HIV-specific Fc effector function early in infection predicts the development of broadly neutralizing antibodies

PLoS Pathogens

Volumn 14, Issue 4, 2018, Pages

  Richardson, Simone I ^a,b   Chung, Amy W ^c   Natarajan, Harini ^d   Mabvakure, Batsirai ^a,b   Mkhize, Nonhlanhla N ^a,b   Garrett, Nigel ^e   Abdool Karim, Salim ^e   Moore, Penny L ^a,b,e   Ackerman, Margaret E ^d   Alter, Galit ^f   Morris, Lynn ^a,b,e  

^a NATIONAL INSTITUTE FOR COMMUNICABLE DISEASES   (South Africa)

^b UNIVERSITY OF THE WITWATERSRAND   (South Africa)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d DARTMOUTH COLLEGE   (United States)

^e UNIVERSITY OF KWAZULU NATAL   (South Africa)

^f MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; CD4 ANTIGEN; COMPLEMENT COMPONENT C1Q; CXCL13 CHEMOKINE; CYTIDINE DEAMINASE; FC RECEPTOR; FC RECEPTOR IIA; FC RECEPTOR IIB; GLYCOPROTEIN GP 120; GRANZYME B; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G4; KI 67 ANTIGEN; NEUTRALIZING ANTIBODY; PALIVIZUMAB; PROTEIN G; VIRUS GLYCOPROTEIN; IMMUNOGLOBULIN G;

ADULT; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY SPECIFICITY; ARTICLE; CD4 LYMPHOCYTE COUNT; COMPLEMENT DEPOSITION; CONTROLLED STUDY; CYTOTOXICITY ASSAY; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENOTYPE; GERMINAL CENTER; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; NONHUMAN; PHAGOCYTOSIS; PROTEIN EXPRESSION; SINGLE NUCLEOTIDE POLYMORPHISM; SIZE EXCLUSION CHROMATOGRAPHY; VIRUS LOAD; VIRUS NEUTRALIZATION; BLOOD; CASE CONTROL STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; VIROLOGY;

ADULT; ANTIBODIES, NEUTRALIZING; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; CASE-CONTROL STUDIES; HIV ANTIBODIES; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOGLOBULIN G;

EID: 85046490139     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1006987     Document Type: Article

References (106)

1. Boesch AW, Brown EP, Ackerman ME, The role of Fc receptors in HIV prevention and therapy. Immunol Rev. 2015;268(1):296–310. doi: 10.1111/imr.12339 26497529
2. Wines BD, Billings H, McLean MR, Kent SJ, Hogarth PM, Antibody Functional Assays as Measures of Fc Receptor-Mediated Immunity to HIV—New Technologies and their Impact on the HIV Vaccine Field. Curr HIV Res. 2017;15(3):202–15. doi: 10.2174/1570162X15666170320112247 28322167
3. Chung AW, Kumar MP, Arnold KB, Yu WH, Schoen MK, Dunphy LJ, et al. Dissecting Polyclonal Vaccine-Induced Humoral Immunity against HIV Using Systems Serology. Cell. 2015;163(4):988–98. doi: 10.1016/j.cell.2015.10.027 26544943
4. Pollara J, Bonsignori M, Moody MA, Liu P, Alam SM, Hwang KK, et al. HIV-1 vaccine-induced C1 and V2 Env-specific antibodies synergize for increased antiviral activities. J Virol. 2014;88(14):7715–26. doi: 10.1128/JVI.00156-14 24807721
5. Chung AW, Ghebremichael M, Robinson H, Brown E, Choi I, Lane S, et al. Polyfunctional Fc-effector profiles mediated by IgG subclass selection distinguish RV144 and VAX003 vaccines. Sci Transl Med. 2014;6(228):228ra38. doi: 10.1126/scitranslmed.3007736 24648341
6. Yates NL, Liao HX, Fong Y, deCamp A, Vandergrift NA, Williams WT, 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(228):228ra39. doi: 10.1126/scitranslmed.3007730 24648342
7. Bonsignori M, Pollara J, Moody MA, Alpert MD, Chen X, Hwang KK, et al. 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. 2012;86(21):11521–32. doi: 10.1128/JVI.01023-12 22896626
8. Haynes BF, Gilbert PB, McElrath MJ, Zolla-Pazner S, Tomaras GD, Alam SM, et al. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med. 2012;366(14):1275–86. doi: 10.1056/NEJMoa1113425 22475592
9. Methot SP, Di Noia JM, Molecular Mechanisms of Somatic Hypermutation and Class Switch Recombination. Adv Immunol. 2017;133:37–87. doi: 10.1016/bs.ai.2016.11.002 28215280
10. Kinoshita K, Honjo T, Linking class-switch recombination with somatic hypermutation. Nat Rev Mol Cell Biol. 2001;2(7):493–503. doi: 10.1038/35080033 11433363
11. Kitaura K, Yamashita H, Ayabe H, Shini T, Matsutani T, Suzuki R, Different Somatic Hypermutation Levels among Antibody Subclasses Disclosed by a New Next-Generation Sequencing-Based Antibody Repertoire Analysis.Front Immunol. 2017;8:389. doi: 10.3389/fimmu.2017.00389 28515723
12. 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. J Virol. 2011;85(10):4828–40. doi: 10.1128/JVI.00198-11 21389135
13. Landais E, Huang X, Havenar-Daughton C, Murrell B, Price MA, Wickramasinghe L, et al. Broadly Neutralizing Antibody Responses in a Large Longitudinal Sub-Saharan HIV Primary Infection Cohort. PLoS Pathog. 2016;12(1):e1005369. doi: 10.1371/journal.ppat.1005369 26766578
14. 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. J Virol. 2009;83(2):757–69. doi: 10.1128/JVI.02036-08 18987148
15. Stamatatos L, Morris L, Burton DR, Mascola JR, Neutralizing antibodies generated during natural HIV-1 infection: good news for an HIV-1 vaccine?Nat Med. 2009;15(8):866–70. doi: 10.1038/nm.1949 19525964
16. Rusert P, Kouyos RD, Kadelka C, Ebner H, Schanz M, Huber M, et al. Determinants of HIV-1 broadly neutralizing antibody induction. Nat Med. 2016;22(11):1260–7. doi: 10.1038/nm.4187 27668936
17. Moore PL, Williamson C, Morris L, Virological features associated with the development of broadly neutralizing antibodies to HIV-1. Trends Microbiol. 2015;23(4):204–11. doi: 10.1016/j.tim.2014.12.007 25572881
18. 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. J Virol. 2009;83(19):10269–74. doi: 10.1128/JVI.01149-09 19640996
19. Locci M, Havenar-Daughton C, Landais E, Wu J, Kroenke MA, Arlehamn CL, et al. Human circulating PD-1+CXCR3-CXCR5+ memory Tfh cells are highly functional and correlate with broadly neutralizing HIV antibody responses. Immunity. 2013;39(4):758–69. doi: 10.1016/j.immuni.2013.08.031 24035365
20. 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. J Virol. 2014;88(22):13310–21. doi: 10.1128/JVI.02186-14 25210168
21. Havenar-Daughton C, Lindqvist M, Heit A, Wu JE, Reiss SM, Kendric K, et al. CXCL13 is a plasma biomarker of germinal center activity. Proc Natl Acad Sci U S A. 2016;113(10):2702–7. doi: 10.1073/pnas.1520112113 26908875
22. Moody MA, Pedroza-Pacheco I, Vandergrift NA, Chui C, Lloyd KE, Parks R, et al. Immune perturbations in HIV-1-infected individuals who make broadly neutralizing antibodies. Sci Immunol. 2016;1(1):aag0851. doi: 10.1126/sciimmunol.aag0851 28783677
23. Klein F, Diskin R, Scheid JF, Gaebler C, Mouquet H, Georgiev IS, et al. Somatic mutations of the immunoglobulin framework are generally required for broad and potent HIV-1 neutralization. Cell. 2013;153(1):126–38. doi: 10.1016/j.cell.2013.03.018 23540694
24. Burton DR, Mascola JR, Antibody responses to envelope glycoproteins in HIV-1 infection. Nat Immunol. 2015;16(6):571–6. doi: 10.1038/ni.3158 25988889
25. Moore PL, Williamson C, Approaches to the induction of HIV broadly neutralizing antibodies. Curr Opin HIV AIDS. 2016;11(6):569–75. doi: 10.1097/COH.0000000000000317 27559709
26. Bournazos S, Ravetch JV, Diversification of IgG effector functions. Int Immunol. 2017;29(7):303–10. doi: 10.1093/intimm/dxx025 28472280
27. Velmurugan R, Challa DK, Ram S, Ober RJ, Ward ES, Macrophage-Mediated Trogocytosis Leads to Death of Antibody-Opsonized Tumor Cells. Mol Cancer Ther. 2016;15(8):1879–89. doi: 10.1158/1535-7163.MCT-15-0335 27226489
28. Joly E, Hudrisier D, What is trogocytosis and what is its purpose?Nat Immunol. 2003;4(9):815. doi: 10.1038/ni0903-815 12942076
29. Jefferis R, Isotype and glycoform selection for antibody therapeutics. Arch Biochem Biophys. 2012;526(2):159–66. doi: 10.1016/j.abb.2012.03.021 22465822
30. Chung AW, Crispin M, Pritchard L, Robinson H, Gorny MK, Yu X, et al. Identification of antibody glycosylation structures that predict monoclonal antibody Fc-effector function. AIDS. 2014;28(17):2523–30. doi: 10.1097/QAD.0000000000000444 25160934
31. Mahan AE, Jennewein MF, Suscovich T, Dionne K, Tedesco J, Chung AW, et al. Antigen-Specific Antibody Glycosylation Is Regulated via Vaccination. PLoS Pathog. 2016;12(3):e1005456. doi: 10.1371/journal.ppat.1005456 26982805
32. Ackerman ME, Crispin M, Yu X, Baruah K, Boesch AW, Harvey DJ, et al. Natural variation in Fc glycosylation of HIV-specific antibodies impacts antiviral activity. J Clin Invest. 2013;123(5):2183–92. doi: 10.1172/JCI65708 23563315
33. Mazor Y, Yang C, Borrok MJ, Ayriss J, Aherne K, Wu H, et al. Enhancement of Immune Effector Functions by Modulating IgG's Intrinsic Affinity for Target Antigen. PLoS One. 2016;11(6):e0157788. doi: 10.1371/journal.pone.0157788 27322177
34. Liu P, Williams LD, Shen X, Bonsignori M, Vandergrift NA, Overman RG, et al. Capacity for infectious HIV-1 virion capture differs by envelope antibody specificity. J Virol. 2014;88(9):5165–70. doi: 10.1128/JVI.03765-13 24554654
35. Musich T, Li L, Liu L, Zolla-Pazner S, Robert-Guroff M, Gorny MK, Monoclonal Antibodies Specific for the V2, V3, CD4-Binding Site, and gp41 of HIV-1 Mediate Phagocytosis in a Dose-Dependent Manner. J Virol. 2017;91(8).
36. Baum LL, Cassutt KJ, Knigge K, Khattri R, Margolick J, Rinaldo C, et al. HIV-1 gp120-specific antibody-dependent cell-mediated cytotoxicity correlates with rate of disease progression. J Immunol. 1996;157(5):2168–73. 8757343
37. Ahmad R, Sindhu ST, Toma E, Morisset R, Vincelette J, Menezes J, et al. Evidence for a correlation between antibody-dependent cellular cytotoxicity-mediating anti-HIV-1 antibodies and prognostic predictors of HIV infection. J Clin Immunol. 2001;21(3):227–33. 11403230
38. Forthal DN, Gilbert PB, Landucci G, Phan T, Recombinant gp120 vaccine-induced antibodies inhibit clinical strains of HIV-1 in the presence of Fc receptor-bearing effector cells and correlate inversely with HIV infection rate. J Immunol. 2007;178(10):6596–603. 17475891
39. Lambotte O, Ferrari G, Moog C, Yates NL, Liao HX, Parks RJ, et al. Heterogeneous neutralizing antibody and antibody-dependent cell cytotoxicity responses in HIV-1 elite controllers. AIDS. 2009;23(8):897–906. doi: 10.1097/QAD.0b013e328329f97d 19414990
40. Milligan C, Richardson BA, John-Stewart G, Nduati R, Overbaugh J, Passively acquired antibody-dependent cellular cytotoxicity (ADCC) activity in HIV-infected infants is associated with reduced mortality. Cell Host Microbe. 2015;17(4):500–6. doi: 10.1016/j.chom.2015.03.002 25856755
41. Lai JI, Licht AF, Dugast AS, Suscovich T, Choi I, Bailey-Kellogg C, 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(5):2799–809. doi: 10.1128/JVI.03130-13 24352471
42. Madhavi V, Wines BD, Amin J, Emery S, Group ES, Lopez E, et al. HIV-1 Env- and Vpu-Specific Antibody-Dependent Cellular Cytotoxicity Responses Associated with Elite Control of HIV. J Virol. 2017;91(18).
43. Huang Y, Ferrari G, Alter G, Forthal DN, Kappes JC, Lewis GK, et al. Diversity of Antiviral IgG Effector Activities Observed in HIV-Infected and Vaccinated Subjects. J Immunol. 2016;197(12):4603–12. doi: 10.4049/jimmunol.1601197 27913647
44. Ackerman ME, Mikhailova A, Brown EP, Dowell KG, Walker BD, Bailey-Kellogg C, et al. Polyfunctional HIV-Specific Antibody Responses Are Associated with Spontaneous HIV Control. PLoS Pathog. 2016;12(1):e1005315. doi: 10.1371/journal.ppat.1005315 26745376
45. Barouch DH, Alter G, Broge T, Linde C, Ackerman ME, Brown EP, et al. Protective efficacy of adenovirus/protein vaccines against SIV challenges in rhesus monkeys. Science. 2015;349(6245):320–4. doi: 10.1126/science.aab3886 26138104
46. Dugast AS, Chan Y, Hoffner M, Licht A, Nkolola J, Li H, et al. Lack of protection following passive transfer of polyclonal highly functional low-dose non-neutralizing antibodies. PLoS One. 2014;9(5):e97229. doi: 10.1371/journal.pone.0097229 24820481
47. Astronomo RD, Santra S, Ballweber-Fleming L, Westerberg KG, Mach L, Hensley-McBain T, et al. Neutralization Takes Precedence Over IgG or IgA Isotype-related Functions in Mucosal HIV-1 Antibody-mediated Protection. EBioMedicine. 2016;14:97–111. doi: 10.1016/j.ebiom.2016.11.024 27919754
48. Burton DR, Hessell AJ, Keele BF, Klasse PJ, Ketas TA, Moldt B, et al. Limited or no protection by weakly or nonneutralizing antibodies against vaginal SHIV challenge of macaques compared with a strongly neutralizing antibody. Proc Natl Acad Sci U S A. 2011;108(27):11181–6. doi: 10.1073/pnas.1103012108 21690411
49. Santra S, Tomaras GD, Warrier R, Nicely NI, Liao HX, Pollara J, et al. Human Non-neutralizing HIV-1 Envelope Monoclonal Antibodies Limit the Number of Founder Viruses during SHIV Mucosal Infection in Rhesus Macaques. PLoS Pathog. 2015;11(8):e1005042. doi: 10.1371/journal.ppat.1005042 26237403
50. Horwitz JA, Bar-On Y, Lu CL, Fera D, Lockhart AAK, Lorenzi JCC, et al. Non-neutralizing Antibodies Alter the Course of HIV-1 Infection In Vivo. Cell. 2017;170(4):637–48 e10. doi: 10.1016/j.cell.2017.06.048 28757252
51. Hessell AJ, Hangartner L, Hunter M, Havenith CE, Beurskens FJ, Bakker JM, et al. Fc receptor but not complement binding is important in antibody protection against HIV. Nature. 2007;449(7158):101–4. doi: 10.1038/nature06106 17805298
52. 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(6):1243–53. doi: 10.1016/j.cell.2014.08.023 25215485
53. Halper-Stromberg A, Lu CL, Klein F, Horwitz JA, Bournazos S, Nogueira L, et al. Broadly neutralizing antibodies and viral inducers decrease rebound from HIV-1 latent reservoirs in humanized mice. Cell. 2014;158(5):989–99. doi: 10.1016/j.cell.2014.07.043 25131989
54. Lu CL, Murakowski DK, Bournazos S, Schoofs T, Sarkar D, Halper-Stromberg A, et al. Enhanced clearance of HIV-1-infected cells by broadly neutralizing antibodies against HIV-1 in vivo. Science. 2016;352(6288):1001–4. doi: 10.1126/science.aaf1279 27199430
55. Lewis GK, Pazgier M, DeVico AL, Survivors Remorse: antibody-mediated protection against HIV-1. Immunol Rev. 2017;275(1):271–84. doi: 10.1111/imr.12510 28133809
56. Dugast AS, Arnold K, Lofano G, Moore S, Hoffner M, Simek M, et al. Virus-driven Inflammation Is Associated With the Development of bNAbs in Spontaneous Controllers of HIV. Clin Infect Dis. 2017;64(8):1098–104. doi: 10.1093/cid/cix057 28158448
57. Brown EP, Dowell KG, Boesch AW, Normandin E, Mahan AE, Chu T, et al. Multiplexed Fc array for evaluation of antigen-specific antibody effector profiles. J Immunol Methods. 2017;443:33–44. doi: 10.1016/j.jim.2017.01.010 28163018
58. Bournazos S, Woof JM, Hart SP, Dransfield I, Functional and clinical consequences of Fc receptor polymorphic and copy number variants. Clin Exp Immunol. 2009;157(2):244–54. doi: 10.1111/j.1365-2249.2009.03980.x 19604264
59. Ackerman ME, Dugast AS, McAndrew EG, Tsoukas S, Licht AF, Irvine DJ, 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(10):5468–76. doi: 10.1128/JVI.03403-12 23468489
60. Nimmerjahn F, Ravetch JV, Divergent immunoglobulin g subclass activity through selective Fc receptor binding. Science. 2005;310(5753):1510–2. doi: 10.1126/science.1118948 16322460
61. Iwasaki S, Masuda S, Baba T, Tomaru U, Katsumata K, Kasahara M, et al. Plasma-dependent, antibody- and Fcgamma receptor-mediated translocation of CD8 molecules from T cells to monocytes. Cytometry A. 2011;79(1):46–56. doi: 10.1002/cyto.a.20984 21182182
62. Boross P, Jansen JH, Pastula A, van der Poel CE, Leusen JH, Both activating and inhibitory Fc gamma receptors mediate rituximab-induced trogocytosis of CD20 in mice. Immunol Lett. 2012;143(1):44–52. doi: 10.1016/j.imlet.2012.01.004 22285696
63. Bruhns P, Iannascoli B, England P, Mancardi DA, Fernandez N, Jorieux S, et al. Specificity and affinity of human Fcgamma receptors and their polymorphic variants for human IgG subclasses. Blood. 2009;113(16):3716–25. doi: 10.1182/blood-2008-09-179754 19018092
64. Kroenke MA, Eto D, Locci M, Cho M, Davidson T, Haddad EK, et al. Bcl6 and Maf cooperate to instruct human follicular helper CD4 T cell differentiation. J Immunol. 2012;188(8):3734–44. doi: 10.4049/jimmunol.1103246 22427637
65. Rasheed AU, Rahn HP, Sallusto F, Lipp M, Muller G, Follicular B helper T cell activity is confined to CXCR5(hi)ICOS(hi) CD4 T cells and is independent of CD57 expression. Eur J Immunol. 2006;36(7):1892–903. doi: 10.1002/eji.200636136 16791882
66. Mabuka JM, Dugast AS, Muema DM, Reddy T, Ramlakhan Y, Euler Z, et al. Plasma CXCL13 but Not B Cell Frequencies in Acute HIV Infection Predicts Emergence of Cross-Neutralizing Antibodies. Front Immunol. 2017;8:1104. doi: 10.3389/fimmu.2017.01104 28943879
67. Tyler DS, Stanley SD, Nastala CA, Austin AA, Bartlett JA, Stine KC, et al. Alterations in antibody-dependent cellular cytotoxicity during the course of HIV-1 infection. Humoral and cellular defects. J Immunol. 1990;144(9):3375–84. 2329275
68. Forthal DN, Landucci G, Keenan B, Relationship between antibody-dependent cellular cytotoxicity, plasma HIV type 1 RNA, and CD4+ lymphocyte count. AIDS Res Hum Retroviruses. 2001;17(6):553–61. doi: 10.1089/08892220151126661 11350669
69. Dugast AS, Stamatatos L, Tonelli A, Suscovich TJ, Licht AF, Mikell I, et al. Independent evolution of Fc- and Fab-mediated HIV-1-specific antiviral antibody activity following acute infection. Eur J Immunol. 2014;44(10):2925–37. doi: 10.1002/eji.201344305 25043633
70. Ana-Sosa-Batiz F, Johnston AP, Liu H, Center RJ, Rerks-Ngarm S, Pitisuttithum P, et al. HIV-specific antibody-dependent phagocytosis matures during HIV infection. Immunol Cell Biol. 2014;92(8):679–87. doi: 10.1038/icb.2014.42 24913323
71. Dugast AS, Tonelli A, Berger CT, Ackerman ME, Sciaranghella G, Liu Q, et al. Decreased Fc receptor expression on innate immune cells is associated with impaired antibody-mediated cellular phagocytic activity in chronically HIV-1 infected individuals. Virology. 2011;415(2):160–7. doi: 10.1016/j.virol.2011.03.012 21565376
72. Tsachouridou O, Skoura L, Chatzidimitriou D, Margariti A, Georgiou A, Chatzidimitriou M, et al. Deficient Phagocytosis Among HIV-1 Infected Adults Over Time Even in HAART Setting. Curr HIV Res. 2017;15(4):285–90. doi: 10.2174/1570162X15666170704101622 28675993
73. Perez LG, Martinez DR, deCamp AC, Pinter A, Berman PW, Francis D, et al. V1V2-specific complement activating serum IgG as a correlate of reduced HIV-1 infection risk in RV144. PLoS One. 2017;12(7):e0180720. doi: 10.1371/journal.pone.0180720 28678869
74. Rossheim AE, Cunningham TD, Hair PS, Shah T, Cunnion KM, Troy SB, Effects of Well-Controlled HIV Infection on Complement Activation and Function. J Acquir Immune Defic Syndr. 2016;73(1):20–6. doi: 10.1097/QAI.0000000000001079 27192377
75. Fang Y, Xu C, Fu YX, Holers VM, Molina H, Expression of complement receptors 1 and 2 on follicular dendritic cells is necessary for the generation of a strong antigen-specific IgG response. J Immunol. 1998;160(11):5273–9. 9605124
76. Carroll MC, Isenman DE, Regulation of humoral immunity by complement. Immunity. 2012;37(2):199–207. doi: 10.1016/j.immuni.2012.08.002 22921118
77. Beum PV, Mack DA, Pawluczkowycz AW, Lindorfer MA, Taylor RP, Binding of rituximab, trastuzumab, cetuximab, or mAb T101 to cancer cells promotes trogocytosis mediated by THP-1 cells and monocytes. J Immunol. 2008;181(11):8120–32. 19018005
78. Daubeuf S, Lindorfer MA, Taylor RP, Joly E, Hudrisier D, The direction of plasma membrane exchange between lymphocytes and accessory cells by trogocytosis is influenced by the nature of the accessory cell. J Immunol. 2010;184(4):1897–908. doi: 10.4049/jimmunol.0901570 20089699
79. Taylor RP, Lindorfer MA, Fcgamma-receptor-mediated trogocytosis impacts mAb-based therapies: historical precedence and recent developments. Blood. 2015;125(5):762–6. doi: 10.1182/blood-2014-10-569244 25498911
80. Bruhns P, Properties of mouse and human IgG receptors and their contribution to disease models. Blood. 2012;119(24):5640–9. doi: 10.1182/blood-2012-01-380121 22535666
81. Pan-Hammarstrom Q, Zhao Y, Hammarstrom L, Class switch recombination: a comparison between mouse and human. Adv Immunol. 2007;93:1–61. doi: 10.1016/S0065-2776(06)93001-6 17383538
82. French MA, Abudulai LN, Fernandez S, Isotype Diversification of IgG Antibodies to HIV Gag Proteins as a Therapeutic Vaccination Strategy for HIV Infection. Vaccines (Basel). 2013;1(3):328–42.
83. Aalberse RC, Stapel SO, Schuurman J, Rispens T, Immunoglobulin G4: an odd antibody. Clin Exp Allergy. 2009;39(4):469–77. doi: 10.1111/j.1365-2222.2009.03207.x 19222496
84. Vidarsson G, Dekkers G, Rispens T, IgG subclasses and allotypes: from structure to effector functions. Front Immunol. 2014;5:520. doi: 10.3389/fimmu.2014.00520 25368619
85. Tjiam MC, Taylor JP, Morshidi MA, Sariputra L, Burrows S, Martin JN, et al. Viremic HIV Controllers Exhibit High Plasmacytoid Dendritic Cell-Reactive Opsonophagocytic IgG Antibody Responses against HIV-1 p24 Associated with Greater Antibody Isotype Diversification. J Immunol. 2015;194(11):5320–8. doi: 10.4049/jimmunol.1402918 25911748
86. Forthal DN, Landucci G, Ding H, Kappes JC, Wang A, Thung I, et al. IgG2 inhibits HIV-1 internalization by monocytes, and IgG subclass binding is affected by gp120 glycosylation. AIDS. 2011;25(17):2099–104. doi: 10.1097/QAD.0b013e32834b64bd 21832933
87. Choi I, Chung AW, Suscovich TJ, Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, et al. Machine learning methods enable predictive modeling of antibody feature:function relationships in RV144 vaccinees. PLoS Comput Biol. 2015;11(4):e1004185. doi: 10.1371/journal.pcbi.1004185 25874406
88. French MA, Center RJ, Wilson KM, Fleyfel I, Fernandez S, Schorcht A, et al. Isotype-switched immunoglobulin G antibodies to HIV Gag proteins may provide alternative or additional immune responses to 'protective' human leukocyte antigen-B alleles in HIV controllers. AIDS. 2013;27(4):519–28. doi: 10.1097/QAD.0b013e32835cb720 23364441
89. Tudor D, Yu H, Maupetit J, Drillet AS, Bouceba T, Schwartz-Cornil I, et al. Isotype modulates epitope specificity, affinity, and antiviral activities of anti-HIV-1 human broadly neutralizing 2F5 antibody. Proc Natl Acad Sci U S A. 2012;109(31):12680–5. doi: 10.1073/pnas.1200024109 22723360
90. Tomaras GD, Ferrari G, Shen X, Alam SM, Liao HX, Pollara J, 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 U S A. 2013;110(22):9019–24. doi: 10.1073/pnas.1301456110 23661056
91. Yang D, Kroe-Barrett R, Singh S, Roberts CJ, Laue TM, IgG cooperativity—Is there allostery? Implications for antibody functions and therapeutic antibody development. MAbs. 2017:1–22. doi: 10.1080/19420862.2017.1389364 28991509
92. Janda A, Bowen A, Greenspan NS, Casadevall A, Ig Constant Region Effects on Variable Region Structure and Function. Front Microbiol. 2016;7:22. doi: 10.3389/fmicb.2016.00022 26870003
93. van Loggerenberg F, Mlisana K, Williamson C, Auld SC, Morris L, Gray CM, et al. Establishing a cohort at high risk of HIV infection in South Africa: challenges and experiences of the CAPRISA 002 acute infection study. PLoS One. 2008;3(4):e1954. doi: 10.1371/journal.pone.0001954 18414658
94. Abdool Karim Q, Abdool Karim SS, Frohlich JA, Grobler AC, Baxter C, Mansoor LE, et al. Effectiveness and safety of tenofovir gel, an antiretroviral microbicide, for the prevention of HIV infection in women. Science. 2010;329(5996):1168–74. doi: 10.1126/science.1193748 20643915
95. Gray ES, Moody MA, Wibmer CK, Chen X, Marshall D, Amos J, et al. Isolation of a monoclonal antibody that targets the alpha-2 helix of gp120 and represents the initial autologous neutralizing-antibody response in an HIV-1 subtype C-infected individual. J Virol. 2011;85(15):7719–29. doi: 10.1128/JVI.00563-11 21613396
96. Sanders RW, Derking R, Cupo A, Julien JP, 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(9):e1003618. doi: 10.1371/journal.ppat.1003618 24068931
97. Schramm CA, Sheng Z, Zhang Z, Mascola JR, Kwong PD, Shapiro L, SONAR: A High-Throughput Pipeline for Inferring Antibody Ontogenies from Longitudinal Sequencing of B Cell Transcripts. Front Immunol. 2016;7:372. doi: 10.3389/fimmu.2016.00372 27708645
98. Kumar S, Stecher G, Peterson D, Tamura K, MEGA-CC: computing core of molecular evolutionary genetics analysis program for automated and iterative data analysis. Bioinformatics. 2012;28(20):2685–6. doi: 10.1093/bioinformatics/bts507 22923298
99. Ackerman ME, Moldt B, Wyatt RT, Dugast AS, McAndrew E, Tsoukas S, et al. A robust, high-throughput assay to determine the phagocytic activity of clinical antibody samples. J Immunol Methods. 2011;366(1–2):8–19. doi: 10.1016/j.jim.2010.12.016 21192942
100. Pollara J, Hart L, Brewer F, Pickeral J, Packard BZ, Hoxie JA, et al. High-throughput quantitative analysis of HIV-1 and SIV-specific ADCC-mediating antibody responses. Cytometry A. 2011;79(8):603–12. doi: 10.1002/cyto.a.21084 21735545
101. Li Y, Svehla K, Louder MK, Wycuff D, Phogat S, Tang M, et al. Analysis of neutralization specificities in polyclonal sera derived from human immunodeficiency virus type 1-infected individuals. J Virol. 2009;83(2):1045–59. doi: 10.1128/JVI.01992-08 19004942
102. Zhou T, Zhu J, Yang Y, Gorman J, Ofek G, Srivatsan S, et al. Transplanting supersites of HIV-1 vulnerability. PLoS One. 2014;9(7):e99881. doi: 10.1371/journal.pone.0099881 24992528
103. Montefiori DC, Measuring HIV neutralization in a luciferase reporter gene assay. Methods Mol Biol. 2009;485:395–405. doi: 10.1007/978-1-59745-170-3_26 19020839
104. Brown EP, Licht AF, Dugast AS, Choi I, Bailey-Kellogg C, Alter G, et al. High-throughput, multiplexed IgG subclassing of antigen-specific antibodies from clinical samples. J Immunol Methods. 2012;386(1–2):117–23. doi: 10.1016/j.jim.2012.09.007 23023091
105. Benjamini Y, Hochberg Y, Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B (Methodological). 1995;57(1):289–300.
106. Menze BH, Kelm BM, Masuch R, Himmelreich U, Bachert P, Petrich W, et al. A comparison of random forest and its Gini importance with standard chemometric methods for the feature selection and classification of spectral data. BMC Bioinformatics. 2009;10:213. doi: 10.1186/1471-2105-10-213 19591666