Water, Shape Recognition, Salt Bridges, and Cation-Pi Interactions Differentiate Peptide Recognition of the HIV Rev-Responsive Element

Journal of Molecular Biology

Volumn 392, Issue 3, 2009, Pages 774-786

  Michael, Lauren A ^a   Chenault, Jessica A ^a   Miller III, Billy R ^a   Knolhoff, Ann M ^a   Nagan, Maria C ^a  

^a TRUMAN STATE UNIVERSITY   (United States)

Author keywords

arginine rich motif; molecular dynamics; Rev; RSG 1.2

Indexed keywords

ARGININE; CATION; PEPTIDE; REV PROTEIN; SODIUM CHLORIDE; VIRUS RNA; WATER;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; HUMAN IMMUNODEFICIENCY VIRUS; HYDROGEN BOND; IN VITRO STUDY; LIFE CYCLE; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN STRUCTURE; RNA SEQUENCE; SIMULATION; WATER ANALYSIS;

HUMAN IMMUNODEFICIENCY VIRUS;

AMINO ACID SEQUENCE; BASE SEQUENCE; CATIONS; COMPUTER SIMULATION; GENES, ENV; HUMANS; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; NUCLEIC ACID CONFORMATION; PEPTIDES; PROTEIN CONFORMATION; PROTEIN STABILITY; SALTS; WATER;

EID: 69349104811     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.07.047     Document Type: Article

References (108)

1. Lazinski D., Grzadzielska E., and Das A. Sequence-specific recognition of RNA hairpins by bacteriophage antiterminators requires a conserved arginine-rich motif. Cell 59 (1989) 207-218
2. Chen Y., and Varani G. Protein families and RNA recognition. FEBS J. 272 (2005) 2088-2097
3. Das C., and Frankel A.D. Sequence and structure space of RNA-binding peptides. Biopolymers 70 (2003) 80-85
4. Draper D.E. Themes in RNA-protein recognition. J. Mol. Biol. 293 (1999) 255-270
5. Weiss M.A., and Narayana N. RNA recognition by arginine-rich peptide motifs. Biopolymers 48 (1998) 167-180
6. Frankel A.D., and Smith C.A. Induced folding in RNA-protein recognition: more than a simple molecular handshake. Cell 92 (1998) 149-151
7. Leulliot N., and Varani G. Current topics in RNA-protein recognition: control of specificity and biological function through induced fit and conformational capture. Biochemistry 40 (2001) 7947-7956
8. Puglisi J.D., Chen L., Blanchard S., and Frankel A.D. Solution structure of a bovine immunodeficiency virus Tat-TAR peptide-RNA complex. Science 270 (1995) 1200-1203
9. Battiste J.L., Mao H., Roa N.S., Tan R., Muhandiram D.R., Kay L.E., et al. α Helix-RNA major groove recognition in an HIV-1 Rev peptide-RRE RNA complex. Science 273 (1996) 1547-1551
10. Tan R., Chen L., Buettner J.A., Hudson D., and Frankel A.D. RNA recognition by an isolated alpha helix. Cell 73 (1993) 1031-1040
11. Legault P., Li J., Mogridge J., Kay L.E., and Greenblatt J. NMR structure of the bacteriophage λ N peptide/boxB RNA complex: recognition of a GNRA fold by an arginine-rich motif. Cell 93 (1998) 289-299
12. Aboul-ela F., Karn J., and Varani G. The structure of the human immunodeficiency virus type-1 TAR RNA reveals principles of RNA recognition by Tat protein. J. Mol. Biol. 253 (1995) 313-332
13. Jiang F., Gorin A., Hu W., Majumdar A., Bakersville S., Xu W., et al. Anchoring an extended HTLV-1 Rex peptide with an RNA major groove containing junctional base triples. Structure 7 (1999) 1461-1472
14. Cook K.S., Fisk G.J., Hauber J., Usman N., Daly T.J., and Rusche J.R. Characterization of HIV-1 REV protein: binding stoichiometry and minimal RNA substrate. Nucleic Acids Res. 19 (1991) 1577-1583
15. Olsen H.S., Nelbock P., Cochrane A.W., and Rosen C.A. Secondary structure is the major determinant for interaction of HIV rev protein with RNA. Science 247 (1990) 845-848
16. Tiley L.S., Mailm M.H., Tewary H.K., Stockley P.G., and Cullen B.R. Identification of high-affinity RNA-binding site for the human immunodeficiency virus type 1 rev protein. Proc. Natl Acad. Sci. USA 89 (1992) 758-762
17. Feinberg M.B., Jarret R.F., Aldovini A., Gallo R.C., and Wong-Staal F. HTLV-III expression and production involve complex regulation at the level of splicing and translation of viral DNA. Cell 46 (1986) 807-817
18. Sodroski J., Goh W.C., Rosen C., Dayton A., Terwillinger E., and Haseltine W. A second post-transcriptional trans-activator gene required for HTLV-III replication. Nature 321 (1986) 412-417
19. Fischer U., Huber J., Boelens W.C., Mattaj I.W., and Lührmann R. The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell 82 (1995) 475-483
20. Cullen B.R. Nuclear RNA export. J. Cell Sci. 116 (2003) 587-597
21. Cochrane A.W., Chen C.-H., and Rosen C.A. Specific interaction of the human immunodeficiency virus Rev protein with a structured region in the env mRNA. Proc. Natl Acad. Sci. USA 87 (1990) 1198-1202
22. Malim M.H., Hauber J., Le S.Y., Maizel J.V., and Cullen B.R. The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature 338 (1989) 254-257
23. Mann D.A., Mikaelian I., Zemmel R.W., Green S.M., Lowe A.D., Kimura T., et al. A molecular rheostat. Co-operative rev binding to stem I of the rev-response element modulates human immunodeficiency virus type-1 late gene expression. J. Mol. Biol. 241 (1994) 193-207
24. Malim M.H., Böhnlein S., Hauber J., and Cullen B.R. Functional dissection of the HIV-1 rev trans-activator-derivation of a trans-dominant repressor of rev function. Cell 58 (1989) 205-214
25. Malim M.H., Tiley L.S., McCarn D.F., Rusche J.R., Hauber J., and Cullen B.R. HIV-1 structural gene expression requires binding of the Rev trans-activator to its RNA target sequence. Cell 60 (1990) 675-683
26. Heaphy S., Finch J.T., Gait M.J., Karn J., and Singh M. Human immunodeficiency virus type 1 regulator of virion expression, rev, forms nucleoprotein filaments after binding to a purine-rich "bubble" located within the rev-responsive region of viral mRNAs. Proc. Natl Acad. Sci. USA 88 (1991) 7366-7370
27. Daly T.J., Doten R.C., Rennert P., Auer M., Jaksche H., Donner A., et al. Biochemical characterization of binding of multiple HIV-1 Rev monomeric proteins to the Rev responsive element. Biochemistry 32 (1993) 10497-10505
28. Pond S.J.K., Ridgeway W.K., Robertson R., Wang J., and Millar D.P. HIV-1 Rev protein assembles on viral RNA one molecule at a time. Proc. Natl Acad. Sci. USA 106 (2009) 1404-1408
29. Malim M.H., and Cullen B.R. HIV-1 structural gene expression requires the binding of multiple rev monomers to the viral RRE: implications for HIV-1 latency. Cell 65 (1991) 241-248
30. Heaphy S., Dingwall C., Ernberg I., Gait M.J., Green M.R., Karn J., et al. HIV-1 regulator of virion expression (Rev) protein binds to an RNA stem-loop structure located within the Rev response element region. Cell 60 (1990) 685-693
31. Bartel D.P., Zapp M.L., Green M.R., and Szostak J.W. HIV-1 Rev regulation involves recognition of non-Watson-Crick base pairs in viral RNA. Cell 67 (1991) 529-536
32. Kjems J., Calnan B.J., Frankel A.D., and Sharp P.A. Specific binding of a basic peptide from HIV-1 Rev. EMBO J. 11 (1992) 1119-1129
33. Tan R., and Frankel A.D. Costabilization of peptide and RNA structure in an HIV Rev peptide-RRE complex. Biochemistry 33 (1994) 14579-14585
34. Pritchard C.E., Grasby J.A., Hamy F., Zacharek A.M., Singh M., Karn J., and Gait M.J. Methylphosphonate mapping of phosphate contacts critical for RNA recognition by the human immunodeficiency virus tat and rev proteins. Nucleic Acids Res. 22 (1994) 2592-2600
35. Iwai S., Pritchard C., Mann D.A., Karn J., and Gait M.J. Recognition of the high affinity binding site in rev-response element RNA by the human immunodeficiency virus type-1 rev protein. Nucleic Acids Res. 20 (1992) 6465-6472
36. Harada K., Martin S.S., and Frankel A.D. Selection of RNA-binding peptides in vivo. Nature 380 (1996) 175-179
37. Harada K., Martin S.S., Tan R., and Frankel A.D. Molding a peptide into an RNA site by in vivo peptide evolution. Proc. Natl Acad. Sci. USA 94 (1997) 11887-11892
38. Gosser Y., Hermann T., Majumdar A., Hu W., Frederick R., Jiang F., et al. Peptide-triggered conformational switch in HIV-1 RRE RNA complexes. Nat. Struct. Biol. 8 (2001) 146-150
39. Iwazaki T., Li X., and Harada K. Evolvability of the mode of peptide binding by an RNA. RNA 11 (2005) 1364-1373
40. Battiste J.L., Tan R., Frankel A.D., and Williamson J.R. Binding of an HIV Rev peptide to Rev responsive element RNA induces formation of purine-purine base pairs. Biochemistry 33 (1994) 2741-2747
41. Scanlon M.J., Fairlie D.P., Craik D.J., Englebretsen D.R., and West M.L. NMR solution structure of the RNA-binding peptide from human immunodeficiency virus (type 1) Rev. Biochemistry 34 (1995) 8242-8249
42. Peterson R.D., and Feigon J. Structural change in Rev response element RNA of HIV-1 on binding Rev peptide. J. Mol. Biol. 264 (1996) 863-877
43. Ippolito J.A., and Steitz T.A. The structure of the HIV-1 RRE high affinity Rev binding site at 1.6 Å resolution. J. Mol. Biol. 295 (2000) 711-717
44. Hung L.-W., Holbrook E.L., and Holbrook S.R. The crystal structure of the Rev binding element of HIV-1 reveals novel base pairing and conformational variability. Proc. Natl Acad. Sci. USA 97 (2000) 5107-5112
45. Cheatham III T.E. Simulation and modeling of nucleic acid structure, dynamics and interactions. Curr. Opin. Struct. Biol. 14 (2004) 360-367
46. Karplus M., and McCammon J.A. Molecular dynamics simulations of biomolecules. Nat. Struct. Biol. 9 (2002) 646-652
47. MacKerrell Jr. A.D., and Nilsson L. Molecular dynamics simulations of nucleic acid-protein complexes. Curr. Opin. Struct. Biol. 18 (2008) 194-199
48. McDowell S.E., Spackova N.A., Sponer J., and Walter N.G. Molecular dynamics simulations of RNA: an in silico single molecule approach. Biopolymers 85 (2007) 169-184
49. van Gunsteren W.F., Bakowies D., Barron R., Chandrasekhar I., Christen M., Daura X., et al. Biomolecular modeling: goals, problems and perspectives. Angew. Chem., Int. Ed. 45 (2006) 4064-4092
50. Auffinger P., and Hashem Y. Nucleic acid solvation: from outside to insight. Curr. Opin. Struct. Biol. 17 (2007) 325-333
51. Auffinger P., and Westhof E. RNA solvation: a molecular dynamics simulation perspective. Biopolymers 56 (2001) 266-274
52. Cheatham III T.E., and Young M.A. Molecular dynamics simulation of nucleic acids: successes, limitations and promise. Biopolymers 56 (2001) 232-256
53. Reblova K., Spackova N.A., Koca J., Neontis N.B., and Sponer J. Long-residency hydration, cation binding, and dynamics of loop E/helix IV rRNA-L25 protein complex. Biophys. J. 87 (2004) 3397-3412
54. Reyes C.M., Nifosi R., Frankel A.D., and Kollman P.A. Molecular dynamics and binding specificity analysis of the bovine immunodeficiency virus BIV tat-TAR complex. Biophys. J. 80 (2001) 2833-2842
55. Tsui V., Radhakrishnan I., Wright P.E., and Case D.A. NMR and molecular dynamics studies of the hydration of a zinc finger-DNA complex. J. Mol. Biol. 302 (2000) 1101-1117
56. Garcia-Garcia C., and Draper D.E. Electrostatic interactions in a peptide-RNA complex. J. Mol. Biol. 331 (2003) 75-88
57. Misra V.K., Hecht J.L., Yang A.-S., and Honig B. Electrostatic contributions to the binding free energy of the lcl repressor to DNA. Biophys. J. 75 (1998) 2262-2273
58. Nifosi R., Reyes C.M., and Kollman P.A. Molecular dynamics studies of the HIV-1 TAR and its complex with argininamide. Nucleic Acids Res. 28 (2000) 4944-4955
59. Lavery R., and Sklenar H. The definition of generalized helicoidal parameters and of axis curvature for irregular nucleic acids. J. Biomol. Struct. Dyn. 6 (1988) 63-91
60. Lavery R., and Sklenar H. Defining the structure of irregular nucleic acids: conventions and principles. J. Biomol. Struct. Dyn. 6 (1989) 655-667
61. Ping Y.H., Liu Y., Wang X., Neenhold H.R., and Rana T.M. Dynamics of RNA-protein interactions in the HIV-1 Rev-RRE complex visualized by 6-thioguanosine-mediated photocrosslinking. RNA 3 (1997) 850-860
62. Wilkinson T.A., Botuyan M.V., Kaplan B.E., Rossi J.J., and Chen Y. Arginine side-chain dynamics in the HIV-1 Rev-RRE complex. J. Mol. Biol. 303 (2000) 515-529
63. Bahadur R.P., Zacharias M., and Janin J. Dissecting protein-RNA recognition sites. Nucleic Acids Res. 36 (2008) 2705-2716
64. Jones S., Daley D.T.A., Luscombe N.M., Berman H.M., and Thornton J.M. Protein-RNA interactions: a structural analysis. Nucleic Acids Res. 29 (2001) 943-954
65. Nadassy K., Wodak S.J., and Janin J. Structural features of protein-nucleic acid recognition sites. Biochemistry 38 (1999) 1999-2017
66. Ala variants. Nucleic Acids Res. 28 (2000) 2527-2534
67. Chen C., Beck B.W., Krause K., and Pettitt B.M. Solvent participation in Serratia marcescens endonuclease complexes. Proteins 62 (2006) 982-995
68. Biot C., Buisine E., Kwasigroch J.-M., Wintjens R., and Rooman M. Probing the energetic and structural role of amino acid/nucleobase cation-pi interactions in protein-ligand complexes. J. Biol. Chem. 277 (2002) 40816-40822
69. Xue S., Calvin K., and Li H. RNA recognition and cleavage by a splicing endonuclease. Science 312 (2006) 906-910
70. Coulocheri S.A., Pigis D.G., Papavassiliou K.A., and Papavassiliou A.G. Hydrogen bonds in protein-DNA complexes: where geometry meets plasticity. Biochimie 89 (2007) 1291-1303
71. Sarai A., and Kono H. Protein-DNA recognition patterns and predictions. Annu. Rev. Biophys. Biomol. Struct. 34 (2005) 379-398
72. Haunstein S., Zhang C.-M., Hou Y.-M., and Perona J.J. Shape-selective RNA recognition by cysteinyl-tRNA synthetase. Nat. Struct. Mol. Biol. 11 (2004) 1134-1141
73. Perona J.J., and Hou Y.-M. Indirect readout of tRNA for aminoacylation. Biochemistry 46 (2007) 10419-10432
74. Litovchick A., and Rando R.R. Stereospecificity of short Rev-derived peptide interactions with RRE IIB RNA. RNA 9 (2003) 937-948
75. Cai Z., Gorin A., Frederick R., Ye X., Hu W., Majumdar A., et al. Solution structure of P22 transcriptional antitermination N peptide-boxB RNA complex. Nat. Struct. Biol. 5 (1998) 203-212
76. Calabro V., Daugherty M.D., and Frankel A.D. Solution structure of BIV TAR hairpin complexed to JDV Tat arginine-rich motif. Proc. Natl Acad. Sci. USA 102 (2005) 6849-6854
77. Cilley C.D., and Williamson J.R. Structural mimicry in the phage phi21 N peptide-boxB RNA complex. RNA 9 (2003) 663-673
78. Faber C., Schaerpf M., Becker T., Sticht H., and Roesch P. The structure of the coliphage Hk022 nun protein-lambda-phage boxb RNA complex. Implications for the mechanism of transcription termination. J. Biol. Chem. 276 (2001) 32064-32070
79. Schaerpf M., Sticht H., Schweimer K., Boehm M., Hoffmann S., and Roesch P. Antitermination in bacteriophage lambda. The structure of the N36 peptide-boxB RNA complex. Eur. J. Biochem. 267 (2000) 2397-2408
80. Ye X., Gorin A., Frederick R., Hu W., Majumdar A., Xu W., et al. RNA architecture dictates the conformations of a bound peptide. Chem. Biol. 6 (1999) 657-669
81. Grate D., and Wilson C. Role REVersal: understanding how RRE RNA binds its peptide ligand. Structure 5 (1997) 7-11
82. Otwinowski Z., Schevitz R.W., Zhang R.G., Lawson C.L., Joachimiak A., Marmorstein R.Q., et al. Crystal structure of trp represser/operator complex at atomic resolution. Nature 335 (1988) 321-329
83. Reddy C.K., Das A., and Jayaram B. Do water molecules mediate protein-DNA recognition?. J. Mol. Biol. 314 (2001) 619-632
84. Asp anticodon hairpin. J. Mol. Biol. 269 (1997) 326-341
85. Ala and 3:70 variants: molecular dynamics analysis of local helical structure and tightly bound water. J. Am. Chem. Soc. 121 (1999) 7310-7317
86. Hashem Y., and Auffinger P. A short guide for molecular dynamics simulations of RNA systems. Methods 47 (2009) 187-197
87. Jorgensen W.L., Chandrasekhar J., and Madura J.D. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79 (1983) 926-935
88. Hawkins G.D., Cramer C.J., and Truhlar D.G. Pairwise solute descreening of solute charges from a dielectric medium. Chem. Phys. Lett. 246 (1995) 122-129
89. Hawkins G.D., Cramer C.J., and Truhlar D.G. Parametrized models of aqueous free energies of solvation based on pairwise descreening of solute atomic charges from a dielectric medium. J. Phys. Chem. 100 (1996) 19824-19839
90. Tsui V., and Case D.A. Theory and applications of the generalized Born solvation model in macromolecular simulations. Biopolymers 56 (2001) 275-291
91. Case D.A., Darden T.A., Cheatham III T.E., Simmerling C.L., Wang J., Duke R.E., et al. AMBER 8.0 (2004), University of California, San Francisco, CA
92. Cornell W.D., Cieplak P., Bayly C.I., Gould I.R., Merz Jr. K.M., Ferguson D.M., et al. A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc. 117 (1995) 5179-5197
93. Cheatham III T.E., Cieplak P., and Kollman P.A. A modified version of the Cornell et al. force field with improved sugar pucker phases and helical repeat. J. Biomol. Struct. Dyn. 16 (1999) 845-862
94. Wang J., Cieplak P., and Kollman P.A. How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules?. J. Comput. Chem. 21 (1999) 1049-1074
95. Åqvist J. Ion-water interaction potentials derived from free energy perturbation simulations. J. Phys. Chem. 94 (1990) 8021-8024
96. Smith D.E., and Dang L.X. Computer simulations of NaCl association in polarizable water. J. Chem. Phys. 100 (1994) 3757-3766
97. Hornak V., Abel R., Okur A., Stockbine B., Roitberg A., and Simmerling C. Comparison of multiple amber force fields and development of improved protein backbone parameters. Proteins: Struct., Funct., Bioinform. 65 (2006) 712-725
98. Perez A., Marchan I., Svozil D., Sponer J., Cheatham III T.E., Laughton C.A., and Orozco M. Refinement of the AMBER force field for nucleic acids: improving the description of α/γ conformers. Biophys. J. 92 (2007) 3817-3829
99. Juong I.S., and Cheatham III T.E. Determination of alkali and halide monovalent ion parameters for use in explicitly solvated biomolecular simulations. J. Phys. Chem. B 112 (2008) 9020-9041
100. Ryckaert J.P., Ciccotti G., and Berendsen H.J.C. Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys. 23 (1977) 327-341
101. Izaguirre J.A., Catarello D.P., Wozniak J.M., and Skeel R.D. Langevin stabilization of molecular dynamics. J. Chem. Phys. 114 (2001) 2090-2098
102. Loncharich R.J., Brooks B.R., and Pastor R.W. Langevin dynamics of peptides: the frictional dependence of isomerization rates of N-acetylalanyl-N′-methylamide. Biopolymers 32 (1992) 523-535
103. Cheatham III T.E., and Kollman P.A. Molecular dynamics simulations highlight the structural differences among DNA:DNA, RNA:RNA, and DNA:RNA hybrid duplexes. J. Am. Chem. Soc. 119 (1997) 4805-4825
104. UUU: the role of modified bases in mRNA recognition. Nucleic Acids Res. 34 (2006) 5361-5368
105. Auffinger P., Cheatham III T.E., and Vaiana A.C. Spontaneous formation of KCl aggregates in biomolecular simulations: a force field issue?. J. Chem. Theory Comp. 3 (2007) 1851-1859
106. Chen A.A., and Pappu R.V. Parameters for monovalent ions in the AMBER-99 forcefield: assessment of inaccuracies and proposed improvements. J. Phys. Chem. B 111 (2007) 11884-11887
107. Humphrey W., Dalke A., and Schulten K. VMD: visual molecular dynamics. J. Mol. Graphics 14 (1996) 33-38
108. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF-Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004) 1605-1612