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Reverse Watson-Crick Base-Pairs in Theá D(GCGCGCG)/D(TCGCGCG)Á and D(GCGCGCG)/ D(CCGCGCG) Heteroduplexes, Respectively

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Reverse Watson-Crick Base-Pairs in Theá D(GCGCGCG)/D(TCGCGCG)Á and D(GCGCGCG)/ D(CCGCGCG) Heteroduplexes, Respectively J. Mol. Biol. (1997) 269, 796±810 The Structures and Relative Stabilities of d(G G) Reverse Hoogsteen, d(G T) Reverse Wobble,Á and d(G C) Reverse Watson-CrickÁ Base-pairs in DNAÁ Crystals BlaineH.M.Mooers,BrandtF.EichmanandP.ShingHo* 5 Department of Biochemistry We have solved the structures of the homoduplex d(Gm CGCGCG)2, and and Biophysics, ALS 2011 the heteroduplexes d(GCGCGCG)/d(TCGCGCG) and d(GCGCGCG)/ Oregon State University d(CCGCGCG). The structures form six base-pairs of identical Z-DNA Corvallis, OR 97331, USA duplexes with single nucleotides overhanging at the 50-ends. The over- hanging nucleotide from one strand remains stacked and sandwiched between the blunt-ends of two adjacent Z-DNA duplexes, while the over- hanging base of the opposing strand is extra-helical. The stacked and the extra-helical bases from adjacent duplexes pair to form a distorted 5 d(G G) reverse Hoogsteen base-pair in the d(Gm CGCGCG)2 homo- duplex,Á and d(G T) reverse wobble and d(G C) reverse Watson-Crick base-pairs in theÁ d(GCGCGCG)/d(TCGCGCG)Á and d(GCGCGCG)/ d(CCGCGCG) heteroduplexes, respectively. Interestingly, only the d(G,T) and d(G C) base-pairs were observed in the heteroduplexes, suggesting that bothÁ the d(G T) reverse wobble and d(G C) reverse Watson-Crick base-pairs are moreÁ stable in this crystal environmentÁ than the d(G G) reverse Hoogsteen base-pair. To estimate the relative stability of the threeÁ types of reverse base-pairs, crystals were grown using various mixtures of sequences and their strand compositions analyzed by mass spec- trometry. The d(G C) reverse Watson-Crick base-pair was estimated to be more stable by Á 1.5 kcal/mol and the d(G T) reverse wobble base- pair more stable by 0.5 kcal/mol than the d(GÁ G) reverse Hoogsteen base-pair. The step during crystallization responsibleÁ for discriminating between the strands in the crystal is highly cooperative, suggesting that it occurs during the initial nucleating event of crystal growth. # 1997 Academic Press Limited Keywords: reverse base-pairs; DNA structure; crystallography; nucleic *Corresponding author acid stability Introduction d(GCGCGCG)/d(TCGCGCG) and d(GCGCGCG)/ d(CCGCGCG) heteroduplexes. A distorted d(G G) Á The proper pairing of nucleotide bases ensures reverse Hoogsteen base-pair is formed in the ®delity in replication and transcription of the gen- homoduplex, while d(G T) reverse wobble and etic information in a cell. The pairing of guanine d(G C) reverse Watson-CrickÁ base-pairs of the with cytosine and adenine with thymine in what is typeÁ observed in RNA structures form in the re- now known as standard Watson-Crick base-pair- spective heteroduplexes. ing forms the basis for the structure of antiparallel The two strands of most DNA and RNA struc- DNA and RNA duplexes. Unusual base-pairs, tures are oriented antiparallel to each other. In however, also play important roles in the trans- DNA duplexes, Watson-Crick-type base-pairs are mission of genetic information. Here, we study the the predominant interactions that hold the two structures of reversed base-pairs formed by strands together. When bases are mismatched in nucleotides that overhang at the 50-end of the 5 DNA, unusual base-pairing can occur, including homoduplex d(Gm CGCGCG)2, and of the wobble base-pairs between G and T and Hoogsteen-type base-pairs between two purine Abbreviations used: RRE, Rev responsive element. nucleotides(Figure1).Thesearelessstablethan 0022±2836/97/250796±15 $25.00/0/mb971100 # 1997 Academic Press Limited Structure and Stability of Reverse Base-pairs 797 Figure 1. Comparison of the normal and reverse Watson-Crick d(G C) base-pairs, wobble d(G T) base-pairs, and Hoogsteen-like d(G G) base-pairs. The nitrogen atoms in the bases of theÁ normal Watson-Crick d(GÁ C) base-pair are numbered to orientÁ the reader to the standard numbering of the purine and pyrimidine bases. TheÁ glycosidic bond that links the bases to the deoxyribose (R) in the reverse base-pairs are oriented antiparallel to each other so that there is no distinction in terms of major and minor grooves, as there are in the normal base-pairs. There is, however, a common guanine in the three structures studied here, and the major and minor grooves of this base are used as the reference in discussing the surfaces in the text. The Watson-Crick face of the bases includes the N1 base nitrogen atom, N2 amino nitrogen atom and O6 keto oxygen atom of the guanine residue and the O2 keto oxygen atom, N3 base nitrogen atom and N4 amino nitrogen atom of the pyrimidine bases of thymine and cytosine. The Hoogsteen face of guanine is de®ned by the O6 keto oxygen atom and the N7 base nitrogen atom of the purine base. standard Watson-Crick-type base-pairs. In RNA mers(Rippeetal.,1992;Robinsonetal.,1994). structures, unusual base-pairing is more prevalent, These are interesting structures, although their bio- and has been observed to stabilize the complex ter- logical relevance has yet to be determined. tiary structures of large polynucleotides such as In large RNA structures, however, loops that tRNA(Quigley&Rich,1976),hammerheadribo- fold into local secondary and tertiary structures zymes(Pleyetal.,1994),andtheself-splicing often require the formation of unusual base-pairs, groupIintronfromTetrahymenathermophila(Cate including reverse base-pairs even if the strands are etal.,1996). in antiparallel orientations. For example, in the Watson-Crick, wobble, and Hoogsteen-type crystal structure of yeast tRNAPhe, a reverse base-pairs all have reverse analogues in which one Watson-Crick base-pair at (G15 C48) links the a base is completely inverted. Here, we refer to ``re- region of the D arm to the variableÁ V loop, and a verse'' base-pairs as the pairing of the nucleotide reverseHoogsteenbase-pairat(G22 m7G46)links bases in which the glycosidic bonds are oriented theDarmtothevariableVloop(KimÁ ,1978).Ina essentiallyantiparalleltoeachother(Figure1).The second example, a reverse Hoogsteen-type base- three base-pairs that we study here are asymmetric pair forms between G7 and G11 at the base of a in the same manner that the normal pairings are GNRA structural motif in an RNA aptamer de- asymmetric. The Hoogsteen and reverse Hoogsteen signedtorecognizeandbindATP(Jiangetal., d(G G) pairs match the Watson-Crick face of one 1996).Finally,intheNMRsolutionstructureof purineÁ with the Hoogsteen face of the second. The the hairpin formed by r(GGAC(UUCG)GUCC), a reverse analogues of the d(G T) wobble and r(G U)reversewobblebase-pairstabilizesthebase d(G C) Watson-Crick base-pairs matchÁ the two re- ofaÁ twonucleotideloop(Varanietal.,1991).This spectiveÁ Watson-Crick faces of the bases. In con- hairpin structure is thought to occur frequently trast, truly symmetric reverse base-pairs, with two in ribosomal and messenger RNAs. Thus, non- identical bases related by a dyad axis perpendicu- Watson-Crick base-pairs are important for the lar to the base-pair plane, have been used in the proper folding of RNA molecules into the compact design of synthetic parallel-stranded DNA oligo- tertiary structure of their functional forms. 798 Structure and Stability of Reverse Base-pairs Non-Watson-Crick base-pairs are also important with overhangs from adjacent duplexes in the crys- for RNA-protein recognition. Genetic and bio- tal lattice to form three different reverse base-pairs. chemical studies have shown that protein binding The overhanging dG nucleotides of the homodu- 5 sites in RNA are often associated with important plexes d(GCGCGCG)2 and d(Gm CGCGCG)2 form non-Watson-Crickbase-pairs(Allmangetal.,1994; nearlyidenticalreverseHoogsteen-typed(G G) Ibbaetal.,1996).Inaddition,proteinbindingof base-pairs(rhGG:Figure2(a)).However,onlyÁthe RNA loops can induce the formation of non- structure of the methylated sequence will be dis- Watson-Crick base-pairs. For example, the HIV cussed here; it provided a more reliable structure, Rev peptide binding to the Rev responsive element as was evident from the ®nal R-factors of the re- (RRE) in the env gene of HIV is associated with the ®ned structures. The duplexes of d(GCGCGCG)/ formation of two homopurine base-pairs in an in- d(TCGCGCG)formreversewobbled(G T)base- ternalRNAloop(Battisteetal.,1994;1996). pairs(rwGT)(Figure2(c)),whiletheÁduplexes The infrequent occurrence of reverse base-pairs of d(GCGCGCG)/d(CCGCGCG) form reverse makes it dif®cult to study the intrinsic stability as- Watson-Crickd(G C)base-pairs(rwcGC) sociated with speci®c structures. We present here (Figure2(b)).Thus,inÁ allthestructures,theover- the atomic resolution structures of three different hanging nucleotide G1 remains stacked against the reverse base-pairs formed by nucleotides that over- Z-DNAduplex,whileN8isextra-helical(Figure3). hang the 50-ends of DNA duplexes. By studying In the remainder of this section, we will ®rst dis- the structures of these base-pairs and their effects cuss the duplex structures and crystal lattice inter- on duplex formation during crystallization, we actions that are common to all the sequences, have estimated the stability of the d(G C) reverse followed by a more detailed description of the Watson-Crick and d(G T) reverse wobbleÁ base- structure for each type of base-pairing. pairs relative to theÁ distorted d(G G) reverse Hoogsteen base-pair. Á Z-DNA duplex structure Results The six bases at the 30-end of each sequence form standard Watson-Crick d(C G) base-pairs. The re- We have solved the structures of the hepta- sulting structure is a left-handedÁ duplex that is 5 nucleotide duplexes d(GCGCGCG)2 d(Gm CGCG- nearly identical to the Z-DNA structure of d(CG)3 5 CG)2) (where m C is cytosine methylated at the C5 (Wangetal.,1979,1981).Thebaseconformations carbon of the base), d(GCGCGCG)/d(TCGCGCG) alternate between anti for the dC nucleotides and d(GCGCGCG)/d(CCGCGCG).
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