Understanding the binding mode and function of BMS-488043 against HIV-1 viral entry

Proteins: Structure, Function and Bioinformatics

Volumn 79, Issue 6, 2011, Pages 1810-1819

  Da, Lin Tai ^a   Quan, Jun Min ^a   Wu, Yun Dong ^a,b  

^a PEKING UNIVERSITY   (China)

^b HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

Author keywords

Binding mode; BMS 488043; Bridging sheeting; Gp120; Viral entry

Indexed keywords

1 BENZOYL 4 [(4,7 DIMETHOXY 1H PYRROLO[2,3 C]PYRIDIN 3 YL)OXOACETYL]PIPERAZINE; CD4 ANTIGEN; GLYCOPROTEIN GP 120; MIDOSTAURIN;

ALPHA HELIX; ANTIVIRAL ACTIVITY; ARTICLE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; DRUG BINDING; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR DOCKING; MOLECULAR DYNAMICS; PRIORITY JOURNAL; VIRUS ENTRY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 79955744829     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.23005     Document Type: Article

References (83)

1. Chan DC, Chutkowski CT, Kim PS. Evidence that a prominent cavity in the coiled coil of HIV type 1 gp41 is an attractive drug target. Proc Natl Acad Sci USA 1998; 95: 15613-15617.
2. Chan DC, Kim PS. HIV Entry and its inhibition. Cell 1998; 93: 681-684.
3. Eckert DM, Malashkevich VN, Hong LH, Carr PA, Kim PS. Inhibiting HIV-1 entry. Cell 1999; 99: 103-115.
4. Eckert DM, Kim PS. Design of potent inhibitors of HIV-1 entry from the gp41 N-peptide region. Proc Natl Acad Sci USA 2001; 98: 11187-11192.
5. Sia SK, Carr PA, Cochran AG, Malashkevich VN, Kim PS. Short constrained peptides that inhibit HIV-1 entry. Proc Natl Acad Sci USA 2002; 99: 14664-14669.
6. Root MJ, Kay MS, Kim PS. Protein design of an HIV-1 entry inhibitor. Science 2001; 291: 884-888.
7. Moore JP, Doms RW. The entry of entry inhibitors: a fusion of science and medicine. Proc Natl Acad Sci USA 2003; 100: 10598-10602.
8. Schon A, Madani N, Klein JC, Hubicki A, Ng D, Yang XZ, Smith ABIII, Sodroski J, Freire E. Thermodynamics of binding of a low-molecular-weight CD4 mimetic to HIV-1 gp120. Biochemistry 2006; 45: 10973-10980.
9. Welch BD, VanDemark AP, Heroux A, Hill CP, Kay MS. Potent D-peptide inhibitors of HIV-1 entry. Proc Natl Acad Sci USA 2007; 104: 16828-16833.
10. Esté J, Telenti A. HIV entry inhibitors. Lancet 2007; 370: 81-88.
11. Xie H, Ng D, Savinov SN, Dey B, Kwong PD, Wyatt R, Smith ABIII, 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.
12. Madani N, Schon A, Princiotto AM, LaLonde JM, Courter JR, Soeta T, Ng D, Wang LP, Brower ET, Xiang SH, Kwon YD, Huang CC, Wyatt R, Kwong PD, Freire E, Smith ABIII, Sodroski J. Small-molecule CD4 mimics interact with a highly conserved pocket on HIV-1 gp120. Structure 2008; 16: 1689-1701.
13. Lu M, Blacklow SC, Kim PS. A trimeric structural domain of the HIV-1 transmembrane glycoprotein. Nat Struct Bio 1995; 2: 1075-1082.
14. Wyatt R, Sodroski J. The HIV-1 envelope glycoproteins: fusogens. antigens, and immunogens. Science 1998; 280: 1884-1888.
15. Liu J, Alberto A, Borgnia MJ, Sapiro G, Subramaniam S. Molecular architecture of native HIV-1 gp120 trimers. Nature 2008; 455: 109-113.
16. Zhu P, Liu J, Bess JJr, Chertova E, Lifson JD Grise H, Ofek GA, Taylor KA, Roux KH. Distribution and three-dimensional structure of AIDS virus envelope spikes. Nature 2006; 441: 847-852.
17. Klatzmann D, Champagne E, Chamaret S, Gruest J, Guetard D, Hercend T, Gluckman JC, Montagnier L. T-lymphocyte T4 molecule behaves as the receptor for human retrovirus LAV. Nature 1984; 312: 767-768.
18. Dalgleish AG, Beverley PCL, 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.
19. Moore JP, McKeating JA, Weiss RA, Sattentau QJ. Dissociation of gp120 from HIV-1 virions induced by soluble CD4. Science 1990; 250: 1139-1142.
20. 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 β-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 1996; 85: 1135-1148.
21. 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.
22. 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 β-chemokine receptors CKR-5. CKR-3, and CKR-2b as fusion cofactors. Cell 1996; 85: 1149-1158.
23. Feng Y, Broder CC, Kennedy PE, Berger EA. HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane. G protein-coupled receptor. Science 1996; 272: 872-877.
24. Wu L, Gerard NP, Wyatt R, Choe H, Parolin C, Ruffing N, Borsetti A, Cardoso AA, Desjardin E, Newman W, Gerard Sodroski J. CD4-induced interaction of primary HIV-1 gp120 glycoproteins with the chemokine receptor CCR-5. Nature 1996; 384: 179-183.
25. Trkola A, Dragic T, Arthos J, Binley JM, Olson WC, Allaway GP, Cheng-Mayer C, Robinson J, Maddon PJ, Moore JP. CD4-dependent, antibody-sensitive interactions between HIV-1 and its co-receptor CCR-5. Nature 1996; 384: 184-187.
26. Huang CC, Lam SN, Acharya P, Tang M, Xiang SH, Hussan SS, Stanfield RL, Robinson J, Sodroski J, Wilson IA, Wyatt R, Bewley CA, Kwong PD. Structures of the CCR5 N terminus and of a tyrosine-sulfated antibody with HIV-1 gp120 and CD4. Science 2007; 317: 1930-1934.
27. Forsell MNE, Dey B, Mörner A, Svehla K, O'dell S, Högerkorp CM, Voss G, Thorstensson R, Shaw GM, Mascola JR, Hedestam GBK, Wyatt RT. B cell recognition of the conserved HIV-1 co-receptor binding site is altered by endogenous primate CD4. PLoS Pathogens 2008; 4: e1000171.
28. D'souza MP, Harden VA. Chemokines and HIV-1 second receptors. Nat Med 1996; 2: 1293-1300.
29. 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.
30. Chan DC, Fass D, Berger JM, Kim PS. Core Structure of gp41 from the HIV envelope glycoprotein. Cell 1997; 89: 263-273.
31. Tan K, Liu J, Wang J, Shen S, Lu M. Atomic structure of a thermostable subdomain of HIV-1gp41. Proc Natl Acad Sci USA 1997; 94: 12303-12308.
32. Weissenhorn W, Dessen A, Harrison SC, Skehel JJ, Wiley DC. Atomic structure of the ectodomain from HIV-1 gp41. Nature 1997; 387: 426-430.
33. Furuta RA, Wild CT, Weng Y, Weiss CD. Capture of an early fusion-active conformation of HIV-1 gp41. Nat Struct Biol 1998; 5: 276-279.
34. Rits-Volloch S, Frey G, Harrison SC, Chen B. Restraining the conformation of HIV-1 gp120 by removing a flexible loop. EMBO J 2006; 25: 5026-5035.
35. 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.
36. Wyatt R, Kwong PD, Desjardins E, Sweet RW, Robinson J, Hendrickson WA, Sodroski JG. The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 1998; 393: 705-711.
37. 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.
38. 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 2000; 8: 1329-1339.
39. Kwong PD, Doyle ML, Casper DJ, Cicala C, Leavitt SA, Majeed S, Steenbeke T.D.Venturi M, Chaiken I, Fung M, Katinger H, Parren PW, Robinson JVan RD, Wang L, Burton DR, Freire E, Wyatt R, Sodroski J, Hendrickson WA, Arthos J. HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature 2002; 420: 678-682.
40. 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.
41. Zhou TQ, Xu L, Dey B, Hessell AJ, Van RD, Xiang SH, Yang X, Zhang MY, Zwick MB, Arthos J, Burthon 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.
42. Kwong PD. Human immunodeficiency virus: refolding the envelope. Nature 2005; 433: 815-816.
43. Diskin R, Marcovecchio PM, Bjorkman AJ. Structure of a clade C HIV-1 gp120 bound to CD4 and CD4-induced antibody reveals anti-CD4 polyreactivity. Nat Struct Mol Bio 2010; 17: 608-613.
44. Flexner C. HIV drug development: the next 25 years. Nat Rev Drug Dis 2007; 6: 959-966.
45. Clercq ED. Anti-HIV drugs: 25 compounds approved within 25 years after the discovery of HIV. Inter J Anti Age 2009; 33: 307-320.
46. Baleux F, Loureiro-Morais L, Hersant Y, Clayette P, Arenzana-Seisdedos F, Bonnaffé D Lortat-Jacob H. A synthetic CD4-heparan sulfate glycoconjugate inhibits CCR5 and CXCR4 HIV-1 attachment and entry. Nat Chem Bio 2009; 5: 743-748.
47. Tilton JC, Doms RW. Entry inhibitors in the treatment of HIV-1 infection. Anti Res 2010; 85: 91-100.
48. Wild C, Greenwell T, Matthews T. A synthetic peptide from HIV-1 gp41 is a potent inhibitor of virus mediated cell-cell fusion. AIDS Res Hum Retroviruses 1993; 9: 1051-1053.
49. Matthews T, Salgo M, Greenberg M, Chung J, DeMasi R, Bolognesi D. Enfuvirtide: the first therapy to inhibit the entry of HIV-1 into host CD4 lymphocytes. Nat Rev Drug Discovery 2004; 3: 215-225.
50. Wang T, Zhang ZX, Wallace OB, Deshpande M, Fang HQ, Yang Z, Zadjura LM, Tweedie DL, Huang S, Zhao F, Ranadive S, Robinson BS, Gong YF, Ricarrdi K, Spicer TP, Deminie C, Rose R, Wang HGH, Blair WS, Shi PY, Liu PF, Colonno RJ, Nicholas AM. Discovery of 4-Benzoyl-1-[(4-methoxy-1H- pyrrolo [2, 3-b]pyridin-3-yl)oxoacetyl]-2- (R)-methylpiperazine (BMS-378806): a Novel HIV-1 attachment inhibitor that interferes with CD4-gp120 interactions. J Med Chem 2003; 46: 4236-4239.
51. Wang HG, Williams RE, Lin PF. A novel class of HIV-1 inhibitors that targets the viral envelope and inhibits CD4 receptor binding. Curr Pharm Des 2004; 10: 1785-1793.
52. Lin PF, Blair W, Wang T, Spicer T, Guo Q, Zhou NN, Gong YF, Wang HGHD, Rose R, Yamanaka G, Robinson B, Li CB, Fridell R, Deminie C, Demers G, Yang Z, Zadjura L, Meanwell N, Colonno R. A small molecule HIV-1 inhibitor that targets the HIV-1 envelope and inhibits CD4 receptor binding. Proc Natl Acad Sci USA 2003; 100: 11013-11018.
53. Guo Q, Ho HT, Dicker I, Fan L, Zhou NN, Friborg J, Wang T, McAuliffe BV, Wang HGHD, Rose R, Fang H, Scarnati HT, Langley DR, Meanwell NA, Abraham R, Colonno RJ, Lin PF. Biochemical and genetic characterizations of a novel human immunodeficiency virus Type 1 inhibitor that blocks gp120-CD4 interactions. J Viro 2003; 77: 10528-10536.
54. Ho HT, Fan L, Nowicka-Sans BB, McAuliffe B, Li CB, Yamanaka G, Zhou NN, Fang H, Dicker I, Dalterio R, Gong YF, Wang T, Yin ZW, Ueda Y, Matiskella J, Kadow J, Clapham P, Robinson J, Colonno R, Lin PF. Envelope conformational changes induced by human immunodeficiency virus type 1 attachment inhibitors prevent CD4 binding and downstream entry events. J Viro 2006; 80: 4017-4025.
55. Wang T, Yin ZW, Zhang ZX, Bender JA, Yang Z, Johnson G, Yang Z, Zadjura LM, D'Arienzo CJ, Parker DD, Gesenberg C, Yamanaka GA, Gong YF, Ho HT, Fang H, Zhou NN, McAuliffe BV, Eggers BJ, Fan L, Nowicka-Sans B, Dicker IB, Gao Q, Colonno RJ, Lin PF, Meanwell NA, Kadow JF. Inhibitors of human immunodeficiency virus type 1 (HIV-1) attachment. 5. An evolution from indole to azaindoles leading to the discovery of 1-(4-benzoylpiperazin-1-yl)-2-(4, 7-dimethoxy-1H-pyrrolo[2, 3-c]pyridin-3-yl) ethane-1, 2-dione (BMS-488043), a drug candidate that demonstrates antiviral activity in HIV-1-infected subjects. J Med Chem 2009; 52: 7778-7787.
56. Si ZH, Madani N, Cox JM, Chruma JJ, Klein JC, Schon A, Phan N, Wang LP, Biorn AC, Cocklin S, Chaiken I, Freire E, Smith ABIII, 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.
57. Madani N, Perdigoto AL, Srinivasan K, Cox JM, Chruma JJ, LaLonde J, Head M, Smith ABIII, Sodroski JG. Localized changes in the gp120 envelope glycoprotein confer resistance to human immunodeficiency virus entry inhibitors BMS-806 and # 155. J Viro 2004; 78: 3742-3752.
58. Kong R, Tan JJ, Ma XH, Chen W, Wang CX. Prediction of the binding mode between BMS-378806 and HIV-1 gp120 by docking and molecular dynamics simulation. Biochim Biophys Acta 2006; 1764: 766-767.
59. Teixeira C, Serradji N, Maurel F, Barbault F. Docking and 3D-QSAR studies of BMS-806 analogs as HIV-1 gp120 entry inhibitors. Euro J Med Chem 2009; 44: 3524-3532.
60. Berro R, Sanders RW, Lu M, Klasse PJ, Moore JP. Two HIV-1 variants resistant to small molecule CCR5 inhibitors differ in how they use CCR5 for entry. PloS Pathogens 2009; 5: e1000548.
61. Da LT, Quan JM, Wu YD. Understanding of the bridging sheet formation of HIV-1 glycoprotein gp120. J Phys Chem B 2009; 113: 14536-14543.
62. Xiang SH, Kwong PD, Gupta R, Rizzuto CD, Casper DJ, Wyatt R, Wang LP, Hendrickson WA, Doyle ML, Sodroski J. Mutagenic stabilization and/or disruption of a CD4-bound state reveals distinct conformations of the human immunodeficiency virus type 1 gp120 envelope glycoprotein. J Virol 2002; 76: 9888-9899.
63. 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.
64. Dey B, Svehla K, Xu L, Wycuff D, Zhou TQ, Voss G, Phogat A, Chakrabarti BK, Li YX, Shaw G, Kwong PD, Nabel GJ, Mascola JR, Wyatt RT. Structure-based stabilization of HIV-1 gp120 enhances humoral immune responses to the induced co-receptor binding site. PLoS Pathogens 2009; 5: e1000445.
65. Mörner A, Douagi I, Forsell MNE, Sundling C, Dosenovic P, O'Dell S, Dey B, Kwong PD, Voss G, Thorstensson R, Mascola JR, Wyatt RT, Hedestam GBK. Human immunodeficiency virus type 1 env trimer immunization of macaques and impact of priming with viral vector or stabilized core protein. J Virol 2009; 83: 540-551.
66. Chen L, Kwon YD, Zhou TQ, Wu XL, O'Dell S, Cavacini L, Hessell AJ, Pancera M, Tang Min, Xu L, Yang ZY, Zhang MY, 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.
67. H-gene usage in antibodies that recognize the HIV type 1 coreceptor-binding site on gp120. Proc Natl Acad Sci USA 2004; 101: 2706-2711.
68. 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.
69. Morris G, M, Huey R, Lindstrom W, Sanner MF, Belew RK, Goodsell DS, Olson AJ. AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J Comput Chem 2009; 30: 2785-2791.
70. Lindahl E, Hess B, Van der Spoel D. GROMACS 3.0: A package for molecular simulation and trajectory analysis. J Mol Mod 2001; 7: 306-317.
71. Price MLP, Ostrovsky D, Jorgensen WL. Gas-phase and liquid-state properties of esters, nitriles, and nitro compounds with the OPLS-AA force field. J Comput Chem 2001; 22: 1340-1352.
72. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. Comparison of simple potential functions for simulating liquid water. J Chem Phys 1983; 79: 926-935.
73. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG. A smooth particle mesh Ewald method. J Chem Phys 1995; 103: 8577-8592.
74. Berendsen HJC, Postma JPM, Van Gunsteren WF, Di Nola A, Haak JR. Molecular dynamics with coupling to an external bath. J Chem Phys 1984; 81: 3684-3690.
75. Hess B, Bekker H, Berendsen HLC, Fraaije JGEM. LINCS: A linear constraint solver for molecular simulations. J Comput Chem 1997; 18: 1463-1472.
76. 2 in noncrystalline environments show a subunit transition from the open to the closed conformation. Protein Sci 1996; 5: 62-71.
77. Hayward S, Kitao A, Berendsen HJC. Model-free methods of analyzing domain motions in proteins from simulation: a comparison of normal mode analysis and molecular dynamics simulation of lysozyme. Proteins 1997; 27: 425-437.
78. Kitao A, Hayward S, Go N. Analysis of domain motions by approximate normal mode calculations. Proteins 1998; 33: 425-437.
79. Pancera M, Majeed S, Ban YA, Chen L, Huang CC, Kong L, Kwon YD, Stuckey J, Zhou TQ, 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 2009; 107: 1166-1171.
80. Kassa A, Madani N, Schön A, Haim H, Finzi A, Xiang SH, Wang LP, Princiotto A, Pancera M, Courter J, Smith ABIII, Freire E, Kwong PD, Sodroski J. Transitions to and from the CD4-bound conformation are modulated by a single-residue change in the human immunodeficiency virus type 1 gp120 inner domain. J Virol 2009; 83: 8364-8378.
81. Finzi A, Xiang SH, Pacheco B, Wang LP, Haight J, Kassa A, Danek B, Pancera M, Kwong PD, Sodroski J. Topological layers in the HIV-1 gp120 inner domain regulate gp41 interaction and CD4-triggered conformational transitions. Molecular Cell 2010; 37: 656-667.
82. Meanwell N, A, Wallace OB, Fang HQ, Wang H, Deshpande M, Wang T, Yin ZW, Zhang ZX, Pearce BC, James J, Yeung KS, Qiu ZL, Wright JJK, Yang Zheng, Zadjura L, Tweedie DL, Yeola S, Zhao F, Ranadive S, Robinson BA, Gong YF, Wang HGH, Blair WS, Shi PY, Colonn RJ, Lin PF. Inhibitors of HIV-1 attachment. Part 2: an initial survey of indole substitution patterns Bio Med Chem Lett 2009; 19: 1977-1981.
83. Lu RJ, Tucker JA, Pickens J, Ma YA, Zinevitch T, Kirichenko O, Konoplev V, Kuznetsova S, Sviridov S, Brahmachary E, Khasanov A, Mikel C, Yang Y, Liu C.H.Wang J, Freel S, Fisher S, Sullivan A, Zhou JY, Stanfield-Oakley S, Baker B, Sailstad J, Greenberg M, Bolognesi D, Bray B, Koszalka B, Jeffs P, Jeffries C, Chucholowski A, Sexton C. Heterobiaryl human immunodeficiency virus entry inhibitors. J Med Chem 2009; 52: 4481-4487.