A crucial role for infected-cell/antibody immune complexes in the enhancement of endogenous antiviral immunity by short passive immunotherapy

PLoS Pathogens

Volumn 6, Issue 6, 2010, Pages

  Michau, Henri Alexandre ^b   Gomard, Tiphanie ^a,b   Gros, Laurent ^a,b   Thiolon, Kevin ^a,b   Nasser, Roudaina ^a,b   Jacquet, Chantal ^a,b   Hernandez, Javier ^a,b   Piechaczyk, Marc ^a,b   Pelegrin, Mireia ^a,b  

^a INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

^b UNIV MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; IMMUNOGLOBULIN G; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 667; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; VIRUS ANTIBODY;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIGEN ANTIBODY COMPLEX; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; ERYTHROLEUKEMIA; FRIEND LEUKEMIA VIRUS; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOTHERAPY; MOUSE; NEWBORN; NONHUMAN; PASSIVE IMMUNIZATION; RETROVIRUS; VIRUS NEUTRALIZATION; ANIMAL; CELL PROLIFERATION; CYTOTOXIC T LYMPHOCYTE; FLOW CYTOMETRY; IMMUNOLOGY; RETROVIRUS INFECTION;

MURINAE; MUS;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, VIRAL; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTIGEN-ANTIBODY COMPLEX; CELL PROLIFERATION; FLOW CYTOMETRY; IMMUNIZATION, PASSIVE; MICE; RETROVIRIDAE; RETROVIRIDAE INFECTIONS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84892993137     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000948     Document Type: Article

References (66)

1. Reichert JM (2007) Trends in the development and approval of monoclonal antibodies for viral infections. BioDrugs 21: 1-7.
2. Marasco WA, Sui J (2007) The growth and potential of human antiviral monoclonal antibody therapeutics. Nat Biotechnol 25: 1421-1434.
3. Takada A, Ebihara H, Jones S, Feldmann H, Kawaoka Y (2007) Protective efficacy of neutralizing antibodies against Ebola virus infection. Vaccine 25: 993-999.
4. Oliphant T, Nybakken GE, Engle M, Xu Q, Nelson CA, et al. (2006) Antibody recognition and neutralization determinants on domains I and II of West Nile Virus envelope protein. J Virol 80: 12149-12159.
5. Hangartner L, Zinkernagel RM, Hengartner H (2006) Antiviral antibody responses: the two extremes of a wide spectrum. Nat Rev Immunol 6: 231- 243.
6. Sui J, Hwang WC, Perez S, Wei G, Aird D, et al. (2009) Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat Struct Mol Biol 16: 265-273.
7. Simmons CP, Bernasconi NL, Suguitan AL, Mills K, Ward JM, et al. (2007) Prophylactic and therapeutic efficacy of human monoclonal antibodies against H5N1 influenza. PLoS Med 4: e178.
8. Zhu Z, Chakraborti S, He Y, Roberts A, Sheahan T, et al. (2007) Potent cross-reactive neutralization of SARS coronavirus isolates by human monoclonal antibodies. Proc Natl Acad Sci U S A 104: 12123-12128.
9. Wu H, Pfarr DS, Johnson S, Brewah YA, Woods RM, et al. (2007) Development of motavizumab, an ultra-potent antibody for the prevention of respiratory syncytial virus infection in the upper and lower respiratory tract. J Mol Biol 368: 652-665.
10. Hong HJ, Ryu CJ, Hur H, Kim S, Oh HK, et al. (2004) In vivo neutralization of hepatitis B virus infection by an anti-preS1 humanized antibody in chimpanzees. Virology 318: 134-141.
11. Galun E, Terrault NA, Eren R, Zauberman A, Nussbaum O, et al. (2007) Clinical evaluation (Phase I) of a human monoclonal antibody against hepatitis C virus: safety and antiviral activity. J Hepatol 46: 37-44.
12. Trkola A, Kuster H, Rusert P, von Wyl V, Leemann C, et al. (2008) In vivo efficacy of human immunodeficiency virus neutralizing antibodies: estimates for protective titers. J Virol 82: 1591-1599.
13. Akiyama K, Ebihara S, Yada A, Matsumura K, Aiba S, et al. (2003) Targeting apoptotic tumor cells to Fc gamma R provides efficient and versatile vaccination against tumors by dendritic cells. J Immunol 170: 1641-1648.
14. Schuurhuis DH, van Montfoort N, Ioan-Facsinay A, Jiawan R, Camps M, et al. (2006) Immune complex-loaded dendritic cells are superior to soluble immune complexes as antitumor vaccine. J Immunol 176: 4573-4580.
15. Portis JL, Czub S, Garon CF, McAtee FJ (1990) 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 64: 1648-1656.
16. Pincus SH, Cole R, Ireland R, McAtee F, Fujisawa R, et al. (1995) Protective efficacy of nonneutralizing monoclonal antibodies in acute infection with murine leukemia virus. J Virol 69: 7152-7158.
17. Pelegrin M, Marin M, Oates A, Noel D, Saller R, et al. (2000) Immunotherapy of a viral disease by in vivo production of therapeutic monoclonal antibodies. Hum Gene Ther 11: 1407-1415.
18. Gros L, Dreja H, Fiser AL, Plays M, Pelegrin M, et al. (2005) Induction of long-term protective antiviral endogenous immune response by short neutralizing monoclonal antibody treatment. J Virol 79: 6272-6280.
19. Lynch WP, Czub S, McAtee FJ, Hayes SF, Portis JL (1991) Murine retrovirus-induced spongiform encephalopathy: productive infection of microglia and cerebellar neurons in accelerated CNS disease. Neuron 7: 365-379.
20. Dreja H, Gros L, Villard S, Bachrach E, Oates A, et al. (2003) Monoclonal antibody 667 recognizes the variable region A motif of the ecotropic retrovirus CasBrE envelope glycoprotein and inhibits Env binding to the viral receptor. J Virol 77: 10984-10993.
21. McAtee FJ, Portis JL (1985) Monoclonal antibodies specific for wild mouse neurotropic retrovirus: detection of comparable levels of virus replication in mouse strains susceptible and resistant to paralytic disease. J Virol 56: 1018-1022.
22. Gros L, Pelegrin M, Michaud HA, Bianco S, Hernandez J, et al. (2008) 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 82: 1339-1349.
23. Gros L, Pelegrin M, Plays M, Piechaczyk M (2006) Efficient mother-to-child transfer of antiretroviral immunity in the context of preclinical monoclonal antibody-based immunotherapy. J Virol 80: 10191-10200.
24. Groh V, Li YQ, Cioca D, Hunder NN, Wang W, et al. (2005) Efficient cross-priming of tumor antigen-specific T cells by dendritic cells sensitized with diverse anti-MICA opsonized tumor cells. Proc Natl Acad Sci U S A 102: 6461-6466.
25. Corbin A, Prats AC, Darlix JL, Sitbon M (1994) A nonstructural gag-encoded glycoprotein precursor is necessary for efficient spreading and pathogenesis of murine leukemia viruses. J Virol 68: 3857-3867.
26. Sitbon M, Sola B, Evans L, Nishio J, Hayes SF, et al. (1986) Hemolytic anemia and erythroleukemia, two distinct pathogenic effects of Friend MuLV: mapping of the effects to different regions of the viral genome. Cell 47: 851-859.
27. Bergthaler A, Flatz L, Verschoor A, Hegazy AN, Holdener M, et al. (2009) Impaired Antibody Response Causes Persistence of Prototypic T Cell-Contained Virus. PLoS Biol 7: e80.
28. Lavillette D, Morice Y, Germanidis G, Donot P, Soulier A, et al. (2005) Human serum facilitates hepatitis C virus infection, and neutralizing responses inversely correlate with viral replication kinetics at the acute phase of hepatitis C virus infection. J Virol 79: 6023-6034.
29. Pestka JM, Zeisel MB, Blaser E, Schurmann P, Bartosch B, et al. (2007) Rapid induction of virus-neutralizing antibodies and viral clearance in a single-source outbreak of hepatitis C. Proc Natl Acad Sci U S A 104: 6025-6030.
30. Pinschewer DD, Perez M, Jeetendra E, Bachi T, Horvath E, et al. (2004) Kinetics of protective antibodies are determined by the viral surface antigen. J Clin Invest 114: 988-993.
31. Weiss R, Teich N, Varmus H, Coffin J (1985) RNA Tumor Viruses. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
32. Stromnes IM, Dittmer U, Schumacher TN, Schepers K, Messer RJ, et al. (2002) Temporal effects of gamma interferon deficiency on the course of Friend retrovirus infection in mice. J Virol 76: 2225-2232.
33. Chen W, Qin H, Chesebro B, Cheever MA (1996) Identification of a gag-encoded cytotoxic T-lymphocyte epitope from FBL-3 leukemia shared by Friend, Moloney, and Rauscher murine leukemia virus-induced tumors. J Virol 70: 7773-7782.
34. Ohlen C, Kalos M, Cheng LE, Shur AC, Hong DJ, et al. (2002) CD8(+) T cell tolerance to a tumor-associated antigen is maintained at the level of expansion rather than effector function. J Exp Med 195: 1407-1418.
35. Kurlander RJ, Ellison DM, Hall J (1984) The blockade of Fc receptor-mediated clearance of immune complexes in vivo by a monoclonal antibody (2.4G2) directed against Fc receptors on murine leukocytes. J Immunol 133: 855-862.
36. Schuurhuis DH, Ioan-Facsinay A, Nagelkerken B, van Schip JJ, Sedlik C, et al. (2002) Antigen-antibody immune complexes empower dendritic cells to efficiently prime specific CD8+ CTL responses in vivo. J Immunol 168: 2240-2246.
37. Balkow S, Krux F, Loser K, Becker JU, Grabbe S, et al. (2007) Friend retrovirus infection of myeloid dendritic cells impairs maturation, prolongs contact to naive T cells, and favors expansion of regulatory T cells. Blood 110: 3949-3958.
38. Brady LJ (2005) Antibody-mediated immunomodulation: a strategy to improve host responses against microbial antigens. Infect Immun 73: 671-678.
39. Carter RH, Fearon DT (1992) CD19: lowering the threshold for antigen receptor stimulation of B lymphocytes. Science 256: 105-107.
40. Heyman B (2000) Regulation of antibody responses via antibodies, complement, and Fc receptors. Annu Rev Immunol 18: 709-737.
41. Song H, Nie X, Basu S, Cerny J (1998) Antibody feedback and somatic mutation in B cells: regulation of mutation by immune complexes with IgG antibody. Immunol Rev 162: 211-218.
42. Wu Y, Sukumar S, El Shikh ME, Best AM, Szakal AK, et al. (2008) Immune complex-bearing follicular dendritic cells deliver a late antigenic signal that promotes somatic hypermutation. J Immunol 180: 281-290.
43. Hamano Y, Arase H, Saisho H, Saito T (2000) Immune complex and Fc receptor-mediated augmentation of antigen presentation for in vivo Th cell responses. J Immunol 164: 6113-6119.
44. Dhodapkar KM, Krasovsky J, Williamson B, Dhodapkar MV (2002) Antitumor monoclonal antibodies enhance cross-presentation ofcCellular antigens and the generation of myeloma-specific killer T cells by dendritic cells. J Exp Med 195: 125-133.
45. Rafiq K, Bergtold A, Clynes R (2002) Immune complex-mediated antigen presentation induces tumor immunity. J Clin Invest 110: 71-79.
46. Yao X, Zheng B, Zhou J, Xu DZ, Zhao K, et al. (2007) Therapeutic effect of hepatitis B surface antigen-antibody complex is associated with cytolytic and non-cytolytic immune responses in hepatitis B patients. Vaccine 25: 1771-1779.
47. Villinger F, Mayne AE, Bostik P, Mori K, Jensen PE, et al. (2003) Evidence for antibody-mediated enhancement of simian immunodeficiency virus (SIV) Gag antigen processing and cross presentation in SIV-infected rhesus macaques. J Virol 77: 10-24.
48. Haigwood NL, Montefiori DC, Sutton WF, McClure J, Watson AJ, et al. (2004) Passive immunotherapy in simian immunodeficiency virus-infected macaques accelerates the development of neutralizing antibodies. J Virol 78: 5983-5995.
49. Regnault A, Lankar D, Lacabanne V, Rodriguez A, Thery C, et al. (1999) Fcgamma receptor-mediated induction of dendritic cell maturation and major histocompatibility complex class I-restricted antigen presentation after immune complex internalization. J Exp Med 189: 371-380.
50. Franki SN, Steward KK, Betting DJ, Kafi K, Yamada RE, et al. (2008) Dendritic cells loaded with apoptotic antibody-coated tumor cells provide protective immunity against B-cell lymphoma in vivo. Blood 111: 1504-1511.
51. Selenko N, Majdic O, Jager U, Sillaber C, Stockl J, et al. (2002) Cross-priming of cytotoxic T cells promoted by apoptosis-inducing tumor cell reactive antibodies? J Clin Immunol 22: 124-130.
52. Vasovic LV, Dyall R, Clynes RA, Ravetch JV, Nikolic-Zugic J (1997) Synergy between an antibody and CD8+ cells in eliminating an established tumor. Eur J Immunol 27: 374-382.
53. Bachmann MF, Hunziker L, Zinkernagel RM, Storni T, Kopf M (2004) Maintenance of memory CTL responses by T helper cells and CD40-CD40 ligand: antibodies provide the key. Eur J Immunol 34: 317-326.
54. Gallimore A, Glithero A, Godkin A, Tissot AC, Pluckthun A, et al. (1998) Induction and exhaustion of lymphocytic choriomeningitis virus-specific cytotoxic T lymphocytes visualized using soluble tetrameric major histocom-patibility complex class I-peptide complexes. J Exp Med 187: 1383-1393.
55. Valmori D, Levy F, Godefroy E, Scotto L, Souleimanian NE, et al. (2007) Epitope clustering in regions undergoing efficient proteasomal processing defines immunodominant CTL regions of a tumor antigen. Clin Immunol 122: 163-172.
56. Hammer SM, Eron JJ, Jr., Reiss P, Schooley RT, Thompson MA (2008) Antiretroviral treatment of adult HIV infection: 2008 recommendations of the International AIDS Society-USA panel. Jama 300: 555-570.
57. Deutsch M, Hadziyannis SJ (2008) Old and emerging therapies in chronic hepatitis C: an update. J Viral Hepat 15: 2-11.
58. Aiuti F, Mezzaroma I (2006) Failure to reconstitute CD4+ T-cells despite suppression of HIV replication under HAART. AIDS Rev 8: 88-97.
59. Elrefaei M, McElroy MD, Preas CP, Hoh R, Deeks S, et al. (2004) Central memory CD4+ T cell responses in chronic HIV infection are not restored by antiretroviral therapy. J Immunol 173: 2184-2189.
60. Pitcher CJ, Quittner C, Peterson DM, Connors M, Koup RA, et al. (1999) HIV-1-specific CD4+ T cells are detectable in most individuals with active HIV-1 infection, but decline with prolonged viral suppression. Nat Med 5: 518-525.
61. Zinkernagel RM (2003) On natural and artificial vaccinations. Annu Rev Immunol 21: 515-546.
62. Sitbon M, Nishio J, Wehrly K, Lodmell D, Chesebro B (1985) Use of a focal immunofluorescence assay on live cells for quantitation of retroviruses: distinction of host range classes in virus mixtures and biological cloning of dual-tropic murine leukemia viruses. Virology 141: 110-118.
63. Schepers K, Toebes M, Sotthewes G, Vyth-Dreese FA, Dellemijn TA, et al. (2002) Differential kinetics of antigen-specific CD4+ and CD8+ T cell responses in the regression of retrovirus-induced sarcomas. J Immunol 169: 3191-3199.
64. Lutz MB, Kukutsch N, Ogilvie AL, Rossner S, Koch F, et al. (1999) An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 223: 77-92.
65. Guyre CA, Gomes D, Smith KA, Kaplan JM, Perricone MA (2008) Development of an in vivo antibody-mediated killing (IVAK) model, a flow cytometric method to rapidly evaluate therapeutic antibodies. J Immunol Methods 333: 51-60.
66. Lee GM, Fong S, Francis K, Oh DJ, Palsson BO (2000) In situ labeling of adherent cells with PKH26. In Vitro Cell Dev Biol Anim 36: 4-6.