used

Matlab to create a 3D histogram for the distribution of distances and angles. This histogram is shown in Figure [3.3]. Our work is summarized by the algorithm below.

Algorithm 1:

❖ Obtaining the Data:

➢ Download the PDB identifiably non-redundant structures of resolution at 3A or

better.

➢ Collected the RNA structures from the Protein Data Bank (PDB).

❖ Processing the Data:

➢ Use DSSR analyze each RNA structure

➢ Store the information from DSSR in a CSV file

➢ Use Matlab to extract and find the required information as follows:

▪ For all the RNA structures in the CSV file

• Check that the number of stems is

• For all the structures where the step above holds, do the following:

 Get the axes for each stem

 Get the end points of each stem which are named as point-1 and point-2

 Use point-1 and point-2 to find the midpoint for each stem

 Find the distance between the mid points of each pair of stem over all

combinations of stems in the dataset

 Find the angle between the axis of each stem over all combinations of

stems in the dataset

 Get the length of the stem, which means the number of base pairs

 Copy the information obtained above into an Excel file

➢ Using DSSR plus a Matlab code, classify the stems into either the same helix or not

➢ Compute the distribution through a 2D histogram, the mean, the variance for the

distances and the angles in Matlab and Excel

➢ Compute the distribution through a 3D histogram in Matlab between the angles and

the distances

➢ Compare the distribution through a 3Dhistogram in Matlab between the lengths

stems.

➢ Use Matlab built-in functions to fit these histograms into probability density functions

Chapter 3

Results

In this chapter, we present our findings using the DSSR software tool, Matlab software, and Excel. Also, we go over the results that we found and analyze them. The results in the first part of this chapter are the distances between the mid points for all the RNA structures. These structures are those identifiers as Leontis and Zirbel at January 2017 [1]. Also, the chapter contains the angles measurements between every two stems for all these structures, and the distribution of the calculated distances and angles. In the second part, we separate the above calculations to consider stems within the same helix and stems in different helix. The third part contains these calculations separated for stems in different helices. Finally, we show the distribution of all stems lengths, and then we separate the stems lengths into stems in the same helix and stems in different helix.

3.1 Results for All the RNA Structures:

We have chosen RNA structures identifiers as Leontis and Zirbel at January 2017 [1].

Then, we processed these structures using the DSSR software to get the data were stored in

“CSV” files. The data were then recalled using Matlab to find the midpoint distances and angles between the axes of each stems for all the RNA structures. Finally, we collected these measurements in an Excel file to get their distributions. The results in Figure 3.1.a show the distribution of stems distances, which vary between 5.2Å to 203 , with an average distance of

68Å, and a standard deviation 37Å. One can see that the distribution more than 88% of stems lie between {20Å–120Å}. Also, it is clear that the distribution is not a normal distribution.

Figure 3.1.a: Histogram showing the distribution of distances in Å between midpoint of stems in the non-redundant dataset of RNA structures with resolution 3Å or better.

3.2 Fitting Data to Selected Probability Distributions:

After plotting the different data histograms, we used Matlab built-in functions to fit these histograms into probability density functions. The goodness of the fit is measured in terms of the negative log likelihood distance (NLL) which is a built-in function in Matlab too. The negative log likelihood distance measures the difference between the experimental distribution and the fitted one by applying some optimization algorithms. A lower value of the (NLL) the closer the fitted distribution to the data. More details for the Matlab built-in function, fitdist, which we used, can be found in [22]. We tried, by means of trial and error, several probability density functions and selected the best two in terms of the negative log likelihood distance.

In Figure 3.1.b, we used Matlab to find the best probability density functions (PDFs) which fit the inter-segment distances distribution. We normalized the distances in Figure 3.1.b, and fit one probability density functions, the Weibull probability density function. This function

18 fit very nicely to our experimental data. However.we believe that the Weibull probability density function gives a goodr description to our experimental distance calculations according to a standard measure of goodness of fitted probability density functions called the negative of the log likelihood function (NLL), where the lower value of this function, the better the fit is. For the

Weibull is -2.2197e+05. The Weibull distribution are given by equations (3.1)

[ 3.1

Figure 3.1.b, For Weibull distribution, the parameters are:

Figure 3.1.b: Normalized histogram of inter segment distances and fitted probability density functions for the non-redundant dataset of RNA structures with resolution 3Å or better.

Figure 3.2 shows the distribution of the angles between stems, which varies from 0 to , with an average 8 and a standard devotion It can be see that there is no specific patteren for the distribution of angles. Figure 3.3 shows the 3D histogram of the distribution of angles and distances.

Figure 3.2: Histogram showing the distribution of angles in the non-redundant dataset of RNA structures with resolution 3Å or better.

Figure 3.3: A 3D histogram showing the relation between angles and distances between stems in the non-redundant dataset composed of structures with resolution 3Å or better

3.3 Results for RNA Structures Grouped by their Coaxial Stack:

Coaxial stacking happens if more than one stem exists in a single helix, such that neighboring stems can stack either above one another, or on either side of each one [5]. In this part, we classified the stems in each RNA structure, using the information provided by DSSR, according to their helix numbers.

3.4 Stems in the Same Helix

Stems that belong to the same helix are grouped together for further investigation. Figure

3.4.a shows the distances histogram, which varies from to , with an average distance of

and a standard deviation , whereas Figure 3.4.b shows the normalized histograms and the fitted probability density functions compersion of Figure 3.4b with Figure 3.1b shows that the distribution of distances is much narrows if the stems occur in the same helix as opposed

21 to all helices. The average distances are also shorter and the standard distribution is much smaller. In Figure 3.4.b, we found, experimentally, that the Inverse Gaussian and Birnbaum-

Sanders probability density functions have the best fit to the experimental data that we have in terms of the NLL function. Specifically, the Inverse Gaussian has NLL = -1.2559e+04, while the

Birnbaum-Sanders’ NLL= -1.2556e+04. Finally, we added the Beta distribution which was found in Figure 3.1.b to be the best fit for the total distance for the comparison purpose. It can be seen that there is a narrower concentration of the distances in the main lobe. That’s, the classification method according to the coaxial stack gives a better resolution for the distance measurements. The parameters of the Inverse Gaussian PDF are: :

While for Birnbaum-Sanders PDF

Figure 3.4.a Histogram showing the distribution of distances between stems in the same

helix in the non-redundant dataset of RNA structures with resolution 3Å or better.

Figure 3.4.b: Normalized histogram and fitted probability density functions for the non-redundant dataset of RNA structures with resolution 3Å or better.

After grouping the distances as above, we obtained the histogram angles shown in Figure

3.5, with an average and standard deviation . The average for the cases of the angles which are less than and their number is 1319. On the other hand, the average for the cases of the angles which are greater than or equal to and their number is 675.

Figure 3.5: Histogram showing the distribution of angles between stems in the same helix in thnon- redundant dataset of RNA structures with resolution 3Å or better

Figure 3.6: A 3D histogram showing the distrinution of angles and distances between stems in the same helix in RNA structures in the non-redundant dataset with resolution 3Å or better.

This figure shows the stems in the same helix can be classified into two groups. The first group has small angles and small distance among its stems. The stems all lie in the same direction. In the second group, the angle is large, while the distance is small, which means that the stem directions are opposite to each other. The distribution of distance is much narrower for

24 the stems pointing in the same direction than those pointing in the opposite directions. There are also more examples of stems that point in the same direction without a given helix that points in the opposite direction. The helix must be longer for stems to point in the opposite direction.

3.5 Stems in the different helix

Stems belonging to different helices are grouped together for further investigation. Figure

3.7 shows the distances histogram, which varies from to with an average distance of

and a standard deviation . The distribution of distances is much wider than that between stems in the same helix (compare Figure 3.7 with Figure 3.4a). Figure 3.8 shows the angles histogram, which varies from to , with an average angle of and a standard deviation .

Figure 3.7: Histogram showing the distribution distance between stems in the different helices in structures from the non-redundant dataset of RNA structures with resolution 3Å or better.

Figure 3.8: Histogram showing the distribution of angles between stems in the different helices in

RNA structures from the non-redundant dataset of structures with resolution 3Å or better.

Figure 3.9: A 3D histogram showing the distribution of angles and distances between stems in the different helices in RNA structures in the non-redundant dataset of RNA structures with resolution

3Å or better.

3.6 Stems lengths

This section includes Figures 3.10-3.12 showing the distribution of stems lengths in the non-redundant dataset of RNA structures. Figure 3.10 shows the distribution of lengths for all stems which varies from to , with an average of and a standard deviation .

Figure 3.11 shows 3D distribution of stems lengths in the non-redundant dataset of RNA structures, with the lengths representing the lengths of the stem in each pair. The diagonal in the plots shows that the lengths interacting stems tend to be of equal lengths and that interacting stems are more likely to be shorter. Stems of lengths (3- have pairs occure in greatest abundance. The distribution of stems length for the stems in the same helix as shows Figure 3.12.

The lengths stems in the different helices as in Figure 3.13.

Figure 3.10: Histogram showing the distribution of stems lengths in RNA structures in the non- redundant dataset of structures with resolution 3Å or better.

Figure 3.11: Histogram showing the distribution of stems lengths in the same helices in RNA structures in the non-redundant dataset of structures with resolution 3Å or better.

Figure 3.12: Histogram showing the distribution of stems lengths in the different helices in RNA structures in the non-redundant dataset of structures with resolution 3Å or better. Chapter 4

Conclusions

In this thesis, we used computational methods to characterize the three-dimensional structure of a group of RNA structures which are obtained from PDB website using the following software tools: DSSR, Matlab, and Excel. We found the distance between the mid points between for all the RNA structures that we chosen from Leontis and Zirbel paper [1], the angles between each two stems for all these structures, and the distribution for the calculated angles and distances. We separated the above calculations to consider stems within the same helix. Furthermore, these calculations are separated for stems in different helices. Based on these calculations, the stems in the same helix are classified into two groups. The first group has small angles and mid distance among its stems. Stems are in the same direction. In the second group, the angle is large, while the distance is small, which means that the stems point in opposite directions. Finally, we found that there are different probability density functions that closely fit the data histograms. The fitted probability density functions confirm that the proposed classification methods are correct. As future work, the stems directions future RNA structures might can be predicted using the method proposed in this thesis. The fitted probability density functions can be the basis of using more advanced concepts like machine learning to develop more sophisticated algorithms. These algorithms can take advantage of the calculations that we have obtained to make a joint decision that is based on the fitted probability density functions, the distances of the midpoints between stems, and the angles between these stems to get a better

29 understanding about new structures or existing ones. Finally, we ploted the distribution of stems lengths to find that the lengths interacting stems tend to be of equal lengths and that interacting stems are more likely to be shorter.

Chapter 5

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Appendix

Table 1: shows PDB and number of stem in the non-redundant dataset of RNA structures with resolution 3Å or better which contain two or more stems.

PDB_ID NUMBER OF STEM 5JCF 2 1DFU 2 1DQF 2 1DQH 2 1EFO 2 1F27 2 1HYS 2 1JBR 2 1JBT 2 1KD4 2 1KD5 2 1LNT 2 1Q2R 2 1QC0 2 3BT7 2 1MSW 2 1s77 2 1QLN 2 1RPU 2 1SDR 2 1T0E 2 1WNE 2 1YVP 2 1ZBH 2 1YYK 2 1ZDJ 2 1XOK 2 2R20 2 1ZH5 2 2A43 2 2AO5 2 2BGG 2 2BH2 2

2DR5 2 2E9T 2 2EC0 2 2OE5 2 2OE8 2 3LRR 2 3SN2 2 3TS0 2 3TS2 2 4ATO 2 4C9D 2 4E5C 2 4E6B 2 4E 59 2 4FXD 2 4GCW 2 4ILL 2 4IQS 2 4PCO 2 4PQU 2 4Q5S 2 4Q5V 2 4QIL 2 4QOZ 2 4TUW 2 4TUX 2 4U6K 2 4U35 2 4WRT 2 4WZM 2 4XW0 2 5AWH 2 5C9H 2 5D0A 2 5ED1 2 5F0Q 2 7MSF 2 165D 2 422D 2 435D 2 437D 2 439D 2 466D 2

1L2X 2 3VJR 2 3CGP 2 3FS0 2 3F73 2 3DD2 2 3CJZ 2 3CGS 2 3CGR 2 3TZR 3 1FUF 3 3LOA 3 1I9X 3 1MZP 3 1NTB 3 1NYI 3 1O9M 3 1S76 3 1SA9 3 1URN 3 1CSL 3 1Z7F 3 1F1T 3 2B3J 3 2DLC 3 2F4S 3 2FQN 3 2G92 3 2EZ6 3 2IZN 3 2JIT 3 2NVQ 3 2PWT 3 2PXV 3 3B31 3 3BNL 3 3E2E 3 3NPN 3 3OK4 3 3R1E 3 5DQK 3 6MSF 3 406D 3

364D 3 409D 3 5HN2 3 2NUG 3 5CKK 3 5B43 3 5AY3 3 4P3S 3 4P3T 3 4P43 3 4PDB 3 4PKD 3 2BU1 4 3AGV 4 2XNZ 4 2P7D 4 2P7E 4 1KH6 4 3FTM 4 3GS5 4 1FEU 4 1OOA 4 1JZV 4 1QF6 4 1QRS 4 1RLG 4 4ERD 4 4G7O 4 1H4S 4 1T0D 4 1TFW 4 1TfY 4 1U1Y 4 1E7K 4 1D4R 4 280D 4 1xjr 4 1Y27 4 1F7V 4 4X4N 4 4X4T 4 4X4V 4 4XWF 4

4YCP 4 4Z31 4 5AXM 4 1YFG 4 5CCB 4 5CNR 4 5DEA 4 5ED2 4 5F5F 4 5FJ4 4 4TZX 4 4QVI 4 4RDX 4 4QI2 4 4PQV 4 4P97 4 4O41 4 4MSR 4 4MCF 4 4M4O 4 4LX6 4 4LGT 4 4KZD 4 4JXZ 4 4JYZ 4 4K4S 4 4K4T 4 3SYW 4 3E5C 4 3DH3 4 3CQS 4 1xjr 4 4KYY 4 2I82 4 2ZUE 4 4QEI 4 3AMT 4 3B5S 4 3GM7 5 3LA5 5 3WBM 5 3SUX 5 2ZZM 5

1H3E 5 1YZ9 5 4N0T 5 3AM1 5 5D8H 5 4RUM 5 4TS0 5 4PR6 5 4PRF 5 4K27 5 4RZD 5 3MOJ 5 4OJI 5 4P5J 5 4ZDO 5 1QBP 6 5BTM 6 4JRC 6 4KQ0 6 4OQ9 6 4QLM 6 2Q1O 6 2PN4 6 2QUS 6 2QUW 6 2OZB 6 1J9H 6 5F9F 6 5G4V 6 1I6U 6 4AOB 7 3GX5 7 5B2Q 7 4WFL 7 3GX5 7 3UCZ 7 5BTP 8 5HR7 8 4ZT0 8 4YYE 8 5HR6 8 4L81 8 4ILM 8

4K4Y 8 4K4Z 8 3SKI 8 3SKL 8 3R1D 8 3IVN 8 5HC9 8 2Z75 8 2ZZN 8 2AZX 8 1ZX7 8 1ZHO 8 2CT8 8 2CV1 8 1EFW 8 1MMS 8 1IL2 8 1L9A 8 1H38 8 1NUJ 8 3DIL 9 3EPK 9 4ZNP 9 5H9F 9 5KX9 9 4X4P 9 2Y9H 9 1HMH 9 1YLS 10 2BTE 10 1ET4 10 2OIU 10 4AQ7 10 5AH5 10 4K50 10 3RW6 10 3RG5 10 3Q3Z 10 3D2V 10 3P59 11 2XD0 11 1G1X 12 3P22 12

5AOX 12 4Y1J 12 4YCO 12 4OO8 12 4FRG 12 2QWY 12 1U9S 13 2GDI 13 4YAZ 14 4P9R 14 3V7E 15 3PDR 20 4FAU 24 2NZ4 39 3R1C 54 1X8W 67 4B3T 97 2VQE 97 1N32 98 2UUA 99 1S72 179 5DM6 182 5J7L 569

Table 2: Types of RNA structures and the number of nucleotides in each structure in the non- redundant dataset of RNA structures with resolution 3Å or better.

PDB_ID Type Nucleotide 5JCF INNATE IMMUNE PATTERN RECOGNITION RECEPTOR 43 1DFU PROTEIN-RNA COMPLEX, RIBOSOME, Escherichia coli 38 1DQF DOUBLE HELIX, CYTOSINE BULGE, RNA 19 1DQH DOUBLE HELIX, CYTOSINE BULGE, RNA 19 1EFO HYBRID, ADENINE BULGE 19 1F27 RNA APTAMER, PSEUDOKNOT, BIOTIN-BINDING RNA 145 1HYS POLYPURINE TRACT, PROTEIN-NUCLEIC ACID COMPLEX, RNASE 45 1JBR PROTEIN-RNA INTERACTION, SPECIFIC RECOGNITION, 62 1JBT RESTRICTOCIN, RIBOTOXIN, HIGHLY SPECIFIC RIBONUCLEASE 58 1KD4 RNA DUPLEX, METAL BINDING 22 1KD5 RNA DUPLEX 22 1LNT SRP, INTERNAL LOOP, MISPAIR, RNA 24 1Q2R PROTEIN-RNA COMPLEX 42 1QC0 A-RNA STRUCTURE, RIBONUCLEIC ACID 57 3BT7 TRANSFERASE-RNA COMPLEX 38 1MSW T7RNAP ELONGATION COMPLEX, TRANSCRIPTION/DNA/RNA 47 1S77 T7 RNA POLYMERASE, TRANSFERASE 48 1QLN NUCLEOTIDYLTRANSFERASE, T7 RNA POLYMERASE 39 1RPU RNAI, PROTEIN-RNA COMPLEX, RNA DOUBLE HELIX 42 1SDR A-RNA, DOUBLE HELIX 48 1T0E CRYSTAL STRUCTURE, BACTERIAL DECODING SITE RNA 66 1WNE PROTEIN-DNA COMPLEX, FOOT AND MOUTH DISEASE VIRUS 13

1YVP RNA BINDING PROTEIN / RNA - XENOPUS LAEVIS 52 1ZBH HYDROLASE /RNA - HOMO SAPIENS 36 1YYK RIBONUCLEASE III, DOUBLE-STRANDED RNA. 48 1ZDJ VIEUS/ RNA - ESCHERICHIAVIRUS MS2 16

1XOK VIRAL PROTEIN/ RNA - ALFALFA MOSAIC VIRUS 36 2R20 ASYMMETRY RNA 26

1ZH5 TRANSCRIPTION / RNA - HOMO SAPIENS 18 2A43 POTATO LEAF ROLL VIRUS, PSEUDOKNOT, RNA 26 2AO5 G-U BASE PAIR, RNA DUPLEX 40 2BGG RNA-BINDING PROTEIN - ARCHAEOGLOBUS FULGIDUS 29 2BH2 TRANSFERASE - ESCHERICHIA COLI 62 2DR5 TRANSFERASE / RNA - ARCHAEOGLOBUS FULGIDUS 32 2E9T TRANSFERASE / RNA - FOOT-AND-MOUTH DISEASE VIRUS 30 2EC0 TRANSFERASE / RNA - FOOT-AND-MOUTH DISEASE VIRUS 30 2I91 RNA BINDING PROTEIN - XENOPUS LAEVIS 45

2OE5 AMINOGLYCOSIDE ANTIBIOTICS, RIBOSOMAL DECODING SITE 33 2OE8 AMINOGLYCOSIDE ANTIBIOTICS, RIBOSOMAL DECODING SITE 33 2ZKO RNA BINDING PROTEIN - INFLUENZA A VIRUS 42 3IAB HYDROLASE / RNA - SACCHAROMYCES CEREVISIAE 46 3LRR HYDROLASE / RNA - HOMO SAPIENS 24 3NVI TRANSFERASE / RNA - PYROCOYROCOCCUS FURIOSUS 48 3R2D TRANSCRIPTION / RNA - AQUIFEX AEOLICUS 20 3SN2 LYASE / RNA - ORYCTOLAGUS CUNICULUS 29 3TS0 RNA BINDING PROTEIN / RNA - MUS MUSCULUS 46 3TS2 RNA BINDING PROTEIN / RNA - MUS MUSCULUS 48 4ATO TOXIN / ANTITOXIN - BACILLUS THURINGIENSIS 34 4C9D HYDROLASE / RNA - THERMUS THERMOPHILUS 25 4E5C SIRNA, TRINUCLEOTIDE REPEAT EXPANSION, RNA 38 4E6B SIRNA, TRINUCLEOTIDE REPEAT EXPANSION, RNA 16 4E 59 3' SLIPPERY DUPLEXES - CCG REPEATS 32 4FXD TRANSFERASE / DNA / RNA - SACCHAROMYCES CEREVISIAE 32 4GCW HYDROLASE / RNA - BACILLUS SUBTILIS 44 4ILL HYDROLASE / RNA - SULFOLOBUS SOLFATARICUS 36 4IQS SELENIUM RNA, RNA 48 4PCO GU WOBBLE BASE PAIR MOTIF, RNA - ENDOTHIA GYROSA 50 4PQU TRANSFERASE HYDROLASE / DNA / RNA, VIRUS 80 4Q5S TRANSCRIPTION-DNA-RNA COMPLEX 36 4Q5V TRANSFERASE-DNA-RNA COMPLEX 48 4QIL RNA BINDING PROTEIN / RNA - HOMO SAIENS 32 4QOZ RNA / HYDROLASE / RNA BINDING PROTEIN 44 4TUW RNA BINDING PROTEIN / RNA 52 4TUX RNA BINDING PROTEIN / RNA - 52 4U6K DNA/RNA DUPLEX, ANTISENSE 36 4U35 RNA, 2-THIO-URIDINE - SYNTHETIC CONSTRUCT 14 4WRT TRANSFERASE / RNA - INFLUENZA B VIRUS 29 4WSB TRANSFERASE-RNA COMPLEX - INFLUENZA A VIRUS 28 4WZM TRANSFERASE - FOOT-AND-MOUTH DISEASE VIRUSE 15 4XW0 CCUG REPEATS, RNA DUPLEX - HOMO SAPIENS 19 5AWH RNA BINDING PROTEIN-DNA-RNA 72 5C9H TELOMERASE, RNA-PROTEIN COMPLEX 42 5D0A TRNA MODIFICATION, HEAT 24 5ED1 DEAMINASE, HUMAN, HYDROLASE-RNA COMPLEX 46 5F0Q TRANFERASE-DNA-RNA COMPLEX 34 7MSF VIRUS/RNA COMPLEX - ESCHERICHIA VIRUS 25 205D A-RNA, DOUBLE HELIX, INTERNAL LOOP, MISMATCHED 24 354D U-RNA, DOUBLE HELIX, MISMATCHED, RNA 24 361D RNA, SINGLE STRAND, MISMATCHED 40 377D A-RNA, DOUBLE HELIX 24

397D DOUBLE HELIX, OVERHANGING BASES, RNA 27 398D A-DNA/RNA, DOUBLE HELIX, DNA-RNA HYBRID 32 402D RNA DOUBLE HELIX, RNA WITH TANDEM 16 422D DOUBLE HELIX, RNA 24 435D DOUBLE HELIX 28 437D DOUBLE HELIX 28 439D FRAGMENT OF 5S RRNA, A-RNA 16 466D DOUBLE HELIX - RIBONUCLEIC ACID, DISORDERED MODE 28 4BW0 RNA-RNA BINDING PROTEIN COMPLEX 26 1QCU A-RNA STRUCTURE, RIBONUCLEIC ACID 44 1L2X PSEUDOKNOT, FRAMESHIFTING, 28 3VJR HYDROLASE-RNA COMPLEX - ESCHERICHIA COLI 72 3FTF TRANSFERASE / RNA - ANTIBIOTIC RESISTANCE 45 3FS0 RIBOZYME - LIGASE 21 3F73 NUCLEIC ACID BINDING PROTEIN / DNA / RNA 43 3DD2 HYDROLASE INHIBITOR / RNA 25 3CJZ TRNA 26 3CGS RNA DOUBLE HELIX 25 3CGR RNA DOUBLE HELIX 25 3CGP RNA DOUBLE HELIX 25 1FUF BULGE, BASE TRIPLE, RNA 28 3LOA LECTIN 44 1I9X PRE-MRNA SPLICING 26 1MZP RIBOSOME, RIBOSOMAL PROTEIN, RNA-PROTEIN COMPLEX 55 1NTB STREPTOMYCIN RNA-APTAMER, MAGNESIUM FORM 40 1NYI HAMMERHEAD RIBOZYME 41 1O9M ANTIBIOTIC/RNA 42 1S76 T7 RNA POLYMERASE, TRANSFERASE 48 1SA9 RNA DOUBLE HELIX 40 1URN PROTEIN-RNA COMPLEX - TRANSCRIPTION-RNA COMPLEX 55 1CSL RRE HIGH AFFINITY SITE, HIV-1, RNA 28 1Z7F RNA, DUPLEX, MISMATCH 48 1F1T RNA 38 2B3J HYDROLASE / RNA 54 2DLC LIGASE-TRNA COMPLEX 67 2F4S A-SITE RNA, NEAMINE 42 2G92 RNA 24 2EZ6 HYDROLASE / RNA 56 2IZN VIRUS / RNA 26 2JIT TRANSFERASE 34 2NVQ TRANSCRIPTION TRANSFERASE / DNA-RNA HYBRID 53 2PWT RIBOSOMAL DECODING SITE 42 2PXV SIGNALING PROTEIN / RNA 49

3B31 TRANSLATION INITIATION, TRNA ANTICODON 43 3BNL RIBOSOME, DECODING SITE, RNA 44 3E2E T7 RNA POLYMERASE, TRANSCRIPTION 66 3EGZ TETRACYCLINE , RIBOSWITCH, ANTIBIOTIC, RNA 64 3MEI S-TURN, C-C BASE PAIR, RNA 46 3NPN RNA, RIBOSWITCH 51 3OK4 ALTRITOL, SUGAR MODIFICATION, RNA 60 3R1E CGG REPEATS, RNA 16 4E 58 CCG REPEATS, 5' SLIPPERY DUPLEXES, RNA 2 3 4FNJ CUG REPEAT GAAA TETRALOOP/RECEPTOR, TOXIC RNA 35 5DQK RIBOZYME, HAMMERHEAD, RNA 68 5EW4 REPEAT EXPANSION DISORDER, GENETIC DISEASE, RNA 39 3S49 RNA, 2-SE-URIDINE 46 6MSF VIRAL COAT PROTEIN/RNA COMPLEX, RNA APTAMER 24 406D DISORDERED, RNA, DOUBLE HELIX 34 364D U-RNA, DOUBLE HELIX, 60 409D DOUBLE HELIX, I.U WOBBLES, RNA 48 420D A-RNA STRUCTURE, MISMATCH A RNA 32 5HN2 RNA, 5-FORMYLCYTOSINE 48 2NUG RIBONUCLEASE III, ENDONUCLEOLYTIC , HYDROLASE/RNA 44 5CKK DEOXYRIBOZYME, RNA-LIGASE, CATALYTIC DNA, LIGASE 59 5B43 NUCLEASE, HYDROLASE-RNA-DNA COMPLEX 80 5AY3 RNA / SYNTHETIC CONSTRUCT 24 4P3S RIBOSOME, ANTIBIOTIC-RESISTANCE 43 4P3T RIBOSOME, ANTIBIOTIC-RESISTANCE 46 4P43 RIBOSOME, ANTIBIOTIC-RESISTANCE 44 4PDB PROTEIN-RNA COMPLEX TRANSLATION, RIBOSOMAL. 38 4PKD U1-70K, U1 SNRNP, GENE REGULATION 55 3TZR REGULATORY MOTIF, AMINOBENZIMIDAZOLE BINDING, RNA 36 3AGV IGG, RNA APTAMER, IMMUNE SYSTEM-RNA COMPLEX 43 2XNZ RNA, APTAMER, RNA-LIGAND COMPLEX, MRNA 65 2P7D HAIRPIN RIBOZYME; PRODUCT MIMIC; TRANSITION 61 2P7E HAIRPIN RIBOZYME; VANADATE; REACTION INTERMEDIATE 61 3FTM RIBOZYME, LIGASE, 2'-5', 2-5, 2P5, RNA 46 3GS5 HAIRPIN RIBOZYME, RNA RIBOZYME 61 3I2S HAIRPIN RIBOZYME, N1-DEAZAADENOSINE, RNA 61 1FEU GENERAL STRESS PROTEIN CTC, 5S RRNA-PROTEIN COMPLEX 80 1OOA PROTEIN-RNA COMPLEX, TRANSCRIPTION FACTOR NF-KB 58 1JZV A-BULGE, A-RNA, HIV-1 SL2 34 1QF6 TRNA SYNTHETASE, TRNA(THR), LIGASE-RNA COMPLEX 77 1QRS TRNA SYNTHASE, PROTEIN BIOSYNTHESIS, LIGASE 75 1RLG PROTEIN-RNA, STRUCTURAL PROTEIN/RNA COMPLEX 50 4ERD RNA BINDING PROTEIN / RNA - TETRAHYMENA THERMOPHILA 44

4G7O TRANSCRIPTION INITIATION COMPLEX, RNAP-PROMOTER 84 1H4S TRANSCRIPTION INITIATION COMPLEX, RNAP-PROMOTER 69 3X1L RNA-RECOGNITION MOTIF, RNA SILENCING, RNA BINDING 54 4JF2 RIBOSWITCH, H-TYPE PSEUDOKNOT, RNA 78 3ZP8 RNA, CATALYTIC RNA 63 4C4W RNA BINDING PROTEIN-RNA COMPLEX 70 4C7O NUCLEAR PROTEIN, PROTEIN TRANSLOCATION 53 1MJI RIBOSOMAL PROTEIN - 5S RRNA COMPLEX 68 1SAQ RNA DOUBLE HELIX, RNA TANDEM G-A BASE PAIR 40 1T0D BACTERIAL DECODING SITE 2 RNA 66 1TFW CCA-ADDING COMPLEX, TRANSFERASE-RNA COMPLEX 78 1TfY CCA-ADDING COMPLEX, TRANSFERASE-RNA COMPLEX 77 1U1Y COMPLEX (CAPSID PROTEIN-RNA HAIRPIN) 33 1E7K RNA-BINDING PROTEIN, RNA RECOGNITION MOTIF 34 1jJU AMINOACYL-TRNA SYNTHETASE, LIGASE, TRNA 74 1Y26 A-RIBOSWITCH ADENINE RECOGNITION, RNA 72 1D4R A-RIBOSWITCH ADENINE RECOGNITION, RNA 84 2BU1 VIRUS/RNA, COMPLEX (CAPSID PROTEIN/RNA HAIRPIN) 34 280D UNUSUAL RNA, DOUBLE HELIX, MISMATCHED 48 1xjr GNRA, 530-LIKE LOOP, S2M, PURINE BULGE 47 1Y27 G-RIBOSWITCH GUANINE RECOGNITION, RNA 69 1F7V TRNA-PROTEIN COMPLEX 73 4X4N PROTEIN-RNA COMPLEX, TRNA, NON-CODING RNA 85 4X4T PROTEIN-RNA COMPLEX, TRNA, NON-CODING RNA 83 4X4V PROTEIN-RNA COMPLEX, TRNA, NON-CODING RNA 64 4XWF RNA, RIBOSWITCH, ZMP, AICAR 64 4YCP TRNA MODIFICATION, OXIDOREDUCTASE-RNA COMPLEX 60 4YVI TRNA, TRANSFERASE-RNA COMPLEX 73 4Z31 ROQUIN2, RNA, STRUCTURAL GENOMICS 58 5AXM TRANSFERASE-RNA COMPLEX 73 5CCB TRNA A58 MODIFICATION 78 5CNR SENECA VALLEY VIRUS 54 5DEA RNA STRUCTURE, RGG BOX, FMRP, G-QUADRUPLEX, RNA 70 5ED2 DEAMINASE, HUMAN, HYDROLASE-RNA COMPLEX 92 5F5F ROQ DOMAIN, WINGED-HELIX DOMAIN, RNA BINDING PROTEIN 80 5FJ4 TRANSCRIPTION, KINK TURN 70 4TZX RIBOSWITCH, ADENINE, RNA, GENE REGULATION 72 4QVI RIBOSOMAL PROTEIN, RRNA, RIBOSOME 80 4RDX TRNA, LIGASE-RNA COMPLEX 78 4QI2 TNF CDE RNA, RNA BINDING PROTEIN-RNA COMPLEX 74 4PQV EXONUCLEASE XRN1, SMALL FLAVIVIRAL RNA 68 4P97 VIRAL GENOME, INTERNAL RIBOSOME, TRANSLATION 54 4O41 VIRAL GENOME, INTERNAL RIBOSOME, TRANSLATION 45

4MSR 2'-5'-LINKAGE, RNA 20 4MCF RNA DOUBLE HELIX, RNA 78 4M4O STRUCTURAL GENOMICS, PROTEIN STRUCTURE INITIATIVE 59 4LX6 RIBOSWITCH GENE EXPRESSION PLATFORM, RNA 72 4LGT E. COLI RIBOSOMAL RNA 41 4KZD G-QUADRUPLEX, FLUORESCENCE RNA 84 4JXZ ROSSMANN FOLD, PROTEIN-RNA COMPLEX 72 4JYZ ROSSMANN FOLD, PROTEIN-RNA COMPLEX 72 4K4S RNA-DEPENDENT RNA POLYMERASE 67 4K4T RNA-DEPENDENT RNA POLYMERASE 66 3SYW CUG REPEAT RNA 38 3SIU RNA-BINDING PROTEIN 56 3SNP LYASE-RNA 58 3E5C TRANSLATION REGULATION SD, RNA 54 3DH3 PROTEIN-RNA COMPLEX 88 3CQS RIBONUCLEASE; 61 2IZ9 VIRUS/RNA 30 1KXK DOUBLE HELIX RNA 70 4KYY RNA DUPLEX 34 2A04 RIBOSOME, RNA, A-SITE. DOUBLE HELIX 58 2DU3 ALPHA4 TETRAMER, LIGASE/RNA COMPLEX 71 2I82 PSEUDOURIDINE SYNTHASE, LYASE/RNA COMPLEX 79 2ZUE LIGASE/RNA COMPLEX 76 4QEI LIGASE/RNA COMPLEX TRNA 70 3AMT TRNA(ILE2), MODIFICATION 79 3B5S HAIRPIN RIBOZYME; RNA 61 3GM7 STRETCHED U-U WOBBLE, RNA, CUG REPEATS 36 3WBM PROTEIN-RNA COMPLEX 50 3SUX PSEUDOKNOT, GENE REGULATOR, THF, RNA 101 2ZZM PROTEIN-RNA COMPLEX, TRANSFERASE/RNA COMPLEX 85 2RFK ARCHAEAL H/ACA RIBONUCLEOPROTEIN 61 1H3E LIGASE TRNA 82 1YZ9 RIBONUCLEASE III, DOUBLE-STRANDED RNA 44 4N0T RNA BINDING PROTEIN-RNA COMPLEX 65 3AM1 KINASE, TRANSFERASE-RNA COMPLEX 82 5D8H KINASE, STE20, HYPERTENSION, STK39, TRANSFERASE 74 4RUM RNA HELIX, LIGAND SENSOR, RNA, RIBOSWITCH 92 4TS0 G-QUADRUPLEX, RNA 88 4PR6 ESCHERICHIA COLI RNA-BINDING PROTEIN 72 4PRF TRANSLATION-RNA COMPLEX 74 4K27 A-FORM RNA, MYOTONIC DYSTROPHY 55 4RZD HL(OUT)-TYPE PSEUDOKNOT, TRANSLATIONAL 100 3MOJ RNA RECOGNITION MOTIF, RNA BINDING PROTEIN, RIBOSOMA 69

2G3S TANDEM GU BASE PAIRS 80 4OJI PSEUDOKNOT, SELF-CLEAVAGE, RNA 52 4P5J TRNA-MIMIC VIRAL RNA PSEUDOKNOT MULTIFUNCTIONAL 84 4ZDO TRNA, MUTATION 78 1QBP MISMATCHED BASE PAIRS, RNA 84 5BTM GENETIC DISEASE, RNA 86 4JRC REGULATORY RNA LEADER SEQUENCE, TRNA BINDING 114 4KQ0 TRINUCLEOTIDE REPEATS, DIMER, RNA BINDING 38 4OQ9 DOUBLE-HELIX RNA, PROTEIN-RNA COMPLEX 159 4QLM SECOND MESSAGE MOLECULE, C-DI-AMP BINDING, RNA 110 4P3U RIBOSOME, ANTIBIOTIC-RESISTANCE, DECODING, RNA 86 3NMU RNA ASSEMBLY MOTIF, TRANSFERASE-RNA COMPLEX 95 3NKB CATALYTIC RNA 72 5DDP RIBOSWITCH, L-GLUTAMINE, RNA BINDING PROTEIN-RNA 122 3FU2 RNA; APTAMER; RIBOSWITCH 96 3GLP STRETCHED U-U WOBBLE, RNA, CUG REPEATS 40 3A6P PROTEIN TRANSPORT-NUCLEAR PROTEIN-RNA COMPLEX 94 2Q1O CHEMICAL MODIFICATION, RNA 48 2PN4 STRONTIUM, HEPATITIS RNA 88 2QUS CATALYTIC RNA, SATELLITE VIRUS 138 2QUW CATALYTIC RNA, RIBOZYME-PRODUCT 138 2OZB RIBONUCLEOPROTEIN PARTICLE (RNP) 66 3BNN RIBOSOME, DECODING SITE, RNA 84 2GJW BULGE-HELIX-BULGE RNA-PROTEIN COMPLEX 75 5F9F COMPLEX, RIG-I, CAPPED RNA, SELF VERSUS NON-SELF 144 5G4V DNA BINDING, KINK TURN 76 1I6U PROTEIN-RNA INTERACTIONS, RIBOSOME 74 4AOB TRANSLATION, K-TURN, RNA 95 3GX5 KINK-TURN, PSEUDOKNOT RIBOSWITCH, RNA 95 5B2Q GENOME ENGINEERING, HYDROLASE-RNA-DNA COMPLEX 132 4WFL NON-CODING, RNA 107 3GX5 KINK-TURN, PSEUDOKNOT, RIBOSWITCH, RNA 95 3UCZ RIBOSWITCH, SIGNALING PROTEIN-RNA COMPLEX 94 5BTP RNA 124 5HR7 PROTEIN-RNA COMPLEX, TRANSFER RNA 142 4ZT0 GENOME EDITING AND REGULATION 144 4YYE LIGASE-RNA COMPLEX 146 5HR6 TRANSFERASE-RNA COMPLEX 136 4L81 RIBOSWITCH, GENE REGULATION 97 4O26 TELOMERASE RNA, PROTEIN-RNA INTERACTION 94 4ILM NDORIBONUCLEASE, RNA, HYDROLASE-RNA COMPLEX 128 4K4Y RNA-DEPENDENT RNA POLYMERASE 142 4K4Z PROTEIN-RNA COMPLEX 134

3SKI RIBOSWITCH, DEOXYGUANOSINE, RNA 138 3SKL RIBOSWITCH, DEOXYGUANOSINE, RNA 134 3R1D CGG REPEATS- RNA 55 3IVN APTAMER, RNA, A-RIBOSWITCH 138 5HC9 TRNA, CCA-ADDING ENZYME, TRANSFERASE 152 2Z75 RIBOZYME, RIBOSWITCH 141 2ZZN PROTEIN-RNA COMPLEX, TRANSFERASE/RNA COMPLEX 144 2AZX LIGASE-RNA COMPLEX 144 1ZX7 RIBOSOME, RNA, A-SITE. DOUBLE HELIX 116 1ZHO RIBOSOMAL PROTEIN, MRNA-PROTEIN COMPLEX 152 2CT8 LIGASE/RNA COMPLEX 150 2CV1 LIGASE/RNA COMPLEX 152 1EFW ASPARTYL-TRNA SYNTHETASE 145 1MMS RNA, RIBOSOME, TRANSLOCATION 116 1IL2 LIGASE/RNA COMPLEX 147 1L9A RECOGNITION PARTICLE- SIGNALING PROTEIN/RNA 126 1H38 TRANSFERASE, RNA POLYMERASE, T7 RNA POLYMERASE 137 1NUJ RIBOZYME 96 5E6M TRNA, LIGASE-RNA 150 3D0U RNA-LIGAND COMPLEX, RIBOSWITCH 161 3DIL RIBOSWITCH, LYSINE, RNA 174 3EPK TRANSFERASE/RNA COMPLEX 138 3F2Q FMN RIBOSWITCH, TRANSCRIPTION, RNA 109 3F4H ROSEOFLAVIN, FMN, RIBOSWITCH, TRANSCRIPTION, RNA 109 4ZNP RIBOSWITCH, RNA, ONE CARBON MECHANISM 139 5C45 RNA, TRANSLATION, RNA-INHIBITOR COMPLEX 109 5G4U RNA-PROTEIN COMPLEX 114 5H9F CRISPR CASCADE, IMMUNE SYSTEM-RNA COMPLEX 139 5KX9 RNA, TRANSLATION, RNA-INHIBITOR COMPLEX 108 4X4P TRNA, NON-CODING RNA 121 2Y9H HYDROLASE-RNA COMPLEX 144 1HMH DNA-RNA HAMMERHEAD RIBOZYME, LOOP 141 1YLS CATALYTIC MECHANISM 98 2BTE LIGASE, CLASS I AMINOACYL-TRNA SYNTHETASE EDITING 158 1ET4 ANTI-SWEETENER FAB, ANTIGEN-ANTIBODY 175 2OIU LIGASE, RIBOZYME 142 4AQ7 LIGASE-RNA COMPLEX 156 5AH5 LIGASE-RNA COMPLEX 163 4K50 RNA-DEPENDENT RNA POLYMERASE 182 3RW6 RNA RECOGNITION 124 3RG5 RNA HYDRATION 172 3Q3Z RIBOSWITCH, C-DI-GMP, RNA 154 3D2V RNA, RIBOSWITCH, ANTIBIOTIC 156

3P59 RNA SQUARE, RNA 98 2XD0 TOXIN-RNA COMPLEX, ABORTIVE INFECTION, PHAGE 211 1M5K CATALYTIC RNA, U1A RNA BINDING PROTEIN DOCKED 226 1G1X RIBOSOMAL PROTEINS 169 3P22 VIRAL NON-CODING RNA 194 5AOX TRANSLATION, RETROTRANSPOSITION 170 4Y1J NUCLEASE, HYPERSTABLE 202 4Y1M RIBOSWITCH, MANGANESE RNA 185 4YCO TRNA MODIFICATION, OXIDOREDUCTASE 212 4OO8 HYDROLASE-DNA-RNA COMPLEX 236 4FRG COBALAMIN, RIBOSWITCH, B12, RNA 168 2QWY LIGAND COMPLEX, DOUBLE HELIX, PSEUDOKNOT 159 1U9S RNASE P, RIBONUCLEASE P RNA 155 2GDI RIBOSWITCH, THIAMINE PYROPHOSPHATE, RNA 160 4YAZ RIBOSWITCH 170 4P9R CATALYTIC RNA, LARIAT-CAPPING RIBOZYME 189 3V7E RNA-PROTEIN COMPLEX, RIBOSWITCH 251 3RKF RIBOSWITCH, M-RNA, THIOGUANINE, RNA 272 5D5L GU WOBBLE, PSEUDOKNOT, RNA 312 3KFU PROTEIN BIOSYNTHESIS, LIGASE-RNA COMPLEX 286 1KOG RNA DOUBLE HELIX, LIGASE/RNA COMPLEX 304 3HHN LIGASE RIBOZYME, RIBOZYME, CATALYTIC RNA 274 4RGE ZINC METALLOENZYME, W5H MUTATION, LYASE 167 3PDR MANGANESE-RNA COMPLEX, RNA 322 4FAU RIBOZYME, SELF-SPLICING, RETROTRANSPOSITION 392 2NZ4 STRUCTURAL PROTEIN/RNA 604 3R1C CGG REPEATS 288 2UXC 30S RIBOSOMAL SUBUNIT 1525 3T1Y RIBOSOME-ANTIBIOTIC COMPLEX 1526 4B3T RIBOSOME, AMINOGLYCOSIDE, ANTIBIOTIC 1531 1X8W CATALYTIC RNA, RIBOZYME 968

Table 3: PDB_ID of the RNA structures in structures in the non-redundant dataset of RNA structures with resolution 3Å or better

PDB_ID Description Reference 5JCF chicken MDA5 with 5'p 10-mer dsRNA and ADP-Mg2+ 1 1DFU Ribosomal protein L25 complex with a 5S rRNA fragment 2 1DQF Xenopus laevis 5S rRNA with a cytosine bulge 3 1DQH Xenopus laevis 5S rRNA with a cytosine bulge 3 1E7K Spliceosomal 15.5Kd Protein Bound to a U4 Snrna Fragment 4 1EFO Adenine bulge in the RNA chain of a DNA.RNA hybrid 5 1EFW Recognition of tRNA(Asp) by aspartyl-tRNA synthetase 6 1F1T Malachite green aptamer 7 1ET4 Vitamin B(12) RNA aptamer 8 1F7V tRNA aminoacylation by arginyl-tRNA synthetase 9 1F27 BIOTIN-BINDING RNA PSEUDOKNOT 10 1FEU Ribosomal protein TL5 complexed with RNA 11 1FUF 14-mer RNA/DNA chimer 12 1H3E Class I Tyrosyl-tRNA Synthetase 13 1H4S Thermus Thermophilus Prolyl-tRNA Synthetase 14 1H38 T7 RNA Polymerase Elongation Complex 15 1HMH Hammerhead ribozyme 16 1HYS HIV-1 reverse transcriptase 17 1I6U Ribosomal protein S8-rRNA complex 18 1I9X Branchpoint-U2 snRNA duplex 19 1IL2 AspRS-tRNA(Asp) complex 20 1J1U Archaeal tyrosyl-tRNA synthetase complexed with tRNA(Tyr) 21 1J9H RNA duplex r(gugucgcac)(2) with uridine bulges 22 1JBR Ribotoxin Restrictocin and a 31-mer SRD RNA Inhibitor 23 1JBT Restrictocin-inhibitor complexes with implications for RNA 24 1JZV SL2 Stem-loop of the HIV-1 psi-RNA 25 1KD4 r(GGUCACAGCCC)2, Barium form 26 1KD5 r(GGUCACAGCCC)2 metal free form 26 1KH6 RNA tertiary domain essential to HCV IRES-mediated 27 1KXK Structural insights into group II intron catalysis 28 1L9A SRP19 in complex with the S domain 29 1LNT SRP domain IV of Escherichia coli 30 1MJI ABT-378 (Lopinavir) Bound to HIV-1 Protease 31 1MMS L11-RNA complex. 32 1MSW T7 RNA Polymerase 33 1MZP L1 protuberance in the ribosome 34 1NTB Encapsulating Streptomycin within a small 40-mer RNA 35

1NUJ Crystal structure of the leadzyme 36 1NYI Hammerhead ribozyme. 37 1O9M 30S Ribosomal Subunit 38 1OOA Crystal structure of NF-kappaB (p50)2 39 1Q2R Elaborate manifold of short hydrogen bond 40 1QBP Brominated RNA helix with four mismatched base pairs 41 1QC0 Plasmid copy control related RNA duplexes 42 1QF6 Threonyl-tRNA synthetase-tRNA(Thr) complex 43 1QLN Transcribing T7 RNA Polymerase Initiation Complex 44 1QRS Misacylating mutants of Escherichia coli glutaminyl-tRNA 45 1RLG Cocrystal Structure of Archaeal L7Ae and a Box C/D RNA. 46 1RPU RNA silencing suppressor 47 1S76 Translocation and helicase activity in T7 RNA polymerase 48 1S77 Translocation and helicase activity in T7 RNA polymerase. 48 1SA9 RNA octamers containing tandem G.A base pairs 49 1SAQ RNA octamers containing tandem G.A base pairs 49 1SDR Escherichia coli Shine-Dalgarno sequence. 50 1T0D Monitoring molecular recognition of the ribosomal decoding 51 1T0E Monitoring molecular recognition of the ribosomal decoding site 51 1TFW Mechanism of transfer RNA maturation 52 1TFY Mechanism of transfer RNA maturation 52 1U1Y RNA stem-loop complexed with the bacteriophage MS2 capsid 53 1U9S Homologous RNAs 54 1URN U1A spliceosomal protein complexed with an RNA hairpin. 55 1WNE Foot-and-Mouth Disease Virus RNA-dependent 56 1XJR RNA element within the SARS virus genome 57 1XOK crystal structure of alfalfa mosaic virus RNA 3'UTR 58 1Y26 A-riboswitch-adenine complex 59 1Y27 G-riboswitch-guanine complex 60 1YFG Yeast initiatortRNA 61 1YLS Structure of selenium-modified Diels-Alder ribozyme 62 1YVP Ro autoantigen complexed with RNAs 63 1YYK Crystal structure of RNase III 64 1YZ9 Intermediate states of ribonuclease III 65 1Z7F Acylation transition States for 2'-amine substituted RNA 66 1ZBH Histone mRNA stem-loop 67 1ZDJ RNA hairpins in complexes with recombinant MS2 capsids 68 1ZH5 Nascent RNA Polymerase III 69 1ZHO Ribosomal protein L1 in complex with mRNA 70 1ZX7 Neomycin and a Restricted Neomycin Derivative 71 165D Structure of a mispaired RNA double helix 72 1D4R 29-mer fragment of human srprna helix 6 73 1M5K Transition state stabilization by a catalytic RNA 74

1G1X Structure of the S15,S6,S18-rRNA complex 76 1KOG Escherichia coli threonyl tRNA synthetase 77 1L2X Metal ions and flexibility in a viral RNA pseudoknot 78 1N32 Selection of tRNA by the Ribosome 79 1QCU Structures of two plasmid copy control related RNA duplexes 80 1S72 Assembly and Evolution of the Large Ribosomal Subunit 81 1VQ6 An induced-fit mechanism to promote peptide bond 82 1VQM The 2' Hydroxyl of the P Site tRNA 83 1VQN An induced-fit mechanism to promote peptide bond 82 1X8W Structure of the Tetrahymena Ribozyme 84 205D RNA double helix including uracil-uracil base pairs 85 280D The structure of an RNA dodecamer 86 2BU1 MS2-RNA hairpin (5BRU -5) complex 87 2UUA Transfer Rnas by Modification of Uridines 88 2VQE Modified Uridines with C5-Methylene Substituents 89 2UXC Structures of Trnas with an Expanded Anticodon Loop 90 2NUG A stepwise model for double-stranded RNA 91 2A04 Molecular recognition of RNA by neomycin 92 2A43 Luteoviral RNA Pseudoknot 93 2AO5 Structure of an RNA duplex r(GGCGBrUGCGCU)2 94 2AZX Human tRNA synthetase-tRNA complex 95 2B3J Staphylococcus aureus tRNA adenosine deaminase TadA 96 2BGG The structure of a piwi protein 97 2BH2 A Unique RNA Fold in the Ruma-RNA-Cofactor Ternary 98 2BTE The Crystal Structure of Leucyl-tRNA Synthetase Complexed 99 2CT8 Methionyl-tRNA synthetase 100 2CV1 Glutamyl-tRNAsynthetas 101 2DLC Yeast tyrosyl-tRNA synthetase 102 2DR5 Analysis of the dynamics of CCA sequence addition 103 2DU3 Crystal structure of VIP36 exoplasmic/lumenal domain 104 2E9T Fidelity of RNA replication 105 2EC0 RNA polymerase of foot-and-mouth disease virus 106 2EZ6 Aquifexaeolicus RNase III (D44N) complex 107 2F4S A-site RNA in complex with neamine 108 2F8S Crystal structure of Aa-Ago with externally-bound siRNA 109 2FQN Homo sapiens cytoplasmic ribosomal decoding A site 110 2G3S RNA structure containing GU base pairs 111 2G92 siRNAs with a ribo-difluorotoluyl nucleotide 112 2GDI Thiamine pyrophosphate-specific riboswitch 113 2GJW RNA Splicing Endonuclease 114 2GUN Crystal Structure of Oligonucleotides 115 2I82 Pseudouridine synthase RluA 116 2IZ9 MS2-RNA hairpin (2ONE-5) complex 118

2IZN MS2-RNA hairpin (G-10) complex 119 2JLT CrystalL structure of an RNA kissing copmlex 120 3BNN Homo sapiens Mitochondrial Ribosomal Decoding Site 121 2NVQ RNA Polymerase II Elongation Complex 122 2NZ4 GlmS ribozyme bound to its catalytic cofactor 123 2OE5 Apramycin recognition by the human ribosomal decoding site 124 2OE8 Apramycin recognition by the human ribosomal decoding site 124 2OIU L1 Ribozyme Ligase circular adduct 125 2OZB Structure of a human Prp31-15.5K-U4 snRNA complex 126 2P7D A Minimal, 'Hinged' Hairpin Ribozyme 127 2P7E Vanadate at the Active Site of a Small Ribozyme 127 2PN4 Hepatitis C Virus IRES Subdomain Iia 128 2PWT bacterial ribosomal complexed with aminoglycoside 129 2PXV Variant 6 of Ribonucleoprotein Core of the E. Coli 130 2Q1O Analysis of the RNA Dodecamer CGC-NF2-AAUUGGCG 131 2QUS Hammerhead Ribozyme G12A mutant pre-cleavage 132 2QUW Hammerhead Ribozyme G12A mutant after cleavage 132 2QWY SAM-II riboswitch bound to S-adenosylmethionine 133 2R20 RNA brominated tridecamer r(GCGUU-5BUGAAACGC) 134 2RFK RNA Positioning in the Archaeal H/ACA Ribonucleoprotei 135 2VAL Structure of an Escherichia Coli Trnagly Microhelix 136 2XD0 RNA Regulates an Altruistic Bacterial Antiviral System 137 2XNZ Purine Riboswitch Discovered by RNA-Ligand Docking 138 2Y9H RNA-Induced Conformational Change Required for Crispr RNA 139 2Z75 T. tengcongensisglmS ribozyme 140 2ZKO dsRNA recognition by NS1 protein of influenza A virus 141 2ZUE Modeling of tRNA-assisted mechanism of Arg activation 142 2ZZM The complex structure of aTrm5 and tRNALeu 143 2ZZN The complex structure of aTrm5 and tRNACys 143 3A6P Structure of Exportin-5:RanGTP:pre-miRNA complex 144 3AGV Structure of a human IgG-aptamer complex 145 3AM1 O-Phosphoseryl-tRNA kinase complexed with anticodon tRNA 146 3AMT Structure of the TiaS-tRNA(Ile2)-ATP complex 147 3B5S Active site residue Ade38 in the hairpin ribozyme. 148 3B31 Structure of domain III of the Cricket Paralysis Virus IRES RNA 149 3BNL Acterialribosomal in the presence of [Co(NH3)6]Cl3 150 3BSB Structure of Human Pumilio1 151 3BT7 Structure of E. coli 5-Methyluridine Methyltransferase TrmA 152 3CGP U2 snRNA-branchpoint containing conserved pseudouridines 153 3CGR U2 snRNA-branchpoint containing conserved pseudouridines 153 3CGS U2 snRNA-branchpoint containing conserved pseudouridines 153 3CJZ Effects of N2,N2-dimethylguanosine on RNA structure 154 3CQS the reaction coordinates of ribonuclease and an RNA enzyme 155

3D0U Crystal Structure of Lysine Riboswitch Bound to Lysine 156 3D2V Eukaryotic TPP-specific riboswitch 157 3DD2 RNA aptamer bound to human thrombin 158 3DH3 RluF in complex with a 22 nucleotide RNA substrate 159 3DIL Thermotogamaritima lysine riboswitch bound to lysine 160 3E2E Intermediate Complex of T7 RNAP and 7nt of RNA 161 3E5C SMK box (SAM-III) Riboswitch with SAM 162 3EGZ In vitro evolved tetracycline aptamer and artificial riboswitch 163 3EPH Eukaryotic dimethylallyltransferase acting on tRNA 164 3EPK eukaryotic dimethylallyltransferase acting on tRNA 164 3F2Q FMN riboswitch bound to FMN 165 3F4H FMN riboswitch bound to roseoflavin 166 3F73 Structure of an argonaute silencing 167 3FS0 Class II ligase ribozyme product-template duplex 168 3FTF A. aeolicusKsgA in complex with RNA and SAH 169 3FTM Class II ligase ribozyme product-template duplex 170 3FU2 Cocrystal structure of a class-I preQ1 riboswitch 171 3GLP 1.23 A resolution X-ray structure of (GCUGCUGC)2 172 3GM7 1.58 A resolution X-ray structure of (CUG)6 172 3GS5 RNA hairpin ribozyme A38N1dA 173 3GX5 T. tencongensis SAM-I riboswitch 174 3HHN Class I ligase ribozyme self-ligation product 175 3I2S Hairpin ribozyme with a 2'OMe substrate 176 3IAB RNase P /RNase MRP proteins Pop6, Pop7 177 3IVN U65C mutant A-riboswitch aptamer 178 3LA5 Mc6 RNA Riboswitch bound to azacytosine 179 3LOA ligand binding to the ribosomal RNA helix h44 180 3LRR human RIG-I CTD bound to a 12 bp AU rich 5' ppp dsRNA 181 3MEI Regulatory motif from the thymidylate synthase mRNA 182 3MOJ DEAD-box helicase bound to its ribosomal RNA 183 3NKB HDV ribozyme precleavage 184 3NMU Substrate-bound halfmer box C/D RNP 185 3NPN s-adenosylhomocysteine riboswitch 186 3NVI N-terminal truncated Nop56/58 185 3OK4 Crystal structure of the ANA:RNAdecamer 187 3SNP Iron regulatory protein 1 in complex with ferritin H IRE RNA 188 3P59 First Crystal Structure of a RNA Nanosquare 189 3Q3Z Structure of a c-di-GMP-II riboswitch 190 3R1C Crystal structure of GCGGCGGC duplex 191 3R1D Crystal structure of GCGGCGGC duplex 191 3R1E Crystal structure of GCGGCGGC duplex 191 3R2D Antitermination Factors NusB and NusE 192 3RG5 Crystal Structure of Mouse tRNA(Sec) 193

3RKF Guanine riboswitch C61U/G37A double mutant 194 3RW6 Nuclear RNA export factor TAP bound to CTE RNA 195 3SIU hPrp31-15.5K-U4atac 5' stem loop complex 196 3SKI Nucleoside selectivity in a 2'-deoxyguanosine riboswitch 197 3SKL Nucleoside selectivity in a 2'-deoxyguanosine riboswitch 197 3SN2 Ttransferrin receptor IRE B RNA 198 3SUX THF riboswitch, bound with THF 199 3SYW Triplet Repeat in Myotonic Dystrophy 200 4JAH 2-Selenouridine containing RNA 201 3TS0 Mouse Lin28A in complex with let-7f-1 202 3TS2 Mouse Lin28A in complex with let-7f-1 202 3TZR Riboswitch-like RNA-ligand complex 203 3UCZ The c-di-GMP-I riboswitch bound to GpG 204 3V7E YbxF bound to the SAM-I riboswitch aptamer 205 3VJR Peptidyl-tRNA hydrolase from Escherichia coli 206 3WBM Crystal Structure of protein-RNA complex 207 3X1L CRISPR-Cas RNA Silencing Cmr Complex 208 3ZP8 Hammerhead Ribozyme Structure 209 354D loop E FROM E. coli 5S RRNA 210 361D Domain E of Thermusflavus 5S rRNA 211 364D Structure of a 5S rRNA domain 212 377D Pyrimidine start alternating A-RNA hexamer r(CGUAC)dG 213 397D Structure of the HIV-1 trans-activation 214 398D Eight-base pair duplex containing the 3'-DNA-RNA-5' junction 215 3KFU Structure of the transamidosome 216 3PDR Structure of manganese bound M-box RNA 217 3P22 Poly(A) tail recognition by a viral RNA element 218 3JCS Cryo-EM Structure of the Large Ribosomal Subunit 219 3T1Y Human tRNA(Lys3)(UUU) 220 4JF2 Class II preQ1 riboswitch reveals ligand 221 4AOB SAM-I riboswitch 222 4AQ7 Ternary complex of E. coli leucyl-tRNA synthetase 223 4ATO Bacterial Type III toxin-antitoxin systems 224 2PJP mRNA-binding domain of elongation factor SelB 225 4C4W Non-standard sequence k-turn bound by L7Ae protein 226 4C7O FtsY recruitment and GTPase 227 4C9D Cas6 (TTHB231) product complex 228 4E5C 19mer double-helical RNA 229 4E6B statistically disordered 19mer duplex p(CGG)3C(CUG)3 230 4E 58 GCC(LCG)CCGC duplex containing LNA residue 231 4E 59 Crystal structure of GCCGCCGC duplex 232 4ERD C-terminal domain of Tetrahymena telomerase protein p65 233 4FAU Oceanobacillusiheyensis group II intron 234

4FNJ Utilizing the GAAA tetraloop/receptor 235 4FRG cobalamin riboswitch aptamer domain 236 4FXD Yeast DNA polymerase alpha bound to DNA/RNA 237 4G7O Thermus thermophilus transcription initiation complex 238 4GCW RNase Z in complex with precursor tRNA(Thr) 239 4ILL Recognition and Cleavage of a non-structured CRISPR RNA 240 4ILM CRISPR RNA Processing endoribonuclease 240 4IQS RNA 8mer duplex modified with 4-Se-Uridine 241 4JRC G. kaustophilusglyQS T box RNA 242 4JXZ E. coli glutaminyl-tRNA synthetase 243 4JYZ E. coli glutaminyl-tRNA synthetase 243 4K4S Poliovirus polymerase elongation complex (r3_form) 244 4K4T Poliovirus polymerase elongation complex (r4_form) 244 4K4Y Coxsackievirus B3 polymerase elongation complex (r2+1_form) 244 4K4Z Coxsackievirus B3 polymerase elongation complex (r2Mg_form) 244 4K27 Myotonic Dystrophy Type 2 RNA 245 4K50 Rhinovirus 16 polymerase elongation complex (r1_form) 246 4KQ0 Double-helical CGG-repetitive RNA 19mer complexed 247 4KYY RNA 17-mer UUCGGUUUUGAUCCGGA duplex 248 4KZD RNA aptamer in complex with fluorophore and Fab 249 4L81 SAM-I/IV riboswitch (env87(deltaU92, deltaG93)) 250 4LGT catalytic domain of RluB in complex with a 21-nucleotide RNA 251 4LX6 M6C" riboswitch aptamer 252 4M4O Aptamer minE-lysozyme complex 253 4MCF Crystal structure of the Gas5 GRE Mimic 254 4MSR RNA 10mer duplex with six 2'-5'-linkages 255 4N0T U6 small nuclear ribonucleoprotein 256 4O26 TRBD domain of TERT and the CR4/5 of TR 257 4O41 Amide linked RNA 258 4OJI Crystal Structure of Twister Ribozyme 259 4OO8 Streptococcus pyogenes Cas9 260 4OQ9 Satellite Tobacco Mosaic Virus 261 4P3S Bacterial A1408C-mutant ribosomal 262 4P3T Bacterial A1408C-mutant ribosomal 262 4P3U bacterial A1408C-mutant ribosomal 262 4P5J The structural basis of transfer RNA mimicry 263 4P9R lariat capping ribozyme 264 4P43 Bacterial A1408U-mutant ribosomal 265 4P97 An internal ribosome entry site (IRES) 266 4PCO RNA with four terminal GU wobble base pairs 267 4PDB RNA against ribosomal protein S8 from Bacillus anthracis 268 4PKD Crystal structure of human U1 snRNP 269 4PQU HIV-1 Reverse Transcriptase in complex with RNA/DNA 270

4PQV Murray Valley Encephalitis virus 271 4PR6 New tools provide a second look at HDV ribozyme structure 272 4PRF New tools provide a second look at HDV ribozyme structure 272 4Q5S Thermus thermophilus RNA polymerase 273 4Q5V RNA-primed DNA template and aphidicolin 274 4QEI GlyRS captured in crystal lattice 275 4QI2 ROQ domain from murine Roquin-1 276 4QIL ROQ domain of human Roquin 277 4QLM Ydao riboswitch binding to c-di-AMP 278 4QOZ Histone mRNA stem-loop, 279 4QVI Mutant ribosomal protein M218L TthL1 280 4RDX Histidinyl-tRNA synthetase 281 4RGE In-line aligned env22 twister ribozyme 282 4RMO CptIN Type III Toxin-Antitoxin System 283 4RUM NiCo transition-metal riboswitch bound to cobalt 284 4RZD Crystal Structure of a PreQ1 Riboswitch 285 4TS0 Spinach RNA aptamer 286 4TUW Histone mRNA stem-loop-binding protein by phosphorylation 287 4TUX Histone mRNA stem-loop-binding protein by phosphorylation. 287 4TZX Vibrio Vulnificus Adenine Riboswitch variant, grown in Mg2+ 288 4U6K DNA/RNA duplex containing 2'-4'-BNA-NC 289 4U35 RNA Duplexes Containing 2-thio-Uridine 290 4WFL Complete bacterial SRP Alu domain 291 4WRT Influenza B polymerase with bound vRNA promoter 292 4WSB Bat Influenza A polymerase with bound vRNA promoter 293 4WZM Mutant K18E of RNA 294 4X4N G70A arginyl-tRNA minihelix 295 4X4T G70A arginyl-tRNA minihelix ending in CCACCA 295 4X4V MenBeta minihelix ending in CCACC and AMPcPP 295 4XW0 GCCU(G-LNA)CCUGC)2 duplex 296 4XWF ZMP riboswitch at 1.80 angstrom 297 4Y1J AnLactococcuslactisyybP-ykoYMn riboswitch 298 4Y1M An Escherichia coli yybP-ykoYMn riboswitch 298 4YAZ 3',3'-cGAMP riboswitch bound with 3',3'-cGAMP 299 4YCO E. coli dihydrouridine synthas)in complex with tRNAPhe 300 4YCP E. coli dihydrouridine synthase in complex with tRNATrp 300 4YVI H. influenzae TrmD in complex with sinefungin and tRNA 301 4YYE yeast mitochondrial threonyl-tRNA synthetase (MST1) 302 4Z31 RC3H2 ROQ domain 303 4ZDO T325S mutant of human SepSecS 304 4ZNP The structure of A pfI Riboswitch Bound to ZMP 305 4ZT0 Catalytically-active Streptococcus pyogenes Cas9 306 402D RNA internal loop consisting of tandem C-A+ base pairs 307

406D Statically disordered 17 base-pair RNA duplex 308 409D RNA octamer duplex r(CCCIUGGG)2 309 422D Dodecamer r(GAUCACUUCGGU) with four 5'-overhang 310 435D Acceptor stem of tRNA(Ala) from Escherichia coli 311 437D Ribosomal frameshifting viral pseudoknot. 312 439D RNA duplex with an unusual G.C pair in wobble) conformation 313 466D Disorder and twin refinement of RNA heptamer double helices 314 420D RNA 16-mer duplex R(GCAGAGUUAAAUCUGC)2 315 4BW0 Recognition of Kink-Turn Structure by L7Ae Class of Proteins 316 4X4P A.fulgidus CCA-adding enzyme 317 4B3T 30S ribosome in complex with compound 39 318 4U4U Lycorine bound to the yeast 80S ribosome 319 4V8C Near-cognate tRNA-leu complex with paromomycin 320 4V8U 70S Ribosome with Both Cognate tRNAs 321 4V90 Thermus ribosome 322 4V8B analysis of decoding (near-cognate tRNA-leu complex) 323 4V9L 70S Ribosome translocation intermediate FA-3.6A 324 4V9R Antibiotic DITYROMYCIN bound to 70S ribosome 325 4V88 The structure of the eukaryotic ribosome at 3.0 A resolution 326 4V9F Haloarculamarismortui large ribosomal 327 4FAU Oceanobacillusiheyensis group II intron 328 5AH5 Agrobacterium radiobacter K84 agnB2 LeuRS-tRNA-LeuAMS 329 5AOX Human Alu RNA retrotransposition complex 330 5AWH RNA and target DNA heteroduplex 331 5AXM Thg1 like protein (TLP) with tRNA(Phe) 332 5AY3 RNA duplex containing C-C base pairs 333 5B2Q Francisellanovicida Cas9 RHA 334 5B43 Acidaminococcus. Cpf1 in complex with crRNA and target DNA 335 5BTM AUUCU repeating RNA that causes spinocerebellar ataxia 10 336 5BTP Fusobacterium ulcerans ZTP riboswitch bound to ZMP 337 5C9H Template Boundary Definition in Tetrahymena Telomerase 338 5C45 Selective Small Molecule Inhibition of the FMN Riboswitch 339 5CCB Human m1A58 methyltransferase 340 5CKK Crystal structure of 9DB1* deoxyribozyme 341 5CNR Guided design of self-assembling RNA nano triangles 342 5D0A Epoxyqueuosine reductase with cleaved RNA stem loop 343 5D5L PreQ1-II riboswitch with an engineered G-U wobble pair 344 5D8H Ribosomal P stalk from methanococcusjannaschii 345 5DDP L-glutamine riboswitch bound with L-glutamine 346 5DEA FMRP RGG motif and G-quadruplex RNA 347 5DQK Hammerhead Ribozyme Cleavage Reaction. 348 5E6M Human wild type GlyRS bound with tRNAGly 349 5ED1 Human ADAR2 bound to dsRNA reveal base-flipping 350

5ED2 Adenosine Deaminase Acting on dsRNA (ADAR2) mutant 351 5EW4 C9ORF72 Antisense CCCCGG repeat RNA 352 5F0Q C-terminal domain of the human DNA primase large subunit 353 5F5F Roquin ROQ domain 354 5F9F RIG-I helicase-RD in complex with 24-mer blunt- hairpin RNA 355 5FJ4 Standard kink turn HmKt-7 as stem loop 356 3S49 RNA crystal structure with 2-Se-uridine modification 357 5G4U Association of three two-k-turn units based on Kt-7 3bU,3nU 358 5G4V Association of four two-k-turn units based on Kt-7 3bG,3nC 358 5H9F E. coli Cascade bound to a PAM-containing dsDNA target 359 5HC9 Thermotogamaritima CCA-adding enzyme 360 5HN2 5-Formylcytosine in RNA Duplex 361 5HR6 C118A RlmN with cross-linked tRNA purified 362 5HR7 C118A RlmN with cross-linked in vitro transcribed tRNA 362 4V5S Gentamicin and ribosome recycling factor (RRF). 363 5KX9 Selective Small Molecule Inhibition of the FMN Riboswitch 364 5J8B Elongation Factor 4 (EF-4/LepA) in complex with GDPCP 365 5J7L 70S E coli ribosome with the U1052G 366 5J5B Structure of the WT E coli ribosome bound to tetracycline 366 5IBB 70S ribosome complex with mRNA, and cognate tRNAVal 367 5IB7 70S with mRNA, tRNAfMet, near-cognate with U-G mismatch 367 5FDU Metalnikowin I antimicrobial peptide 368 5DM6 50S ribosomal subunit from Deinococcusradiodurans 369 1CSL The structure of the HIV-1 RRE 370 6MSF F6 APTAMER MS2 COAT PROTEIN COMPLEX 371 7MSF MS2 PROTEIN CAPSID/RNA COMPLEX 372

4B3T Crystal structure of the 30S ribose 373

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