The Broad Neutralizing Antibody Responses after HIV-1 Superinfection Are Not Dominated by Antibodies Directed to Epitopes Common in Single Infection

PLoS Pathogens

Volumn 11, Issue 7, 2015, Pages

  Cortez, Valerie ^a,b   Wang, Bingjie ^b   Dingens, Adam ^a,b   Chen, Mitchell M ^b   Ronen, Keshet ^b   Georgiev, Ivelin S ^c   McClelland, R Scott ^d   Overbaugh, Julie ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CORE PROTEIN; EPITOPE; GLYCOPROTEIN GP 41; NEUTRALIZING ANTIBODY; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; HUMAN IMMUNODEFICIENCY VIRUS VACCINE;

AFFINITY CHROMATOGRAPHY; ANTIBODY COMBINING SITE; ANTIBODY TITER; ARTICLE; BLOOD SAMPLING; CLINICAL ARTICLE; CONTROLLED STUDY; EPITOPE MAPPING; FEMALE; GENE SEQUENCE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; ION EXCHANGE CHROMATOGRAPHY; MATHEMATICAL COMPUTING; MOLECULAR CLONING; NESTED POLYMERASE CHAIN REACTION; NUCLEOTIDE SEQUENCE; POINT MUTATION; POLYMERASE CHAIN REACTION; PROTEIN PURIFICATION; RNA EXTRACTION; SITE DIRECTED MUTAGENESIS; ADULT; ANTIBODY SPECIFICITY; BLOOD; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; SERODIAGNOSIS; SUPERINFECTION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ADULT; AIDS VACCINES; ANTIBODIES, NEUTRALIZING; ANTIBODY SPECIFICITY; EPITOPE MAPPING; EPITOPES; FEMALE; HIV ANTIBODIES; HIV INFECTIONS; HIV-1; HUMANS; NEUTRALIZATION TESTS; SUPERINFECTION;

EID: 84938808649     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004973     Document Type: Article

References (66)

1. Fauci AS, Folkers GK, Marston HD, (2014) Ending the global HIV/AIDS pandemic: the critical role of an HIV vaccine. CLIN INFECT DIS 59 Suppl 2: S80–S84. doi: 10.1093/cid/ciu420 25151483
2. Stephenson KE, Barouch DH, (2013) A global approach to HIV-1 vaccine development. Immunol Rev 254: 295–304. doi: 10.1111/imr.12073 23772627
3. Zolla-Pazner S, (2014) A critical question for HIV vaccine development: Which antibodies to induce? Science 345: 167–168. doi: 10.1126/science.1256526 25013066
4. Gray ES, Taylor N, Wycuff D, Moore PL, Tomaras GD, et al. (2009) Antibody specificities associated with neutralization breadth in plasma from human immunodeficiency virus type 1 subtype C-infected blood donors. Journal of Virology 83: 8925–8937. doi: 10.1128/JVI.00758-09 19553335
5. Lynch RM, Tran L, Louder MK, Schmidt SD, Cohen M, et al. (2012) The development of CD4 binding site antibodies during HIV-1 infection. Journal of Virology 86: 7588–7595. doi: 10.1128/JVI.00734-12 22573869
6. 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. Journal of Virology 85: 4828–4840. doi: 10.1128/JVI.00198-11 21389135
7. Gray ES, Madiga MC, Moore PL, Mlisana K, Karim SSA, et al. (2009) Broad neutralization of human immunodeficiency virus type 1 mediated by plasma antibodies against the gp41 membrane proximal external region. Journal of Virology 83: 11265–11274. doi: 10.1128/JVI.01359-09 19692477
8. 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.
9. Tomaras GD, Binley JM, Gray ES, Crooks ET, Osawa K, et al. (2011) Polyclonal B cell responses to conserved neutralization epitopes in a subset of HIV-1-infected individuals. Journal of Virology 85: 11502–11519. doi: 10.1128/JVI.05363-11 21849452
10. Binley JM, Lybarger EA, Crooks ET, Seaman MS, Gray E, et al. (2008) 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 82: 11651–11668. doi: 10.1128/JVI.01762-08 18815292
11. Sather DN, Stamatatos L, (2010) Epitope specificities of broadly neutralizing plasmas from HIV-1 infected subjects. Vaccine 28: B8–B12. doi: 10.1016/j.vaccine.2009.07.085 20510750
12. 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. doi: 10.1371/journal.ppat.1001251 21249232
13. 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. doi: 10.1038/nature11544 23151583
14. 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. Journal of Virology 75: 10892–10905. 11602729
15. Purtscher M, Trkola A, Gruber G, Buchacher A, Predl R, et al. (1994) A broadly neutralizing human monoclonal antibody against gp41 of human immunodeficiency virus type 1. AIDS Res Hum Retroviruses 10: 1651–1658. 7888224
16. Wu X, Yang Z-Y, Li Y, Hogerkorp C-M, Schief WR, et al. (2010) Rational Design of Envelope Identifies Broadly Neutralizing Human Monoclonal Antibodies to HIV-1. Science.
17. 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. doi: 10.1126/science.1207227 21764753
18. Diskin R, Scheid JF, Marcovecchio PM, West AP, Klein F, et al. (2011) Increasing the potency and breadth of an HIV antibody by using structure-based rational design. Science 334: 1289–1293. doi: 10.1126/science.1213782 22033520
19. Corti D, Langedijk JPM, Hinz A, Seaman MS, Vanzetta F, et al. (2010) Analysis of memory B cell responses and isolation of novel monoclonal antibodies with neutralizing breadth from HIV-1-infected individuals. PLoS ONE 5: e8805. doi: 10.1371/journal.pone.0008805 20098712
20. Walker LM, Phogat SK, Chan-Hui P-Y, 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. doi: 10.1126/science.1178746 19729618
21. Walker LM, Huber M, Doores KJ, Falkowska E, Pejchal R, et al. (2011) Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature.
22. Blattner C, Lee JH, Sliepen K, Derking R, Falkowska E, et al. (2014) Structural Delineation of a Quaternary, Cleavage-Dependent Epitope at the gp41-gp120 Interface on Intact HIV-1 Env Trimers. Immunity 40: 669–680. doi: 10.1016/j.immuni.2014.04.008 24768348
23. Falkowska E, Le KM, Ramos A, Doores KJ, Lee JH, et al. (2014) Broadly Neutralizing HIV Antibodies Definea Glycan-Dependent Epitope on the Prefusion Conformation of gp41 on Cleaved Envelope Trimers. Immunity 40: 657–668. doi: 10.1016/j.immuni.2014.04.009 24768347
24. Scharf L, Scheid JF, Lee JH, West AP, JrChen C, et al. (2014) Antibody 8ANC195 Reveals a Site of Broad Vulnerability on the HIV-1 Envelope Spike. CellReports 7: 785–795.
25. Huang J, Kang BH, Pancera M, Lee JH, Tong T, et al. (2014) Broad and potent HIV-1 neutralization by a human antibody that binds the gp41–gp120 interface. Nature 515: 138–142. http://www.nature.com/doifinder/10.1038/nature13601. doi: 10.1038/nature13601 25186731
26. Powell RLR, Kinge T, Nyambi PN, (2010) Infection by discordant strains of HIV-1 markedly enhances the neutralizing antibody response against heterologous virus. Journal of Virology 84: 9415–9426. doi: 10.1128/JVI.02732-09 20631143
27. Cortez V, Odem-Davis K, McClelland RS, Jaoko W, Overbaugh J, (2012) HIV-1 Superinfection in Women Broadens and Strengthens the Neutralizing Antibody Response. PLoS Pathog 8: e1002611. doi: 10.1371/journal.ppat.1002611 22479183
28. Chohan B, Lavreys L, Rainwater SMJ, Overbaugh J, (2005) Evidence for frequent reinfection with human immunodeficiency virus type 1 of a different subtype. Journal of Virology 79: 10701–10708. 16051862
29. Piantadosi A, Chohan B, Chohan V, McClelland RS, Overbaugh J, (2007) Chronic HIV-1 infection frequently fails to protect against superinfection. PLoS Pathog 3: e177. 18020705
30. Piantadosi A, Ngayo MO, Chohan B, Overbaugh J, (2008) Examination of a second region of the HIV type 1 genome reveals additional cases of superinfection. AIDS Res Hum Retroviruses 24: 1221. doi: 10.1089/aid.2008.0100 18729772
31. Ronen K, McCoy CO, Matsen FA, Boyd DF, Emery S, et al. (2013) HIV-1 Superinfection Occurs Less Frequently Than Initial Infection in a Cohort of High-Risk Kenyan Women. PLoS Pathog 9: e1003593. doi: 10.1371/journal.ppat.1003593 24009513
32. Carter CC, Wagner GA, Hightower GK, Caballero G, Phung P, et al. (2015) HIV-1 neutralizing antibody response and viral genetic diversity characterized with next generation sequencing. Virology 474: 34–40. doi: 10.1016/j.virol.2014.10.019 25463602
33. 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. Journal of Virology 80: 6155–6164. 16731954
34. Piantadosi A, Panteleeff D, Blish CA, Baeten JM, Jaoko W, et al. (2009) 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 83: 10269–10274. doi: 10.1128/JVI.01149-09 19640996
35. 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. Journal of Virology 83: 757–769. doi: 10.1128/JVI.02036-08 18987148
36. Alter G, Moody MA, (2010) The humoral response to HIV-1: new insights, renewed focus. J INFECT DIS 202 Suppl 2: S315–S322. doi: 10.1086/655654 20846039
37. Kong L, Lee JH, Doores KJ, Murin CD, Julien J-P, et al. (2013) Supersite of immune vulnerability on the glycosylated face of HIV-1 envelope glycoprotein gp120. Nat Struct Mol Biol 20: 796–803. doi: 10.1038/nsmb.2594 23708606
38. Sok D, Doores KJ, Briney B, Le KM, Saye-Francisco KL, et al. (2014) Promiscuous Glycan Site Recognition by Antibodies to the High-Mannose Patch of gp120 Broadens Neutralization of HIV. Sci Transl Med 6: 236ra63–236ra63. doi: 10.1126/scitranslmed.3008104 24828077
39. Doria-Rose NA, Schramm CA, Gorman J, Moore PL, Bhiman JN, et al. (2014) Developmental pathway for potent V1V2-directed HIV-neutralizing antibodies. Nature.
40. Moore PL, Gray ES, Sheward D, Madiga M, Ranchobe N, et al. (2011) 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 85: 3128–3141. doi: 10.1128/JVI.02658-10 21270156
41. Derking R, Ozorowski G, Sliepen K, Yasmeen A, Cupo A, et al. (2015) Comprehensive Antigenic Map of a Cleaved Soluble HIV-1 Envelope Trimer. PLoS Pathog 11: e1004767. doi: 10.1371/journal.ppat.1004767 25807248
42. Balla-Jhagjhoorsingh SS, Corti D, Heyndrickx L, Willems E, Vereecken K, et al. (2013) The N276 Glycosylation Site Is Required for HIV-1 Neutralization by the CD4 Binding Site Specific HJ16 Monoclonal Antibody. PLoS ONE 8: e68863. doi: 10.1371/journal.pone.0068863 23874792
43. Doores KJ, Kong L, Krumm SA, Le KM, Sok D, et al. (2015) Two Classes of Broadly Neutralizing Antibodies within a Single Lineage Directed to the High-Mannose Patch of HIV Envelope. Journal of Virology 89: 1105–1118. doi: 10.1128/JVI.02905-14 25378488
44. Moore PL, Sheward D, Nonyane M, Ranchobe N, Hermanus T, et al. (2013) Multiple pathways of escape from HIV broadly cross-neutralizing V2-dependent antibodies. Journal of Virology 87: 4882–4894. doi: 10.1128/JVI.03424-12 23408621
45. Wibmer CK, Bhiman JN, Gray ES, Tumba N, Karim SSA, et al. (2013) Viral Escape from HIV-1 Neutralizing Antibodies Drives Increased Plasma Neutralization Breadth through Sequential Recognition of Multiple Epitopes and Immunotypes. PLoS Pathog 9: e1003738. doi: 10.1371/journal.ppat.1003738 24204277
46. Bonsignori M, Montefiori DC, Wu X, Chen X, Hwang K-K, et al. (2012) Two distinct broadly neutralizing antibody specificities of different clonal lineages in a single HIV-1-infected donor: implications for vaccine design. Journal of Virology 86: 4688–4692. doi: 10.1128/JVI.07163-11 22301150
47. Georgiev IS, Doria-Rose NA, Zhou T, Kwon YD, Staupe RP, et al. (2013) Delineating antibody recognition in polyclonal sera from patterns of HIV-1 isolate neutralization. Science 340: 751–756. doi: 10.1126/science.1233989 23661761
48. Fauci AS, Marston HD, (2014) Ending AIDS—is an HIV vaccine necessary? N Engl J Med 370: 495–498. doi: 10.1056/NEJMp1313771 24499210
49. Kwong PD, Mascola JR, (2012) Human antibodies that neutralize HIV-1: identification, structures, and B cell ontogenies. Immunity 37: 412–425. doi: 10.1016/j.immuni.2012.08.012 22999947
50. Moore PL, Moore PL, Gray ES, Gray ES, Wibmer CK, et al. (2012) Evolution of an HIV glycan-dependent broadly neutralizing antibody epitope through immune escape. Nat Med 18: 1688. doi: 10.1038/nm.2985 23086475
51. Doria-Rose NA, Schramm CA, Gorman J, Moore PL, Bhiman JN, et al. (2014) nature13036. Nature 508: 55–62. doi: 10.1038/nature13165 24670647
52. Van Gils MJ, Sanders RW, (2013) Broadly neutralizing antibodies against HIV-1: templates for a vaccine. Virology 435: 46–56. doi: 10.1016/j.virol.2012.10.004 23217615
53. Malenbaum SE, Yang D, Cavacini L, Posner M, Robinson J, et al. (2000) The N-terminal V3 loop glycan modulates the interaction of clade A and B human immunodeficiency virus type 1 envelopes with CD4 and chemokine receptors. Journal of Virology 74: 11008–11016. 11069996
54. Koch M, Pancera M, Kwong PD, Kolchinsky P, Grundner C, et al. (2003) Structure-based, targeted deglycosylation of HIV-1 gp120 and effects on neutralization sensitivity and antibody recognition. Virology 313: 387–400. 12954207
55. Lyumkis D, Julien J-P, De Val N, Cupo A, Potter CS, et al. (2013) Cryo-EM structure of a fully glycosylated soluble cleaved HIV-1 envelope trimer. Science 342: 1484–1490. doi: 10.1126/science.1245627 24179160
56. Schiffner T, Sattentau QJ, Dorrell L, (2013) Development of prophylactic vaccines against HIV-1. Retrovirology 10: 72. doi: 10.1186/1742-4690-10-72 23866844
57. Klein F, Mouquet H, Dosenovic P, Scheid JF, Scharf L, et al. (2013) Antibodies in HIV-1 vaccine development and therapy. Science 341: 1199–1204. doi: 10.1126/science.1241144 24031012
58. West AP, Scharf L, Scheid JF, Klein F, Bjorkman PJ, et al. (2014) Structural Insights on the Role of Antibodies in HIV-1 Vaccine and Therapy. Cell 156: 633–648. doi: 10.1016/j.cell.2014.01.052 24529371
59. Goo L, Jalalian-Lechak Z, Richardson BA, Overbaugh J, (2012) A combination of broadly neutralizing HIV-1 monoclonal antibodies targeting distinct epitopes effectively neutralizes variants found in early infection. Journal of Virology 86: 10857–10861. doi: 10.1128/JVI.01414-12 22837204
60. Mabuka J, Goo L, Omenda MM, Nduati R, Overbaugh J, (2013) HIV-1 maternal and infant variants show similar sensitivity to broadly neutralizing antibodies, but sensitivity varies by subtype. AIDS 27: 1535–1544. doi: 10.1097/QAD.0b013e32835faba5 23856624
61. Doria-Rose NA, Louder MK, Yang Z, O'Dell S, Nason M, et al. (2012) HIV-1 neutralization coverage is improved by combining monoclonal antibodies that target independent epitopes. Journal of Virology 86: 3393–3397. doi: 10.1128/JVI.06745-11 22258252
62. Barouch DH, Whitney JB, Moldt B, Klein F, Oliveira TY, et al. (2013) Therapeutic efficacy of potent neutralizing HIV-1-specific monoclonal antibodies in SHIV-infected rhesus monkeys. Nature 503: 224–228. doi: 10.1038/nature12744 24172905
63. Shingai M, Nishimura Y, Klein F, Mouquet H, Donau OK, et al. (2013) Antibody-mediated immunotherapy of macaques chronically infected with SHIV suppresses viraemia. Nature 503: 277–280. doi: 10.1038/nature12746 24172896
64. Martin HL, Jackson DJ, Mandaliya K, Bwayo J, Rakwar JP, et al. (1994) Preparation for AIDS vaccine evaluation in Mombasa, Kenya: establishment of seronegative cohorts of commercial sex workers and trucking company employees. AIDS Res Hum Retroviruses 10 Suppl 2: S235–S237. 7865309
65. Wu X, Parast AB, Richardson BA, Nduati R, John-Stewart G, et al. (2006) Neutralization escape variants of human immunodeficiency virus type 1 are transmitted from mother to infant. Journal of Virology 80: 835–844. 16378985
66. Decker JM, Bibollet-Ruche F, Wei X, Wang S, Levy DN, et al. (2005) Antigenic conservation and immunogenicity of the HIV coreceptor binding site. J Exp Med 201: 1407–1419. 15867093