Structure and stability of RNA/RNA kissing complex: With application to HIV dimerization initiation signal

RNA

Volumn 17, Issue 12, 2011, Pages 2130-2143

  Cao, Song ^a   Chen, Shi Jie ^a  

^a University of Missouri   (United States)

Author keywords

Energy landscape; Folding thermodynamics; HIV dimerization; RNA RNA kissing complex; Structural predictions; Three dimensional structure (3D)

Indexed keywords

VIRUS RNA;

ARTICLE; ENTROPY; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; RNA RNA KISSING LOOP COMPLEX; RNA STABILITY; RNA STRUCTURE; THERMODYNAMICS;

BASE SEQUENCE; DIMERIZATION; HIV-1; HUMANS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; RNA STABILITY; RNA, VIRAL; THERMODYNAMICS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 81755162785     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.026658.111     Document Type: Article

References (97)

1. Andronescu M, Zhang Z, Condon A. 2005. Secondary structure prediction of interacting RNA molecules. J Mol Biol 345: 987-1001. (Pubitemid 40092219)
2. Andronescu MS, Pop C, Condon A. 2010. Improved free energy parameters for RNA pseudoknotted secondary structure prediction. RNA 16: 26-42.
3. Argaman L, Altuvia S. 2000. f hlA repression by OxyS RNA: kissing complex formation at two sites results in a stable antisense-target RNA complex. J Mol Biol 300: 1101-1112.
4. Arnott S, Hukins DWL. 1972. Optimised parameters for RNA double-helices. Biochem Biophys Res Commun 48: 1392-1399.
5. Bartel DP. 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
6. Bernhart SH, Tafer H, Muckstein U, Flamm C, Stadler PF, Hofacker IL. 2006. Partition function and base pairing probabilities of RNA heterodimers. Algorithms Mol Biol 1: 3. doi: 10.1186/1748-7188-1-3.
7. Brunel C, Marquet R, Romby P, Ehresmann C. 2002. RNA loop-loop interactions as dynamic functional motifs. Biochimie 84: 925-944. (Pubitemid 35422919)
8. Cao S, Chen S-J. 2005. Predicting RNA folding thermodynamics with a reduced chain representation model. RNA 11: 1884-1897. (Pubitemid 41720037)
9. Cao S, Chen S-J. 2006a. Free energy landscapes of RNA/RNA complexes: with applications to snRNA complexes in spliceosomes. J Mol Biol 357: 292-312. (Pubitemid 43339332)
10. Cao S, Chen S-J. 2006b. Predicting RNA pseudoknot folding thermodynamics. Nucleic Acids Res 34: 2634-2652. (Pubitemid 43985627)
11. Cao S, Chen S-J. 2009. Predicting structures and stabilities for H-type pseudoknots with interhelix loops. RNA 15: 696-706.
12. Cao S, Chen S-J. 2011. Physics-based de novo prediction of RNA 3D structures. J Phys Chem B 115: 4216-4226.
13. Case DA, Cheatham TE III, Darden T, Gohlke H, Luo R, Merz KM Jr, Onufriev A, Simmerling C, Wang B, Woods RJ. 2005. The Amber biomolecular simulation programs. J Comput Chem 26: 1668-1688. (Pubitemid 43076180)
14. Case DA, Darden TA, Cheatham TE III, Simmerling J, Wang RE, Duke R, Luo KM, Merz KM, Pearlman DA, Crowley M, et al. 2006. AMBER 9, University of California, San Francisco.
15. Cheatham TE III, Case DA. 2006. Using Amber to simulate DNA and RNA. In Computational studies of DNA and RNA (ed. J Sponer, F Lankas), pp. 45-72. Springer, Dordrecht.
16. Chen S-J. 2008. RNA folding: Conformational statistics, folding kinetics, and ion electrostatics. Annu Rev Biophys 37: 197-214.
17. Chen S-J, Dill KA. 1995. Statistical thermodynamics of double-stranded polymer molecules. J Chem Phys 103: 5802-5813.
18. Chen S-J, Dill KA. 1998. Theory for the conformational changes of double-stranded chain molecules. J Chem Phys 109: 4602-4616. (Pubitemid 128678675)
19. Cornell WD, Cieplak P, Bayly CI, Gould IR, Merz KM Jr, Ferguson DM, Spellmeyer DC, Fox T, Caldwell JW, Kollman PA. 1995. A second generation force-field for the simulation of proteins, nucleic-acids, and organic-molecules. J Am Chem Soc 117: 5179-5197.
20. Das R, Baker D. 2007. Automated de novo prediction of native-like RNA tertiary structures. Proc Natl Acad Sci 104: 14664-14669. (Pubitemid 350003200)
21. Didiano D, Hobert O. 2006. Perfect seed pairing is not a generally reliable predictor for miRNA-target interactions. Nat Struct Mol Biol 13: 849-851. (Pubitemid 44338780)
22. Dill KA. 1990. Dominant forces in protein folding. Biochemistry 29: 7133-7155. (Pubitemid 20230041)
23. Dimitrov RA, Zuker M. 2004. Prediction of hybridization and melting for double-stranded nucleic acids. Biophys J 87: 215-226. (Pubitemid 38880079)
24. Ding F, Sharma S, Chalasani P, Demidov VV, Broude N, Dokholyan NV. 2008. Ab initio RNA folding by discrete molecular dynamics: From structure prediction to folding mechanisms. RNA 14: 1164-1173. (Pubitemid 351717496)
25. Dirks RM, Bois JS, Schaeffer JM, Winfree E, Pierce NA. 2007. Thermodynamic analysis of interacting nucleic acid strands. SIAM Rev 49: 65-88. (Pubitemid 46351352)
26. Do CB, Woods DA, Batzoglou S. 2006. CONTRAfold: RNA secondary structure prediction without physics-based models. Bioinformatics 22: e90-e98. (Pubitemid 44288277)
27. Duarte CM, Pyle AM. 1998. Stepping through an RNA structure: a novel approach to conformational analysis. J Mol Biol 284: 1465-1478. (Pubitemid 28566081)
28. Ennifar E, Yusupov M, Walter P, Marquet R, Ehresmann B, Ehresmann C, Dumas P. 1999. The crystal structure of the dimerization initiation site of genomic HIV-1 RNA reveals an extended duplex with two adenine bulges. Structure 7: 1439-1449. (Pubitemid 29529884)
29. 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. (Pubitemid 33101628)
30. Ferro DR, Hermans J. 1971. A different best rigid-body molecular fit routine. Acta Crystallogr A 33: 345-347.
31. Freier SM, Kierzek R, Jaeger JA, Sugimoto N, Caruthers MH, Neilson T, Turner DH. 1986. Improved free-energy parameters for predictions of RNA duplex stability. Proc Natl Acad Sci 83: 9373-9377. (Pubitemid 17223363)
32. Greenleaf WJ, Frieda KL, Foster DAN, Woodside MT, Block SM. 2008. Direct observation of hierarchical folding in single riboswitch aptamers. Science 319: 630-633. (Pubitemid 351197067)
33. Huang FWD, Qin J, Reidys CM, Stadler PF. 2009. Partition function and base pairing probabilities for RNA-RNA interaction prediction. Bioinformatics 25: 2646-2654.
34. Isambert H, Siggia ED. 2000. Modeling RNA folding paths with pseudoknots: application to hepatitis delta virus ribozyme. Proc Natl Acad Sci 97: 6515-6520. (Pubitemid 30412745)
35. Jossinet F, Paillart J-C, Westhof E, Hermann T, Skripkin E, Lodmell JS, Ehresmann C, Ehresmann B, Marquet R. 1999. Dimerization of HIV-1 genomic RNA of subtypes A and B: RNA loop structure and magnesium binding. RNA 9: 1222-1234. (Pubitemid 29422764)
36. Kolb FA, Malmgren C, Westhof E, Ehresmann C, Ehresmann B, Wagner EG, Romby P. 2000a. An unusual structure formed by antisense-target RNA binding involves an extended kissing complex with a four-way junction and a side-by-side helical alignment. RNA 6: 311-324. (Pubitemid 30161277)
37. Kolb FA, Engdahl HM, Slagter-Jäger J, Ehresmann B, Ehresmann C, Westhof E, Wagner EG, Romby P. 2000b. Progression of a loop-loop complex to a four-way junction is crucial for the activity of a regulatory antisense RNA. EMBO J 19: 5905-5915.
38. Kolb FA, Westhof E, Ehresmann B, Ehresmann C, Wagner EG, Romby P. 2001a. Four-way junctions in antisense RNA-mRNA complexes involved in plasmid replication control: a common theme? J Mol Biol 309: 605-614. (Pubitemid 32595095)
39. Kolb FA, Westhof E, Ehresmann C, Ehresmann B, Wagner EG, Romby P. 2001b. Bulged residues promote the progression of a loop-loop interaction to a stable and inhibitory antisense-target RNA complex. Nucleic Acids Res 29: 3145-3153. (Pubitemid 32750560)
40. Kopeikin Z, Chen S-J. 2006. Folding thermodynamics of pseudoknotted chain conformations. J Chem Phys 124: 154903. doi: 10.1063/1.2188940.
41. Lai EC. 2003. microRNAs: Runts of the genome assert themselves. Curr Biol 13: R925-R936. (Pubitemid 37502516)
42. Laederach A. 2007. Informatics challenges in structured RNA. Brief Bioinform 8: 294-303. (Pubitemid 350142619)
43. Laughrea M, Jetté L. 1994. A 19-nucleotide sequence upstream of the 5′ major splice donor is part of the dimerization domain of human immunodeficiency virus 1 genomeric RNA. Biochemistry 33: 13464-13474. (Pubitemid 24373263)
44. Lebars I, Legrand P, Aimé A, Pinaud N, Fribourg S, Di Primo C. 2008. Exploring TAR-RNA aptamer loop-loop interaction by X-ray crystallography, UV spectroscopy and surface plasmon resonance. Nucleic Acids Res 36: 7146-7156.
45. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB. 2003. Prediction of mammalian microRNA targets. Cell 115: 787-798. (Pubitemid 38058492)
46. Li PTX, Bustamante C, Tinoco I Jr. 2006. Unusual mechanical stability of a minimal RNA kissing complex. Proc Natl Sci Acad 43: 15847-15852. (Pubitemid 44657555)
47. Li PTX, Vieregg J, Tinoco I Jr. 2008. How RNA unfolds and refolds. Annu Rev Biochem 77: 77-100.
48. Liu L, Chen S-J. 2010. Computing the conformational entropy for RNA folds. J Chem Phys 132: 235104. doi: 10.1063/1.3447385.
49. Long D, Lee R, Williams P, Chan CY, Ambros V, Ding Y. 2007. Potent effect of target structure on microRNA function. Nat Struct Mol Biol 14: 287-294. (Pubitemid 46608348)
50. 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. (Pubitemid 43160056)
51. Lu M, Ma J. 2005. The role of shape in determining molecular motions. Biophys J 89: 2395-2401. (Pubitemid 41401029)
52. Lu ZJ, Gloor JW, Mathews DH. 2009. Improved RNA secondary structure prediction by maximizing expected pair accuracy. RNA 15: 1805-1813.
53. Madhani HD, Guthrie C. 1992. A novel base-pairing interaction between U2 and U6 snRNAs suggests a mechanism for the catalytic activation of the spliceosome. Cell 71: 803-817.
54. Madhani HD, Guthrie C. 1994. Dynamic RNA-RNA interactions in the spliceosome. Annu Rev Genet 28: 1-26.
55. Mathews DH, Burkard ME, Freier SM, Wyatt JR, Turner DH. 1999. Predicting oligonucleotide affinity to nucleic acid targets. RNA 5: 1458-1469. (Pubitemid 29530490)
56. Michel F, Westhof E. 1990. Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J Mol Biol 216: 585-610. (Pubitemid 120037393)
57. Mitrovich QM, Guthrie C. 2007. Evolution of small nuclear RNAs in S. cerevisiae, C. albicans, and other hemiascomycetous yeasts. RNA 13: 2066-2080. (Pubitemid 350127549)
58. Montange RK, Batey RT. 2008. Riboswitches: emerging themes in RNA structure and function. Annu Rev Biophys 37: 117-133.
59. 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. (Pubitemid 28265024)
60. Mujeeb A, Parslow TG, Zarrinpar A, Das C, James TL. 1999. NMR structure of the mature dimer initiation complex of HIV-1 genomic RNA. FEBS Lett 458: 387-392. (Pubitemid 29433841)
61. Muriaux D, De Rocquigny H, Roques BP, Paoletti J. 1996a. NCp7 activates HIV-1Lai RNA dimerization by converting a transient loop-loop complex into a stable dimer. J Biol Chem 271: 33686-33692.
62. Muriaux D, Fossé P, Paoletti J. 1996b. A kissing complex together with a stable dimer is involved in the HIV-1(Lai) RNA dimerization process in vitro. Biochemistry 35: 5075-5082.
63. Nagel JHA, Pleij CWA. 2002. Self-induced structural switches in RNA. Bichimie 84: 913-923. (Pubitemid 35422918)
64. Olson WK. 1980. Configurational statistics of polynucleotide chains: an updated virtual bond model to treat effects of base stacking. Macromolecules 13: 721-728.
65. Paillart J-C, Skripkin E, Ehresmann B, Ehresmann C, Marquet R. 1996. A loop-loop "kissing" complex is the essential part of the dimer linkage of genomic HIV-1 RNA. Proc Natl Acad Sci 93: 5572-5577.
66. Paillart JC, Shehu-Xhilaga M, Marquet R, Mak J. 2004. Dimerization of retroviral RNA genomes: An inseparable pair. Nat Rev Microbiol 2: 461-472. (Pubitemid 39200013)
67. Parisien M, Major F. 2008. The MC-Fold and MC-Sym pipeline infers RNA structure from sequence data. Nature 452: 51-55. (Pubitemid 351355097)
68. Pearlman DA, Case DA, Caldwell JW, Ross WS, Cheatham TE, Debolt S, Ferguson D, Seibel G, Kollman P. 1995. AMBER: a package of computer-programs for applying molecular mechanics, normalmode analysis, molecular-dynamics and free-energy calculations to stimulate the structural and energetic properties of molecules. Comput Phys Commun 91: 1-41.
69. Réblová K, Fadrná E, Sarzynska J, Kulinski T, Kulhánek P, Ennifar E, Koča J, Šponer J. 2007. Conformations of flanking bases in HIV-1 RNA DIS kissing complexes studied by molecular dynamics. Biophys J 93: 3932-3949.
70. Rehmsmeier M, Steffen P, Höchsmann M, Giegerich R. 2004. Fast and effective prediction of microRNA/target duplexes. RNA 10: 1507-1517. (Pubitemid 39288185)
71. Rother M, Rother K, Puton T, Bujnicki JM. 2011. ModeRNA: a tool for comparative modeling of RNA 3D structure. Nucleic Acid Res 39: 4007-4022.
72. Russell RS, Liang C, Wainberg MA. 2004. Is HIV-1 RNA dimerization a prerequisite for packaging? Yes, no, probably? Retrovirology 1: 23-36.
73. SantaLucia J Jr, Hicks D. 2004. The thermodynamics of DNA structural motifs. Annu Rev Biophys Biomol Struct 33: 415-440. (Pubitemid 38829966)
74. Sarzyńska J, Réblová K, Šponer J. 2008. Conformational transitions of flanking purines in HIV-1 RNA dimerization initiation site kissing complexes studied by CHARMM explicit solvent molecular dynamics. Biopolymer 89: 732-746.
75. Sashital DG, Cornilescu G, Butcher SE. 2004. U2-U6 RNA folding reveals a group II intron-like domain and a four-helix junction. Nat Struct Mol Biol 11: 1237-1242.
76. Sashital DG, Venditti V, Angers CG, Cornilescu G, Butcher SE. 2007. Structure and thermodynamics of a conserved U2 snRNA domain from yeast and human. RNA 13: 328-338. (Pubitemid 46327536)
77. Schultes EA, Bartel DP. 2000. One sequence, two ribozymes: Implications for the emergence of new ribozyme folds. Science 289: 448-452. (Pubitemid 30490456)
78. Shapiro BA, Yingling YG, Kasprzak W, Bindewald E. 2007. Bridging the gap in RNA structure prediction. Curr Opin Struct Biol 17: 157-165. (Pubitemid 46575248)
79. Skripkin E, Paillart J-C, Marquest R, Ehresmann B, Ehresmann C. 1994. Identification of the primary site of the human immunodeficiency virus type 1 RNA dimerization in vitro. Proc Natl Acad Sci 91: 4945-4949. (Pubitemid 24177767)
80. Sperschneider J, Datta A. 2010. DotKnot: pseudoknot prediction using the probability dot plot under a refined energy model. Nucleic Acids Res 38: e103.
81. Sperschneider J, Datta A, Wise MJ. 2011. Heuristic RNA pseudoknot prediction including intramolecular kissing hairpins. RNA 17: 27-38.
82. Takahashi KI, Baba S, Chattopadhyay P, Koyanagi Y, Yamamoto N, Takaku H, Kawai G. 2000. Structural requirement for the two-step dimerization of human immunodeficiency virus type 1 genome. RNA 6: 96-102. (Pubitemid 30069040)
83. Takahashi K, Baba S, Hayashi Y, Koyanagi Y, Yamamoto N, Takaku H, Kawai G. 2005. NMR analysis of intra- and inter-molecular stems in the dimerization initiation site of the HIV-1 genome. J Biochem 138: 583-592.
84. Tan RKZ, Petrov AS, Harvey SC. 2006. YUP: A molecular simulation program for coarse-grained and multiscaled models. J Chem Theory Comput 2: 529-540.
85. Tirion M. 1996. Large amplitude elastic motions in proteins from a single-parameter, atomic analysis. Phys Rev Lett 77: 1905-1908. (Pubitemid 126625816)
86. Tucker BJ, Breaker RR. 2005. Riboswitches as versatile gene control elements. Curr Opin Struct Biol 15: 342-348. (Pubitemid 40826454)
87. Ulyanov NB, Mujeeb A, Du Z, Tonelli M, Parslow TG, James TL. 2006. NMR structure of the full-length linear dimer of stem-loop-1 RNA in the HIV-1 dimer initiation site. J Biol Chem 281: 16168-16177. (Pubitemid 43848512)
88. Valadlkhan S. 2007. The spliceosome: a ribozyme at heart? Biol Chem 388: 693-697.
89. Walter AE, Turner DH. 1994. Sequence dependence of stability for coaxial stacking of RNA helixes with Watson-Crick base paired interfaces. Biochemistry 33: 12715-12719. (Pubitemid 24345905)
90. Wang JM, Cieplak P, Kollman PA. 2000. How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J Comput Chem 21: 1049-1074.
91. Wang Y, Rader AJ, Bahar I, Jernigan RL. 2004. Global ribosome motions revealed with elastic network model. J Struct Biol 147: 302-314. (Pubitemid 39140737)
92. Weixlbaumer A, Werner A, Flamm C, Westhof E, Schroeder R. 2004. Determination of thermodynamic parameters for HIV DIS type loop-loop kissing complexes. Nucleic Acids Res 32: 5126-5133. (Pubitemid 39445500)
93. Westhof E, Masquida B, Jossinet F. 2011. Predicting and modeling RNA architecture. Cold Spring Harb Perspect Biol. 3: a003632. doi: 10.1101/cshperspect.a003632.
94. Wickiser JK, Cheah MT, Breaker RR, Crothers DM. 2005. The kinetics of ligand binding by an adenine-sensing riboswitch. Biochemistry 44: 13404-13414. (Pubitemid 41429463)
95. Xia TB, SantaLucia J Jr, Burkard ME, Kierzek R, Schroeder SJ, Jiao XQ, Cox C, Turner DH. 1998. Thermodynamic parameters for an expanded nearest-neighbor model for formation of RNA duplexes with Watson-Crick base pairs. Biochemistry 37: 14719-14735. (Pubitemid 28487580)
96. Yang L, Song G, Jernigan RL. 2009. Protein elastic network models and the ranges of cooperativity. Proc Natl Acad Sci 106: 12347-12352.
97. Zhang WB, Chen S-J. 2001. Predicting free energy landscapes for complexes of double stranded chain molecules. J Chem Phys 114: 4253-4266. (Pubitemid 32255052)