Viral Escape from Neutralizing Antibodies in Early Subtype A HIV-1 Infection Drives an Increase in Autologous Neutralization Breadth

PLoS Pathogens

Volumn 9, Issue 2, 2013, Pages

  Murphy, Megan K ^a   Yue, Ling ^a   Pan, Ruimin ^b   Boliar, Saikat ^a   Sethi, Anurag ^c   Tian, Jianhui ^c   Pfafferot, Katja ^d   Karita, Etienne ^e   Allen, Susan A ^a,f   Cormier, Emmanuel ^g   Goepfert, Paul A ^h   Borrow, Persephone ^d   Robinson, James E ⁱ   Gnanakaran, S ^c   Hunter, Eric ^a,f   Kong, Xiang Peng ^b   Derdeyn, Cynthia A ^a,f  

^a EMORY UNIVERSITY   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c LOS ALAMOS NATIONAL LABORATORY   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e Projet San Francisco   (Rwanda)

^f EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g INTERNATIONAL AIDS VACCINE INITIATIVE   (United States)

^h University of Alabama at Birmingham   (United States)

ⁱ TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 120; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN LIGHT CHAIN; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY;

AFFINITY CHROMATOGRAPHY; AMINO ACID SEQUENCE; ARTICLE; BIOTINYLATION; CELL CULTURE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCAPE BEHAVIOR; GLYCOSYLATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMORAL IMMUNITY; MOLECULAR MODEL; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; VIRUS LOAD; VIRUS NEUTRALIZATION;

AMINO ACID SEQUENCE; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CROSS REACTIONS; FEMALE; HIV INFECTIONS; HIV SEROPOSITIVITY; HIV-1; HUMANS; IMMUNE EVASION; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN LIGHT CHAINS; MALE; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT;

EID: 84877626973     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003173     Document Type: Article

References (85)

1. Plotkin SA, (2010) Correlates of protection induced by vaccination. Clin Vaccine Immunol 17: 1055-1065.
2. Haynes BF, Gilbert PB, McElrath MJ, Zolla-Pazner S, Tomaras GD, et al. (2012) Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med 366: 1275-1286.
3. Barouch DH, Liu J, Li H, Maxfield LF, Abbink P, et al. (2012) Vaccine protection against acquisition of neutralization-resistant SIV challenges in rhesus monkeys. Nature 482: 89-93.
4. Nabel GJ, Kwong PD, Mascola JR, (2011) Progress in the rational design of an AIDS vaccine. Philos Trans R Soc Lond B Biol Sci 366: 2759-2765.
5. Falkowska E, Ramos A, Feng Y, Zhou T, Moquin S, et al. (2012) PGV04, an HIV-1 gp120 CD4 Binding Site Antibody, Is Broad and Potent in Neutralization but Does Not Induce Conformational Changes Characteristic of CD4. J Virol 86: 4394-4403.
6. 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.
7. Zhou T, Georgiev I, Wu X, Yang ZY, Dai K, et al. (2010) Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329: 811-817.
8. Pejchal R, Doores KJ, Walker LM, Khayat R, Huang PS, et al. (2011) A potent and broad neutralizing antibody recognizes and penetrates the HIV glycan shield. Science 334: 1097-1103.
9. Zwick MB, Labrijn AF, Wang M, Spenlehauer C, Saphire EO, et al. (2001) Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J Virol 75: 10892-10905.
10. 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.
11. Huang J, Ofek G, Laub L, Louder MK, Doria-Rose NA, et al. (2012) Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature 491: 406-412.
12. McLellan JS, Pancera M, Carrico C, Gorman J, Julien JP, et al. (2011) Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 480: 336-343.
13. Wu X, Zhou T, Zhu J, Zhang B, Georgiev I, et al. (2011) Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing. Science 333: 1593-1602.
14. 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.
15. Scheid JF, Mouquet H, Ueberheide B, Diskin R, Klein F, et al. (2011) Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 333: 1633-1637.
16. Mikell I, Sather DN, Kalams SA, Altfeld M, Alter G, et al. (2011) Characteristics of the earliest cross-neutralizing antibody response to HIV-1. PLoS Pathog 7: e1001251.
17. Gray ES, Madiga MC, Hermanus T, Moore PL, Wibmer CK, et al. (2011) The neutralization breadth of HIV-1 develops incrementally over four years and is associated with CD4+ T cell decline and high viral load during acute infection. J Virol 85: 4828-4840.
18. Simek MD, Rida W, Priddy FH, Pung P, Carrow E, et al. (2009) Human immunodeficiency virus type 1 elite neutralizers: individuals with broad and potent neutralizing activity identified by using a high-throughput neutralization assay together with an analytical selection algorithm. J Virol 83: 7337-7348.
19. Verkoczy L, Diaz M, Holl TM, Ouyang YB, Bouton-Verville H, et al. (2010) Autoreactivity in an HIV-1 broadly reactive neutralizing antibody variable region heavy chain induces immunologic tolerance. Proc Natl Acad Sci U S A 107: 181-186.
20. Sather DN, Armann J, Ching LK, Mavrantoni A, Sellhorn G, et al. (2009) Factors associated with the development of cross-reactive neutralizing antibodies during human immunodeficiency virus type 1 infection. J Virol 83: 757-769.
21. Racanelli V, Brunetti C, De Re V, Caggiari L, De Zorzi M, et al. (2011) Antibody V(h) repertoire differences between resolving and chronically evolving hepatitis C virus infections. PLoS One 6: e25606.
22. Huang CC, Venturi M, Majeed S, Moore MJ, Phogat S, et al. (2004) Structural basis of tyrosine sulfation and VH-gene usage in antibodies that recognize the HIV type 1 coreceptor-binding site on gp120. Proc Natl Acad Sci U S A 101: 2706-2711.
23. Moore PL, Gray ES, Hermanus T, Sheward D, Tumba N, et al. (2011) Evolution of HIV-1 Transmitted/Founder Viruses Results in the Formation of Epitopes for Later Broadly Cross-Neutralizing Antibodies. In: Retroviruses ARaH, editor. AIDS Vaccine 2011. Bangkok, Thailand: Mary Ann Liebert, Inc.
24. Moore PL, Gray ES, Wibmer CK, Bhiman JN, Nonyane M, et al. (2012) Evolution of an HIV glycan-dependent broadly neutralizing antibody epitope through immune escape. Nat Med 18: 1688-1692.
25. Bar KJ, Tsao CY, Iyer SS, Decker JM, Yang Y, et al. (2012) Early Low-Titer Neutralizing Antibodies Impede HIV-1 Replication and Select for Virus Escape. PLoS Pathog 8: e1002721.
26. 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.
27. Wei X, Decker JM, Wang S, Hui H, Kappes JC, et al. (2003) Antibody Neutralization and Escape by HIV-1. Nature 422: 307-312.
28. Moore PL, Ranchobe N, Lambson BE, Gray ES, Cave E, et al. (2009) Limited neutralizing antibody specificities drive neutralization escape in early HIV-1 subtype C infection. PLoS Pathog 5: e1000598.
29. Rong R, Li B, Lynch RM, Haaland RE, Murphy MK, et al. (2009) Escape from autologous neutralizing antibodies in acute/early subtype C HIV-1 infection requires multiple pathways. PLoS Pathog 5: e1000594.
30. Bosch KA, Rainwater S, Jaoko W, Overbaugh J, (2009) Temporal analysis of HIV envelope sequence evolution and antibody escape in a subtype A-infected individual with a broad neutralizing antibody response. Virology 398: 115-124.
31. Lynch RM, Rong R, Boliar S, Sethi A, Li B, et al. (2011) The B cell response is redundant and highly focused on V1V2 during early subtype C infection in a Zambian seroconverter. J Virol 85: 905-915.
32. Volpe JM, Cowell LG, Kepler TB, (2006) SoDA: implementation of a 3D alignment algorithm for inference of antigen receptor recombinations. Bioinformatics 22: 438-444.
33. Kabat EA, Wu TT, (1991) Identical V region amino acid sequences and segments of sequences in antibodies of different specificities. Relative contributions of VH and VL genes, minigenes, and complementarity-determining regions to binding of antibody-combining sites. J Immunol 147: 1709-1719.
34. Sanders RW, Venturi M, Schiffner L, Kalyanaraman R, Katinger H, et al. (2002) The mannose-dependent epitope for neutralizing antibody 2G12 on human immunodeficiency virus type 1 glycoprotein gp120. J Virol 76: 7293-7305.
35. Scanlan CN, Pantophlet R, Wormald MR, Ollmann Saphire E, Stanfield R, et al. (2002) The broadly neutralizing anti-human immunodeficiency virus type 1 antibody 2G12 recognizes a cluster of alpha1→2 mannose residues on the outer face of gp120. J Virol 76: 7306-7321.
36. Moore PL, Gray ES, Choge IA, Ranchobe N, Mlisana K, et al. (2007) The C3-V4 Region Is a Major Target of Autologous Neutralizing Antibodies in Hiv-1 Subtype C Infection. J Virol 82: 1860-9.
37. 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.
38. Tang H, Robinson JE, Gnanakaran S, Li M, Rosenberg ES, et al. (2011) Epitopes immediately below the base of the V3 loop of gp120 as targets for the initial autologous neutralizing antibody response in two HIV-1 subtype B-infected individuals. J Virol 85: 9286-9299.
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. Bonsignori M, Hwang KK, Chen X, Tsao CY, Morris L, et al. (2011) Analysis of a clonal lineage of HIV-1 envelope V2/V3 conformational epitope-specific broadly neutralizing antibodies and their inferred unmutated common ancestors. J Virol 85: 9998-10009.
41. Gorny MK, Sampson J, Li H, Jiang X, Totrov M, et al. (2011) Human Anti-V3 HIV-1 Monoclonal Antibodies Encoded by the VH5-51/VL Lambda Genes Define a Conserved Antigenic Structure. PLoS One 6: e27780.
42. Gorny MK, Wang XH, Williams C, Volsky B, Revesz K, et al. (2009) Preferential use of the VH5-51 gene segment by the human immune response to code for antibodies against the V3 domain of HIV-1. Mol Immunol 46: 917-926.
43. Diskin R, Scheid JF, Marcovecchio PM, West AP Jr, Klein F, et al. (2011) Increasing the potency and breadth of an HIV antibody by using structure-based rational design. Science 334: 1289-1293.
44. Changela A, Wu X, Yang Y, Zhang B, Zhu J, et al. (2011) Crystal structure of human antibody 2909 reveals conserved features of quaternary structure-specific antibodies that potently neutralize HIV-1. J Virol 85: 2524-2535.
45. MacDonald KS, Embree J, Njenga S, Nagelkerke NJ, Ngatia I, et al. (1998) Mother-child class I HLA concordance increases perinatal human immunodeficiency virus type 1 transmission. J Infect Dis 177: 551-556.
46. Malherbe DC, Doria-Rose NA, Misher L, Beckett T, Puryear WB, et al. (2011) Sequential immunization with a subtype B HIV-1 envelope quasispecies partially mimics the in vivo development of neutralizing antibodies. J Virol 85: 5262-5274.
47. Haaland RE, Hawkins PA, Salazar-Gonzalez J, Johnson A, Tichacek A, et al. (2009) Inflammatory genital infections mitigate a severe genetic bottleneck in heterosexual transmission of subtype A and C HIV-1. PLoS Pathog 5: e1000274.
48. Price MA, Wallis CL, Lakhi S, Karita E, Kamali A, et al. (2011) Transmitted HIV type 1 drug resistance among individuals with recent HIV infection in East and Southern Africa. AIDS Res Hum Retroviruses 27: 5-12.
49. Salazar-Gonzalez JF, Bailes E, Pham KT, Salazar MG, Guffey MB, et al. (2008) Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by single-genome amplification and sequencing. J Virol 82: 3952-3970.
50. Blish CA, Nedellec R, Mandaliya K, Mosier DE, Overbaugh J, (2007) HIV-1 subtype A envelope variants from early in infection have variable sensitivity to neutralization and to inhibitors of viral entry. Aids 21: 693-702.
51. Long EM, Rainwater SM, Lavreys L, Mandaliya K, Overbaugh J, (2002) HIV type 1 variants transmitted to women in Kenya require the CCR5 coreceptor for entry, regardless of the genetic complexity of the infecting virus. AIDS Res Hum Retroviruses 18: 567-576.
52. Poss M, Overbaugh J, (1999) Variants from the diverse virus population identified at seroconversion of a clade A human immunodeficiency virus type 1-infected woman have distinct biological properties. J Virol 73: 5255-5264.
53. 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.
54. Kothe DL, Decker JM, Li Y, Weng Z, Bibollet-Ruche F, et al. (2007) Antigenicity and immunogenicity of HIV-1 consensus subtype B envelope glycoproteins. Virology 360: 218-234.
55. Kothe DL, Li Y, Decker JM, Bibollet-Ruche F, Zammit KP, et al. (2006) Ancestral and consensus envelope immunogens for HIV-1 subtype C. Virology 352: 438-449.
56. Li M, Salazar-Gonzalez JF, Derdeyn CA, Morris L, Williamson C, et al. (2006) Genetic and neutralization properties of subtype C human immunodeficiency virus type 1 molecular env clones from acute and early heterosexually acquired infections in Southern Africa. J Virol 80: 11776-11790.
57. Derdeyn CA, Decker JM, Bibollet-Ruche F, Mokili JL, Muldoon M, et al. (2004) Envelope-Constrained Neutralization-Sensitive HIV-1 After Heterosexual Transmission. Science 303: 2019-2022.
58. Rong R, Bibollet-Ruche F, Mulenga J, Allen S, Blackwell JL, et al. (2007) Role of V1V2 and other human immunodeficiency virus type 1 envelope domains in resistance to autologous neutralization during clade C infection. J Virol 81: 1350-1359.
59. Lynch RM, Rong R, Li B, Shen T, Honnen W, et al. (2010) Subtype-specific conservation of isoleucine 309 in the envelope V3 domain is linked to immune evasion in subtype C HIV-1 infection. Virology 404: 59-70.
60. Rong R, Gnanakaran S, Decker JM, Bibollet-Ruche F, Taylor J, et al. (2007) Unique Mutational Patterns in the Envelope {alpha}2 Amphipathic Helix and Acquisition of Length in gp120 Hyper-variable Domains are Associated with Resistance to Autologous Neutralization of Subtype C Human Immunodeficiency Virus type 1. J Virol 81: 5658-5668.
61. Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, et al. (2006) Comparative protein structure modeling using Modeller. Curr Protoc Bioinformatics Chapter 5: Unit 5 6.
62. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26: 1781-1802.
63. Kwong PD, Wyatt R, Majeed S, Robinson J, Sweet RW, et al. (2000) Structures of HIV-1 gp120 envelope glycoproteins from laboratory-adapted and primary isolates. Structure Fold Des 8: 1329-1339.
64. Huang CC, Tang M, Zhang MY, Majeed S, Montabana E, et al. (2005) Structure of a V3-containing HIV-1 gp120 core. Science 310: 1025-1028.
65. 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.
66. Pancera M, Majeed S, Ban YE, Chen L, Huang CC, et al. (2010) Structure of HIV-1 gp120 with gp41-interactive region reveals layered envelope architecture and basis of conformational mobility. Proc Natl Acad Sci U S A 107: 1166-1171.
67. Liu J, Bartesaghi A, Borgnia MJ, Sapiro G, Subramaniam S, (2008) Molecular architecture of native HIV-1 gp120 trimers. Nature 455: 109-113.
68. Doores KJ, Bonomelli C, Harvey DJ, Vasiljevic S, Dwek RA, et al. (2010) Envelope glycans of immunodeficiency virions are almost entirely oligomannose antigens. Proc Natl Acad Sci U S A 107: 13800-13805.
69. Hornak V, Abel R, Okur A, Strockbine B, Roitberg A, et al. (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65: 712-725.
70. Kirschner KN, Yongye AB, Tschampel SM, Gonzalez-Outeirino J, Daniels CR, et al. (2008) GLYCAM06: a generalizable biomolecular force field. Carbohydrates. J Comput Chem 29: 622-655.
71. Lahm HW, Stein S, (1985) Characterization of recombinant human interleukin-2 with micromethods. J Chromatogr 326: 357-361.
72. Liao HX, Levesque MC, Nagel A, Dixon A, Zhang R, et al. (2009) High-throughput isolation of immunoglobulin genes from single human B cells and expression as monoclonal antibodies. J Virol Methods 158: 171-179.
73. Benoit RM, Wilhelm RN, Scherer-Becker D, Ostermeier C, (2006) An improved method for fast, robust, and seamless integration of DNA fragments into multiple plasmids. Protein Expr Purif 45: 66-71.
74. Tiller T, Meffre E, Yurasov S, Tsuiji M, Nussenzweig MC, et al. (2008) Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J Immunol Methods 329: 112-124.
75. Smith K, Garman L, Wrammert J, Zheng NY, Capra JD, et al. (2009) Rapid generation of fully human monoclonal antibodies specific to a vaccinating antigen. Nat Protoc 4: 372-384.
76. 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.
77. Jiang X, Burke V, Totrov M, Williams C, Cardozo T, et al. (2010) Conserved structural elements in the V3 crown of HIV-1 gp120. Nat Struct Mol Biol 17: 955-961.
78. Spurrier B, Sampson JM, Totrov M, Li H, O'Neal T, et al. (2011) Structural analysis of human and macaque mAbs 2909 and 2.5B: implications for the configuration of the quaternary neutralizing epitope of HIV-1 gp120. Structure 19: 691-699.
79. Burke V, Williams C, Sukumaran M, Kim SS, Li H, et al. (2009) Structural basis of the cross-reactivity of genetically related human anti-HIV-1 mAbs: implications for design of V3-based immunogens. Structure 17: 1538-1546.
80. Otwinowski Z, Minor W (1997) Processing of X-Ray Diffraction Data Collected in Oscillation Mode. In: Carter CW, editor. Methods in Enzymology. Salt Lake City, UT: Academic Press, Inc. pp. 307-326.
81. Vagin A, Teplyakov A, (2010) Molecular replacement with MOLREP. Acta Crystallogr D Biol Crystallogr 66: 22-25.
82. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67: 235-242.
83. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
84. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, et al. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 58: 1948-1954.
85. Abagyan R, Totrov M, Kuznetsov D, (1994) ICM-A new method for protein modeling and design: Applications to docking and structure prediction from the distorted native conformation. J Comput Chem 15: 488-506.