HLA class II genes modulate vaccine-induced antibody responses to affect HIV-1 acquisition

Science Translational Medicine

Volumn 7, Issue 296, 2015, Pages

  Prentice, Heather A ^a,b,l   Tomaras, Georgia D ^c   Geraghty, Daniel E ^d   Apps, Richard ^e   Fong, Youyi ^d   Ehrenberg, Philip K ^a   Rolland, Morgane ^a,b   Kijak, Gustavo H ^a,b   Krebs, Shelly J ^a,b   Nelson, Wyatt ^d   DeCamp, Allan ^d   Shen, Xiaoying ^c   Yates, Nicole L ^c   Zolla Pazner, Susan ^f   Nitayaphan, Sorachai ^g   Rerks Ngarm, Supachai ^h   Kaewkungwal, Jaranit ⁱ   Pitisuttithum, Punnee ^j   Ferrari, Guido ^c   McElrath, M Juliana ^d   Montefiori, David C ^c   Bailer, Robert T ^k   Koup, Richard A ^k   O'Connell, Robert J ^f   Robb, Merlin L ^a,b   Michael, Nelson L ^a   Gilbert, Peter B ^d   Kim, Jerome H ^a   Thomas, Rasmi ^a,b   more..

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

^b HENRY M JACKSON FOUNDATION FOR THE ADVANCEMENT OF MILITARY MEDICINE   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Fred Hutchinson Cancer Research Center   (United States)

^e FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

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

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

^h MINISTRY OF PUBLIC HEALTH   (Thailand)

ⁱ MAHIDOL UNIVERSITY   (Thailand)

^j MAHIDOL UNIVERSITY   (Thailand)

^k NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^l NONE   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

HLA ANTIGEN CLASS 2; HLA DPB1 ANTIGEN; HLA DQB1 ANTIGEN; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; NEUTRALIZING ANTIBODY; VIRUS ENVELOPE PROTEIN; EPITOPE; GLYCOPROTEIN GP 120; HLA DP ANTIGEN; HLA DQ ANTIGEN; HLA-DPB1 ANTIGEN; HLA-DQB1 ANTIGEN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G;

ALLELE; AMINO TERMINAL SEQUENCE; ANTIBODY RESPONSE; ANTIGEN ANTIBODY REACTION; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DPB1 13 GENE; DQB1 06 GENE; GENOTYPE; HLA CLASS 2 GENE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOMODULATION; INNATE IMMUNITY; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; TREATMENT OUTCOME; VIRUS ENVELOPE; ANTIBODY PRODUCTION; CHEMISTRY; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; METABOLISM; MULTIVARIATE ANALYSIS; PROTEIN TERTIARY STRUCTURE; REGRESSION ANALYSIS;

AIDS VACCINES; ALLELES; ANTIBODY FORMATION; EPITOPES; GENOTYPE; HISTOCOMPATIBILITY ANTIGENS CLASS II; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-1; HLA-DP BETA-CHAINS; HLA-DQ BETA-CHAINS; HUMANS; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; MULTIVARIATE ANALYSIS; PROTEIN STRUCTURE, TERTIARY; REGRESSION ANALYSIS;

EID: 84937131006     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aab4005     Document Type: Article

References (43)

1. S. Rerks-Ngarm, P. Pitisuttithum, S. Nitayaphan, J. Kaewkungwal, J. Chiu, R. Paris, N. Premsri, C. Namwat, M. de Souza, E. Adams, M. Benenson, S. Gurunathan, J. Tartaglia, J. G. McNeil, D. P. Francis, D. Stablein, D. L. Birx, S. Chunsuttiwat, C. Khamboonruang, P. Thongcharoen, M. L. Robb, N. L. Michael, P. Kunasol, J. H. Kim; MOPH-TAVEG Investigators, Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361, 2209-2220 (2009).
2. M. L. Robb, S. Rerks-Ngarm, S. Nitayaphan, P. Pitisuttithum, J. Kaewkungwal, P. Kunasol, C. Khamboonruang, P. Thongcharoen, P. Morgan, M. Benenson, R. M. Paris, J. Chiu, E. Adams, D. Francis, S. Gurunathan, J. Tartaglia, P. Gilbert, D. Stablein, N. L. Michael, J. H. Kim, Risk behaviour and time as covariates for efficacy of the HIV vaccine regimen ALVAC-HIV (vCP1521) and AIDSVAX B/E: A post-hoc analysis of the Thai phase 3 efficacy trial RV 144. Lancet Infect. Dis. 12, 531-537 (2012).
3. B. F. Haynes, P. B. Gilbert, M. J. McElrath, S. Zolla-Pazner, G. D. Tomaras, S. M. Alam, D. T. Evans, D. C. Montefiori, C. Karnasuta, R. Sutthent, H.-X. Liao, A. L. DeVico, G. K. Lewis, C. Williams, A. Pinter, Y. Fong, H. Janes, A. DeCamp, Y. Huang, M. Rao, E. Billings, N. Karasavvas, M. L. Robb, V. Ngauy, M. S. de Souza, R. Paris, G. Ferrari, R. T. Bailer, K. A. Soderberg, C. Andrews, P. W. Berman, N. Frahm, S. C. De Rosa, M. D. Alpert, N. L. Yates, X. Shen, R. A. Koup, P. Pitisuttithum, J. Kaewkungwal, S. Nitayaphan, S. Rerks-Ngarm, N. L. Michael, J. H. Kim, Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N. Engl. J. Med. 366, 1275-1286 (2012).
4. A. Pinter, W. J. Honnen, S. C. Kayman, O. Trochev, Z. Wu, Potent neutralization of primary HIV-1 isolates by antibodies directed against epitopes present in the V1/V2 domain of HIV-1 gp120. Vaccine 16, 1803-1811 (1998).
5. J. H. Kim, J.-L. Excler, N. L. Michael, Lessons from the RV144 Thai phase III HIV-1 vaccine trial and the search for correlates of protection. Annu. Rev. Med. 66, 423-437 (2015).
6. G. D. Tomaras, G. Ferrari, X. Shen, S. M. Alam, H.-X. Liao, J. Pollara, M. Bonsignori, M. A. Moody, Y. Fong, X. Chen, B. Poling, C. O. Nicholson, R. Zhang, X. Lu, R. Parks, J. Kaewkungwal, S. Nitayaphan, P. Pitisuttithum, S. Rerks-Ngarm, P. B. Gilbert, J. H. Kim, N. L. Michael, D. C. Montefiori, B. F. Haynes, Vaccine-induced plasma IgA specific for the C1 region of the HIV-1 envelope blocks binding and effector function of IgG. Proc. Natl. Acad. Sci. U.S.A. 110, 9019-9024 (2013).
7. M. Rolland, P. T. Edlefsen, B. B. Larsen, S. Tovanabutra, E. Sanders-Buell, T. Hertz, A. C. deCamp, C. Carrico, S. Menis, C. A. Magaret, H. Ahmed, M. Juraska, L. Chen, P. Konopa, S. Nariya, J. N. Stoddard, K. Wong, H. Zhao, W. Deng, B. S. Maust, M. Bose, S. Howell, A. Bates, M. Lazzaro, A. O'Sullivan, E. Lei, A. Bradfield, G. Ibitamuno, V. Assawadarachai, R. J. O'Connell, M. S. deSouza, S. Nitayaphan, S. Rerks-Ngarm, M. L. Robb, J. S. McLellan, I. Georgiev, P. D. Kwong, J. M. Carlson, N. L. Michael, W. R. Schief, P. B. Gilbert, J. I. Mullins, J. H. Kim, Increased HIV-1 vaccine efficacy against viruses with genetic signatures in Env V2. Nature 490, 417-420 (2012).
8. H.-X. Liao, M. Bonsignori, S. M. Alam, J. S. McLellan, G. D. Tomaras, M. A. Moody, D. M. Kozink, K.-K. Hwang, X. Chen, C.-Y. Tsao, P. Liu, X. Lu, R. J. Parks, D. C. Montefiori, G. Ferrari, J. Pollara, M. Rao, K. K. Peachman, S. Santra, N. L. Letvin, N. Karasavvas, Z.-Y. Yang, K. Dai, M. Pancera, J. Gorman, K. Wiehe, N. I. Nicely, S. Rerks-Ngarm, S. Nitayaphan, J. Kaewkungwal, P. Pitisuttithum, J. Tartaglia, F. Sinangil, J. H. Kim, N. L. Michael, T. B. Kepler, P. D. Kwong, J. R. Mascola, G. J. Nabel, A. Pinter, S. Zolla-Pazner, B. F. Haynes, Vaccine induction of antibodies against a structurally heterogeneous site of immune pressure within HIV-1 envelope protein variable regions 1 and 2. Immunity 38, 176-186 (2013).
9. N. L. Yates, H.-X. Liao, Y. Fong, A. deCamp, N. A. Vandergrift, W. T. Williams, S. M. Alam, G. Ferrari, Z.-Y. Yang, K. E. Seaton, P. W. Berman, M. D. Alpert, D. T. Evans, R. J. O'Connell, D. Francis, F. Sinangil, C. Lee, S. Nitayaphan, S. Rerks-Ngarm, J. Kaewkungwal, P. Pitisuttithum, J. Tartaglia, A. Pinter, S. Zolla-Pazner, P. B. Gilbert, G. J. Nabel, N. L. Michael, J. H. Kim, D. C. Montefiori, B. F. Haynes, G. D. Tomaras, Vaccine-induced Env V1-V2 IgG3 correlates with lower HIV-1 infection risk and declines soon after vaccination. Sci. Transl. Med. 6, 228-239 (2014).
10. A. W. Chung, M. Ghebremichael, H. Robinson, E. Brown, I. Choi, S. Lane, A.-S. Dugast, M. K. Schoen, M. Rolland, T. J. Suscovich, A. E. Mahan, L. Liao, H. Streeck, C. Andrews, S. Rerks-Ngarm, S. Nitayaphan, M. S. de Souza, J. Kaewkungwal, P. Pitisuttithum, D. Francis, N. L. Michael, J. H. Kim, C. Bailey-Kellogg, M. E. Ackerman, G. Alter, Polyfunctional Fc-effector profiles mediated by IgG subclass selection distinguish RV144 and VAX003 vaccines. Sci. Transl. Med. 6, 228-238 (2014).
11. M. S. de Souza, S. Ratto-Kim, W. Chuenarom, A. Schuetz, S. Chantakulkij, B. Nuntapinit, A. Valencia-Micolta, D. Thelian, S. Nitayaphan, P. Pitisuttithum, R. M. Paris, J. Kaewkungwal, N. L. Michael, S. Rerks-Ngarm, B. Mathieson, M. Marovich, J. R. Currier, J. H. Kim; Ministry of Public Health-Thai AIDS Vaccine Evaluation Group Collaborators, The Thai phase III trial (RV144) vaccine regimen induces T cell responses that preferentially target epitopes within the V2 region of HIV-1 envelope. J. Immunol. 188, 5166-5176 (2012).
12. C. A. Alper, M. S. Kruskall, D. Marcus-Bagley, D. E. Craven, A. J. Katz, S. J. Brink, J. L. Dienstag, Z. Awdeh, E. J. Yunis, Genetic prediction of nonresponse to hepatitis B vaccine. N. Engl. J. Med. 321, 708-712 (1989).
13. S. Caillat-Zucman, J.-J. Gimenez, F. Wambergue, G. Albouze, B. Lebkiri, C. Naret, A. Moynot, P. Jungers, J. F. Bach, Distinct HLA class II alleles determine antibody response to vaccination with hepatitis B surface antigen. Kidney Int. 53, 1626-1630 (1998).
14. H. A. Stephens, A. E. Brown, D. Chandanayingyong, H. K. Webster, M. Sirikong, P. Longta, R. Vangseratthana, D. M. Gordon, S. Lekmak, E. Rungruang, The presence of the HLA class II allele DPB1∗0501 in ethnic Thais correlates with an enhanced vaccine-induced antibody response to a malaria sporozoite antigen. Eur. J. Immunol. 25, 3142-3147 (1995).
15. I. G. Ovsyannikova, V. S. Pankratz, R. A. Vierkant, R. M. Jacobson, G. A. Poland, Human leukocyte antigen haplotypes in the genetic control of immune response to measles-mumps-rubella vaccine. J. Infect. Dis. 193, 655-663 (2006).
16. R. Paris, S. Bejrachandra, P. Thongcharoen, S. Nitayaphan, P. Pitisuttithum, A. Sambor, S. Gurunathan, D. Francis, S. Ratto-Kim, C. Karnasuta, M. S. de Souza, V. R. Polonis, A. E. Brown, J. H. Kim, H. A. Stephens; Thai AIDS Vaccine Evaluation Group, HLA class II restriction of HIV-1 cladespecific neutralizing antibody responses in ethnic Thai recipients of the RV144 prime-boost vaccine combination of ALVAC-HIV and AIDSVAX® B/E. Vaccine 30, 832-836 (2012).
17. + T cell responses with HIV immune control. Nat. Med. 19, 930-933 (2013).
18. S. J. Spencer, A. Burns, G. Gaskin, C. D. Pusey, A. J. Rees, HLA class II specificities in vasculitis with antibodies to neutrophil cytoplasmic antigens. Kidney Int. 41, 1059-1063 (1992).
19. B. Julg, E. S. Moodley, Y. Qi, D. Ramduth, S. Reddy, Z. Mncube, X. Gao, P. J. Goulder, R. Detels, T. Ndung'u, B. D. Walker, M. Carrington, Possession of HLA class II DRB1∗1303 associates with reduced viral loads in chronic HIV-1 clade C and B infection. J. Infect. Dis. 203, 803-809 (2011).
20. K. M. Baldwin, P. K. Ehrenberg, A. Geretz, H. A. Prentice, S. Nitayaphan, S. Rerks-Ngarm, J. Kaewkungwal, P. Pitisuttithum, R. J. O'Connell, J. H. Kim, R. Thomas, HLA class II diversity in HIV-1 uninfected individuals from the placebo arm of the RV144 Thai vaccine efficacy trial. Tissue Antigens 85, 117-126 (2015).
21. T. Zhou, I. Georgiev, X. Wu, Z. Y. Yang, K. Dai, A. Finzi, Y. D. Kwon, J. F. Scheid, W. Shi, L. Xu, Y. Yang, J. Zhu, M. C. Nussenzweig, J. Sodroski, L. Shapiro, G. J. Nabel, J. R. Mascola, P. D. Kwong, Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329, 811-817 (2010).
22. C. D. Rizzuto, R. Wyatt, N. Hernández-Ramos, Y. Sun, P. D. Kwong, W. A. Hendrickson, J. Sodroski, A conserved HIV gp120 glycoprotein structure involved in chemokine receptor binding. Science 280, 1949-1953 (1998).
23. P. D. Kwong, R. Wyatt, J. Robinson, R. W. Sweet, J. Sodroski, W. A. Hendrickson, Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393, 648-659 (1998).
24. W. Zhang, A. P. Godillot, R. Wyatt, J. Sodroski, I. Chaiken, Antibody 17b binding at the coreceptor site weakens the kinetics of the interaction of envelope glycoprotein gp120 with CD4. Biochemistry 40, 1662-1670 (2001).
25. J. Klein, A. Sato, The HLA system. Second of two parts. N. Engl. J. Med. 343, 782-786 (2000).
26. M. M. Fernando, C. R. Stevens, E. C. Walsh, P. L. De Jager, P. Goyette, R. M. Plenge, T. J. Vyse, J. D. Rioux, Defining the role of the MHC in autoimmunity: A review and pooled analysis. PLOS Genet. 4, e1000024 (2008).
27. H. K. Machulla, U. Schönermarck, A. Schaaf, L. P. Müller, C. Kloß, J. Krüger, G. Kunze, G. Schönermarck, J. Langner, HLA-A, B, Cw and DRB1, DRB3/4/5, DQB1, DPB1 frequencies in German immunoglobulin A-deficient individuals. Scand. J. Immunol. 52, 207-211 (2000).
28. J. Kralovicova, L. Hammarström, A. Plebani, A. D. Webster, I. Vorechovsky, Fine-scale mapping at IGAD1 and genome-wide genetic linkage analysis implicate HLA-DQ/DR as a major susceptibility locus in selective IgA deficiency and common variable immunodeficiency. J. Immunol. 170, 2765-2775 (2003).
29. G. H. Jorgensen, A. E. Ornolfsson, A. Johannesson, S. Gudmundsson, M. Janzi, N. Wang, L. Hammarström, B. R. Ludviksson, Association of immunoglobulin A deficiency and elevated thyrotropin-receptor autoantibodies in two Nordic countries. Hum. Immunol. 72, 166-172 (2010).
30. J. A. Todd, J. I. Bell, H. O. McDevitt, HLA-DQb gene contributes to susceptibility and resistance to insulin-dependent diabetes mellitus. Nature 329, 599-604 (1987).
31. R. J. O'Connell, J.-L. Excler, HIV vaccine efficacy and immune correlates of risk. Curr. HIV Res. 11, 450-463 (2013).
32. G. D. Tomaras, B. F. Haynes, Advancing toward HIV-1 vaccine efficacy through the intersections of immune correlates. Vaccines 2, 15-35 (2014).
33. A. J. Gartland, S. Li, J. McNevin, G. D. Tomaras, R. Gottardo, H. Janes, Y. Fong, D. Morris, D. E. Geraghty, G. H. Kijak, P. T. Edlefsen, N. Frahm, B. B. Larsen, S. Tovanabutra, E. Sanders-Buell, A. C. deCamp, C. A. Magaret, H. Ahmed, J. P. Goodridge, L. Chen, P. Konopa, S. Nariya, J. N. Stoddard, K. Wong, H. Zhao, W. Deng, B. S. Maust, M. Bose, S. Howell, A. Bates, M. Lazzaro, A. O'Sullivan, E. Lei, A. Bradfield, G. Ibitamuno, V. Assawadarachai, R. J. O'Connell, M. S. deSouza, S. Nitayaphan, S. Rerks-Ngarm, M. L. Robb, J. Sidney, A. Sette, S. Zolla-Pazner, D. Montefiori, M. J. McElrath, J. I. Mullins, J. H. Kim, P. B. Gilbert, T. Hertz, Analysis of HLA A∗02 association with vaccine efficacy in the RV144 HIV-1 vaccine trial. J. Virol. 88, 8242-8255 (2014).
34. S. S. Li, P. B. Gilbert, G. D. Tomaras, G. Kijak, G. Ferrari, R. Thomas, C.-W. Pyo, S. Zolla-Pazner, D. Montefiori, H.-X. Liao, G. Nabel, A. Pinter, D. T. Evans, R. Gottardo, J. Y. Dai, H. Janes, D. Morris, Y. Fong, P. T. Edlefsen, F. Li, N. Frahm, M. D. Alpert, H. Prentice, S. Rerks-Ngarm, P. Pitisuttithum, J. Kaewkungwal, S. Nitayaphan, M. L. Robb, R. J. O'Connell, B. F. Haynes, N. L. Michael, J. H. Kim, M. J. McElrath, D. E. Geraghty, FCGR2C polymorphisms associate with HIV-1 vaccine protection in RV144 trial. J. Clin. Invest. 124, 3879-3890 (2014).
35. H. A. Prentice, P. K. Ehrenberg, K. M. Baldwin, A. Geretz, C. Andrews, S. Nitayaphan, S. Rerks-Ngarm, J. Kaewkungwal, P. Pitisuttithum, R. J. O'Connell, M. L. Robb, J. H. Kim, N. L. Michael, R. Thomas, HLA class I, KIR, and genome-wide SNP diversity in the RV144 Thai phase 3 HIV vaccine clinical trial. Immunogenetics 66, 299-310 (2014).
36. P. K. Ehrenberg, A. Geretz, K. M. Baldwin, R. Apps, V. R. Polonis, M. L. Robb, J. H. Kim, N. L. Michael, R. Thomas, High-throughput multiplex HLA genotyping by next-generation sequencing using multi-locus individual tagging. BMC Genomics 15, 864 (2014).
37. R. Kosoy, R. Nassir, C. Tian, P. A. White, L. M. Butler, G. Silva, R. Kittles, M. E. Alarcon-Riquelme, P. K. Gregersen, J. W. Belmont, F. M. De La Vega, M. F. Seldin, Ancestry informative marker sets for determining continental origin and admixture proportions in common populations in America. Hum. Mutat. 30, 69-78 (2009).
38. A. L. Price, N. J. Patterson, R. M. Plenge, M. E. Weinblatt, N. A. Shadick, D. Reich, Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet. 38, 904-909 (2006).
39. O. Borgan, B. Langholz, S. O. Samuelsen, L. Goldstein, J. Pogoda, Exposure stratified case-cohort designs. Lifetime Data Anal. 6, 39-58 (2000).
40. N. E. Breslow, R. Holubkov, Weighted likelihood, pseudo-likelihood and maximum likelihood methods for logistic regression analysis of two-stage data. Stat. Med. 16, 103-116 (1997).
41. Y. Benjamini, Y. Hochberg, Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Stat. Methodol. 57, 289-300 (1995).
42. S. Holm, A simple sequentially rejective multiple test procedure. Scand. J. Statist. 6, 65-70 (1979).
43. S. Zolla-Pazner, A. deCamp, P. B. Gilbert, C. Williams, N. L. Yates, W. T. Williams, R. Howington, Y. Fong, D. E. Morris, K. A. Soderberg, C. Irene, C. Reichman, A. Pinter, R. Parks, P. Pitisuttithum, J. Kaewkungwal, S. Rerks-Ngarm, S. Nitayaphan, C. Andrews, R. J. O'Connell, Z.-Y. Yang, G. J. Nabel, J. H. Kim, N. L. Michael, D. C. Montefiori, H.-X. Liao, B. F. Haynes, G. D. Tomaras, Vaccine-induced IgG antibodies to V1V2 regions of multiple HIV-1 subtypes correlate with decreased risk of HIV-1 infection. PLOS One 9, e87572 (2014).