Liquid-crystal NMR structure of HIV TAR RNA bound to its SELEX RNA aptamer reveals the origins of the high stability of the complex

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 27, 2008, Pages 9210-9215

  Van Melckebeke, Hélène ^a,b   Devany, Matthew ^a,b   Di Primo, Carmelo ^c,d   Beaurain, François ^c,d   Toulmé, Jean Jacques ^c,d   Bryce, David L ^e   Boisbouvier, Jérôme ^e  

^a INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^b DIF   (France)

^c INSTITUT EUROPÉEN DE CHIMIE ET BIOLOGIE   (France)

^d UNIVERSITÉ DE BORDEAUX   (France)

^e UNIVERSITY OF OTTAWA   (Canada)

Author keywords

GA base pair; Kissing complex; Residual dipolar coupling; RNA RNA complex

Indexed keywords

APTAMER; VIRUS RNA;

ACCURACY; ARTICLE; BASE MISPAIRING; COMBINATORIAL CHEMISTRY; CONTROLLED STUDY; CRYSTAL STRUCTURE; HUMAN IMMUNODEFICIENCY VIRUS; HYDROGEN BOND; LIQUID CRYSTAL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; RNA CONFORMATION; RNA STABILITY; RNA STRUCTURE;

EID: 48249122367     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0712121105     Document Type: Article

References (57)

1. Muesing MA, Smith DH, Capon DJ (1987) Regulation of messenger-RNA accumulation by a human-immunodeficiency-virus transactivator protein. Cell 48:691-701.
2. Weeks KM, Ampe C, Schultz SC, Steitz TA, Crothers DM (1990) Fragments of the HIV-1 TAT protein specifically bind TAR RNA. Science 249:1281-1285.
3. Kao SY, Calman AF, Luciw PA, Peterlin BM (1987) Anti-termination of transcription within the long terminal repeat of HIV-1 by TAT gene-product. Nature 330:489-493.
4. Feng S, Holland EC (1988) HIV-1 TAT trans-activation requires the loop sequence within TAR. Nature 334:165-167.
5. Wei P, Garber ME, Fang SM, Fischer WH, Jones KA (1998) A novel CDK9-associated C-type cyclin interacts directly with HIV-1 Tat and mediates its high-affinity, loop-specific binding to TAR RNA. Cell 92:451-462.
6. Ivanov D, et al. (1999) Cyclin T1 domains involved in complex formation with Tat and TAR RNA are critical for tat-activation. J Mol Biol 288:41-56.
7. Bieniasz PD, Grdina TA, Bogerd HP, Cullen BR (1999) Recruitment of cyclin T1/P-TEFb to an HIV type I long terminal repeat promoter proximal RNA target is both necessary and sufficient for full activation of transcription. Proc Natl Acad Sci USA 96:7791-7796.
8. Hamy F, et al. (1997) An inhibitor of the Tat/TAR RNA interaction that effectively suppresses HIV-1 replication. Proc Natl Acad Sci USA 94:3548-3553.
9. Dassonneville L, Hamy F, Colson P, Houssier C, Bailly C (1997) Binding of Hoechst 33258 to the TAR RNA of HIV-1. Recognition of a pyrimidine bulge-dependent structure. Nucleic Acids Res 25:4487-4492.
10. Sullenger BA, Gallardo HF, Ungers GE, Gilboa E (1990) Overexpression of TAR sequences renders cells resistant to Human-Immunodeficiency-Virus replication. Cell 63:601-608.
11. Boiziau C, Dausse E, Yurchenko L, Toulme JJ (1999) DNA aptamers selected against the HIV-1 trans-activation-responsive RNA element form RNA-DNA kissing complexes. J Biol Chem 274:12730-12737.
12. Ecker DJ, et al. (1992) Pseudo half-knot formation with RNA. Science 257:958-961.
13. Chang KY, Tinoco I (1994) Characterization of a kissing hairpin complex derived from the human-immunodeficiency-virus genome. Proc Natl Acad Sci USA 91:8705-8709.
14. Chang KY, Tinoco I (1997) The structure of an RNA "kissing" hairpin complex of the HIV TAR hairpin loop and its complement. J Mol Biol 269:52-66.
15. Duconge F, Toulme JJ (1999) In vitro selection identifies key determinants for loop-loop interactions: RNA aptamers selective for the TAR RNA element of HIV-1. RNA 5:1605-1614.
16. Duconge F, Di Primo C, Toulme JJ (2000) Is a closing "GA pair" a rule for stable loop-loop RNA complexes? J Biol Chem 275:21287-21294.
17. Beaurain F, Di Primo C, Toulme JJ, Laguerre M (2003) Molecular dynamics reveals the stabilizing role of loop-closing residues in kissing interactions: comparison between TAR-TAR* and TAR-aptamer. Nucleic Acids Res 31:4275-4284.
18. Darfeuille F, et al. (2002) Loop-loop interaction of HIV-1 TAR RNA with N3′-> P5′ deoxyphosphoramidate aptamers inhibits in vitro Tat-mediated transcription. Proc Natl Acad Sci USA 99:9709-9714.
19. Kolb G, et al. (2005) Hexitol nucleic acid-containing aptamers are efficient ligands of HIV-1 TAR RNA. Biochemistry 44:2926-2933.
20. Lebars I, Richard T, Di Primo C, Toulme JJ (2007) NMR structure of a kissing complex formed between the TAR RNA element of HIV-1 and a LNA-modified aptamer. Nucleic Acids Res 35:6103-6114.
21. Darfeuille F, et al. (2006) Aptamers targeted to an RNA hairpin show improved specificity compared to that of complementary oligonucleotides. Biochemistry 45:12076-12082.
22. Kim CH, Tinoco I (2000) A retroviral RNA kissing complex containing only two G center dot C base pairs. Proc Natl Acad Sci USA 97:9396-9401.
23. Lee AJ, Crothers DM (1998) The solution structure of an RNA loop-loop complex: the ColE1 inverted loop sequence. Structure 6:993-1005.
24. Dardel F, Marquet R, Ehresmann C, Ehresmann B, Blanquet S (1998) Solution studies of the dimerization initiation site of HIV-1 genomic RNA. Nucleic Acids Res 26:3567-3571.
25. Mujeeb A, Clever JL, Billeci TM, James TL, Parslow TG (1998) Structure of the dimer initiation complex of HIV-1 genomic RNA. Nat Struct Biol 5:432-436.
26. Baba S, et al. (2005) Solution RNA structures of the HIV-1 dimerization initiation site in the kissing-loop and extended-duplex dimers. J Biochem 138:583-592.
27. Gregorian RS, Crothers DM (1995) Determinants of RNA hairpin loop-loop complex stability. J Mol Biol 248:968-984.
28. Dingley AJ, Grzesiek S (1998) Direct observation of hydrogen bonds in nucleic acid base pairs by internucleotide (2)J(NN) couplings. J Am Chem Soc 120:8293-8297.
29. Wu Z, Delaglio F, Tjandra N, Zhurkin VB, Bax A (2003) Overall structure and sugar dynamics of a DNA dodecamer from homo and heteronuclear dipolar couplings and P-31 chemical shift anisotropy. J Biomol Nmr 26:297-315.
30. Cornilescu G, Marquardt JL, Ottiger M, Bax A (1998) Validation of protein structure from anisotropic carbonyl chemical shifts in a dilute liquid crystalline phase. J Am Chem Soc 120:6836-6837.
31. Bax A, Grishaev A (2005) Weak alignment NMR: a hawk-eyed view of biomolecular structure. Curr Opin Struct Biol 15:563-570.
32. Ying J, Bax A (2006) 2-hydroxyl proton positions in helical RNA from simultaneously measured heteronuclear scalar couplings and NOEs. J Am Chem Soc 128:8372-8373.
33. Hennig M, Fohrer J, Carlomagno T (2005) Assignment and NOE analysis of 2′-hydroxyl protons in RNA: implications for stabilization of RNA A-form duplexes. J Am Chem Soc 127:2028-2029.
34. Scarabino D, Crisari A, Lorenzini S, Williams K, Tocchini-Valentini GP (1999) tRNA prefers to kiss. EMBO J 18:4571-4578.
35. Marino JP, Gregorian RS, Csankovszki G, Crothers DM (1995) Bent helix formation between RNA hairpins with complementary loops. Science 268:1448-1454.
36. Lorenz C, Piganeau N, Schroeder R (2006) Stabilities of HIV-1 DIS type RNA loop-loop interactions in vitro and in vivo. Nucleic Acids Res 34:334-342.
37. Tjandra N, Bax A (1997) Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 278:1111-1114.
38. Tjandra N, Garrett DS, Gronenborn AM, Bax A, Clore GM (1997) Defining long range order in NMR structure determination from the dependence of heteronuclear relaxation times on rotational diffusion anisotropy. Nat Struct Biol 4:443-449.
39. Hansen MR, Mueller L, Pardi A (1998) Tunable alignment of macromolecules by filamentous phage yields dipolar coupling interactions. Nat Struct Biol 5:1065-1074.
40. Bayer P, Varani L, Varani G (1999) Refinement of the structure of protein-RNA complexes by residual dipolar coupling analysis. J Biomol Nmr 14:149-155.
41. Vermeulen A, Zhou HJ, Pardi A (2000) Determining DNA global structure and DNA bending by application of NMR residual dipolar couplings. J Am Chem Soc 122:9638-9647.
42. Mollova ET, Hansen MR, Pardi A (2000) Global structure of RNA determined with residual dipolar couplings. J Am Chem Soc 122:11561-11562.
43. Warren JJ, Moore PB (2001) Application of dipolar coupling data to the refinement of the solution structure of the Sarcin-Ricin loop RNA. J Biomol Nmr 20:311-323.
44. Sibille N, Pardi A, Simorre JP, Blackledge M (2001) Refinement of local and long-range structural order in theophylline-binding RNA using C-13-H-1 residual dipolar couplings and restrained molecular dynamics. J Am Chem Soc 123:12135-12146.
45. Padrta P, Stefl R, Kralik L, Zidek L, Sklenar V (2002) Refinement of d(GCGAAGC) hairpin structure using one- and two-bond residual dipolar couplings. J Biomol Nmr 24:1-14.
46. Wu Z, Maderia M, Barchi JJ, Marquez VE, Bax A (2005) Changes in DNA bending induced by restricting nucleotide ring pucker studied by weak alignment NMR spectroscopy. Proc Natl Acad Sci USA 102:24-28.
47. Westhof E, Dumas P, Moras D (1988) Restrained refinement of 2 crytalline forms of yeast aspartic-acid and phenylalanine transfer-RNA crystals. Acta Crystallogr A 44:112-123.
48. Ban N, Nissen P, Hansen J, Moore PB, Steitz TA (2000) The complete atomic structure of the large ribosomal subunit at 2.4 angstrom resolution. Science 289:905-920.
49. Ennifar E, Walter P, Ehresmann B, Ehresmann C, Dumas P (2001) Crystal structures of coaxially stacked kissing complexes of the HIV-1 RNA dimerization initiation site. Nat Struct Biol 8:1064-1068.
50. Brutscher B, Boisbouvier J, Pardi A, Marion D, Simorre JP (1998) Improved sensitivity and resolution in H-1-C-13 NMR experiments of RNA. J Am Chem Soc 120:11845-11851.
51. Miclet E, Boisbouvier J, Bax A (2005) Measurement of eight scalar and dipolar couplings for methine-methylene pairs in proteins and nucleic acids. J Biomol Nmr 31:201-216.
52. Boisbouvier J, Bryce DL, O'Neil-Cabello E, Nikonowicz EP, Bax A (2004) Resolution-optimized NMR measurement of D-1(CH), D-1(CH) and D-2(CH) residual dipolar couplings in nucleic acid bases. J Biomol Nmr 30:287-301.
53. Clore GM, Gronenborn AM, Bax A (1998) A robust method for determining the magnitude of the fully asymmetric alignment tensor of oriented macromolecules in the absence of structural information. J Magn Reson 133:216-221.
54. McCallum SA, Pardi A (2003) Refined solution structure of the iron-responsive element RNA using residual dipolar couplings. J Mol Biol 326:1037-1050.
55. Bryce DL, Bax A (2004) Application of correlated residual dipolar couplings to the determination of the molecular alignment tensor magnitude of oriented proteins and nucleic acids J Biomol NMR 28:273-287.
56. Schwieters CD, Kuszewski JJ, Tjandra N, Clore GM (2003) The Xplor-NIH NMR molecular structure determination package. J Mag Reson 160:65-73.
57. Bryce DL, Grishaev A, Bax A (2005) Measurement of ribose carbon chemical shift tensors for A-form RNA by liquid crystal NMR spectroscopy. J Am Chem Soc 127:7387-7396.