Fluctuation dynamics analysis of gp120 envelope protein reveals a topologically based communication network

Proteins: Structure, Function and Bioinformatics

Volumn 78, Issue 14, 2010, Pages 2935-2949

  Shrivastava, Indira ^a   LaLonde, Judith M ^b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b Chemistry Department   (China)

Author keywords

Cd4 binding; Chemokine receptor; Communication propensities; Commute times; Gaussian network model; Gp120; HIV; Molecular dynamics; Signal propagation; Slow mode

Indexed keywords

CD4 ANTIGEN; GLYCOPROTEIN GP 120;

ARTICLE; CELL ADHESION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN STRUCTURE;

HUMAN IMMUNODEFICIENCY VIRUS;

EID: 77957968574     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22816     Document Type: Article

References (72)

1. Barre-Sinoussi F, Chermann JC, Rey F, Nugeyre MT, Chamaret S, Gruest J, Dauguet C, Axler-Blin C, Vezinet-Brun F, Rouzioux C, Rozenbaum W, Montagnier L. Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science 1983;220:868-871.
2. Gallo RC, Salahuddin SZ, Popovic M, Shearer GM, Kaplan M, Haynes BF, Palker TJ, Redfield R, Oleske J, Safai B, Gilbert W, Paul P, Phillip M. Frequent detection and isolation of cytopathic retroviruses (HTLV-III) from patients with AIDS and at risk for AIDS. Science 1984;224:500-503.
3. Kowalski M, Potz J, Basiripour L, Dorfman T, Goh WC, Terwilliger E, Dayton A, Rosen C, Haseltine W, Sodroski J. Functional regions of the envelope glycoprotein of human immunodeficiency virus type 1. Science 1987;237:1351-1355.
4. Lu M, Blacklow SC, Kim PS. A trimeric structural domain of the HIV-1 transmembrane glycoprotein. Nat Struct Biol 1995;2:1075-1082.
5. Blacklow SC, Lu M, Kim PS. A trimeric subdomain of the simian immunodeficiency virus envelope glycoprotein. Biochemistry 1995; 34:14955-14962.
6. Dalgleish AG, Beverley PC, Clapham PR, Crawford DH, Greaves MF, Weiss RA. The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature 1984;312:763-767.
7. Dragic T, Litwin V, Allaway GP, Martin SR, Huang Y, Nagashima KA, Cayanan C, Maddon PJ, Koup RA, Moore JP, Paxton WA. HIV-1 entry into CD41 cells is mediated by the chemokine receptor CC-CKR-5. Nature 1996;381:667-673.
8. Sattentau QJ, Moore JP. Conformational changes induced in the human immunodeficiency virus envelope glycoprotein by soluble CD4 binding. J Exp Med 1991;174:407-415.
9. Sattentau QJ, Moore JP, Vignaux F, Traincard F, Poignard P. Conformational changes induced in the envelope glycoproteins of the human and simian immunodeficiency viruses by soluble receptor binding. J Virol 1993;67:7383-7393.
10. Feng Y, Broder CC, Kennedy PE, Berger EA. HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G proteincoupled receptor. Science 1996;272:872-877.
11. Deng H, Liu R, Ellmeier W, Choe S, Unutmaz D, Burkhart M, Di Marzio P, Marmon S, Sutton RE, Hill CM, Davis CB, Peiper SC, Schall TJ, Littman DR, Landau NR. Identification of a major co-receptor for primary isolates of HIV-1. Nature 1996;381:661-666.
12. Doranz BJ, Rucker J, Yi Y, Smyth RJ, Samson M, Peiper SC, Parmentier M, Collman RG, Doms RW. A dual-tropic primary HIV-1 isolate that uses fusin and the beta-chemokine receptors CKR-5, CKR-3, and CKR-2b as fusion cofactors. Cell 1996;85:1149-1158.
13. Choe H, Farzan M, Sun Y, Sullivan N, Rollins B, Ponath PD, Wu L, Mackay CR, LaRosa G, Newman W, Gerard N, Gerard C, Sodroski J. The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 1996;85:1135-1148.
14. Bosch ML, Earl PL, Fargnoli K, Picciafuoco S, Giombini F, WongStaal F, Franchini G. Identification of the fusion peptide of primate immunodeficiency viruses. Science 1989;244:694-697.
15. Brasseur R, Cornet B, Burny A, Vandenbranden M, Ruysschaert JM. Mode of insertion into a lipid membrane of the N-terminal HIV gp41 peptide segment. AIDS Res Hum Retroviruses 1988;4:83-90.
16. Helseth E, Olshevsky U, Gabuzda D, Ardman B, Haseltine W, Sodroski J. Changes in the transmembrane region of the human immunodeficiency virus type 1 gp41 envelope glycoprotein affect membrane fusion. J Virol 1990;64:6314-6318.
17. Wyatt R, Sodroski J. The HIV-1 envelope glycoproteins fusogens antigens and immunogens. Science 1998;280:1884-1888.
18. Kwong PD, Wyatt R, Robinson J, Sweet RW, Sodroski J, Hendrickson WA. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 1998;393:648-659.
19. Kwong PD, Wyatt R, Majeed S, Robinson J, Sweet RW, Sodroski J, Hendrickson WA. Structures of HIV-1 gp120 envelope glycoproteins from laboratory-adapted and primary isolates. Structure Fold Des 2000;8:1329-1339.
20. Moebius U, Clayton LK, Abraham S, Harrison SC, Reinherz EL. The human immunodeficiency virus gp120 binding site on CD4: delineation by quantitative equilibrium and kinetic binding studies of mutants in conjunction with a high-resolution CD4 atomic structure. J Exp Med 1992;176:507-517.
21. Huang CC, Tang M, Zhang MY, Majeed S, Montabana E, Stanfield RL, Dimitrov DS, Korber B, Sodroski J, Wilson IA, Wyatt R, Kwong PD. Structure of a V3-containing HIV-1 gp120 core. Science 2005;310:1025-1028.
22. Huang CC, Stricher F, Martin L, Decker JM, Majeed S, Barthe P, Hendrickson WA, Robinson J, Roumestand C, Sodroski J, Wyatt R, Shaw GM, Vita C, Kwong PD. Scorpion-toxin mimics of CD4 in complex with human immunodeficiency virus gp120 crystal structures, molecular mimicry, and neutralization breadth. Structure 2005;13:755-768.
23. Pancera M, Majeed S, Ban YE, Chen L, Huang CC, Kong L, Kwon YD, Stuckey J, Zhou T, Robinson JE, Schief WR, Sodroski J, Wyatt R, Kwong PD. Structure of HIV-1 gp120 with gp41-interactive region reveals layered envelope architecture and basis of conformational mobility. Proc Natl Acad Sci USA 2010;107:1166-1171.
24. Chen L, Kwon YD, Zhou T, Wu X, O'Dell S, Cavacini L, Hessell AJ, Pancera M, Tang M, Xu L, Yang Z-Y, Zhang M-Y, Arthos J, Burton DR, Dimitrov DS, Nabel GJ, Posner MR, Sodroski J, Wyatt R, Mascola JR, Kwong PD. Structural Basis of Immune Evasion at the Site of CD4 Attachment on HIV-1 gp120. Science 2009;326:1123-1127.
25. Xie H, Ng D, Savinov SN, Dey B, Kwong PD, Wyatt R, Smith AB, 3rd, Hendrickson WA. Structure-activity relationships in the binding of chemically derivatized CD4 to gp120 from human immunodeficiency virus. J Med Chem 2007;50:4898-4908.
26. Chen B, Vogan EM, Gong H, Skehel JJ, Wiley DC, Harrison SC. Structure of an unliganded simian immunodeficiency virus gp120 core. Nature 2005;433:834-841.
27. Myszka DG, Sweet RW, Hensley P, Brigham-Burke M, Kwong PD, Hendrickson WA, Wyatt R, Sodroski J, Doyle ML. Energetics of the HIV gp120-CD4 binding reaction. Proc Natl Acad Sci USA 2000;97:9026-9031.
28. Dey B, Pancera M, Svehla K, Shu Y, Xiang SH, Vainshtein J, Li Y, Sodroski J, Kwong PD, Mascola JR, Wyatt R. Characterization of human immunodeficiency virus type 1 monomeric and trimeric gp120 glycoproteins stabilized in the CD4-bound state: antigenicity, biophysics, and immunogenicity. J Virol 2007;81:5579-5593.
29. Si Z, Madani N, Cox JM, Chruma JJ, Klein JC, Schon A, Phan N, Wang L, Biorn AC, Cocklin S, Chaiken I, Freire E, Smith AB III, Sodroski JG. Small-molecule inhibitors of HIV-1 entry block receptor-induced conformational changes in the viral envelope glycoproteins. Proc Natl Acad Sci USA 2004;101:5036-5041.
30. Madani N, Perdigoto AL, Srinivasan K, Cox JM, Chruma JJ, LaLonde J, Head M, Smith AB III, Sodroski JG. Localized changes in the gp120 envelope glycoprotein confer resistance to human immunodeficiency virus entry inhibitors BMS-806 and 155. J Virol 2004;78:3742-3752.
31. Zhao Q, Ma L, Jiang S, Lu H, Liu S, He Y, Strick N, Neamati N, Debnath AK. Identification of N-phenyl-N'-(2,2,6,6-tetramethyl-piperidin-4-yl)-oxalamides as a new class of HIV-1 entry inhibitors that prevent gp120 binding to CD4. Virology 2005;339:213-225.
32. Schon A, Madani N, Klein JC, Hubicki A, Ng D, Yang X, Smith AB III, Sodroski J, Freire E. Thermodynamics of binding of a low-molecular-weight CD4 mimetic to HIV-1 gp120. Biochemistry 2006;45:10973-10980.
33. Madani N, Schon A, Princiotto AM, Lalonde JM, Courter JR, Soeta T, Ng D, Wang L, Brower ET, Xiang SH, Kwon YD, Huang CC, Wyatt R, Kwong PD, Freire E, Smith AB III, Sodroski J. Small-molecule CD4 mimics interact with a highly conserved pocket on HIV-1 gp120. Structure 2008;16:1689-1701.
34. Haim H, Si Z, Madani N, Wang L, Courter JR, Princiotto A, Kassa A, DeGrace M, McGee-Estrada K, Mefford M, Gabuzda D, Smith AB III, Sodroski J. Soluble CD4 and CD4-mimetic compounds in-hibit HIV-1 infection by induction of a short-lived activated state. PLoS Pathog 2009;5:e1000360.
35. Ptasek LM, Vijayakumar S, Ravishanker C, Beveridge DL. Molecular dynamics studies of the human CD4 protein. Biopolymers 1994;34:1145-1153.
36. Hsu S-TD, Bonvin AMJJ. Atomic insight into the CD4 binding-induced conformational changes in HIV-1 gp120. Proteins 2004;55:582-593.
37. Hsu S-TD, Peter D, van Gunsteren WF, Bonvin AMJJ. Entropy calculation of HIV-1 Env gp120, its receptor CD4, and their complex: an analysis of configurational entropy changes upon complexation. Biophys J 2005;88:14-24.
38. Liu SQ, Liu SX, Fu YX. Molecular motions of human HIV-1 gp120 envelope glycoproteins. J Mol Model 2008;14:857-870.
39. Pan Y, Ma B, Nussinov R. CD4 binding partially locks the bridging sheet in gp120 but leaves the beta2/3 strands flexible. J Mol Biol 2005;350:514-527.
40. Pan Y, Ma B, Keskin O, Nussinov R. Characterization of the conformational state and flexibility of HIV-1 glycoprotein gp120 core domain. J Biol Chem 2004;279:30523-30530.
41. Tan H, Rader AJ. Identification of putative, stable binding regions through flexibility analysis of HIV-1 gp120. Proteins 2009;74:881-894.
42. Abrams CF, Vanden-Eijnden E. Large-scale conformational sampling of proteins using temperature-accelerated molecular dynamics. Proc Natl Acad Sci USA 2010;107:4961-4966.
43. Jacobs DJ, Rader AJ, Kuhn LA, Thorpe MF. Protein flexibility predictions using graph theory. Proteins 2001;44:150-165.
44. Bahar I, Atilgan AR, Demirel MC, Erman B. Vibrational dynamics of folded proteins: significance of slow and fast modes in relation to function and stability. Phys Rev Lett 1998;80:2733-2736.
45. Haliloglu T, Bahar I, Erman B. Gaussian dynamics of folded proteins. Phys Rev Lett 1997;79:3090-3093.
46. Bahar I, Wallqvist DG, Covell DG, Jernigan RL. Correlation between native-state hydrogen exchange and cooperative residue fluctuations from a simple model. Biochemistry 1998;37:1067-1075.
47. Bahar I, Jernigan RL. Vibrational dynamics of transfer RNAs: a comparison of the free synthetase bound forms. J Mol Biol 1998;281:871-884
48. Yang LW, Bahar I. Coupling between catalytic site and collective Dynamics: a requirement for mechanochemical activity of Enzymes. Structure 2005;13:893-904.
49. Tama F, Wriggers W, Brooks CL III. Exploring global distortions of biological macromolecules and assemblies from low-resolution structural information and elastic network theory. J Mol Biol 2002;321:297-305.
50. Chacon P, Tama F, Wriggers W. Mega-Dalton biomolecular motion captured from electron microscopy reconstructions. J Mol Biol 2003;326:485-492.
51. Chennubhotla C, Bahar I. Signal propagation in proteins and relation to equilibrium fluctuations. PLoS Comput Biol 2007;3:1716-1726.
52. Halle B. Flexibility and packing in proteins. Proc Natl Acad Sci 2002;99:1274-1279.
53. Hinsen K. Structural flexibility in proteins: impact of the crystal environment. Bioinformatics 2008;24:521-528.
54. Eyal E, Yang LW, Bahar I. Anisotropic network model: systematic evaluation and a new web interface. Bioinformatics 2006;22:2619-2627.
55. Bahar I, Atilgan AR, Erman B. Direct evaluation of thermal fluctations in protein, using a single parameter harmonic potentia. Fold Des 1997;2:173-181.
56. Zhou T, Xu L, Dey B, Hessell AJ, Van Ryk D, Xiang SH, Yang X, Zhang MY, Zwick MB, Arthos J, Burton DR, Dimitrov DS, Sodroski J, Wyatt R, Nabel GJ, Kwong PD. Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature 2007;445: 732-737.
57. Olshevsky U, Helseth E, Furman C, Li J, Haseltine W, Sodroski J. Identification of individual human immunodeficiency virus type 1 gp120 amino acids important for CD4 receptor binding. J Virol 1990;64:5701-5707.
58. Cordonnier A, Montagnier L, Emerman M. Single amino-acid changes in HIV envelope affect viral tropism and receptor binding. Nature 1989;340:571-574.
59. VanDerSpoel E, Lindahl B, Hess G, Groenhof AM, Berendsen H. GROMACS fast flexible and free. J Comput Chem 2005;26:1701-1718.
60. Scott WRP, Hunenberger PH, Tironi IG, Mark AE, Billeter SR, Fennen J, Torda AE, Huber T, Kruger P, van Gunsteren WF. The GROMOS biomolecular simulation program package. J Phys Chem A 1999;103:3596-3607.
61. Morra G, Verkhivker C, Colombo G. Modeling singal propogation mechanism and ligand-based conformational dynamics of the Hsp90 molecular chaperone full-length dimer. PLoS Comp Biol 2009;5:e1000323.
62. Xiang SH, Finzi A, Pacheco B, Alexander K, Yuan W, Rizzuto C, Huang CC, Kwong PD, Sodroski J. A V3 loop-dependent gp120 element disrupted by CD4 binding stabilizes the human immuno-deficiency virus envelope glycoprotein trimer. J Virol 2010;84: 3147-3161.
63. Amadei A, Linssen A, Berendsen H. Essential dynamics of proteins. Proteins 1993;17:412-415.
64. Liu J, Bartesaghi A, Borgnia MJ, Sapiro G, Subramaniam S. Molecular architecture of native HIV-1 gp120 trimers. Nature 2008;455:w109-w113.
65. Rizzuto CD, Wyatt R, Hernandez-Ramos N, Sun Y, Kwong PD, Hendrickson WA, Sodroski J. A conserved HIV gp120 glycoprotein structure involved in chemokine receptor binding. Science 1998;280:1949-1953.
66. Haliloglu T, Ben-Tal N. Cooperative transition between open and closed conformations in potassium channels. PLoS Comp Biol 2008;4:e1000164.
67. Potestio R, Pontiggia F, Michelett C. Coarse-grained description of protein internal dynamics: an optimal strategy for decomposing proteins in rigid subunits. Biophys J 2009;96:4993-5002.
68. Word JM, Lovell SC, Richardson JS, Richardson DC. Asparagine and glutamine: using hydrogen atom contacts in the choice of sidechain amide orientation. J Mol Biol 1999;285:1735-1747.
69. Lovell SC, Davis IW, Arendall WB III, de Bakker PI, Word JM, Prisant MG, Richardson JS, Richardson DC. Structure validation by Calpha geometry: phi, psi and Cbeta deviation. Proteins 2003; 50:437-450.
70. MOE 2009.10. Molecular Operating Environment Chemical Computing Group Montreal Canada. http://www.chemcomp.com/.
71. Jorgensen WL, Maxwell DS, Tirado-Rives J. Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J Am Chem Soc 1996;117:11225-11236.
72. Tirion MM. Large amplitude elastic motions in proteins from a single-parameter, atomic analysis. Phys Rev Lett 1996;77:1905-1908.