Emerging concepts on the role of innate immunity in the prevention and control of HIV infection

Annual Review of Medicine

Volumn 63, Issue , 2012, Pages 113-130

  Ackerman, Margaret E ^a,b   Dugast, Anne Sophie ^a   Alter, Galit ^a  

^a HARVARD UNIVERSITY   (United States)

^b DARTMOUTH COLLEGE   (United States)

Author keywords

Antibody dependent cellular cytotoxicity; Antibody dependent cellular viral inhibition; Effector function; Fc R; IgG; IgG Fc

Indexed keywords

COMPLEMENT; EPITOPE; FC RECEPTOR; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G3; IMMUNOGLOBULIN G4; NEUTRALIZING ANTIBODY; SIMIAN IMMUNODEFICIENCY VIRUS VACCINE; TENOFOVIR;

ANTIBODY AFFINITY; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY DEPENDENT CELLULAR PHAGOCYTOSIS; ANTIBODY RESPONSE; ANTIBODY TITER; CELL PHAGOCYTOSIS; COMPLEMENT DEPENDENT CYTOTOXICITY; DISEASE COURSE; EFFECTOR CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMORAL IMMUNITY; INFECTION CONTROL; INFECTION PREVENTION; INNATE IMMUNITY; NATURAL KILLER CELL; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN POLYMORPHISM; REVIEW; VACCINATION;

AIDS VACCINES; ANTIBODIES, NEUTRALIZING; HIV INFECTIONS; HUMANS; IMMUNITY, INNATE;

EID: 84855970041     PISSN: 00664219     EISSN: 1545326X     Source Type: Book Series    
DOI: 10.1146/annurev-med-050310-085221     Document Type: Review

References (101)

1. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, et al. 2009. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361:2209-20
2. Belshe RB, Gorse GJ, Mulligan MJ, et al. 1998. Induction of immune responses to HIV-1 by canarypox virus (ALVAC) HIV-1 and gp120 SF-2 recombinant vaccines in uninfected volunteers. NIAID AIDS Vaccine Evaluation Group. AIDS 12:2407-15 (Pubitemid 28558598)
3. Belshe RB, Graham BS, Keefer MC, et al. 1994. Neutralizing antibodies to HIV-1 in seronegative volunteers immunized with recombinant gp120 from the MN strain of HIV-1. NIAID AIDS Vaccine Clinical Trials Network. JAMA 272:475-80 (Pubitemid 24235698)
4. Russell ND, Graham BS, Keefer MC, et al. 2007. Phase 2 study of an HIV-1 canarypox vaccine (vCP1452) alone and in combination with rgp120: negative results fail to trigger a phase 3 correlates trial. J. Acquir. Immune Defic. Syndr. 44:203-12 (Pubitemid 46292224)
5. Haigwood NL, Watson A, Sutton WF, et al. 1996. Passive immune globulin therapy in the SIV/macaque model: early intervention can alter disease profile. Immunol. Lett. 51:107-14 (Pubitemid 26227479)
6. Shibata R, Igarashi T, Haigwood N, et al. 1999. Neutralizing antibody directed against the HIV-1 envelope glycoprotein can completely block HIV-1/SIV chimeric virus infections of macaque monkeys. Nat. Med. 5:204-10 (Pubitemid 29068528)
7. Mikell I, Sather DN, Kalams SA, et al. 2011. Characteristics of the earliest cross-neutralizing antibody response to HIV-1. PLoS Pathog. 7:e1001251
8. Corti D, Langedijk JP, Hinz A, 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
9. Walker LM, Phogat SK, Chan-Hui PY, et al. 2009. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326:285-89
10. Wu X, Yang ZY, Li Y, et al. 2010. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329:856-61
11. McElrath MJ, Haynes BF. 2010. Induction of immunity to human immunodeficiency virus type-1 by vaccination. Immunity 33:542-54
12. Labrijn AF, Poignard P, Raja A, et al. 2003. Access of antibody molecules to the conserved coreceptor binding site on glycoprotein gp120 is sterically restricted on primary human immunodeficiency virus type 1. J. Virol. 77:10557-65 (Pubitemid 37129699)
13. Mouquet H, Scheid JF, Zoller MJ, et al. 2010. Polyreactivity increases the apparent affinity of anti-HIV antibodies by heteroligation. Nature 467:591-95
14. Richman DD, Wrin T, Little SJ, et al. 2003. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc. Natl. Acad. Sci. USA 100:4144-49 (Pubitemid 36418171)
15. Wei X, Decker JM, Wang S, et al. 2003. Antibody neutralization and escape byHIV-1. Nature 422:307-12
16. Ofek G, Guenaga FJ, Schief WR, et al. 2010. Elicitation of structure-specific antibodies by epitope scaffolds. Proc. Natl. Acad. Sci. USA 107:17880-87
17. Hessell AJ, Hangartner L, Hunter M, et al. 2007. Fc receptor but not complement binding is important in antibody protection against HI V. Nature 449:101-4 (Pubitemid 47373775)
18. Kekow J, Hobusch G, GrossW L. 1988. Predominance of the IgG1 subclass in the hypergammaglobulinemia observed in pre-AIDS and AID S. Cancer Detect. Prev. 12:211-16
19. Banerjee K, Klasse PJ, Sanders RW, et al. 2010. IgG subclass profiles in infected HIV type 1 controllers and chronic progressors and in uninfected recipients of Env vaccines. AIDS Res. Hum. Retroviruses 26:445-58
20. Tomaras GD, Yates NL, Liu P, et al. 2008. Initial B-cell responses to transmitted human immunodeficiency virus type 1: virion-binding immunoglobulin M (IgM) and IgG antibodies followed by plasma anti-gp41 antibodies with ineffective control of initial viremia. J. Virol. 82:12449-63
21. Tomaras GD, Haynes BF. 2009. HIV-1-specific antibody responses during acute and chronic HIV-1 infection. Curr. Opin. HIV AIDS 4:373-79
22. Moore PL, Gray ES, Morris L. 2009. Specificity of the autologous neutralizing antibody response. Curr. Opin. HIV AIDS 4:358-63
23. Mascola JR, Montefiori DC. 2010. The role of antibodies in HIV vaccines. Annu. Rev. Immunol. 28:413-44
24. Seaman MS, Janes H, Hawkins N, et al. 2010. Tiered categorization of a diverse panel of HIV-1 Env pseudoviruses for assessment of neutralizing antibodies. J. Virol. 84:1439-52
25. Baum LL, Cassutt KJ, Knigge K, et al. 1996. HIV-1 gp120-specific antibody-dependent cell-mediated cytotoxicity correlates with rate of disease progression. J. Immunol. 157:2168-73 (Pubitemid 126449697)
26. Forthal DN, Landucci G, Keenan B. 2001. Relationship between antibody-dependent cellular cytotoxicity, plasma HIV type 1 RNA, and CD4+ lymphocyte count. AIDS Res. Hum. Retrovir. 17:553-61 (Pubitemid 32692337)
27. Asmal M, Sun Y, Lane S, et al. 2011. Antibody-dependent cell-mediated viral inhibition emerges after simian immunodeficiency virus SIVmac251 infection of rhesus monkeys coincident with gp140-binding antibodies and is effective against neutralization-resistant viruses. J. Virol. 85:5465-75
28. Yeh WW, Rahman I, Hraber P, et al. 2010. Autologous neutralizing antibodies to the transmitted/founder viruses emerge late after simian immunodeficiency virus SIVmac251 infection of rhesus monkeys. J. Virol. 84:6018-32
29. Shikata K, Yasuda T, Takeuchi F, et al. 1998. Structural changes in the oligosaccharidemoiety of human IgG with aging. Glycoconj. J. 15:683-89 (Pubitemid 28380331)
30. Arnold JN, Dwek RA, Rudd PM, et al. 2006. Mannan binding lectin and its interactionwith immunoglobulins in health and in disease. Immunol. Lett. 106:103-10 (Pubitemid 44223746)
31. Moore JS, Wu X, Kulhavy R, et al. 2005. Increased levels of galactose-deficient IgG in sera of HIV-1-infected individuals. AIDS 19:381-89 (Pubitemid 40446184)
32. Schroeder HW Jr, Cavacini L. 2010. Structure and function of immunoglobulins. J. Allergy Clin. Immunol. 125:S41-52
33. Shields RL, Lai J, Keck R, et al. 2002. Lack of fucose on human IgG1N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity. J. Biol. Chem. 277:26733-40 (Pubitemid 34951677)
34. Miranda LR, Duval M, Doherty H, et al. 2007. The neutralization properties of a HIV-specific antibody aremarkedly altered by glycosylation events outside the antigen-binding domain. J. Immunol. 178:7132-38 (Pubitemid 46847439)
35. Nimmerjahn F, Ravetch JV. 2008. Analyzing antibody-Fc-receptor interactions. Methods Mol. Biol. 415:151-62
36. Liu Q, Sun Y, Rihn S, et al. 2009. Matrix metalloprotease inhibitors restore impaired NK cell-mediated antibody-dependent cellular cytotoxicity in human immunodeficiency virus type 1 infection. J. Virol. 83:8705-12
37. Aitman TJ, Dong R, Vyse TJ, et al. 2006. Copy number polymorphism in Fcgr3 predisposes to glomerulonephritis in rats and humans. Nature 439:851-55 (Pubitemid 43255703)
38. Anthony RM, Ravetch JV. 2010. A novel role for the IgG Fc glycan: the anti-inflammatory activity of sialylated IgG Fcs. J. Clin. Immunol. 30(Suppl. 1):S9-14
39. Willcocks LC, Carr EJ, Niederer HA, et al. 2010. A defunctioning polymorphism in FCGR2B is associated with protection against malaria but susceptibility to systemic lupus erythematosus. Proc. Natl. Acad. Sci. USA 107:7881-85
40. Forthal DN, Landucci G, Bream J, et al. 2007. FcgammaRIIa genotype predicts progression of HIV infection. J. Immunol. 179:7916-23
41. Poonia B, Kijak GH, Pauza CD. 2010. High affinity allele for the gene of FCGR3A is risk factor for HIV infection and progression. PLoS One 5:e15562
42. Brouwer KC, Lal RB, Mirel LB, et al. 2004. Polymorphism of Fc receptor IIa for IgG in infants is associated with susceptibility to perinatal HIV-1 infection. AIDS 18:1187-94 (Pubitemid 38738518)
43. Garred P, Richter C, Andersen AB, et al. 1997. Mannan-binding lectin in the sub-Saharan HIV and tuberculosis epidemics. Scand. J. Immunol. 46:204-8 (Pubitemid 27323849)
44. Dzwonek A, Novelli V, Bajaj-Elliott M, et al. 2006. Mannose-binding lectin in susceptibility and progression of HIV-1 infection in children. Antivir. Ther. 11:499-505 (Pubitemid 44024858)
45. Szabo J, Prohaszka Z, Toth FD, et al. 1999. Strong correlation between the complement-mediated antibody-dependent enhancement of HIV-1 infection and plasma viral load. AIDS 13:1841-49 (Pubitemid 29509542)
46. Fauci AS, Mavilio D, Kottilil S. 2005. NK cells in HIV infection: paradigm for protection or targets for ambush. Nat. Rev. Immunol. 5:835-43 (Pubitemid 41581665)
47. Ahmad A, Menezes J. 1996. Defective killing activity against gp120/41-expressing human erythroleukaemic K562 cell line by monocytes and natural killer cells from HIV-infected individuals. AIDS 10:143-49 (Pubitemid 26056006)
48. Collini P, Noursadeghi M, Sabroe I, et al. 2010. Monocyte and macrophage dysfunction as a cause of HIV-1 induced dysfunction of innate immunity. Curr. Mol. Med. 10:727-40
49. Coleman CM, Wu L. 2009. HIV interactions with monocytes and dendritic cells: viral latency and reservoirs. Retrovirology 6:51
50. Monari C, Casadevall A, Pietrella D, et al. 1999. Neutrophils from patients with advanced human immunodeficiency virus infection have impaired complement receptor function and preserved Fcgamma receptor function. J. Infect. Dis. 180:1542-49 (Pubitemid 29506456)
51. Thomas CA, Weinberger OK, Ziegler BL, et al. 1997. Human immunodeficiency virus-1 env impairs Fc receptor-mediated phagocytosis via a cyclic adenosine monophosphate-dependent mechanism. Blood 90:3760-65 (Pubitemid 27473449)
52. Kedzierska K, Ellery P, Mak J, et al. 2002. HIV-1 down-modulates gamma signaling chain of Fc gammaR in human macrophages: a possible mechanism for inhibition of phagocytosis. J. Immunol. 168:2895-903 (Pubitemid 34211669)
53. Dugast AS, Tonelli A, Berger CT, et al. 2011. Decreased Fc receptor expression on innate immune cells is associated with impaired antibody-mediated cellular phagocytic activity in chronically HIV-1 infected individuals. Virology 415(2):160-67
54. Pan LY, Mendel DB, Zurlo J, et al. 1990. Regulation of the steady state level of Fc gamma RI mRNA by IFN-gamma and dexamethasone in human monocytes, neutrophils, and U-937 cells. J. Immunol. 145:267-75 (Pubitemid 20217411)
55. Stone KD, Prussin C, Metcalfe DD. 2010. Ig E, mast cells, basophils, and eosinophils. J. Allergy Clin. Immunol. 125:S73-80
56. Hashimoto G, Wright PF, Karzon DT. 1983. Antibody-dependent cell-mediated cytotoxicity against influenza virus-infected cells. J. Infect Dis. 148:785-94 (Pubitemid 14244263)
57. Kohl S, Charlebois ED, Sigouroudinia M, et al. 2000. Limited antibody-dependent cellular cytotoxicity antibody response induced by a herpes simplex virus type 2 subunit vaccine. J. Infect. Dis. 181:335-39 (Pubitemid 30049066)
58. Moore T, Ananaba GA, Bolier J, et al. 2002. Fc receptor regulation of protective immunity against Chlamydia trachomatis. Immunology 105:213-21 (Pubitemid 34146688)
59. Iida S, Kuni-Kamochi R, Mori K, et al. 2009. Two mechanisms of the enhanced antibody-dependent cellular cytotoxicity (ADCC) efficacy of non-fucosylated therapeutic antibodies in human blood. BMC Cancer 9:58
60. Sawyer LA, Katzenstein DA, Hendry RM, et al. 1990. Possible beneficial effects of neutralizing antibodies and antibody-dependent, cell-mediated cytotoxicity in human immunodeficiency virus infection. AIDS Res. Hum. Retrovir. 6:341-56 (Pubitemid 20278795)
61. Tyler DS, Lyerly HK, Weinhold KJ. 1989. Anti-HIV-1 ADC C. AIDS Res. Hum. Retrovir. 5:557-63
62. Lambotte O, Ferrari G, Moog C, et al. 2009. Heterogeneous neutralizing antibody and antibodydependent cell cytotoxicity responses in HIV-1 elite controllers. AIDS 23:897-906
63. Ahmad R, Sindhu ST, Toma E, et al. 2001. Evidence for a correlation between antibody-dependent cellular cytotoxicity-mediating anti-HIV-1 antibodies and prognostic predictors of HIV infection. J. Clin. Immunol. 21:227-33 (Pubitemid 32434310)
64. Banks ND, Kinsey N, Clements J, et al. 2002. Sustained antibody-dependent cell-mediated cytotoxicity (ADCC) in SIV-infected macaques correlates with delayed progression to AID S. AIDS Res. Hum. Retrovir. 18:1197-205 (Pubitemid 35370608)
65. Binley JM, Ban YE, Crooks ET, et al. 2010. Role of complex carbohydrates in human immunodeficiency virus type 1 infection and resistance to antibody neutralization. J. Virol. 84:5637-55
66. Forthal DN, Landucci G, Haubrich R, et al. 1999. Antibody-dependent cellular cytotoxicity independently predicts survival in severely immunocompromised human immunodeficiency virus-infected patients. J. Infect. Dis. 180:1338-41 (Pubitemid 30070224)
67. Forthal DN, Landucci G, Cole KS, et al. 2006. Rhesus macaque polyclonal and monoclonal antibodies inhibit simian immunodeficiency virus in the presence of human or autologous rhesus effector cells. J. Virol. 80:9217-25 (Pubitemid 44359994)
68. Van Rompay KK, Berardi CJ, Dillard-Telm S, et al. 1998. Passive immunization of newborn rhesus macaques prevents oral simian immunodeficiency virus infection. J. Infect. Dis. 177:1247-59 (Pubitemid 28194263)
69. Florese RH, Van Rompay KK, Aldrich K, et al. 2006. Evaluation of passively transferred, nonneutralizing antibody-dependent cellular cytotoxicity-mediating IgG in protection of neonatal rhesus macaques against oral SIVmac251 challenge. J. Immunol. 177:4028-36 (Pubitemid 44359936)
70. Gomez-Roman VR, Patterson LJ, Venzon D, et al. 2005. Vaccine-elicited antibodies mediate antibodydependent cellular cytotoxicity correlated with significantly reduced acute viremia in rhesus macaques challenged with SIVmac251. J. Immunol. 174:2185-89 (Pubitemid 40223963)
71. Patterson LJ, Malkevitch N, Venzon D, et al. 2004. Protection against mucosal simian immunodeficiency virus SIV(mac251) challenge by using replicating adenovirus-SIVmultigene vaccine priming and subunit boosting. J. Virol. 78:2212-21 (Pubitemid 38228914)
72. Karnasuta C, Paris RM, Cox JH, et al. 2005. Antibody-dependent cell-mediated cytotoxic responses in participants enrolled in a phase I/II ALVAC-HIV/AIDSVAX B/E prime-boost HIV-1 vaccine trial in Thailand. Vaccine 23:2522-29 (Pubitemid 40332524)
73. McHugh TM, Stites DP, Busch MP, et al. 1988. Relation of circulating levels of human immunodeficiency virus (HIV) antigen, antibody to p24, and HIV-containing immune complexes in HIV-infected patients. J. Infect. Dis. 158:1088-91 (Pubitemid 18266062)
74. Azzam R, Kedzierska K, Leeansyah E, et al. 2006. Impaired complement-mediated phagocytosis byHIV type-1-infected human monocyte-derived macrophages involves a cAMP-dependent mechanism. AIDS Res. Hum. Retrovir. 22:619-29 (Pubitemid 44061398)
75. French MA, Tanaskovic S, Law MG, et al. 2010. Vaccine-induced IgG2 anti-HIV p24 is associated with control of HIV in patients with a 'high-affinity' FcgammaRIIa genotype. AIDS 24:1983-90
76. Ngo-Giang-Huong N, Candotti D, Goubar A, et al. 2001. HIV type 1-specific IgG2 antibodies:markers of helper T cell type 1 response and prognostic marker of long-term nonprogression. AIDS Res. Hum. Retrovir. 17:1435-46 (Pubitemid 33042811)
77. Xu W, Santini PA, Sullivan JS, et al. 2009. HIV-1 evades virus-specific IgG2 and IgA responses by targeting systemic and intestinal B cells via long-range intercellular conduits. Nat. Immunol. 10:1008-17
78. Stoermer KA, Morrison TE. 2011. Complement and viral pathogenesis. Virology 411:362-73
79. Huber M, Fischer M, Misselwitz B, et al. 2006. Complement lysis activity in autologous plasma is associated with lower viral loads during the acute phase of HIV-1 infection. PLoS Med. 3:e441
80. Aasa-Chapman MM, Holuigue S, Aubin K, et al. 2005. Detection of antibody-dependent complementmediated inactivation of both autologous and heterologous virus in primary human immunodeficiency virus type 1 infection. J. Virol. 79:2823-30 (Pubitemid 40270560)
81. Garred P, Madsen HO, Balslev U, et al. 1997. Susceptibility to HIV infection and progression of AIDS in relation to variant alleles of mannose-binding lectin. Lancet 349:236-40 (Pubitemid 27050989)
82. Stoiber H, Banki Z, Wilflingseder D, et al. 2008. Complement-HIV interactions during all steps of viral pathogenesis. Vaccine 26:3046-54
83. Putkonen P, Thorstensson R, Ghavamzadeh L, et al. 1991. Prevention of HIV-2 and SIVsm infection by passive immunization in cynomolgus monkeys. Nature 352:436-38 (Pubitemid 21896742)
84. Lewis MG, Elkins WR, McCutchan FE, et al. 1993. Passively transferred antibodies directed against conserved regions of SIV envelope protect macaques from SIV infection. Vaccine 11:1347-55 (Pubitemid 23319664)
85. Kent KA, Kitchin P, Mills KH, et al. 1994. Passive immunization of cynomolgus macaques with immune sera or a pool of neutralizing monoclonal antibodies failed to protect against challenge with SIVmac251. AIDS Res. Hum. Retrovir. 10:189-94 (Pubitemid 24086143)
86. Gardner M, Rosenthal A, Jennings M, et al. 1995. Passive immunization of rhesus macaques against SIV infection and disease. AIDS Res. Hum. Retrovir. 11:843-54
87. Binley JM, Clas B, Gettie A, et al. 2000. Passive infusion of immune serum into simian immunodeficiency virus-infected rhesus macaques undergoing a rapid disease course has minimal effect on plasma viremia. Virology 270:237-49 (Pubitemid 30256556)
88. Hidajat R, Xiao P, Zhou Q, et al. 2009. Correlation of vaccine-elicited systemic and mucosal nonneutralizing antibody activities with reduced acute viremia following intrarectal simian immunodeficiency virus SIVmac251 challenge of rhesus macaques. J. Virol. 83:791-801
89. Florese RH, Demberg T, Xiao P, et al. 2009. Contribution of nonneutralizing vaccine-elicited antibody activities to improved protective efficacy in rhesus macaques immunized with Tat/Env compared with multigenic vaccines. J. Immunol. 182:3718-27
90. Xiao P, Zhao J, Patterson LJ, et al. 2010. Multiple vaccine-elicited nonneutralizing antienvelope antibody activities contribute to protective efficacy by reducing both acute and chronic viremia following simian/human immunodeficiency virus SHIV89. 6P challenge in rhesus macaques. J. Virol. 84:7161-73
91. Bohring C, Krause W. 2005. The role of antisperm antibodies during fertilization and for immunological infertility. Chem. Immunol. Allergy 88:15-26 (Pubitemid 43094375)
92. vonBubnoff A. 2011. Antibody news. IAVIReport. http://www. iavireport. org/IRblog/Lists/Posts/Post. aspx?ID=67
93. Banki Z, Kacani L, Rusert P, et al. 2005. Complement dependent trapping of infectious HIV in human lymphoid tissues. AIDS 19:481-86 (Pubitemid 40515851)
94. Harada N, Iijima S, Kobayashi K, et al. 1997. Human IgGFc binding protein (FcgammaBP) in colonic epithelial cells exhibits mucin-like structure. J. Biol. Chem. 272:15232-41 (Pubitemid 27255541)
95. Schmidt AC. 2010. Response to dengue fever-the good, the bad, and the ugly? N. Engl. J. Med. 363:484-87
96. Beck Z, Prohaszka Z, Fust G. 2008. Traitors of the immune system-enhancing antibodies in HIV infection: their possible implication in HIV vaccine development. Vaccine 26:3078-85
97. Connor RI, Dinces NB, Howell AL, et al. 1991. Fc receptors for IgG (Fc gamma Rs) on human monocytes andmacrophages are not infectivity receptors for human immunodeficiency virus type 1 (HIV-1): studies using bispecific antibodies to target HIV-1 to various myeloid cell surface molecules, including the Fc gamma R. Proc. Natl. Acad. Sci. USA 88:9593-97 (Pubitemid 21915677)
98. Willey S, Aasa-Chapman MM, O'Farrell S, et al. 2011. Extensive complement-dependent enhancement of HIV-1 by autologous non-neutralising antibodies at early stages of infection. Retrovirology 8:16
99. Racila E, Link BK, Weng WK, et al. 2008. A polymorphism in the complement component C1qA correlates with prolonged response following rituximab therapy of follicular lymphoma. Clin. Cancer Res. 14:6697-703
100. Wang SY, Veeramani S, Racila E, et al. 2009. Depletion of the C3 component of complement enhances the ability of rituximab-coated target cells to activate human NK cells and improves the efficacy of monoclonal antibody therapy in an in vivo model. Blood 114:5322-30
101. Zhu P, Chertova E, Bess J Jr, et al. 2003. Electron tomography analysis of envelope glycoprotein trimers on HIV and simian immunodeficiency virus virions. Proc. Natl. Acad. Sci. USA 100:15812-17 (Pubitemid 38021072)