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This Thesis Has Been Submitted in Fulfilment of the Requirements for a Postgraduate Degree (E.G This thesis has been submitted in fulfilment of the requirements for a postgraduate degree (e.g. PhD, MPhil, DClinPsychol) at the University of Edinburgh. Please note the following terms and conditions of use: This work is protected by copyright and other intellectual property rights, which are retained by the thesis author, unless otherwise stated. A copy can be downloaded for personal non-commercial research or study, without prior permission or charge. This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the author. The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the author. When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given. Identifying novel targets for the snoRNA class of stable non-coding RNAs Rosie Peters Thesis presented for the degree of Doctor of Philosophy University of Edinburgh 2018 1 DECLARATION I declare that this thesis was composed by myself. The research in this thesis is my own, unless otherwise stated, and has not been submitted for any other degree or professional qualification. Rosie Peters 2 ACKNOWLEDGEMENTS I would first like to thank my supervisor, David, for his help and guidance throughout the PhD project. Many thanks to Tanya, for her supervision in the lab and her advice throughout, and also to Hywel, for all of his work and assistance in bioinformatics. I’d like to thank everyone in the Tollervey lab - past and present - for their advice, and whose work provided the foundation on which to develop my research. I would also like to thank my thesis committee - Jean Beggs, Sander Granneman and Bill Earnshaw - for their support and guidance over the years. In addition, I thank David Barrass, for his invaluable help and instruction during certain experiments, and Alastair Kerr for his statistical expertise. I am very grateful to the Wellcome Trust for funding this four year PhD Programme in Cell Biology, and to Karen Traill for the excellent work she does. Furthermore, I’d like to thank members of the Wellcome Centre for Cell Biology, for their encouragement and know-how. I would like to thank my close friends for their unwavering support and humour, throughout times which were not stress-free. Their friendship facilitated my work on this project. Finally, I’d like to thank my parents and my brother, Dan. Without their constant support and encouragement, I could not have completed this PhD, and I am incredibly grateful to them. 3 ABSTRACT Non-coding RNAs (ncRNAs) are a subset of RNAs that do not code for protein. They are divided into a number of different groups based on their function and targets. Small nucleolar RNAs (snoRNAs) are ncRNAs that have long been known to function as guides for ribosomal RNA (rRNA) modifying enzymes. They are classified into two major groups: box C/D snoRNAs and box H/ACA snoRNAs. Most box C/D snoRNAs direct the 2’-O-methylation of rRNA substrates, but some lack known targets and are therefore termed ‘orphan snoRNAs’. Studies have implicated orphan snoRNAs in pre-mRNA processing and stability, but the functional consequence of snoRNA binding to mRNAs has not been fully determined. Saccharomyces cerevisiae had two orphan snoRNAs, snR4 and snR45, with no known function in ribosome synthesis. This project aimed to determine the targets of these snoRNAs, and investigate the effects of snoRNA binding to non-canonical target RNAs, as well as the underlying mechanism. Synthetic gene array screens with deletions of the SNR4 and SNR45 genes identified multiple positive and negative genetic interactions. In particular, deletion of either snoRNA gene was synthetic-lethal with mutation of the snoRNA-associated methyltransferase, Nop1 (Fibrillarin in humans), demonstrating that both have important functions. CLASH analyses of RNA-RNA interactions showed that these snoRNAs bind multiple mRNAs, while RNA sequencing and RT-qPCR revealed that snoRNA deletion altered mRNA abundance. Both orphan snoRNAs were well conserved between fungi, with a region of high conservation indicating a potential binding site. Associations were identified between snR4 and snR45 and multiple sequences within rRNA, including two recently identified sites of 18S rRNA acetylation. Work elsewhere showed that snR4 and snR45 function as guides for the acetyltransferase Kre33 using the region of high conservation, removing their ‘orphan’ status. Orphan snoRNAs have been implicated in human diseases, such as Prader Willi Syndrome and cancers. The work discussed in this thesis helps to elucidate the RNA interactions of yeast orphan snoRNAs. It has provided a greater understanding of the mechanisms involved, and may inform future work in combatting human disease. 4 LAY SUMMARY Genetic information is encoded in the sequences of long regions of DNA. RNA is similar to DNA and carries a copy of a region of the genetic information. The best known class of RNA is messenger RNA (mRNA), which carries the information used to programme protein synthesis. However, there are numerous other classes of RNA, which do not encode protein, named ‘non-coding RNA’ (ncRNA). Every cell needs to make a vast number of proteins, and these are made by cellular machines called ‘ribosomes’. The main component of this machine is a large ncRNA called ‘ribosomal RNA’ (rRNA). To make the ribosome, the rRNA first needs to be synthesised, processed and modified. Small ncRNAs called ‘snoRNAs’ have long been known to direct these modifications, but it has more recently been discovered that snoRNAs can also bind to mRNA. The effect of snoRNA binding to mRNAs is currently unknown, though evidence suggests that snoRNAs may affect the quantity or processing of target mRNAs. Recent studies have revealed links between abnormal amounts of individual snoRNAs in the cell and cancer, indicating the importance of researching these interactions. Furthermore, the lack of one type of snoRNA in humans is directly linked to the genetic disease Prader Willi Syndrome, due to the loss of interactions with mRNA. In this study, individual snoRNAs that lacked a known function in ribosome synthesis were deleted from the DNA in baker’s yeast (a model organism for human cells). The project aimed to investigate how well or poorly the yeast grew without the snoRNAs, whether the quantity of mRNA changed, and whether other functional interactions could be discovered. Lack of these snoRNAs did not clearly affect how well the yeast grew, but did result in sickness or cell death when combined with other particular mutations. The snoRNAs were shown to bind to specific mRNAs, and deletion of the snoRNAs affected the amount of mRNAs present in the cell. Furthermore, these snoRNAs were found to guide a type of modification on rRNA that was different from that directed by other snoRNAs. This research has provided a better understanding of the role snoRNAs play in yeast, which can potentially help understand the mechanistic basis of human diseases. 5 CONTENTS DECLARATION ........................................................................................................... 2 ACKNOWLEDGEMENTS ............................................................................................... 3 ABSTRACT ................................................................................................................ 4 LAY SUMMARY .......................................................................................................... 5 CONTENTS ................................................................................................................ 6 TABLE OF FIGURES .................................................................................................... 8 1 INTRODUCTION ..................................................................................................... 11 1.1: Ribosome biogenesis .................................................................................. 11 1.2: The different classes of snoRNA ................................................................. 16 1.3: Potential targets of orphan snoRNAs ........................................................... 22 1.4: Orphan snoRNAs are implicated in human disease ..................................... 23 1.5: Methods of identifying the RNA targets of orphan snoRNAs ........................ 25 1.6: Aims ............................................................................................................ 30 2 MATERIALS AND METHODS .................................................................................... 32 2.1: Materials...................................................................................................... 32 2.2: Strain generation ......................................................................................... 36 2.3: Cell growth and harvesting .......................................................................... 39 2.4: DNA isolation .............................................................................................. 41 2.5: RNA isolation .............................................................................................. 42 2.6: RNA sequencing library preparation ............................................................ 43 2.7: Quantitative PCR ......................................................................................... 46 2.8: Northern blotting .........................................................................................
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