Vaccine-induced human antibodies specific for the third variable region of HIV-1 gp120 impose immune pressure on infecting viruses

EBioMedicine

Volumn 1, Issue 1, 2014, Pages 37-45

  Zolla Pazner, Susan ^a,b   Edlefsen, Paul T ^c   Rolland, Morgane ^d   Kong, Xiang Peng ^b   deCamp, Allan ^c   Gottardo, Raphael ^c   Williams, Constance ^b   Tovanabutra, Sodsai ^d   Sharpe Cohen, Sandra ^b   Mullins, James I ^e   deSouza, Mark S ^f   Karasavvas, Nicos ^g   Nitayaphan, Sorachai ^g   Rerks Ngarm, Supachai ^h   Pitisuttihumi, Punnee ⁱ   Kaewkungwal, Jaranit ⁱ   O'Connell, Robert J ^g   Robb, Merlin L ^j   Michael, Nelson L ^j   Kim, Jerome H ^j   Gilbert, Peter ^c   more..

^a New York Veterans Affairs Harbor Healthcare System   (United States)

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

^c Fred Hutchinson Cancer Research Center   (United States)

^d WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

^f THAI RED CROSS AIDS RESEARCH CENTRE   (Thailand)

^g ARMED FORCES RESEARCH INSTITUTE OF MEDICAL SCIENCES   (Thailand)

^h MINISTRY OF PUBLIC HEALTH   (Thailand)

ⁱ MAHIDOL UNIVERSITY   (Thailand)

^j US Military HIV Research Program   (United States)

more..

Author keywords

Antibody; Clinical trial; HIV; Vaccine

Indexed keywords

ERDOSTEINE; GLYCOPROTEIN GP 120; IMMUNOGLOBULIN G ANTIBODY; PLACEBO;

ADULT; AMINO ACID SEQUENCE; ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; CROSS REACTION; DOUBLE BLIND PROCEDURE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE SEQUENCE; HUMAN; HUMAN EXPERIMENT; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOGLOBULIN VARIABLE REGION; MULTICENTER STUDY; NORMAL HUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN MICROARRAY; RANDOMIZED CONTROLLED TRIAL; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS;

EID: 84921972284     PISSN: None     EISSN: 23523964     Source Type: Journal    
DOI: 10.1016/j.ebiom.2014.10.022     Document Type: Article

References (68)

1. Abagyan, R., Batalov, S., et al., 1997. Homology modeling with internal coordinate mechanics: deformation zonemapping and improvements ofmodels via conformational search. Proteins (Suppl. 1), 29-37.
2. Almond, D., Kimura, T., et al., 2010. Structural conservation predominates over sequence variability in the crown of HIV-1'S V3 loop. AIDS Res. Hum. Retroviruses 26 (6), 717-723.
3. Andrabi, R., Williams, C., et al., 2013. Cross-neutralizing activity of human anti-V3 monoclonal antibodies derived from non-B clade HIV-1 infected individuals. Virology 439 (2), 81-88.
4. Andrus, L., Prince, A.M., et al., 1998. Passive immunization with a human immunodeficiency virus type-1 neutralizing monoclonal antibody in Hu-PBL-SCID mice: isolation of a neutralization escape variant. J. Infect. Dis. 177 (4), 889-897.
5. Bartesaghi, A., Merk, A., et al., 2013. Prefusion structure of trimeric HIV-1 envelope glycoprotein determined by cryo-electron microscopy. Nat. Struct. Mol. Biol. 20 (12), 1352-1357.
6. Bonsignori, M., Pollara, J., et al., 2012. Antibody-dependent cellular cytotoxicity-mediating antibodies from an HIV-1 vaccine efficacy trial target multiple epitopes and preferentially use the VH1 gene family. J. Virol. 86 (21), 11521-11532.
7. Burke, V., Williams, C., et al., 2009. Structural basis of the cross-reactivity of genetically related human anti-HIV-1 monoclonal antibodies: implications for design of V3-based immunogens. Structure 17 (11), 1538-1546.
8. Carlson, J.M., Brumme, Z.L., et al., 2008. Phylogenetic dependency networks: inferring patterns of CTL escape and codon covariation in HIV-1 Gag. PLoS Comput. Biol. 4 (11), e1000225.
9. Conley, A.J., Gorny, M.K., et al., 1994. Neutralization of primary human immunodeficiency virus type 1 isolates by the broadly reactive anti-V3 monoclonal antibody, 447-52D. J. Virol. 68 (11), 6994-7000.
10. Corti, D., Langedijk, J.P., 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 (1), e8805.
11. Eda, Y., Murakami, T., et al., 2006. Anti-V3 humanized antibody KD-247 effectively suppresses ex vivo generation of human immunodeficiency virus type 1 and affords sterile protection of monkeys against a heterologous simian/human immunodeficiency virus infection. J. Virol. 80 (11), 5563-5570.
12. Edlefsen, P.T., Rolland, M., et al., 2014. Comprehensive sieve analysis of breakthrough HIV- 1 sequences in the RV144 vaccine efficacy trial. PLoS Comput. Biol. http://dx.doi.org/10.1371/journal.pcbi.1003973 (in press).
13. Emini, E.A., Schleif, W.A., et al., 1992. Prevention of HIV-1 infection in chimpanzees by gp120 V3 domain-specific monoclonal antibody. Nature 355 (6362), 728-730.
14. Gilbert, P.B., 2000. Comparison of competing risks failure time methods and time-independent methods for assessing strain variations in vaccine protection. Stat. Med. 19 (22), 3065-3086.
15. Gilbert, P.B., Novitsky, V., et al., 2005. Covariability of selected amino acid positions for HIV type 1 subtypes C and B. AIDS Res. Hum. Retroviruses 21 (12), 1016-1030.
16. Gorny, M.K., Conley, A.J., et al., 1992. Neutralization of diverse HIV-1 variants by an anti-V3 human monoclonal antibody. J. Virol. 66 (12), 7538-7542.
17. Gorny, M.K., Xu, J.-Y., et al., 1993. Repertoire of neutralizing human monoclonal antibodies specific for the V3 domain of HIV-1 gp120. J. Immunol. 150 (2), 635-643.
18. Gorny, M.K., VanCott, T.C., et al., 1997. Human monoclonal antibodies to the V3 loop of HIV-1 with intra- and interclade cross-reactivity. J. Immunol. 159 (10), 5114-5122.
19. Gorny, M.K., Williams, C., et al., 2002. Human monoclonal antibodies specific for conformation-sensitive epitopes of V3 neutralize HIV-1 primary isolates fromvarious clades. J. Virol. 76 (18), 9035-9045.
20. Gorny, M.K., Revesz, K., et al., 2004. The V3 loop is accessible on the surface of most human immunodeficiency virus type 1 primary isolates and serves as a neutralization epitope. J. Virol. 78 (5), 2394-2404.
21. Gorny, M.K., Wang, X.H., 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 (5), 917-926.
22. Gorny, M.K., Pan, R., et al., 2012. Functional and immunochemical cross-reactivity of V2-specific monoclonal antibodies from human immunodeficiency virus type 1-infected individuals. Virology 427, 198-207.
23. + to linear epitopes in the V2 and V3 regions of HIV-1 gp120 as correlates of infection risk in the RV144 vaccine efficacy trial. PLoS One 8 (9), e75665.
24. Haynes, B.F., Gilbert, P.B., et al., 2012. Immune correlates analysis of the ALVAC-AIDSVAX HIV-1 vaccine efficacy trial. N. Engl. J. Med. 366 (14), 1275-1286.
25. Hill, C.M., Deng, H.K., et al., 1997. Envelope glycoproteins from HIV-1, HIV-2 and SIV can use human CCR5 as a coreceptor for viral entry and make direct CD4-dependent interactions with this chemokine receptor. J. Virol. 71, 6296-6304.
26. Hioe, C.E., Wrin, T., et al., 2010. Anti-V3 monoclonal antibodies display broad neutralizing activities against multiple HIV-1 subtypes. PLoS One 5 (4), e10254.
27. Holm, S., 1979. A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6 (65-70).
28. Jiang, X., Burke, V., et al., 2010. Conserved structural elements in the V3 crown of HIV-1 GP120. Nat. Struct. Mol. Biol. 17 (8), 955-961.
29. Julien, J.-P., Cupo, A., et al., 2013. Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science 342 (6165), 1477-1483.
30. Karasavvas, N., Billings, E., et al., 2012. The Thai phase III HIV type 1 vaccine trial (RV144) regimen induces antibodies that target conserved regions within the V2 loop of gp120. AIDS Res. Hum. Retroviruses 28 (11).
31. Killikelly, A., Zhang, H.-T., et al., 2013. Thermodynamic signatures of the antigen binding site ofmAb 447-52D targeting the third variable region of HIV-1 gp120. Biochemistry 52 (36), 6249-6257.
32. Klein, F., Gaebler, C., et al., 2012. Broad neutralization by a combination of antibodies recognizing the CD4 binding site and a new conformational epitope on the HIV-1 envelope protein. J. Exp. Med. 209 (8), 1469-1479.
33. Liao, H.-X., Bonsignori, M., et al., 2013. Vaccine induction of antibodies against a structurally heterogeneous site of immune pressure within HIV-1 envelope protein variable regions 1 and 2. Immunity 38 (1), 176-186.
34. + from RV144 vaccinees. J. Virol. 87 (14), 7828-7836.
35. Lunn, M., McNeil, D., 1995. Applying Cox regression to competing risks. Biometrics 51 (2), 524-532.
36. Lynch, R.M., Shen, T., et al., 2009. Appreciating HIV type 1 diversity: subtype differences in Env. AIDS Res. Hum. Retroviruses 25 (3), 237-248.
37. Lyumkis, D., Julien, J.P., et al., 2013. Cryo-EM structure of a fully glycosylated soluble cleaved HIV-1 envelope trimer. Science 342 (6165), 1484-1490.
38. Mascola, J.R., Haynes, B.F., 2013. HIV-1 neutralizing antibodies: understanding nature's pathways. Immunol. Rev. 254 (1), 225-244.
39. Mayr, L.M., Cohen, S., et al., 2013. Epitopemapping of conformational V2-specific anti-HIV human monoclonal antibodies reveals an immunodominant site in V2. PLoS One 8 (7), e70859.
40. Montefiori, D.C., Karnasuta, C., et al., 2012. Magnitude and breadth of the neutralizing antibody response in the RV144 and Vax003 HIV-1 vaccine efficacy trials. J. Infect. Dis. 206 (3), 431-441.
41. Mouquet, H., Klein, F., et al., 2011. Memory B cell antibodies to HIV-1 gp140 cloned from individuals infected with clade A and B viruses. PLoS One 6 (9), e24078.
42. Nyambi, P.N., Mbah, H.A., et al., 2000. Conserved and exposed epitopes on intact, native, primary human immunodeficiency virus type 1 virions of group M. J. Virol. 74 (15), 7096-7107.
43. Pancera, M., Zhou, T., et al., 2014. Structure and immune recognition of trimeric pre-fusion HIV-1 Env. Nature 514 (7523), 455-461. http://dx.doi.org/10.1038/nature 13808.
44. Pejchal, R., Doores, K.J., et al., 2011. A potent and broad neutralizing antibody recognizes and penetrates the HIV glycan shield. Science 334 (6059), 1097-1103.
45. Pollara, J., Bonsignori, M., et al., 2014. HIV-1 vaccine-induced C1 and V2 Env-specific antibodies synergize for increased antiviral activities. J. Virol. 88 (14), 7715-7726.
46. Poon, A.F., Lewis, F.I., et al., 2007. An evolutionary-network model reveals stratified interactions in the V3 loop of the HIV-1 envelope. PLoS Comput. Biol. 3 (11), e231.
47. Prentice, R.L., Kalbfleisch, J.D., et al., 1978. The analysis of failure times in the presence of competing risks. Biometrics 34 (4), 541-554.
48. Ratner, L., Fisher, A., et al., 1987. Complete nucleotide sequences of functional clones of the AIDS virus. AIDS Res. Hum. Retroviruses 3 (1), 57-69.
49. Rerks-Ngarm, S., Pitisuttithum, P., et al., 2009. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361 (23), 2209-2220.
50. Rolland, M., Edlefsen, P.T., et al., 2012. Increased HIV-1 vaccine efficacy against viruses with genetic signatures in Env V2. Nature 490 (7420), 417-420.
51. Safrit, J.T., Fung, M.S., et al., 1993. Hu-PBL-SCID mice can be protected from HIV-1 infection by passive transfer of monoclonal antibody to the principal neutralizing determinant of envelope gp120. Aids 7 (1), 15-21.
52. Shioda, T., Levy, J.A., et al., 1991. Macrophage and T cell line tropisms of HIV-1 are determined by specific regions of the envelope gp120 gene. Nature 349 (6305), 167-169.
53. Shioda, T., Levy, J.A., et al., 1992. Small amino acid changes in the V3 hypervariable region of gp120 can affect the T-cell-line and macrophage tropism of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. U. S. A. 89 (20), 9434-9438.
54. Spurrier, B., Sampson, J., et al., 2014. Functional implications of the binding mode of a human conformation-dependent V2 monoclonal antibody against HIV. J. Virol. 88 (8), 4100-4112.
55. Stanfield, R.L., Gorny, M.K., et al., 2004. Structural rationale for the broad neutralization of HIV-1 by human antibody 447-52D. Structure 12 (2), 193-204.
56. Stanfield, R.L., Gorny, M.K., et al., 2006. Crystal structures of HIV-1 neutralizing antibody 2219 in complex with three different V3 peptides reveal a new binding mode for HIV-1 cross-reactivity. J. Virol. 80 (12), 6093-6105.
57. + memory B cells. Immunity 26 (2), 205-213.
58. + antibodies followed by plasma anti-gp41 antibodies with ineffective control of initial viremia. J. Virol. 82 (24), 12449-12463.
59. Trkola, A., Dragic, T., et al., 1996. CD4-dependent, antibody-sensitive interactions between HIV-1 and its co-receptor CCR-5. Nature 384 (6605), 184-187.
60. Walker, L.M., Huber, M., et al., 2011. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477, 466-470.
61. Watkins, J.D., Siddappa, N.B., et al., 2011. An anti-HIV-1V3 loop antibody fully protects cross-clade and elicits T-cell immunity in macaques mucosally challenged with an R5 clade C SHIV. PLoS One 6 (3), e18207.
62. Xiang, S.H., Finzi, A., et al., 2010. A V3 loop-dependent gp120 element disrupted by CD4 binding stabilizes the human immunodeficiency virus envelope glycoprotein trimer. J. Virol. 84 (7), 3147-3161.
63. Yates, N.L., Liao, H.X., et al., 2014. Vaccine-induced Env V1-V2 IgG+3 correlates with lower HIV-1 infection risk and declines soon after vaccination. Sci. Transl. Med. 6 (228), 228ra239.
64. Zolla-Pazner, S., 2005. Improving on nature: focusing the immune response on the V3 loop. Hum. Antibodies 14 (3-4), 69-72.
65. Zolla-Pazner, S., 2014. A critical question for HIV vaccine development:Which antibodies to induce? Science 345 (6193), 167-168.
66. Zolla-Pazner, S., Cardozo, T., 2010. Structure-function relationships of HIV-1 envelope sequence-variable regions provide a paradigm for vaccine design. Nat. Rev. Immunol. 10 (7), 527-535.
67. Zolla-Pazner, S., deCamp, A.C., et al., 2013. Analysis of V2 antibody responses induced in vaccinees in the ALVAC/AIDSVAX HIV-1 Vaccine Efficacy Trial. PLoS One 8 (1), e53629.
68. + antibodies to V1V2 regions of multiple HIV-1 subtypes correlate with decreased risk of HIV-1 infection. PLoS One 9 (2), e87572.