Broadly Neutralizing Antibody Responses in a Large Longitudinal Sub-Saharan HIV Primary Infection Cohort

PLoS Pathogens

Volumn 12, Issue 1, 2016, Pages

  Landais, Elise ^a   Huang, Xiayu ^b   Havenar Daughton, Colin ^c,d   Murrell, Ben ^d   Price, Matt A ^a,e   Wickramasinghe, Lalinda ^a   Ramos, Alejandra ^a   Bian, Charoan B ^a   Simek, Melissa ^a   Allen, Susan ^f,g   Karita, Etienne ^h   Kilembe, William ^g   Lakhi, Shabir ^g   Inambao, Mubiana ^g   Kamali, Anatoli ⁱ   Sanders, Eduard J ^j,k   Anzala, Omu ^l   Edward, Vinodh ^m   Bekker, Linda Gail ⁿ   Tang, Jianming ^o   Gilmour, Jill ^p   Kosakovsky Pond, Sergei L ^d   Phung, Pham ^q   Wrin, Terri ^q   Crotty, Shane ^c,d,r   Godzik, Adam ^b,r   Poignard, Pascal ^a,s,t   more..

^a INTERNATIONAL AIDS VACCINE INITIATIVE   (United States)

^b BURNHAM INSTITUTE   (United States)

^c LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g Rwanda Zambia HIV Research Group   (Zambia)

^h Project San Francisco   (Rwanda)

ⁱ MEDICAL RESEARCH COUNCIL   (United Kingdom)

^j Centre for Geographic Medicine Coast Medical Research Institute   (Kenya)

^k UNIVERSITY OF OXFORD   (United Kingdom)

^l Kenya AIDS Vaccine Initiative   (Kenya)

^m AURUM INSTITUTE   (South Africa)

ⁿ UNIVERSITY OF CAPE TOWN   (South Africa)

^o University of Alabama at Birmingham   (United States)

^p CHELSEA AND WESTMINSTER HOSPITAL   (United Kingdom)

^q LABORATORY CORPORATION OF AMERICA   (United States)

^r Center for HIV/AIDS Vaccine Immunology and Immunogen Discovery   (United States)

^s SCRIPPS RESEARCH INSTITUTE   (United States)

^t UNIV GRENOBLE ALPES   (France)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; ENVELOPE PROTEIN; GLYCOPROTEIN GP 120; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; IMMUNOGLOBULIN G; NEUTRALIZING ANTIBODY; RECOMBINANT PROTEIN; EPITOPE; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN;

ANTIBODY COMBINING SITE; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIBODY TITER; ARTICLE; CD4 LYMPHOCYTE COUNT; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITOPE MAPPING; GENETIC TRANSFECTION; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; VIRUS LOAD; VIRUS NEUTRALIZATION; ADULT; AFRICA SOUTH OF THE SAHARA; COHORT ANALYSIS; FEMALE; IMMUNOLOGY; MALE; MIDDLE AGED; YOUNG ADULT;

ADULT; AFRICA SOUTH OF THE SAHARA; AIDS VACCINES; ANTIBODIES, NEUTRALIZING; COHORT STUDIES; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITOPES, B-LYMPHOCYTE; FEMALE; HIV ANTIBODIES; HIV INFECTIONS; HUMANS; LONGITUDINAL STUDIES; MALE; MIDDLE AGED; YOUNG ADULT;

EID: 84956714697     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005369     Document Type: Article

References (88)

1. Walker LM, Phogat SK, Chan-Hui PY, Wagner D, Phung P, Goss JL, et al. Broad and Potent Neutralizing Antibodies from an African Donor Reveal a New HIV-1 Vaccine Target. Science. 2009;326: 285–289. doi: 10.1126/science.1178746 19729618
2. Walker LM, Simek MD, Priddy F, Gach JS, Wagner D, Zwick MB, Trkola A, et al. A Limited Number of Antibody Specificities Mediate Broad and Potent Serum Neutralization in Selected HIV-1 Infected Individuals. PLoS Pathog. 2010;6: e1001028. doi: 10.1371/journal.ppat.1001028.g009 20700449
3. Wu X, Yang ZY, Li Y, Hogerkorp CM, Schief WR, Seaman MS, et al. Rational Design of Envelope Identifies Broadly Neutralizing Human Monoclonal Antibodies to HIV-1. Science. 2010;329: 856–861. doi: 10.1126/science.1187659 20616233
4. Scheid JF, Mouquet H, Ueberheide B, Diskin R, Klein F, Olivera TYK, et al. Sequence and Structural Convergence of Broad and Potent HIV Antibodies That Mimic CD4 Binding. Science. 2011. doi: 10.1126/science.1207227
5. Huang J, Ofek G, Laub L, Louder MK, Doria-Rose NA, Longo NS, et al. Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature. 2012;491: 406–412. doi: 10.1038/nature11544 23151583
6. Falkowska E, Le KM, Ramos A, Doores KJ, Lee JH, Blattner C, et al. Broadly Neutralizing HIV Antibodies Definea Glycan-Dependent Epitope on the Prefusion Conformation of gp41 on Cleaved Envelope Trimers. Immunity. Elsevier Inc; 2014;: 1–12. doi: 10.1016/j.immuni.2014.04.009
7. Mascola JR, Stiegler G, VanCott TC, Katinger H, Carpenter CB, Hanson CE, et al. Protection of macaques against vaginal transmission of a pathogenic HIV-1/SIV chimeric virus by passive infusion of neutralizing antibodies. Nat Med. 2000;6: 207–210. doi: 10.1038/72318 10655111
8. Hessell AJ, Poignard P, Hunter M, Hangartner L, Tehrani DM, Bleeker WK, et al. Effective, low-titer antibody protection against low-dose repeated mucosal SHIV challenge in macaques. Nature Publishing Group. Nature Publishing Group; 2009;: 1–5. doi: 10.1038/nm.1974
9. Moldt B, Rakasz EG, Schultz N, Chan-Hui PY, Swiderek K, Weisgrau KL, et al. Highly potent HIV-specific antibody neutralization in vitro translates into effective protection against mucosal SHIV challenge in vivo. Proceedings of the National Academy of Sciences. 2012. doi: 10.1073/pnas.1214785109
10. Shingai M, Donau OK, Plishka RJ, Buckler-White A, Mascola JR, Nabel GJ, et al. Passive transfer of modest titers of potent and broadly neutralizing anti-HIV monoclonal antibodies block SHIV infection in macaques. Journal of Experimental Medicine. 2014;211: 2061–2074. doi: 10.1084/jem.20132494 25155019
11. Mascola JR, Haynes BF, HIV-1 neutralizing antibodies: understanding nature's pathways. Immunol Rev. 2013;254: 225–244. doi: 10.1111/imr.12075 23772623
12. Fauci AS, Marston HD, Ending AIDS—is an HIV vaccine necessary? N Engl J Med. 2014;370: 495–498. doi: 10.1056/NEJMp1313771 24499210
13. Gray ES, Moore PL, Choge IA, Decker JM, Bibollet-Ruche F, Li H, et al. Neutralizing antibody responses in acute human immunodeficiency virus type 1 subtype C infection. JOURNAL OF VIROLOGY. 2007;81: 6187–6196. doi: 10.1128/JVI.00239-07 17409164
14. Binley JM, Lybarger EA, Crooks ET, Seaman MS, Gray E, Davis KL, et al. Profiling the specificity of neutralizing antibodies in a large panel of plasmas from patients chronically infected with human immunodeficiency virus type 1 subtypes B and C. JOURNAL OF VIROLOGY. 2008;82: 11651–11668. doi: 10.1128/JVI.01762-08 18815292
15. Sather DN, Armann J, Ching LK, Mavrantoni A, Sellhorn G, Caldwell Z, et al. Factors Associated with the Development of Cross-Reactive Neutralizing Antibodies during Human Immunodeficiency Virus Type 1 Infection. JOURNAL OF VIROLOGY. 2008;83: 757–769. doi: 10.1128/JVI.02036-08 18987148
16. Simek MD, Rida W, Priddy FH, Pung P, Carrow E, Laufer DS, et al. 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. JOURNAL OF VIROLOGY. 2009;83: 7337–7348. doi: 10.1128/JVI.00110-09 19439467
17. Doria-Rose NA, Klein RM, Daniels MG, O'Dell S, Nason M, Lapedes A, et al. Breadth of human immunodeficiency virus-specific neutralizing activity in sera: clustering analysis and association with clinical variables. JOURNAL OF VIROLOGY. 2010;84: 1631–1636. doi: 10.1128/JVI.01482-09 19923174
18. Euler Z, van Gils MJ, Bunnik EM, Phung P, Schweighardt B, Wrin T, et al. Cross-reactive neutralizing humoral immunity does not protect from HIV type 1 disease progression. J Infect Dis. 2010;201: 1045–1053. doi: 10.1086/651144 20170371
19. Mikell I, Sather DN, Kalams SA, Altfeld M, Alter G, Stamatatos L, Characteristics of the earliest cross-neutralizing antibody response to HIV-1. PLoS Pathog. 2011;7: e1001251. doi: 10.1371/journal.ppat.1001251 21249232
20. Gray ES, Madiga MC, Hermanus T, Moore PL, Wibmer CK, Tumba NL, et al. 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. JOURNAL OF VIROLOGY. 2011;85: 4828–4840. doi: 10.1128/JVI.00198-11 21389135
21. Hraber P, Seaman MS, Bailer RT, Mascola JR, Montefiori DC, Korber BT, Prevalence of broadly neutralizing antibody responses during chronic HIV-1 infection. AIDS. 2014;28: 163–169. doi: 10.1097/QAD.0000000000000106 24361678
22. van Gils MJ, Euler Z, Schweighardt B, Wrin T, Schuitemaker H, Prevalence of cross-reactive HIV-1-neutralizing activity in HIV-1-infected patients with rapid or slow disease progression. AIDS. 2009;23: 2405–2414. doi: 10.1097/QAD.0b013e32833243e7 19770692
23. Piantadosi A, Panteleeff D, Blish CA, Baeten JM, Jaoko W, McClelland RS, et al. Breadth of neutralizing antibody response to human immunodeficiency virus type 1 is affected by factors early in infection but does not influence disease progression. JOURNAL OF VIROLOGY. 2009;83: 10269–10274. doi: 10.1128/JVI.01149-09 19640996
24. van den Kerkhof TLGM, Feenstra K, Euler Z, van Gils MJ, Rijsdijk LWE, Boeser-Nunnink BD, et al. HIV-1 envelope glycoprotein signatures that correlate with the development of cross-reactive neutralizing activity. Retrovirology. 2013;10: 102. doi: 10.1186/1742-4690-10-102 24059682
25. Euler Z, van Gils MJ, Schuitemaker H, Cross-reactive neutralizing activity in HIV-1 infected injecting drug users. Retrovirology. BioMed Central; 2012;9: P56. doi: 10.1186/1742-4690-9-S2-P56
26. Burton DR, Ahmed R, Barouch DH, Butera ST, Crotty S, Godzik A, et al. A Blueprint for HIV Vaccine Discovery. Cell Host and Microbe. Elsevier Inc; 2012;12: 396–407. doi: 10.1016/j.chom.2012.09.008 23084910
27. Burton DR, Mascola JR, Antibody responses to envelope glycoproteins in HIV-1 infection. Nat Immunol. 2015;16: 571–576. doi: 10.1038/ni.3158 25988889
28. Amornkul PN, Karita E, Kamali A, Rida WN, Sanders EJ, Lakhi S, et al. Disease progression by infecting HIV-1 subtype in a seroconverter cohort in sub-Saharan Africa. AIDS. 2013;27: 2775–2786. doi: 10.1097/QAD.0000000000000012 24113395
29. Prentice HA, Price MA, Porter TR, Cormier E, Mugavero MJ, Kamali A, et al. Dynamics of viremia in primary HIV-1 infection in Africans: Insights from analyses of host and viral correlates. Virology. 2014;449: 254–262. doi: 10.1016/j.virol.2013.11.024 24418560
30. Walker LM, Huber M, Doores KJ, Falkowska E, Pejchal R, Julien J-P, et al. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature. Nature Publishing Group; 2011;: 1–6. doi: 10.1038/nature10373
31. Seaman MS, Janes H, Hawkins N, Grandpre LE, Devoy C, Giri A, et al. Tiered Categorization of a Diverse Panel of HIV-1 Env Pseudoviruses for Assessment of Neutralizing Antibodies. JOURNAL OF VIROLOGY. 2010;84: 1439–1452. doi: 10.1128/JVI.02108-09 19939925
32. Locci M, Havenar-Daughton C, Landais E, Wu J, Kroenke MA, Arlehamn CL, et al. Human Circulating PD-1. Immunity. Elsevier Inc; 2013;: 1–12. doi: 10.1016/j.immuni.2013.08.031
33. Binley JM, Klasse PJ, Cao Y, Jones I, Markowitz M, Ho DD, et al. Differential regulation of the antibody responses to Gag and Env proteins of human immunodeficiency virus type 1. JOURNAL OF VIROLOGY. 1997;71: 2799–2809. 9060635
34. Lynch RM, Tran L, Louder MK, Schmidt SD, Cohen M, CHAVI 001 Clinical Team Memberset al. The development of CD4 binding site antibodies during HIV-1 infection. JOURNAL OF VIROLOGY. 2012;86: 7588–7595. doi: 10.1128/JVI.00734-12 22573869
35. Feng Y, McKee K, Tran K, O'Dell S, Schmidt SD, Phogat A, et al. Biochemically defined HIV-1 Env variant immunogens display differential binding and neutralizing specificities to the CD4 binding site. Journal of Biological Chemistry. 2011. doi: 10.1074/jbc.M111.317776
36. Jardine J, Julien J-P, Menis S, Ota T, Kalyuzhniy O, McGuire A, et al. Rational HIV immunogen design to target specific germline B cell receptors. Science. 2013;340: 711–716. doi: 10.1126/science.1234150 23539181
37. Doores KJ, Burton DR, Variable loop glycan dependency of the broad and potent HIV-1-neutralizing antibodies PG9 and PG16. JOURNAL OF VIROLOGY. 2010;84: 10510–10521. doi: 10.1128/JVI.00552-10 20686044
38. Bonsignori M, Hwang K-K, Chen X, Tsao C-Y, Morris L, Gray E, et al. Analysis of a clonal lineage of HIV-1 envelope V2/V3 conformational epitope-specific broadly neutralizing antibodies and their inferred unmutated common ancestors. JOURNAL OF VIROLOGY. 2011;85: 9998–10009. doi: 10.1128/JVI.05045-11 21795340
39. Doria-Rose NA, Schramm CA, Gorman J, Moore PL, Bhiman JN, Dekosky BJ, et al. Developmental pathway for potent V1V2-directed HIV-neutralizing antibodies. Nature. 2014;509: 55–62. doi: 10.1038/nature13036 24590074
40. Scharf L, Scheid JF, Lee JH, West AP, JrChen C, Gao H, et al. Antibody 8ANC195 Reveals a Site of Broad Vulnerability on the HIV-1 Envelope Spike. CellReports. The Authors; 2014;7: 785–795. doi: 10.1016/j.celrep.2014.04.001
41. Huang J, Kang BH, Pancera M, Lee JH, Tong T, Feng Y, et al. Broad and potent HIV-1 neutralization by a human antibody that binds the gp41–gp120 interface. Nature. Nature Publishing Group; 2014;: 1–17. doi: 10.1038/nature13601
42. Lavine CL, Lao S, Montefiori DC, Haynes BF, Sodroski JG, Yang X, et al. High-Mannose Glycan-Dependent Epitopes Are Frequently Targeted in Broad Neutralizing Antibody Responses during Infection of Human Immunodeficiency Virus Type 1. JOURNAL OF VIROLOGY. 2011. doi: 10.1128/JVI.06201-11
43. Mouquet H, Klein F, Scheid JF, Warncke M, Pietzsch J, Oliveira TYK, et al. Memory B cell antibodies to HIV-1 gp140 cloned from individuals infected with clade A and B viruses. PLoS ONE. 2011;6: e24078. doi: 10.1371/journal.pone.0024078 21931643
44. Doores KJ, Kong L, Krumm SA, Le KM, Sok D, Laserson U, Doms RW, et al. Two Classes of Broadly Neutralizing Antibodies within a Single Lineage Directed to the High-Mannose Patch of HIV Envelope. JOURNAL OF VIROLOGY. 2015;89: 1105–1118. doi: 10.1128/JVI.02905-14 25378488
45. Goo L, Chohan V, Nduati R, Overbaugh J. Early development of broadly neutralizing antibodies in HIV-1–infected infants. Nature Publishing Group. Nature Publishing Group; 2014;: 1–6. doi: 10.1038/nm.3565
46. Kroon FP, van Dissel JT, de Jong JC, van Furth R, Antibody response to influenza, tetanus and pneumococcal vaccines in HIV-seropositive individuals in relation to the number of CD4+ lymphocytes. AIDS. 1994;8: 469–476. 7912086
47. Fonseca MO, Pang LW, de Paula Cavalheiro N, Barone AA, Heloisa Lopes M, Randomized trial of recombinant hepatitis B vaccine in HIV-infected adult patients comparing a standard dose to a double dose. Vaccine. 2005;23: 2902–2908. doi: 10.1016/j.vaccine.2004.11.057 15780739
48. Euler Z, van den Kerkhof TLGM, van Gils MJ, Burger JA, Edo-Matas D, Phung P, et al. Longitudinal Analysis of Early HIV-1-Specific Neutralizing Activity in an Elite Neutralizer and in Five Patients Who Developed Cross-Reactive Neutralizing Activity. JOURNAL OF VIROLOGY. 2012;86: 2045–2055. doi: 10.1128/JVI.06091-11 22156522
49. Borrow P, Lewicki H, Hahn BH, Shaw GM, Oldstone MB, Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. JOURNAL OF VIROLOGY. 1994;68: 6103–6110. 8057491
50. Schmitz JE, Kuroda MJ, Santra S, Sasseville VG, Simon MA, Lifton MA, et al. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science. 1999;283: 857–860. 9933172
51. Kaslow RA, Rivers C, Tang J, Bender TJ, Goepfert PA, Habib El R, et al. Polymorphisms in HLA class I genes associated with both favorable prognosis of human immunodeficiency virus (HIV) type 1 infection and positive cytotoxic T-lymphocyte responses to ALVAC-HIV recombinant canarypox vaccines. JOURNAL OF VIROLOGY. 2001;75: 8681–8689. 11507213
52. Carrington M, O'Brien SJ, The influence of HLA genotype on AIDS. Annu Rev Med. 2003;54: 535–551. doi: 10.1146/annurev.med.54.101601.152346 12525683
53. Brumme ZL, Brumme ZL, Poon AFY, Poon AFY, Carlson JM, Carlson JM, et al. Identifying HLA-Associated Polymorphisms in HIV-1. HIV Molecular Immunology 2010. 2011;: 1–14.
54. Carrington M, Carrington M, Walker BD, Walker BD, Immunogenetics of spontaneous control of HIV. Annu Rev Med. 2012;63: 131–145. doi: 10.1146/annurev-med-062909-130018 22248321
55. Ranasinghe S, Ranasinghe S, Cutler S, Cutler S, Davis I, Davis I, et al. Association of HLA-DRB1-restricted CD4(+) T cell responses with HIV immune control. Nat Med. 2013;19: 930–933. doi: 10.1038/nm.3229 23793098
56. Goepfert PA, Lumm W, Farmer P, Matthews P, Prendergast A, Carlson JM, et al. Transmission of HIV-1 Gag immune escape mutations is associated with reduced viral load in linked recipients. Journal of Experimental Medicine. 2008;205: 1009–1017. doi: 10.1084/jem.20072457 18426987
57. Yue L, Prentice HA, Farmer P, Song W, He D, Lakhi S, et al. Cumulative impact of host and viral factors on HIV-1 viral-load control during early infection. JOURNAL OF VIROLOGY. 2013;87: 708–715. doi: 10.1128/JVI.02118-12 23115285
58. Fraser C, Mugo PM, McCoy LE, Jaafoura S, Payne RP, Mann JK, et al. Virulence and pathogenesis of HIV-1 infection: an evolutionary perspective. Science. 2014;343: 1243727. doi: 10.1126/science.1243727 24653038
59. Claiborne DT, Prince JL, Scully E, Macharia G, Micci L, Lawson B, et al. Replicative fitness of transmitted HIV-1 drives acute immune activation, proviral load in memory CD4 +T cells, and disease progression. Proceedings of the National Academy of Sciences. 2015;: 201421607. doi: 10.1073/pnas.1421607112
60. Li X, Price MA, He D, Kamali A, Karita E, Lakhi S, et al. Host genetics and viral load in primary HIV-1 infection: clear evidence for gene by sex interactions. Hum Genet. 2014;133: 1187–1197. doi: 10.1007/s00439-014-1465-x 24969460
61. Rademeyer C, Moore PL, Taylor N, Martin DP, Choge IA, Gray ES, et al. Genetic characteristics of HIV-1 subtype C envelopes inducing cross-neutralizing antibodies. Virology. 2007;368: 172–181. doi: 10.1016/j.virol.2007.06.013 17632196
62. Baalwa J, Wang S, Parrish NF, Decker JM, Keele BF, Learn GH, et al. Molecular identification, cloning and characterization of transmitted/founder HIV-1 subtype A, D and A/D infectious molecular clones. Virology. Elsevier; 2012;: 1–16. doi: 10.1016/j.virol.2012.10.009
63. Parrish NF, Gao F, Li H, Giorgi EE, Barbian HJ, Parrish EH, et al. Phenotypic properties of transmitted founder HIV-1. Proceedings of the National Academy of Sciences. 2013. doi: 10.1073/pnas.1304288110
64. Derdeyn CA, Sok D, Valdez KPR, Gardner MR, Hunter E, Sok D, et al. Viral characteristics of transmitted HIV. Curr Opin HIV AIDS. 2008;3: 16–21. doi: 10.1097/COH.0b013e3282f2982c 19372939
65. Piantadosi A, Chohan B, Chohan V, McClelland RS, Overbaugh J, Chronic HIV-1 infection frequently fails to protect against superinfection. PLoS Pathog. 2007;3: e177. doi: 10.1371/journal.ppat.0030177 18020705
66. Cohen K, Altfeld M, Alter G, Stamatatos L, Early preservation of CXCR5+ PD-1+ helper T cells and B cell activation predict the breadth of neutralizing antibody responses in chronic HIV-1 infection. JOURNAL OF VIROLOGY. 2014;88: 13310–13321. doi: 10.1128/JVI.02186-14 25210168
67. Boliar S, Murphy MK, Tran TC, Carnathan DG, Armstrong WS, Silvestri G, et al. B-lymphocyte dysfunction in chronic HIV-1 infection does not prevent cross-clade neutralization breadth. JOURNAL OF VIROLOGY. 2012;86: 8031–8040. doi: 10.1128/JVI.00771-12 22623771
68. Gao F, Bonsignori M, Liao H- X, Kumar A, Xia S-M, Lu X, et al. Cooperation of B Cell Lineages in Induction of HIV-1-Broadly Neutralizing Antibodies. Cell. Elsevier Inc; 2014;: 1–11. doi: 10.1016/j.cell.2014.06.022 25065977
69. Wibmer CK, Bhiman JN, Gray ES, Tumba N, Abdool Karim SS, Williamson C, et al. Viral Escape from HIV-1 Neutralizing Antibodies Drives Increased Plasma Neutralization Breadth through Sequential Recognition of Multiple Epitopes and Immunotypes. PLoS Pathog. 2013;9: e1003738. doi: 10.1371/journal.ppat.1003738 24204277
70. Liao HX, Tsao CY, Alam SM, Muldoon M, Vandergrift N, Ma BJ, et al. Antigenicity and Immunogenicity of Transmitted/Founder, Consensus and Chronic Envelope Glycoproteins of Human Immunodeficiency Virus Type 1. JOURNAL OF VIROLOGY. 2013. doi: 10.1128/JVI.02297-12
71. Moore PL, Gray ES, Wibmer CK, Bhiman JN, Nonyane M, Sheward DJ, et al. Evolution of an HIV glycan-dependent broadly neutralizing antibody epitope through immune escape. Nature Publishing Group. 2012;18: 1688–1692. doi: 10.1038/nm.2985
72. Moore PL, Williamson C, Morris L, Virological features associated with the development of broadly neutralizing antibodies to HIV-1. Trends Microbiol. 2015. doi: 10.1016/j.tim.2014.12.007
73. Moore PL, Ranchobe N, Lambson BE, Gray ES, Cave E, Abrahams M-R, et al. Limited neutralizing antibody specificities drive neutralization escape in early HIV-1 subtype C infection. PLoS Pathog. 2009;5: e1000598. doi: 10.1371/journal.ppat.1000598 19763271
74. Tomaras GD, Binley JM, Gray ES, Crooks ET, Osawa K, Moore PL, et al. Polyclonal B Cell Responses to Conserved Neutralization Epitopes in a Subset of HIV-1-Infected Individuals. JOURNAL OF VIROLOGY. 2011;85: 11502–11519. doi: 10.1128/JVI.05363-11 21849452
75. Bonsignori M, Montefiori DC, Wu X, Chen X, Hwang K-K, Tsao C-Y, et al. Two distinct broadly neutralizing antibody specificities of different clonal lineages in a single HIV-1-infected donor: implications for vaccine design. JOURNAL OF VIROLOGY. 2012;86: 4688–4692. doi: 10.1128/JVI.07163-11 22301150
76. Klein F, Gaebler C, Mouquet H, Sather DN, Lehmann C, Scheid JF, et al. Broad neutralization by a combination of antibodies recognizing the CD4 binding site and a new conformational epitope on the HIV-1 envelope protein. Journal of Experimental Medicine. 2012;209: 1469–1479. doi: 10.1084/jem.20120423 22826297
77. Gray ES, Madiga MC, Moore PL, Mlisana K, Abdool Karim SS, Binley JM, et al. Broad Neutralization of Human Immunodeficiency Virus Type 1 Mediated by Plasma Antibodies against the gp41 Membrane Proximal External Region. JOURNAL OF VIROLOGY. 2009;83: 11265–11274. doi: 10.1128/JVI.01359-09 19692477
78. Moore PL, Gray ES, Sheward D, Madiga M, Ranchobe N, Lai Z, et al. Potent and Broad Neutralization of HIV-1 Subtype C by Plasma Antibodies Targeting a Quaternary Epitope Including Residues in the V2 Loop. JOURNAL OF VIROLOGY. 2011;85: 3128–3141. doi: 10.1128/JVI.02658-10 21270156
79. Euler Z, van Gils MJ, Schuitemaker H. Cross-Reactive Neutralizing Activity in HIV-1 Infected Injection Drug Users. AIDS Vaccine Conference, Boston 2012; 2012.
80. Liao Hua-Xin, Lynch R, Zhou T, Gao Feng, Alam S Munir, Boyd SD, et al. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature. Nature Publishing Group; 2013;: 1–11. doi: 10.1038/nature12053
81. Haynes BF, Verkoczy L, AIDS/HIV. Host controls of HIV neutralizing antibodies. Science. 2014;344: 588–589. doi: 10.1126/science.1254990 24812389
82. Sanders RW, Derking R, Cupo A, Julien J- P, Yasmeen A, de Val N, et al. A Next-Generation Cleaved, Soluble HIV-1 Env Trimer, BG505 SOSIP.664 gp140, Expresses Multiple Epitopes for Broadly Neutralizing but Not Non-Neutralizing Antibodies. PLoS Pathog. 2013;9: e1003618. doi: 10.1371/journal.ppat.1003618 24068931
83. Sharma SK, de Val N, Bale S, Guenaga J, Tran K, Feng Y, et al. Cleavage-Independent HIV-1 Env Trimers Engineered as Soluble Native Spike Mimetics for Vaccine Design. CellReports. The Authors; 2015;: 1–13. doi: 10.1016/j.celrep.2015.03.047
84. Kong L, Lee JH, Doores KJ, Murin CD, Julien J-P, McBride R, et al. Supersite of immune vulnerability on the glycosylated face of HIV-1 envelope glycoprotein gp120. Nat Struct Mol Biol. Nature Publishing Group; 2013;: 1–10. doi: 10.1038/nsmb.2594 23708606
85. Sok D, Doores KJ, Briney B, Le KM, Saye-Francisco KL, Ramos A, et al. Promiscuous Glycan Site Recognition by Antibodies to the High-Mannose Patch of gp120 Broadens Neutralization of HIV. Science Translational Medicine. 2014;6: 236ra63–236ra63. doi: 10.1126/scitranslmed.3008104 24828077
86. Li M, Gao F, Mascola JR, Stamatatos L, Polonis VR, Koutsoukos M, et al. Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. JOURNAL OF VIROLOGY. 2005;79: 10108–10125. doi: 10.1128/JVI.79.16.10108–10125.2005 16051804
87. Doores KJ, Fulton Z, Huber M, Wilson IA, Burton DR, Antibody 2G12 Recognizes Di-Mannose Equivalently in Domain- and Nondomain-Exchanged Forms but Only Binds the HIV-1 Glycan Shield if Domain Exchanged. JOURNAL OF VIROLOGY. 2010;84: 10690–10699. doi: 10.1128/JVI.01110-10 20702629
88. Li Y, Migueles SA, Welcher B, Svehla K, Phogat A, Louder MK, et al. Broad HIV-1 neutralization mediated by CD4-binding site antibodies. Nat Med. 2007;13: 1032–1034. doi: 10.1038/nm1624 17721546