Association of enhanced HIV-1 neutralization by a single y681h substitution in gp41 with increased gp120-CD4 interaction and macrophage infectivity

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Ringe, Rajesh ^a   Bhattacharya, Jayanta ^a  

^a NATIONAL AIDS RESEARCH INSTITUTE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; EPITOPE; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 41; MONOCLONAL ANTIBODY 4E10; MONOCLONAL ANTIBODY B12; GP120 PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; GP41 PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; NEUTRALIZING ANTIBODY;

AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INDIAN; MACROPHAGE; PROTEIN PROTEIN INTERACTION; PSEUDOTYPING; SENSITIVITY ANALYSIS; VIRAL GENETICS; VIRUS ENVELOPE; VIRUS NEUTRALIZATION; BLOOD; GENETICS; HOST PATHOGEN INTERACTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; PATHOGENICITY; VIROLOGY; VIRUS SHEDDING;

HUMAN IMMUNODEFICIENCY VIRUS 1;

AMINO ACID SUBSTITUTION; ANTIBODIES, NEUTRALIZING; ANTIGENS, CD4; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV ENVELOPE PROTEIN GP41; HIV INFECTIONS; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; MACROPHAGES; VIRUS SHEDDING;

EID: 84860998995     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037157     Document Type: Article

References (84)

1. Walker LM, Burton DR, (2010) Rational antibody-based HIV-1 vaccine design: current approaches and future directions. Curr Opin Immunol 22: 358-366.
2. Pantophlet R, Burton DR, (2006) GP120: target for neutralizing HIV-1 antibodies. Annu Rev Immunol 24: 739-769.
3. Zolla-Pazner S, (2004) Identifying epitopes of HIV-1 that induce protective antibodies. Nat Rev Immunol 4: 199-210.
4. Gnanakaran S, Daniels MG, Bhattacharya T, Lapedes AS, Sethi A, et al. (2010) Genetic signatures in the envelope glycoproteins of HIV-1 that associate with broadly neutralizing antibodies. PLoS Comput Biol 6: e1000955.
5. Wyatt R, Kwong PD, Desjardins E, Sweet RW, Robinson J, et al. (1998) The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393: 705-711.
6. Wyatt R, Sodroski J, (1998) The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280: 1884-1888.
7. Parren PW, Burton DR, (2001) The antiviral activity of antibodies in vitro and in vivo. Adv Immunol 77: 195-262.
8. Phogat S, Wyatt R, (2007) Rational modifications of HIV-1 envelope glycoproteins for immunogen design. Curr Pharm Des 13: 213-227.
9. Moore JP, Cao Y, Ho DD, Koup RA, (1994) Development of the anti-gp120 antibody response during seroconversion to human immunodeficiency virus type 1. J Virol 68: 5142-5155.
10. Tomaras GD, Yates NL, Liu P, Qin L, Fouda GG, et al. (2008) Initial B-cell responses to transmitted human immunodeficiency virus type 1: virion-binding immunoglobulin M (IgM) and IgG antibodies followed by plasma anti-gp41 antibodies with ineffective control of initial viremia. J Virol 82: 12449-12463.
11. Mascola JR, Montefiori DC, (2010) The role of antibodies in HIV vaccines. Annu Rev Immunol 28: 413-444.
12. Frost SD, Wrin T, Smith DM, Kosakovsky Pond SL, Liu Y, et al. (2005) Neutralizing antibody responses drive the evolution of human immunodeficiency virus type 1 envelope during recent HIV infection. Proc Natl Acad Sci U S A 102: 18514-18519.
13. Deeks SG, Schweighardt B, Wrin T, Galovich J, Hoh R, et al. (2006) Neutralizing antibody responses against autologous and heterologous viruses in acute versus chronic human immunodeficiency virus (HIV) infection: evidence for a constraint on the ability of HIV to completely evade neutralizing antibody responses. J Virol 80: 6155-6164.
14. Tremblay M, Wainberg MA, (1990) Neutralization of multiple HIV-1 isolates from a single subject by autologous sequential sera. J Infect Dis 162: 735-737.
15. Bradney AP, Scheer S, Crawford JM, Buchbinder SP, Montefiori DC, (1999) Neutralization escape in human immunodeficiency virus type 1-infected long-term nonprogressors. J Infect Dis 179: 1264-1267.
16. Wei X, Decker JM, Wang S, Hui H, Kappes JC, et al. (2003) Antibody neutralization and escape by HIV-1. Nature 422: 307-312.
17. Gray ES, Moore PL, Choge IA, Decker JM, Bibollet-Ruche F, et al. (2007) Neutralizing antibody responses in acute human immunodeficiency virus type 1 subtype C infection. J Virol 81: 6187-6196.
18. Liu J, Bartesaghi A, Borgnia MJ, Sapiro G, Subramaniam S, (2008) Molecular architecture of native HIV-1 gp120 trimers. Nature 455: 109-113.
19. Kwong PD, Wyatt R, Robinson J, Sweet RW, Sodroski J, et al. (1998) Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393: 648-659.
20. Chen B, Vogan EM, Gong H, Skehel JJ, Wiley DC, et al. (2005) Structure of an unliganded simian immunodeficiency virus gp120 core. Nature 433: 834-841.
21. Finzi A, Xiang SH, Pacheco B, Wang L, Haight J, et al. (2010) Topological layers in the HIV-1 gp120 inner domain regulate gp41 interaction and CD4-triggered conformational transitions. Mol Cell 37: 656-667.
22. Scheid JF, Mouquet H, Feldhahn N, Seaman MS, Velinzon K, et al. (2009) Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature 458: 636-640.
23. Pinter A, Honnen WJ, He Y, Gorny MK, Zolla-Pazner S, et al. (2004) The V1/V2 domain of gp120 is a global regulator of the sensitivity of primary human immunodeficiency virus type 1 isolates to neutralization by antibodies commonly induced upon infection. J Virol 78: 5205-5215.
24. Kwong PD, Doyle ML, Casper DJ, Cicala C, Leavitt SA, et al. (2002) HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature 420: 678-682.
25. Davis KL, Bibollet-Ruche F, Li H, Decker JM, Kutsch O, et al. (2009) Human immunodeficiency virus type 2 (HIV-2)/HIV-1 envelope chimeras detect high titers of broadly reactive HIV-1 V3-specific antibodies in human plasma. J Virol 83: 1240-1259.
26. Aasa-Chapman MM, Hayman A, Newton P, Cornforth D, Williams I, et al. (2004) Development of the antibody response in acute HIV-1 infection. Aids 18: 371-381.
27. Bunnik EM, Pisas L, van Nuenen AC, Schuitemaker H, (2008) Autologous neutralizing humoral immunity and evolution of the viral envelope in the course of subtype B human immunodeficiency virus type 1 infection. J Virol 82: 7932-7941.
28. Li B, Decker JM, Johnson RW, Bibollet-Ruche F, Wei X, et al. (2006) Evidence for potent autologous neutralizing antibody titers and compact envelopes in early infection with subtype C human immunodeficiency virus type 1. J Virol 80: 5211-5218.
29. Arendrup M, Nielsen C, Hansen JE, Pedersen C, Mathiesen L, et al. (1992) Autologous HIV-1 neutralizing antibodies: emergence of neutralization-resistant escape virus and subsequent development of escape virus neutralizing antibodies. J Acquir Immune Defic Syndr 5: 303-307.
30. Richman DD, Wrin T, Little SJ, Petropoulos CJ, (2003) Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc Natl Acad Sci U S A 100: 4144-4149.
31. Draenert R, Allen TM, Liu Y, Wrin T, Chappey C, et al. (2006) Constraints on HIV-1 evolution and immunodominance revealed in monozygotic adult twins infected with the same virus. J Exp Med 203: 529-539.
32. Wu X, Yang ZY, Li Y, Hogerkorp CM, Schief WR, et al. (2010) Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329: 856-861.
33. Walker LM, Huber M, Doores KJ, Falkowska E, Pejchal R, et al. (2011) Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477: 466-470.
34. Walker LM, Phogat SK, Chan-Hui PY, Wagner D, Phung P, et al. (2009) Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326: 285-289.
35. Pejchal R, Walker LM, Stanfield RL, Phogat SK, Koff WC, et al. (2010) Structure and function of broadly reactive antibody PG16 reveal an H3 subdomain that mediates potent neutralization of HIV-1. Proc Natl Acad Sci U S A 107: 11483-11488.
36. Pancera M, McLellan JS, Wu X, Zhu J, Changela A, et al. (2010) Crystal structure of PG16 and chimeric dissection with somatically related PG9: Structure-function analysis of two quaternary-specific antibodies that effectively neutralize HIV-1. J Virol 84: 8098-8110.
37. Haynes BF, Montefiori DC, (2006) Aiming to induce broadly reactive neutralizing antibody responses with HIV-1 vaccine candidates. Expert Rev Vaccines 5: 579-595.
38. Burton DR, Stanfield RL, Wilson IA, (2005) Antibody vs. HIV in a clash of evolutionary titans. Proc Natl Acad Sci U S A 102: 14943-14948.
39. Zhu Z, Qin HR, Chen W, Zhao Q, Shen X, et al. (2011) Cross-reactive HIV-1-neutralizing human monoclonal antibodies identified from a patient with 2F5-like antibodies. J Virol 85: 11401-11408.
40. Morris L, Chen X, Alam M, Tomaras G, Zhang R, et al. (2011) Isolation of a human anti-HIV gp41 membrane proximal region neutralizing antibody by antigen-specific single B cell sorting. PLoS One 6: e23532.
41. Alam SM, McAdams M, Boren D, Rak M, Scearce RM, et al. (2007) The role of antibody polyspecificity and lipid reactivity in binding of broadly neutralizing anti-HIV-1 envelope human monoclonal antibodies 2F5 and 4E10 to glycoprotein 41 membrane proximal envelope epitopes. J Immunol 178: 4424-4435.
42. Haynes BF, Fleming J, St Clair EW, Katinger H, Stiegler G, et al. (2005) Cardiolipin polyspecific autoreactivity in two broadly neutralizing HIV-1 antibodies. Science 308: 1906-1908.
43. Blish CA, Nguyen MA, Overbaugh J, (2008) Enhancing exposure of HIV-1 neutralization epitopes through mutations in gp41. PLoS Med 5: e9.
44. Shen X, Dennison SM, Liu P, Gao F, Jaeger F, et al. (2010) Prolonged exposure of the HIV-1 gp41 membrane proximal region with L669S substitution. Proc Natl Acad Sci U S A 107: 5972-5977.
45. Ringe R, Sharma D, Zolla-Pazner S, Phogat S, Risbud A, et al. (2011) A single amino acid substitution in the C4 region in gp120 confers enhanced neutralization of HIV-1 by modulating CD4 binding sites and V3 loop. Virology 418: 123-132.
46. Ringe R, Thakar M, Bhattacharya J, (2010) Variations in autologous neutralization and CD4 dependence of b12 resistant HIV-1 clade C env clones obtained at different time points from antiretroviral naive Indian patients with recent infection. Retrovirology 7: 76.
47. Ringe R, Phogat S, Bhattacharya J, (2012) Subtle alteration of residues including N-linked glycans in V2 loop modulates HIV-1 neutralization by PG9 and PG16 monoclonal antibodies. Virology 426: 34-41.
48. Platt EJ, Wehrly K, Kuhmann SE, Chesebro B, Kabat D, (1998) Effects of CCR5 and CD4 cell surface concentrations on infections by macrophage tropic isolates of human immunodeficiency virus type 1. J Virol 72: 2855-2864.
49. Kazazi F, Mathijs JM, Foley P, Cunningham AL, (1989) Variations in CD4 expression by human monocytes and macrophages and their relationships to infection with the human immunodeficiency virus. J Gen Virol 70 (Pt 10): 2661-2672.
50. Walter BL, Wehrly K, Swanstrom R, Platt E, Kabat D, et al. (2005) Role of low CD4 levels in the influence of human immunodeficiency virus type 1 envelope V1 and V2 regions on entry and spread in macrophages. J Virol 79: 4828-4837.
51. Peters PJ, Bhattacharya J, Hibbitts S, Dittmar MT, Simmons G, et al. (2004) Biological analysis of human immunodeficiency virus type 1 R5 envelopes amplified from brain and lymph node tissues of AIDS patients with neuropathology reveals two distinct tropism phenotypes and identifies envelopes in the brain that confer an enhanced tropism and fusigenicity for macrophages. J Virol 78: 6915-6926.
52. Peters PJ, Duenas-Decamp MJ, Sullivan WM, Brown R, Ankghuambom C, et al. (2008) Variation in HIV-1 R5 macrophage-tropism correlates with sensitivity to reagents that block envelope: CD4 interactions but not with sensitivity to other entry inhibitors. Retrovirology 5: 5.
53. Kolchinsky P, Kiprilov E, Sodroski J, (2001) Increased neutralization sensitivity of CD4-independent human immunodeficiency virus variants. J Virol 75: 2041-2050.
54. Kolchinsky P, Mirzabekov T, Farzan M, Kiprilov E, Cayabyab M, et al. (1999) Adaptation of a CCR5-using, primary human immunodeficiency virus type 1 isolate for CD4-independent replication. J Virol 73: 8120-8126.
55. Li Y, O'Dell S, Walker LM, Wu X, Guenaga J, et al. (2011) Mechanism of neutralization by the broadly neutralizing HIV-1 monoclonal antibody VRC01. J Virol 85: 8954-8967.
56. Kulkarni SS, Lapedes A, Tang H, Gnanakaran S, Daniels MG, et al. (2009) Highly complex neutralization determinants on a monophyletic lineage of newly transmitted subtype C HIV-1 Env clones from India. Virology 385: 505-520.
57. Brunel FM, Zwick MB, Cardoso RM, Nelson JD, Wilson IA, et al. (2006) Structure-function analysis of the epitope for 4E10, a broadly neutralizing human immunodeficiency virus type 1 antibody. J Virol 80: 1680-1687.
58. Nelson JD, Brunel FM, Jensen R, Crooks ET, Cardoso RM, et al. (2007) An affinity-enhanced neutralizing antibody against the membrane-proximal external region of human immunodeficiency virus type 1 gp41 recognizes an epitope between those of 2F5 and 4E10. J Virol 81: 4033-4043.
59. Montero M, Gulzar N, Klaric KA, Donald JE, Lepik C, et al. (2012) Neutralizing Epitopes in the Membrane-Proximal External Region of HIV-1 gp41 Are Influenced by the Transmembrane Domain and the Plasma Membrane. J Virol 86: 2930-2941.
60. Back NK, Smit L, Schutten M, Nara PL, Tersmette M, et al. (1993) Mutations in human immunodeficiency virus type 1 gp41 affect sensitivity to neutralization by gp120 antibodies. J Virol 67: 6897-6902.
61. Richards KH, Aasa-Chapman MM, McKnight A, Clapham PR, (2010) Modulation of HIV-1 macrophage-tropism among R5 envelopes occurs before detection of neutralizing antibodies. Retrovirology 7: 48.
62. O'Rourke SM, Schweighardt B, Scott WG, Wrin T, Fonseca DP, et al. (2009) Novel ring structure in the gp41 trimer of human immunodeficiency virus type 1 that modulates sensitivity and resistance to broadly neutralizing antibodies. J Virol 83: 7728-7738.
63. Nawaz F, Cicala C, Van Ryk D, Block KE, Jelicic K, et al. (2011) The genotype of early-transmitting HIV gp120s promotes alpha (4) beta(7)-reactivity, revealing alpha (4) beta(7) +/CD4+ T cells as key targets in mucosal transmission. PLoS Pathog 7: e1001301.
64. Musich T, Peters PJ, Duenas-Decamp MJ, Gonzalez-Perez MP, Robinson J, et al. (2011) A Conserved Determinant in the V1 Loop of HIV-1 Modulates the V3 Loop To Prime Low CD4 Use and Macrophage Infection. J Virol 85: 2397-2405.
65. Chen SS, Yang P, Ke PY, Li HF, Chan WE, et al. (2009) Identification of the LWYIK motif located in the human immunodeficiency virus type 1 transmembrane gp41 protein as a distinct determinant for viral infection. J Virol 83: 870-883.
66. Gabuzda DH, Lever A, Terwilliger E, Sodroski J, (1992) Effects of deletions in the cytoplasmic domain on biological functions of human immunodeficiency virus type 1 envelope glycoproteins. J Virol 66: 3306-3315.
67. Yue L, Shang L, Hunter E, (2009) Truncation of the membrane-spanning domain of human immunodeficiency virus type 1 envelope glycoprotein defines elements required for fusion, incorporation, and infectivity. J Virol 83: 11588-11598.
68. Munoz-Barroso I, Durell S, Sakaguchi K, Appella E, Blumenthal R, (1998) Dilation of the human immunodeficiency virus-1 envelope glycoprotein fusion pore revealed by the inhibitory action of a synthetic peptide from gp41. J Cell Biol 140: 315-323.
69. Salzwedel K, West JT, Hunter E, (1999) A conserved tryptophan-rich motif in the membrane-proximal region of the human immunodeficiency virus type 1 gp41 ectodomain is important for Env-mediated fusion and virus infectivity. J Virol 73: 2469-2480.
70. Vishwanathan SA, Hunter E, (2008) The membrane proximal external region (MPER) of HIV-1 gp41: importance of its membrane perturbing properties to viral fusion. J Virol 82: 5118-5126.
71. Saez-Cirion A, Nir S, Lorizate M, Agirre A, Cruz A, et al. (2002) Sphingomyelin and cholesterol promote HIV-1 gp41 pretransmembrane sequence surface aggregation and membrane restructuring. J Biol Chem 277: 21776-21785.
72. Frey G, Peng H, Rits-Volloch S, Morelli M, Cheng Y, et al. (2008) A fusion-intermediate state of HIV-1 gp41 targeted by broadly neutralizing antibodies. Proc Natl Acad Sci U S A 105: 3739-3744.
73. Sun ZY, Oh KJ, Kim M, Yu J, Brusic V, et al. (2008) HIV-1 broadly neutralizing antibody extracts its epitope from a kinked gp41 ectodomain region on the viral membrane. Immunity 28: 52-63.
74. Song L, Sun ZY, Coleman KE, Zwick MB, Gach JS, et al. (2009) Broadly neutralizing anti-HIV-1 antibodies disrupt a hinge-related function of gp41 at the membrane interface. Proc Natl Acad Sci U S A 106: 9057-9062.
75. Walker LM, Simek MD, Priddy F, Gach JS, Wagner D, et al. (2010) A limited number of antibody specificities mediate broad and potent serum neutralization in selected HIV-1 infected individuals. PLoS Pathog 6.
76. Zhou T, Xu L, Dey B, Hessell AJ, Van Ryk D, et al. (2007) Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature 445: 732-737.
77. Freed EO, Englund G, Martin MA, (1995) Role of the basic domain of human immunodeficiency virus type 1 matrix in macrophage infection. J Virol 69: 3949-3954.
78. Li M, Gao F, Mascola JR, Stamatatos L, Polonis VR, et al. (2005) Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. J Virol 79: 10108-10125.
79. Richards KH, Clapham PR, (2007) Effects of vpu start-codon mutations on human immunodeficiency virus type 1 replication in macrophages. J Gen Virol 88: 2780-2792.
80. O'Doherty U, Swiggard WJ, Malim MH, (2000) Human immunodeficiency virus type 1 spinoculation enhances infection through virus binding. J Virol 74: 10074-10080.
81. Hioe CE, Wrin T, Seaman MS, Yu X, Wood B, et al. (2010) Anti-V3 monoclonal antibodies display broad neutralizing activities against multiple HIV-1 subtypes. PLoS One 5: e10254.
82. Davis MR, Jiang J, Zhou J, Freed EO, Aiken C, (2006) A mutation in the human immunodeficiency virus type 1 Gag protein destabilizes the interaction of the envelope protein subunits gp120 and gp41. J Virol 80: 2405-2417.
83. Haim H, Si Z, Madani N, Wang L, Courter JR, et al. (2009) Soluble CD4 and CD4-mimetic compounds inhibit HIV-1 infection by induction of a short-lived activated state. PLoS Pathog 5: e1000360.
84. Wilen CB, Parrish NF, Pfaff JM, Decker JM, Henning EA, et al. (2011) Phenotypic and Immunologic Comparison of Clade B Transmitted/Founder and Chronic HIV-1 Envelope Glycoproteins. J Virol 85: 8514-8527.