Phagocytosis: Cell biology view of antiviral function

Current Opinion in HIV and AIDS

Volumn 9, Issue 3, 2014, Pages 271-277

  Carias, Ann M ^a   Hope, Thomas J ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

antibody effector functions; Antibody dependent cellular phagocytosis; complement mediated phagocytosis; HIV; phagocytosis

Indexed keywords

FC RECEPTOR; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY;

ANTIVIRAL ACTIVITY; COMPLEMENT SYSTEM; COMPLEMENT-MEDIATED PHAGOCYTOSIS; CYTOLOGY; GENETIC POLYMORPHISM; GLYCOSYLATION; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE SYSTEM; PHAGOCYTOSIS; PRIORITY JOURNAL; REVIEW; VIRUS TRANSMISSION; HUMAN; IMMUNOLOGY;

HIV ANTIBODIES; HIV INFECTIONS; HUMANS; PHAGOCYTOSIS;

EID: 84898541281     PISSN: 1746630X     EISSN: 17466318     Source Type: Journal    
DOI: 10.1097/COH.0000000000000050     Document Type: Review

References (109)

1. Velasco-Hernandez JX, Gershengorn HB, Blower SM. Could widespread use of combination antiretroviral therapy eradicate HIV epidemics? Lancet Infect Dis 2002; 2:487-493.
2. UNAIDS. 2012 Report on the global AIDS epidemic. 2012.
3. Van Damme L, Govinden R, Mirembe FM, et al. Lack of effectiveness of cellulose sulfate gel for the prevention of vaginal HIV transmission. N Engl J Med 2008; 359:463-472.
4. Watkins DI, Burton DR, Kallas EG, et al. Nonhuman primate models and the failure of the Merck HIV-1 vaccine in humans. Nat Med 2008; 14:617-621.
5. Skoler-Karpoff S, Ramjee G, Ahmed K, et al. Efficacy of Carraguard for prevention of HIV infection in women in South Africa: a randomised, double-blind, placebo-controlled trial. Lancet 2008; 372:1977-1987.
6. Halpern V, Ogunsola F, Obunge O, et al. Effectiveness of cellulose sulfate vaginal gel for the prevention of HIV infection: results of a Phase III trial in Nigeria. PLoS One 2008; 3:e3784.
7. Murphy K, Travers P, Walport M, et al. Janeway's Immunobiology. 8th edn. New York: Garland Science; 2012; xix, 868 pp.
8. Rabinovitch M. Professional and nonprofessional phagocytes: an introduction. Trends Cell Biol 1995; 5:85-87.
9. Holl V, Hemmerter S, Burrer R, et al. Involvement of Fc gamma RI (CD64) in the mechanism of HIV-1 inhibition by polyclonal IgG purified from infected patients in cultured monocyte-derived macrophages. J Immunol 2004; 173:6274-6283.
10. Stuart LM, Ezekowitz RA. Phagocytosis: elegant complexity. Immunity 2005; 22:539-550.
11. Aderem A, Underhill DM. Mechanisms of phagocytosis in macrophages. Annu Rev Immunol 1999; 17:593-623.
12. Aderem AA, Wright SD, Silverstein SC, et al. Ligated complement receptors do not activate the arachidonic acid cascade in resident peritoneal macro-phages. J Exp Med 1985; 161:617-622.
13. Yu Q, Yu R, Qin X. The good and evil of complement activation in HIV-1 infection. Cell Mol Immunol 2010; 7:334-340.
14. Fearon DT. Identification of the membrane glycoprotein that is the C3b receptor of the human erythrocyte, polymorphonuclear leukocyte, B lymphocyte, and monocyte. J Exp Med 1980; 152:20-30.
15. Tohyama Y, Yamamura H. Complement-mediated phagocytosis: the role of Syk. IUBMB life 2006; 58:304-308.
16. Carroll MC. The role of complement and complement receptors in induction and regulation of immunity. Annu Rev Immunol 1998; 16:545-568.
17. Graham IL, Gresham HD, Brown EJ. An immobile subset of plasma membrane CD11b/CD18 (Mac-1) is involved in phagocytosis of targets recognized by multiple receptors. J Immunol 1989; 142:2352-2358.
18. Rosen H, Law SK. The leukocyte cell surface receptor(s) for the iC3b product of complement. Curr Top Microbiol ImmunolV 153 1990; 99-122.
19. Wright SD, Craigmyle LS, Silverstein SC. Fibronectin and serum amyloid P component stimulate C3b-and C3bi-mediated phagocytosis in cultured human monocytes. J Exp Med 1983; 158:1338-1343.
20. Wright SD, Griffin FM Jr. Activation of phagocytic cells' C3 receptors for phagocytosis. J Leukoc Biol 1985; 38:327-339.
21. Caron E, Hall A. Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science 1998; 282:1717-1721.
22. Holl V, Peressin M, Moog C. Antibody-mediated Fcgamma receptor-based mechanisms of HIV inhibition: recent findings and new vaccination strategies. Viruses 2009; 1:1265-1294.
23. Fanger MW, Shen L, Graziano RF, et al. Cytotoxicity mediated by human Fc receptors for IgG. Immunol Today 1989; 10:92-99.
24. Jouault T, Chapuis F, Olivier R, et al. HIV infection of monocytic cells: role of antibody-mediated virus binding to Fc-gamma receptors. AIDS 1989; 3:125-133.
25. Gallo P, Goncalves R, Mosser DM. The influence of IgG density and macrophage Fc (gamma) receptor cross-linking on phagocytosis and IL-10 production. Immunol Lett 2010; 133:70-77.
26. Ravetch JV, Bolland S. IgGFc receptors. Annu Rev Immunol 2001; 19:275-290.
27. Mellman IS, Plutner H, Steinman RM, et al. Internalization and degradation of macrophage Fc receptors during receptor-mediated phagocytosis. J Cell Biol 1983; 96:887-895.
28. Hulett MD, Hogarth PM. Molecular basis of Fc receptor function. Adv Immunol 1994; 57:1-127.
29. Indik ZK, Hunter S, Huang MM, et al. The high affinity Fc gamma receptor (CD64) induces phagocytosis in the absence of its cytoplasmic domain: the gamma subunit of Fc gamma RIIIA imparts phagocytic function to Fc gamma RI. Exp Hematol 1994; 22:599-606.
30. Tuijnman WB, Capel PJ, van de Winkel JG. Human low-affinity IgG receptor Fc gamma RIIa (CD32) introduced into mouse fibroblasts mediates phagocytosis of sensitized erythrocytes. Blood 1992; 79:1651-1656.
31. Park JG, Isaacs RE, Chien P, et al. In the absence of other Fc receptors, Fc gamma RIIIA transmits a phagocytic signal that requires the cytoplasmic domain of its gamma subunit. J Clin Invest 1993; 92:1967-1973.
32. Tridandapani S, Siefker K, Teillaud JL, et al. Regulated expression and inhibitory function of Fcgamma RIIb in human monocytic cells. J Biol Chem 2002; 277:5082-5089.
33. Hunter S, Indik ZK, Kim MK, et al. Inhibition of Fcgamma receptor-mediated phagocytosis by a nonphagocytic Fcgamma receptor. Blood 1998; 91:1762-1768.
34. Nimmerjahn F, Ravetch JV. Fcgamma receptors as regulators of immune responses. Nat Rev Immunol 2008; 8:34-47.
35. Daeron M. Fc receptor biology. Annu Rev Immunol 1997; 15:203-234.
36. Morton HC, van den Herik-Oudijk IE, Vossebeld P, et al. Functional association between the human myeloid immunoglobulin A Fc receptor (CD89) and FcR gamma chain. Molecular basis for CD89/FcR gamma chain association. J Biol Chem 1995; 270:29781-29787.
37. Bakema JE, van Egmond M. The human immunoglobulin A Fc receptor FcalphaRI: a multifaceted regulator of mucosal immunity. Mucosal Immunol 2011; 4:612-624.
38. Shen R, Richter HE, Clements RH, et al. Macrophages in vaginal but not intestinal mucosa are monocyte-like and permissive to human immunodeficiency virus type 1 infection. J Virol 2009; 83:3258-3267.
39. Herr AB, Ballister ER, Bjorkman PJ. Insights into IgA-mediated immune responses from the crystal structures of human FcalphaRI and its complex with IgA1-Fc. Nature 2003; 423:614-620.
40. Phalipon A, Corthesy B. Novel functions of the polymeric Ig receptor: well beyond transport of immunoglobulins. Trends Immunol 2003; 24:55-58.
41. Anthony RM, Wermeling F, Ravetch JV. Novel roles for the IgG Fc glycan. Ann N Y Acad Sci 2012; 1253:170-180.
42. Forthal DN, Moog C. Fc receptor-mediated antiviral antibodies. Curr Opin HIV AIDS 2009; 4:388-393.
43. Vargas-Inchaustegui DA, Robert-Guroff M. Fc receptor-mediated immune responses: new tools but increased complexity in hiv prevention. Curr HIV Res 2013; 11:407-420.
44. Brenner BG, Gryllis C, Wainberg MA. Role of antibody-dependent cellular cytotoxicity and lymphokine-activated killer cells in AIDS and related diseases. J Leukoc Biol 1991; 50:628-640.
45. May RC, Machesky LM. Phagocytosis and the actin cytoskeleton. J Cell Sci 2001; 114 (Pt 6):1061-1077.
46. Sanchez-Mejorada G, Rosales C. Signal transduction by immunoglobulin Fc receptors. J Leukoc Biol 1998; 63:521-533.
47. Garcia-Garcia E, Rosales C. Signal transduction during Fc receptor-mediated phagocytosis. J Leukoc Biol 2002; 72:1092-1108.
48. Silverstein SC. Phagocytosis of microbes: insights and prospects. Trends Cell Biol 1995; 5:141-142.
49. Allen LA, Aderem A. Molecular definition of distinct cytoskeletal structures involved in complement-and Fc receptor-mediated phagocytosis in macro-phages. J Exp Med 1996; 184:627-637.
50. Kaplan G. Differences in the mode of phagocytosis with Fcand C3 receptors in macrophages. Scand J Immunol 1977; 6:797-807.
51. Stoiber H, Banki Z, Wilflingseder D, et al. Complement-HIV interactions during all steps of viral pathogenesis. Vaccine 2008; 26:3046-3054.
52. Vanderpuye OA, Labarrere CA, McIntyre JA. The complement system in human reproduction. Am J Reprod Immunol 1992; 27:145-155.
53. Marschang P, Kruger U, Ochsenbauer C, et al. Complement activation by HIV-1-infected cells: the role of transmembrane glycoprotein gp41. J Acquir Immune Defic Syndr Hum Retrovirol 1997; 14:102-109.
54. Doepper S, Stoiber H, Kacani L, et al. B cell-mediated infection of stimulated and unstimulated autologous T lymphocytes with HIV-1: role of complement. Immunobiology 2000; 202:293-305.
55. Banki Z, Kacani L, Rusert P, et al. Complement dependent trapping of infectious HIV in human lymphoid tissues. AIDS 2005; 19:481-486.
56. Ebenbichler CF, Thielens NM, Vornhagen R, et al. Human immunodeficiency virus type 1 activates the classical pathway of complement by direct C1 binding through specific sites in the transmembrane glycoprotein gp41. J Exp Med 1991; 174:1417-1424.
57. Ji X, Gewurz H, Spear GT. Mannose binding lectin (MBL) and HIV. Mol Immunol 2005; 42:145-152.
58. Susal C, Kirschfink M, Kropelin M, et al. Complement activation by recombi-nant HIV-1 glycoprotein gp120. J Immunol 1994; 152:6028-6034.
59. Haurum JS, Thiel S, Jones IM, et al. Complement activation upon binding of mannan-binding protein to HIV envelope glycoproteins. AIDS 1993; 7:1307-1313.
60. Banki Z, Stoiber H, Dierich MP. HIV and human complement: inefficient virolysis and effective adherence. Immunol Lett 2005; 97:209-214.
61. Delibrias CC, Fischer EM, Kazatchkine MD. The enhancing role of complement in human immunodeficiency virus infection: soluble recombinant CR1 (CD35) inhibits complement-mediated enhancement of infection of a CD4-positive T-cell line with human immunodeficiency virus-1. Scand J Immunol 2000; 51:526-529.
62. Tacnet-Delorme P, Boyer V, Thielens NM, et al. In vitro analysis of complement-dependent HIV-1 cell infection using a model system. J Immunol 1999; 162:4088-4093.
63. Stoiber H, Frank I, Spruth M, et al. Inhibition of HIV-1 infection in vitro by monoclonal antibodies to the complement receptor type 3 (CR3): an accessory role for CR3 during virus entry? Mol Immunol 1997; 34:855-863.
64. Bouhlal H, Galon J, Kazatchkine MD, et al. Soluble CD16 inhibits CR3(CD11b/CD18)-mediated infection of monocytes/macrophages by opsonized primary R5 HIV-1. J Immunol 2001; 166:3377-3383.
65. Bender BS, Davidson BL, Kline R, et al. Role of the mononuclear phagocyte system in the immunopathogenesis of human immunodeficiency virus infection and the acquired immunodeficiency syndrome. Rev Infect Dis 1988; 10:1142-1154.
66. Stoiber H, Kacani L, Speth C, et al. The supportive role of complement in HIV pathogenesis. Immunol Rev 2001; 180:168-176.
67. Stoiber H, Ebenbichler C, Schneider R, et al. Interaction of several complement proteins with gp120 and gp41, the two envelope glycoproteins of HIV-1. AIDS 1995; 9:19-26.
68. Jakubik JJ, Saifuddin M, Takefman DM, et al. B lymphocytes in lymph nodes and peripheral blood are important for binding immune complexes containing HIV-1. Immunology 1999; 96:612-619.
69. Schmitz J, Zimmer JP, Kluxen B, et al. Antibody-dependent complement-mediated cytotoxicity in sera from patients with HIV-1 infection is controlled by CD55 and CD59. J Clin Invest 1995; 96:1520-1526.
70. Huber VC, Lynch JM, Bucher DJ, et al. Fc receptor-mediated phagocytosis makes a significant contribution to clearance of influenza virus infections. J Immunol 2001; 166:7381-7388.
71. McCullough KC, Smale CJ, Carpenter WC, et al. Conformational alteration in foot-and-mouth disease virus virion capsid structure after complexing with monospecific antibody. Immunology 1987; 60:75-82.
72. McCullough KC, Parkinson D, Crowther JR. Opsonization-enhanced phagocytosis of foot-and-mouth disease virus. Immunology 1988; 65:187-191.
73. Chung KM, Thompson BS, Fremont DH, et al. Antibody recognition of cell surface-associated NS1 triggers Fc-gamma receptor-mediated phagocytosis and clearance of West Nile virus-infected cells. J Virol 2007; 81:9551-9555.
74. Ngo-Giang-Huong N, Candotti D, Goubar A, et al. HIV type 1-specific IgG2 antibodies: markers of helper T cell type 1 response and prognostic marker of long-term nonprogression. AIDS Res Hum Retroviruses 2001; 17:1435-1446.
75. Bruhns P. Properties of mouse and human IgG receptors and their contribution to disease models. Blood 2012; 119:5640-5649.
76. Dugast AS, Tonelli A, Berger CT, 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; 415:160-167.
77. Ackerman ME, Dugast AS, McAndrew EG, et al. Enhanced phagocytic activity of HIV-specific antibodies correlates with natural production of mmunoglobulins with skewed affinity for FcgammaR2a and FcgammaR2b. J Virol 2013; 87:5468-5476.
78. Gomez-Roman VR, Patterson LJ, Venzon D, et al. Vaccine-elicited antibodies mediate antibody-dependent cellular cytotoxicity correlated with significantly reduced acute viremia in rhesus macaques challenged with SIVmac251. J Immunol 2005; 174:2185-2189.
79. Forthal DN, Gilbert PB, Landucci G, et al. 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; 178:6596-6603.
80. 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.
81. Florese RH, Demberg T, Xiao P, et al. Contribution of nonneutralizing vaccine-elicited antibody activities to improved protective efficacy in rhesus macaques immunized with Tat/Env compared with multigenic vaccines. J Immunol 2009; 182:3718-3727.
82. 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.
83. Hidajat R, Xiao P, Zhou Q, et al. 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 VirolV 83 2009; 791-801.
84. Banks ND, Kinsey N, Clements J, et al. Sustained antibody-dependent cell-mediated cytotoxicity (ADCC) in SIV-infected macaques correlates with delayed progression to AIDS. AIDS Res Hum Retroviruses 2002; 18:1197-1205.
85. Perez-Bercoff D, David A, Sudry H, et al. Fcgamma receptor-mediated suppression of human immunodeficiency virus type 1 replication in primary human macrophages. J Virol 2003; 77:4081-4094.
86. Hessell AJ, Rakasz EG, Poignard P, et al. Broadly neutralizing human anti-HIV antibody 2G12 is effective in protection against mucosal SHIV challenge even at low serum neutralizing titers. PLoS Pathog 2009; 5:e1000433.
87. Mascola JR, Lewis MG, Stiegler G, et al. Protection of macaques against pathogenic simian/human immunodeficiency virus 89.6PD by passive transfer of neutralizing antibodies. J Virol 1999; 73:4009-4018.
88. 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.
89. Trifonova RT, Lieberman J, van Baarle D. Distribution of immune cells in the human cervix and implications for HIV transmission. Am J Reprod Immunol 2014; 71:252-264.
90. Wira CR, Fahey JV, Sentman CL, et al. Innate and adaptive immunityin female genital tract: cellular responses and interactions. Immunol Rev 2005; 206:306-335.
91. Givan AL, White HD, Stern JE, et al. Flow cytometric analysis of leukocytes in the human female reproductive tract: comparison of fallopian tube, uterus, cervix, and vagina. Am J Reprod ImmunolV 38 1997; 350-359.
92. Szelc CM, Mitcheltree C, Roberts RL, et al. Deficient polymorphonuclear cell and mononuclear cell antibody-dependent cellular cytotoxicity in pediatric and adult human immunodeficiency virus infection. J Infect Dis 1992; 166:486-493.
93. 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.
94. Van Rompay KK, Berardi CJ, Dillard-Telm S, et al. Passive immunization of newborn rhesus macaques prevents oral simian immunodeficiency virus infection. J Infect Dis 1998; 177:1247-1259.
95. Holl V, Peressin M, Decoville T, et al. Nonneutralizing antibodies are able to inhibit human immunodeficiency virus type 1 replication in macrophages and immature dendritic cells. J Virol 2006; 80:6177-6181.
96. Burton DR, Hessell AJ, Keele BF, 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 USA 2011; 108:11181-11186.
97. Moog C, Dereuddre-Bosquet N, Teillaud JL, et al. Protective effect of vaginal application of neutralizing and nonneutralizing inhibitory antibodies against vaginal SHIV challenge in macaques. Mucosal Immunol 2014; 7:46-56.
98. 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.
99. Flynn NM, Forthal DN, Harro CD, et al. Placebo-controlled phase 3 trial of a recombinant glycoprotein 120 vaccine to prevent HIV-1 infection. J Infect DisV 191 2005; 654-665.
100. Montefiori DC, Karnasuta C, Huang Y, et al. Magnitude and breadth of the neutralizing antibody response in the RV144 and Vax003 HIV-1 vaccine efficacy trials. J Infect Dis 2012; 206:431-441.
101. Burton DR, Dwek RA. Immunology. Sugar determines antibody activity. Science 2006; 313:627-628.
102. Warmerdam PA, van de Winkel JG, Vlug A, et al. A single amino acid in the second Ig-like domain of the human Fc gamma receptor II is critical for human IgG2 binding. J Immunol 1991; 147:1338-1343.
103. Clark MR, Clarkson SB, Goldstein IM. Molecular basis for a polymorphism involving Fc receptor II on human monocytes. Trans Assoc Am PhysiciansV 102 1989; 252-259.
104. Poonia B, Kijak GH, Pauza CD. High affinity allele for the gene of FCGR3A is risk factor for HIV infection and progression. PLoS One 2010; 5:e15562.
105. Forthal DN, Landucci G, Bream J, et al. FcgammaRIIa genotype predicts progression of HIV infection. J Immunol 2007; 179:7916-7923.
106. Brouwer KC, Lal RB, Mirel LB, et al. Polymorphism of Fc receptor IIa for IgG in infants is associated with susceptibility to perinatal HIV-1 infection. AIDS 2004; 18:1187-1194.
107. Arnold JN, Wormald MR, Sim RB, et al. The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu Rev ImmunolV 25 2007; 21-50.
108. 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.
109. 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.