Antiviral Monoclonal Antibodies: Can They Be More Than Simple Neutralizing Agents?

Trends in Microbiology

Volumn 23, Issue 10, 2015, Pages 653-665

  Pelegrin, Mireia ^a,b   Naranjo Gomez, Mar ^a,b   Piechaczyk, Marc ^a,b  

^a INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

^b UNIV MONTPELLIER   (France)

Author keywords

Antiviral therapy; Fc receptors; Immune complexes; Immunotherapy; Monoclonal antibodies; Vaccine like effects

Indexed keywords

ANTIVIRUS AGENT; MONOCLONAL ANTIBODY; VIRUS ANTIBODY; VIRUS ANTIGEN;

ANTIBODY DEPENDENT CELL MEDIATED VIRUS INHIBITION; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY DEPENDENT CELLULAR PHAGOCYTOSIS; ANTIGEN BINDING; ANTIGEN RECOGNITION; ANTIVIRAL ACTIVITY; CELL PHAGOCYTOSIS; DRUG MECHANISM; HENDRA VIRUS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN RESPIRATORY SYNCYTIAL VIRUS; IMMUNE RESPONSE; IMMUNOTHERAPY; INNATE IMMUNITY; MURINE LEUKEMIA VIRUS; NIPAH VIRUS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIMIAN IMMUNODEFICIENCY VIRUS; VIRION; VIRUS INFECTION; VIRUS INHIBITION; VIRUS STRAIN; IMMUNOLOGY;

ANTIBODIES, MONOCLONAL; ANTIBODIES, VIRAL; ANTIVIRAL AGENTS; HUMANS;

EID: 84943597136     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2015.07.005     Document Type: Review

References (97)

1. Beck A., et al. Strategies and challenges for the next generation of therapeutic antibodies. Nat. Rev. Immunol. 2010, 10:345-352.
2. Reichert J.M. Antibodies to watch in 2015. MAbs 2015, 7:1-8.
3. Vacchelli E., et al. Trial watch: monoclonal antibodies in cancer therapy. Oncoimmunology 2013, 2:e22789.
4. Berry J.D., Gaudet R.G. Antibodies in infectious diseases: polyclonals, monoclonals and niche biotechnology. Nat. Biotechnol. 2011, 28:489-501.
5. Bossart K.N., et al. A neutralizing human monoclonal antibody protects against lethal disease in a new ferret model of acute nipah virus infection. PLoS Pathog. 2009, 5:e1000642.
6. Both L., et al. Monoclonal antibodies for prophylactic and therapeutic use against viral infections. Vaccine 2013, 31:1553-1559.
7. Corti D., Lanzavecchia A. Broadly neutralizing antiviral antibodies. Annu. Rev. Immunol. 2013, 31:705-742.
8. Krawczyk A., et al. Overcoming drug-resistant herpes simplex virus (HSV) infection by a humanized antibody. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:6760-6765.
9. Marasco W.A., Sui J. The growth and potential of human antiviral monoclonal antibody therapeutics. Nat. Biotechnol. 2007, 25:1421-1434.
10. Flego M., et al. Clinical development of monoclonal antibody-based drugs in HIV and HCV diseases. BMC Med. 2013, 11:4.
11. Qiu X., et al. Reversion of advanced Ebola virus disease in nonhuman primates with ZMapp. Nature 2014, 514:47-53.
12. Sautto G., et al. Possible future monoclonal antibody (mAb)-based therapy against arbovirus infections. Biomed. Res. Int. 2013, 2013:838491.
13. Williams K.L., et al. Therapeutic efficacy of antibodies lacking Fcgamma receptor binding against lethal dengue virus infection is due to neutralizing potency and blocking of enhancing antibodies [corrected]. PLoS Pathog. 2013, 9:e1003157.
14. Dejnirattisai W., et al. A new class of highly potent, broadly neutralizing antibodies isolated from viremic patients infected with dengue virus. Nat. Immunol. 2015, 16:170-177.
15. Flyak A.I., et al. Mechanism of human antibody-mediated neutralization of Marburg virus. Cell 2015, 160:893-903.
16. Qin Y., et al. Characterization of a large panel of rabbit monoclonal antibodies against HIV-1 gp120 and isolation of novel neutralizing antibodies against the V3 loop. PLoS ONE 2015, 10:e0128823.
17. Tan Y., et al. A novel humanized antibody neutralizes H5N1 influenza virus via two different mechanisms. J. Virol. 2015, 89:3712-3722.
18. Cohen J. Immunology. Bound for glory. Science 2013, 341:1168-1171.
19. Euler Z., Alter G. Exploring the potential of monoclonal antibody therapeutics for HIV-1 eradication. AIDS Res. Hum. Retroviruses 2014, 31:13-24.
20. Huang J., et al. Broad and potent HIV-1 neutralization by a human antibody that binds the gp41-gp120 interface. Nature 2014, 515:138-142.
21. Klein F., et al. Antibodies in HIV-1 vaccine development and therapy. Science 2013, 341:1199-1204.
22. Kwong P.D., et al. Broadly neutralizing antibodies and the search for an HIV-1 vaccine: the end of the beginning. Nat. Rev. Immunol. 2013, 13:693-701.
23. Barouch D.H., et al. Therapeutic efficacy of potent neutralizing HIV-1-specific monoclonal antibodies in SHIV-infected rhesus monkeys. Nature 2013, 503:224-228.
24. de Jong Y.P., et al. Broadly neutralizing antibodies abrogate established hepatitis C virus infection. Sci. Transl. Med. 2014, 6:254ra129.
25. Forthal D.N., Moog C. Fc receptor-mediated antiviral antibodies. Curr. Opin. HIV AIDS 2009, 4:388-393.
26. Hessell A.J., Haigwood N.L. Neutralizing antibodies and control of HIV: moves and countermoves. Curr. HIV/AIDS Rep. 2012, 9:64-72.
27. Su B., Moog C. Which antibody functions are important for an HIV vaccine?. Front. Immunol. 2014, 5:289.
28. Akkina R. New generation humanized mice for virus research: comparative aspects and future prospects. Virology 2013, 435:14-28.
29. Brehm M.A., et al. Generation of improved humanized mouse models for human infectious diseases. J. Immunol. Methods 2014, 410:3-17.
30. Klein F., et al. Enhanced HIV-1 immunotherapy by commonly arising antibodies that target virus escape variants. J. Exp. Med. 2014, 211:2361-2372.
31. Lux A., Nimmerjahn F. Of mice and men: the need for humanized mouse models to study human IgG activity in vivo. J. Clin. Immunol. 2012, 33(Suppl. 1):S4-S8.
32. Shultz L.D., et al. Humanized mice for immune system investigation: progress, promise and challenges. Nat. Rev. Immunol. 2012, 12:786-798.
33. Portis J.L., et al. Neurodegenerative disease induced by the wild mouse ecotropic retrovirus is markedly accelerated by long terminal repeat and gag-pol sequences from nondefective Friend murine leukemia virus. J. Virol. 1990, 64:1648-1656.
34. Gros L., et al. Induction of long-term protective antiviral endogenous immune response by short neutralizing monoclonal antibody treatment. J. Virol. 2005, 79:6272-6280.
35. Gros L., et al. Endogenous cytotoxic T-cell response contributes to the long-term antiretroviral protection induced by a short period of antibody-based immunotherapy of neonatally infected mice. J. Virol. 2008, 82:1339-1349.
36. Michaud H.A., et al. A crucial role for infected-cell/antibody immune complexes in the enhancement of endogenous antiviral immunity by short passive immunotherapy. PLoS Pathog. 2010, 6:e1000948.
37. Nasser R., et al. Long-lasting protective antiviral immunity induced by passive immunotherapies requires both neutralizing and effector functions of the administered monoclonal antibody. J. Virol. 2010, 84:10169-10181.
38. Nasser R., et al. Control of regulatory T cells is necessary for vaccine-like effects of antiviral immunotherapy by monoclonal antibodies. Blood 2013, 121:1102-1111.
39. Haigwood N.L., et al. Passive immunotherapy in simian immunodeficiency virus-infected macaques accelerates the development of neutralizing antibodies. J. Virol. 2004, 78:5983-5995.
40. + T-cell induction in neutralizing antibody-triggered control of simian immunodeficiency virus infection. J. Virol. 2009, 83:5514-5524.
41. Yamamoto H., et al. Post-infection immunodeficiency virus control by neutralizing antibodies. PLoS ONE 2007, 2:e540.
42. Villinger F., et al. Evidence for antibody-mediated enhancement of simian immunodeficiency virus (SIV) Gag antigen processing and cross presentation in SIV-infected rhesus macaques. J. Virol. 2003, 77:10-24.
43. Ng C.T., et al. Passive neutralizing antibody controls SHIV viremia and enhances B cell responses in infant macaques. Nat. Med. 2010, 16:1117-1119.
44. Jaworski J.P., et al. Neutralizing polyclonal IgG present during acute infection prevents rapid disease onset in simian-human immunodeficiency virus SHIVSF162P3-infected infant rhesus macaques. J. Virol. 2013, 87:10447-10459.
45. Caskey M., et al. Viraemia suppressed in HIV-1-infected humans by broadly neutralizing antibody 3BNC117. Nature 2015, Published online April 8, 2015. 10.1038/nature14411.
46. Watkins J.D., et al. An anti-HIV-1 V3 loop antibody fully protects cross-clade and elicits T-cell immunity in macaques mucosally challenged with an R5 clade C SHIV. PLoS ONE 2011, 6:e18207.
47. Boyoglu-Barnum S., et al. Prophylaxis with a respiratory syncytial virus (RSV) anti-G protein monoclonal antibody shifts the adaptive immune response to RSV rA2-line19F infection from Th2 to Th1 in BALB/c mice. J. Virol. 2014, 88:10569-10583.
48. Kauvar L.M., et al. Therapeutic targeting of respiratory syncytial virus G-protein. Immunotherapy 2010, 2:655-661.
49. Swedan S., et al. Multiple functional domains and complexes of the two nonstructural proteins of human respiratory syncytial virus contribute to interferon suppression and cellular location. J. Virol. 2011, 85:10090-10100.
50. Bossart K.N., et al. A neutralizing human monoclonal antibody protects African Green monkeys from hendra virus challenge. Sci. Transl. Med. 2011, 3:105ra103.
51. Geisbert T.W., et al. Therapeutic treatment of Nipah virus infection in nonhuman primates with a neutralizing human monoclonal antibody. Sci. Transl. Med. 2014, 6:242ra282.
52. Broder C.C., et al. A treatment for and vaccine against the deadly Hendra and Nipah viruses. Antiviral. Res. 2013, 100:8-13.
53. Nishikawa H., Sakaguchi S. Regulatory T cells in cancer immunotherapy. Curr. Opin. Immunol. 2014, 27:1-7.
54. Pardoll D.M. The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer 2012, 12:252-264.
55. Sharma P., Allison J.P. Immune checkpoint targeting in cancer therapy: toward combination strategies with curative potential. Cell 2015, 161:205-214.
56. Fuller M.J., et al. Immunotherapy of chronic hepatitis C virus infection with antibodies against programmed cell death-1 (PD-1). Proc. Natl. Acad. Sci. U.S.A. 2013, 110:15001-15006.
57. Liu J., et al. Enhancing virus-specific immunity in vivo by combining therapeutic vaccination and PD-L1 blockade in chronic hepadnaviral infection. PLoS Pathog. 2014, 10:e1003856.
58. Tzeng H.T., et al. PD-1 blockage reverses immune dysfunction and hepatitis B viral persistence in a mouse animal model. PLoS ONE 2012, 7:e39179.
59. Seung E., et al. PD-1 blockade in chronically HIV-1-infected humanized mice suppresses viral loads. PLoS ONE 2013, 8:e77780.
60. Velu V., et al. Enhancing SIV-specific immunity in vivo by PD-1 blockade. Nature 2009, 458:206-210.
61. + T cells and efficiently reduces chronic retroviral loads. PLoS Pathog. 2013, 9:e1003798.
62. Bengsch B., et al. Restoration of HBV-specific CD8+ T cell function by PD-1 blockade in inactive carrier patients is linked to T cell differentiation. J. Hepatol. 2014, 61:1212-1219.
63. Sherman A.C., et al. Augmentation of hepatitis B virus-specific cellular immunity with programmed death receptor-1/programmed death receptor-L1 blockade in hepatitis B virus and HIV/hepatitis B virus coinfected patients treated with adefovir. AIDS Res. Hum. Retroviruses 2013, 29:665-672.
64. Gardiner D., et al. A randomized, double-blind, placebo-controlled assessment of BMS-936558, a fully human monoclonal antibody to programmed death-1 (PD-1), in patients with chronic hepatitis C virus infection. PLoS ONE 2013, 8:e63818.
65. Aranda F., et al. Trial watch: immunostimulatory monoclonal antibodies in cancer therapy. Oncoimmunology 2014, 3:e27297.
66. Goulding J., et al. OX40:OX40L axis: emerging targets for improving poxvirus-based CD8(+) T-cell vaccines against respiratory viruses. Immunol. Rev. 2012, 244:149-168.
67. + T cell responses in aged mice. J. Immunol. 2014, 192:293-299.
68. Vezys V., et al. 4-1BB signaling synergizes with programmed death ligand 1 blockade to augment CD8 T cell responses during chronic viral infection. J. Immunol. 2011, 187:1634-1642.
69. Zhao Y., et al. Targeting 4-1BB (CD137) to enhance CD8 T cell responses with poxviruses and viral antigens. Front. Immunol. 2012, 3:332.
70. Moody M.A., et al. Toll-like receptor 7/8 (TLR7/8) and TLR9 agonists cooperate to enhance HIV-1 envelope antibody responses in rhesus macaques. J. Virol. 2014, 88:3329-3339.
71. Sommariva M., et al. High efficacy of CpG-ODN, cetuximab and cisplatin combination for very advanced ovarian xenograft tumors. J. Transl. Med. 2013, 11:25.
72. Halper-Stromberg A., et al. Broadly neutralizing antibodies and viral inducers decrease rebound from HIV-1 latent reservoirs in humanized mice. Cell 2014, 158:989-999.
73. Bournazos S., et al. humanized mice to study FcgammaR function. Curr. Top. Microbiol. Immunol. 2014, 382:237-248.
74. Bournazos S., et al. Broadly neutralizing anti-HIV-1 antibodies require Fc effector functions for in vivo activity. Cell 2014, 158:1243-1253.
75. DiLillo D.J., et al. Broadly neutralizing hemagglutinin stalk-specific antibodies require FcgammaR interactions for protection against influenza virus in vivo. Nat. Med. 2014, 20:143-151.
76. Dugast A.S., 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. Hessell A.J., et al. Fc receptor but not complement binding is important in antibody protection against HIV. Nature 2007, 449:101-104.
78. Lazar G.A., et al. Engineered antibody Fc variants with enhanced effector function. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:4005-4010.
79. Moldt B., et al. A nonfucosylated variant of the anti-HIV-1 monoclonal antibody b12 has enhanced FcgammaRIIIa-mediated antiviral activity in vitro but does not improve protection against mucosal SHIV challenge in macaques. J. Virol. 2012, 86:6189-6196.
80. Natsume A., et al. Fucose removal from complex-type oligosaccharide enhances the antibody-dependent cellular cytotoxicity of single-gene-encoded bispecific antibody comprising of two single-chain antibodies linked to the antibody constant region. J. Biochem. 2006, 140:359-368.
81. Niwa R., et al. IgG subclass-independent improvement of antibody-dependent cellular cytotoxicity by fucose removal from Asn297-linked oligosaccharides. J. Immunol. Methods 2005, 306:151-160.
82. Zeitlin L., et al. Enhanced potency of a fucose-free monoclonal antibody being developed as an Ebola virus immunoprotectant. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:20690-20694.
83. Chung A.W., et al. Identification of antibody glycosylation structures that predict monoclonal antibody Fc-effector function. AIDS 2014, 28:2523-2530.
84. Ackerman M.E., et al. Natural variation in Fc glycosylation of HIV-specific antibodies impacts antiviral activity. J. Clin. Invest. 2013, 123:2183-2192.
85. Giragossian C., et al. Neonatal Fc receptor and its role in the absorption, distribution, metabolism and excretion of immunoglobulin G-based biotherapeutics. Curr. Drug Metab. 2013, 14:764-790.
86. Baker K., et al. The role of FcRn in antigen presentation. Front. Immunol. 2014, 5:408.
87. Rath T., et al. Regulation of immune responses by the neonatal fc receptor and its therapeutic implications. Front. Immunol. 2015, 5:664.
88. Ko S.Y., et al. Enhanced neonatal Fc receptor function improves protection against primate SHIV infection. Nature 2014, 514:642-645.
89. French M.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, 27:519-528.
90. Chung A.W., et al. Polyfunctional Fc-effector profiles mediated by IgG subclass selection distinguish RV144 and VAX003 vaccines. Sci. Transl. Med. 2014, 6:228ra238.
91. Yates N.L., et al. Vaccine-induced Env V1-V2 IgG3 correlates with lower HIV-1 infection risk and declines soon after vaccination. Sci. Transl. Med. 2014, 6:228ra239.
92. Zolla-Pazner S., 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.
93. Diamantopoulos P.T., et al. Correlation of Fc-gamma RIIA polymorphisms with latent Epstein-Barr virus infection and latent membrane protein 1 expression in patients with low grade B-cell lymphomas. Leuk. Lymphoma 2013, 54:2030-2034.
94. Cocklin S.L., Schmitz J.E. The role of Fc receptors in HIV infection and vaccine efficacy. Curr. Opin. HIV AIDS 2014, 9:257-262.
95. Li S.S., et al. FCGR2C polymorphisms associate with HIV-1 vaccine protection in RV144 trial. J. Clin. Invest. 2014, 124:3879-3890.
96. Lepelley A., et al. Innate sensing of HIV-infected cells. PLoS Pathog. 2011, 7:e1001284.
97. Ebihara T., et al. Hepatitis C virus-infected hepatocytes extrinsically modulate dendritic cell maturation to activate T cells and natural killer cells. Hepatology 2008, 48:48-58.