Systems serology for evaluation of HIV vaccine trials

Immunological Reviews

Volumn 275, Issue 1, 2017, Pages 262-270

  Ackerman, Margaret E ^a   Barouch, Dan H ^b,c   Alter, Galit ^b  

^a DARTMOUTH COLLEGE   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

antibody; effector function; Fc receptor; machine learning; vaccine

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS VACCINE; NEUTRALIZING ANTIBODY; POLYCLONAL ANTIBODY; VIRUS VECTOR; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY;

ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; CELLULAR IMMUNITY; CLINICAL TRIAL (TOPIC); DRUG DESIGN; DRUG EFFICACY; EPIGENETICS; EVALUATION STUDY; FLOW CYTOMETRY; GENETIC TRANSCRIPTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMORAL IMMUNITY; IMMUNIZATION; MACHINE LEARNING; METABOLOMICS; NONHUMAN; PRIMATE; PRIORITY JOURNAL; REVIEW; SEROLOGY; ANIMAL; HIV INFECTIONS; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; SERODIAGNOSIS; SYSTEM ANALYSIS; TREATMENT OUTCOME; VACCINATION;

AIDS SERODIAGNOSIS; AIDS VACCINES; ANIMALS; ANTIBODIES, NEUTRALIZING; HIV ANTIBODIES; HIV INFECTIONS; HIV-1; HUMANS; PRIMATES; SYSTEMS ANALYSIS; TREATMENT OUTCOME; VACCINATION;

EID: 85010875145     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12503     Document Type: Review

References (68)

1. Plotkin SA. Correlates of protection induced by vaccination. Clin Vaccine Immunol. 2010;17:1055–1065.
2. Burton DR, Ahmed R, Barouch DH, et al. A blueprint for HIV vaccine discovery. Cell Host Microbe. 2012;12:396–407.
3. Rappuoli R. Reverse vaccinology. Curr Opin Microbiol. 2000;3:445–450.
4. Kulp DW, Schief WR. Advances in structure-based vaccine design. Curr Opin Virol. 2013;3:322–331.
5. Rappuoli R, Bottomley MJ, D'Oro U, Finco O, De Gregorio E. Reverse vaccinology 2.0: Human immunology instructs vaccine antigen design. J Exp Med. 2016;213:469–481.
6. Pulendran B, Li S, Nakaya HI. Systems vaccinology. Immunity. 2010;33:516–529.
7. Querec TD, Akondy RS, Lee EK, et al. Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nat Immunol. 2009;10:116–125.
8. Lin L, Finak G, Ushey K, et al. COMPASS identifies T-cell subsets correlated with clinical outcomes. Nat Biotechnol. 2015;33:610–616.
9. Plotkin SA. Vaccines: correlates of vaccine-induced immunity. Clin Infect Dis. 2008;47:401–409.
10. Hessell AJ, Hangartner L, Hunter M, et al. Fc receptor but not complement binding is important in antibody protection against HIV. Nature. 2007;449:101–104.
11. Barouch DH, Stephenson KE, Borducchi EN, et al. Protective efficacy of a global HIV-1 mosaic vaccine against heterologous SHIV challenges in rhesus monkeys. Cell. 2013;155:531–539.
12. Bournazos S, Klein F, Pietzsch J, Seaman MS, Nussenzweig MC, Ravetch JV. Broadly neutralizing anti-HIV-1 antibodies require Fc effector functions for in vivo activity. Cell. 2014;158:1243–1253.
13. Forthal DN, Landucci G, Daar ES. Antibody from patients with acute human immunodeficiency virus (HIV) infection inhibits primary strains of HIV type 1 in the presence of natural-killer effector cells. J Virol. 2001;75:6953–6961.
14. DiLillo DJ, Tan GS, Palese P, Ravetch JV. Broadly neutralizing hemagglutinin stalk-specific antibodies require FcgammaR interactions for protection against influenza virus in vivo. Nat Med. 2014;20:143–151.
15. Jegerlehner A, Schmitz N, Storni T, Bachmann MF. Influenza A vaccine based on the extracellular domain of M2: Weak protection mediated via antibody-dependent NK cell activity. J Immunol. 2004;172:5598–5605.
16. Kohl S, Loo LS, Pickering LK. Protection of neonatal mice against herpes simplex viral infection by human antibody and leukocytes from adult, but not neonatal humans. J Immunol. 1981;127:1273–1275.
17. Kohl S, Loo LS. Protection of neonatal mice against herpes simplex virus infection: Probable in vivo antibody-dependent cellular cytotoxicity. J Immunol. 1982;129:370–376.
18. Warfield KL, Swenson DL, Olinger GG, Kalina WV, Aman MJ, Bavari S. Ebola virus-like particle-based vaccine protects nonhuman primates against lethal Ebola virus challenge. J Infect Dis. 2007;196(Suppl 2):S430–S437.
19. Bouharoun-Tayoun H, Oeuvray C, Lunel F, Druilhe P. Mechanisms underlying the monocyte-mediated antibody-dependent killing of Plasmodium falciparum asexual blood stages. J Exp Med. 1995;182:409–418.
20. Shi J, McIntosh RS, Pleass RJ. Antibody- and Fc-receptor-based therapeutics for malaria. Clin Sci. 2006;110:11–19.
21. Chung AW, Kumar MP, Arnold KB, et al. Dissecting polyclonal vaccine-induced humoral immunity against HIV using systems serology. Cell. 2015;163:988–998.
22. Chung AW, Ghebremichael M, Robinson H, et al. Polyfunctional Fc-effector profiles mediated by IgG subclass selection distinguish RV144 and VAX003 vaccines. Sci Transl Med. 2014;6:228ra38.
23. Ackerman ME, Crispin M, Yu X, et al. Natural variation in Fc glycosylation of HIV-specific antibodies impacts antiviral activity. J Clin Invest. 2013;123:2183–2192.
24. Ackerman ME, Dugast AS, McAndrew EG, et al. Enhanced phagocytic activity of HIV-specific antibodies correlates with natural production of immunoglobulins with skewed affinity for FcgammaR2a and FcgammaR2b. J Virol. 2013;87:5468–5476.
25. Lai JI, Licht AF, Dugast AS, et al. Divergent antibody subclass and specificity profiles but not protective HLA-B alleles are associated with variable antibody effector function among HIV-1 controllers. J Virol. 2014;88:2799–2809.
26. Ackerman ME, Moldt B, Wyatt RT, et al. A robust, high-throughput assay to determine the phagocytic activity of clinical antibody samples. J Immunol Methods. 2011;366:8–19.
27. Brown EP, Licht AF, Dugast AS, et al. High-throughput, multiplexed IgG subclassing of antigen-specific antibodies from clinical samples. J Immunol Methods. 2012;386:117–123.
28. Sajadi MM, Farshidpour M, Brown EP, et al. Lambda light chain bias associated with enhanced binding and function of anti-HIV Env glycoprotein antibodies. J Infect Dis. 2015;. doi:10.1093/infdis/jiv448.
29. Storcksdieck Genannt Bonsmann M, Niezold T, Temchura V, et al. Enhancing the quality of antibodies to HIV-1 envelope by GagPol-specific Th cells. J Immunol. 2015;195:4861–4872.
30. Chung AW, Crispin M, Pritchard L, et al. Identification of antibody glycosylation structures that predict monoclonal antibody Fc-effector function. AIDS. 2014;28:2523–2530.
31. Choi I, Chung AW, Suscovich TJ, et al. Machine learning methods enable predictive modeling of antibody feature:Function relationships in RV144 vaccinees. PLoS Comput Biol. 2015;11:e1004185.
32. Barouch DH, Alter G, Broge T, et al. HIV-1 vaccines. Protective efficacy of adenovirus/protein vaccines against SIV challenges in rhesus monkeys. Science. 2015;349:320–324.
33. Barouch DH, Liu J, Peter L, et al. Characterization of humoral and cellular immune responses elicited by a recombinant adenovirus serotype 26 HIV-1 Env vaccine in healthy adults (IPCAVD 001). J Infect Dis. 2013;207:248–256.
34. Ackerman ME, Mikhailova A, Brown EP, et al. Polyfunctional HIV-specific antibody responses are associated with spontaneous HIV control. PLoS Pathog. 2016;12:e1005315.
35. Georgiev IS, Doria-Rose NA, Zhou T, et al. Delineating antibody recognition in polyclonal sera from patterns of HIV-1 isolate neutralization. Science. 2013;340:751–756.
36. Ackerman ME, Dugast AS, McAndrew EG, et al. Enhanced phagocytic activity of HIV-specific antibodies correlates with natural production of immunoglobulins with skewed affinity for FcgammaR2a and FcgammaR2b. J Virol. 2013;. doi:10.1128/JVI.03403-12.
37. Ackerman ME, Crispin M, Yu X, et al. Natural variation in Fc glycosylation of HIV-specific antibodies impacts antiviral activity. J Clin Invest. 2013;. doi:10.1172/JCI65708.
38. Baum LL, Cassutt KJ, Knigge K, et al. HIV-1 gp120-specific antibody-dependent cell-mediated cytotoxicity correlates with rate of disease progression. J Immunol. 1996;157:2168–2173.
39. Dugast AS, Stamatatos L, Tonelli A, et al. Independent evolution of Fc- and Fab-mediated HIV-1-specific antiviral antibody activity following acute infection. Eur J Immunol. 2014;44:2925–2937.
40. Pollara J, Bonsignori M, Moody MA, et al. HIV-1 vaccine-induced C1 and V2 Env-specific antibodies synergize for increased antiviral activities. J Virol. 2014;88:7715–7726.
41. Forthal DN, Landucci G, Ding H, et al. IgG2 inhibits HIV-1 internalization by monocytes, and IgG subclass binding is affected by gp120 glycosylation. AIDS. 2011;25:2099–2104.
42. Haynes BF, Gilbert PB, McElrath MJ, et al. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med. 2012;366:1275–1286.
43. Tomaras GD, Ferrari G, Shen X, et al. 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 USA. 2013;110:9019–9024.
44. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, et al. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med. 2009;361:2209–2220.
45. Rolland M, Edlefsen PT, Larsen BB, et al. Increased HIV-1 vaccine efficacy against viruses with genetic signatures in Env V2. Nature. 2012;490:417–420.
46. Li SS, Gilbert PB, Tomaras GD, et al. FCGR2C polymorphisms associate with HIV-1 vaccine protection in RV144 trial. J Clin Invest. 2014;124:3879–3890.
47. Prentice HA, Tomaras GD, Geraghty DE, et al. HLA class II genes modulate vaccine-induced antibody responses to affect HIV-1 acquisition. Sci Transl Med. 2015;7:296ra112.
48. Yates NL, Liao HX, Fong Y, et al. Vaccine-induced Env V1-V2 IgG3 correlates with lower HIV-1 infection risk and declines soon after vaccination. Sci Transl Med. 2014;6:228ra39.
49. Zolla-Pazner S, deCamp A, Gilbert PB, et al. Vaccine-induced IgG antibodies to V1V2 regions of multiple HIV-1 subtypes correlate with decreased risk of HIV-1 infection. PLoS ONE. 2014;9:e87572.
50. Tarca AL, Carey VJ, Chen XW, Romero R, Draghici S. Machine learning and its applications to biology. PLoS Comput Biol. 2007;3:e116.
51. Rost B, Sander C. Combining evolutionary information and neural networks to predict protein secondary structure. Proteins. 1994;19:55–72.
52. Tarca AL, Cooke JE, Mackay J. A robust neural networks approach for spatial and intensity-dependent normalization of cDNA microarray data. Bioinformatics. 2005;21:2674–2683.
53. Alizadeh AA, Eisen MB, Davis RE, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature. 2000;403:503–511.
54. Vaccari M, Gordon SN, Fourati S, et al. Adjuvant-dependent innate and adaptive immune signatures of risk of SIVmac251 acquisition. Nat Med. 2016;22:762–770.
55. Li S, Rouphael N, Duraisingham S, et al. Molecular signatures of antibody responses derived from a systems biology study of five human vaccines. Nat Immunol. 2014;15:195–204.
56. Ovsyannikova IG, Oberg AL, Kennedy RB, et al. Gene signatures related to HAI response following influenza A/H1N1 vaccine in older individuals. Heliyon. 2016;2:e00098.
57. Boesch AW, Brown EP, Ackerman ME. The role of Fc receptors in HIV prevention and therapy. Immunol Rev. 2015;268:296–310.
58. Pitisuttithum P, Gilbert P, Gurwith M, et al. Randomized, double-blind, placebo-controlled efficacy trial of a bivalent recombinant glycoprotein 120 HIV-1 vaccine among injection drug users in Bangkok, Thailand. J Infect Dis. 2006;194:1661–1671.
59. Churchyard GJ, Morgan C, Adams E, et al. A phase IIA randomized clinical trial of a multiclade HIV-1 DNA prime followed by a multiclade rAd5 HIV-1 vaccine boost in healthy adults (HVTN204). PLoS ONE. 2011;6:e21225.
60. Tibshirani R. The lasso method for variable selection in the Cox model. Stat Med. 1997;16:385–395.
61. Brereton R, Lloyd G. Partial least squares discriminant analysis: Taking the magic away. J Chemometrics. 2014;28:213–225.
62. Manrique A, Adams E, Barouch DH, et al. The immune space: A concept and template for rationalizing vaccine development. AIDS Res Hum Retroviruses. 2014;30:1017–1022.
63. Barouch DH, Liu J, Li H, et al. Vaccine protection against acquisition of neutralization-resistant SIV challenges in rhesus monkeys. Nature. 2012;482:89–93.
64. Roederer M, Keele BF, Schmidt SD, et al. Immunological and virological mechanisms of vaccine-mediated protection against SIV and HIV. Nature. 2014;505:502–508.
65. Mohanram V, Demberg T, Musich T, et al. B cell responses associated with vaccine-induced delayed SIVmac251 acquisition in female rhesus macaques. J Immunol. 2016;197:2316–2324.
66. Li Q, Zeng M, Duan L, et al. Live simian immunodeficiency virus vaccine correlate of protection: Local antibody production and concentration on the path of virus entry. J Immunol. 2014;193:3113–3125.
67. Fouts TR, Bagley K, Prado IJ, et al. Balance of cellular and humoral immunity determines the level of protection by HIV vaccines in rhesus macaque models of HIV infection. Proc Natl Acad Sci USA. 2015;112:E992–E999.
68. Fourati S, Vaccari M, Gordon SN, et al. Modulation of RAS pathways as a biomarker of protection against HIV and as a means to improve vaccine efficacy. AIDS Res Hum Retroviruses. 2014;30:A99-A.