Neutralizing antibodies inhibit HIV-1 infection of plasmacytoid dendritic cells by an FcγRIIa independent mechanism and do not diminish cytokines production

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Lederle, Alexandre ^a   Su, Bin ^a   Holl, Vincent ^a   Penichon, Julien ^a   Schmidt, Sylvie ^a   Decoville, Thomas ^a   Laumond, Géraldine ^a   Moog, Christiane ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; FC RECEPTOR; FC RECEPTOR IIA; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; IL6 PROTEIN, HUMAN; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; NEUTRALIZING ANTIBODY; TUMOR NECROSIS FACTOR ALPHA;

BIOSYNTHESIS; CELL CULTURE; DENDRITIC CELL; HIV INFECTIONS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; INNATE IMMUNITY; SERODIAGNOSIS; VIROLOGY; VIRUS REPLICATION;

ANTIBODIES, NEUTRALIZING; CELLS, CULTURED; CHEMOKINE CCL3; CHEMOKINE CCL4; DENDRITIC CELLS; HIV ANTIBODIES; HIV INFECTIONS; HIV-1; HUMANS; IMMUNITY, INNATE; INTERFERON-ALPHA; INTERLEUKIN-6; NEUTRALIZATION TESTS; RECEPTORS, IGG; TUMOR NECROSIS FACTOR-ALPHA; VIRUS REPLICATION;

EID: 84906273410     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep05845     Document Type: Article

References (52)

1. Schiffner, T., Sattentau, Q. J. & Dorrell, L. Development of prophylactic vaccines against HIV-1. Retrovirology 10, 72 (2013).
2. Kwong, P. D., Mascola, J. R. & Nabel, G. J. Broadly neutralizing antibodies and the search for an HIV-1 vaccine: the end of the beginning. Nat Rev Immunol 13, 693-701 (2013).
3. Mascola, J. R. & Montefiori, D. C. The role of antibodies in HIV vaccines. Annu Rev Immunol 28, 413-444 (2010).
4. Binley, J. M. et al. Comprehensive cross-clade neutralization analysis of a panel of anti-human immunodeficiency virus type 1 monoclonal antibodies. J Virol 78, 13232-13252 (2004). (Pubitemid 39507829)
5. Polonis, V. R. et al. Recent advances in the characterization of HIV-1 neutralization assays for standardized evaluation of the antibody response to infection and vaccination. Virology 375, 315-320 (2008).
6. Scheid, J. F. et al. Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature 458, 636-640 (2009).
7. Walker, L. M. et al. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326, 285-289 (2009).
8. Wu, X. et al. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329, 856-861 (2010).
9. Scheid, J. F. et al. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 333, 1633-1637 (2011).
10. Walker, L. M. et al. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477, 466-470 (2011).
11. Mascola, J. R. & Haynes, B. F. HIV-1 neutralizing antibodies: understanding nature's pathways. Immunol Rev 254, 225-244 (2013).
12. Hessell, A. J. et al. Fc receptor but not complement binding is important in antibody protection against HIV. Nature 449, 101-104 (2007). (Pubitemid 47373775)
13. Hessell, A. J. et al. Effective, low-titer antibody protection against low-dose repeated mucosal SHIV challenge in macaques. Nat Med 15, 951-954 (2009).
14. Moldt, B. et al. A nonfucosylated variant of the anti-HIV-1 monoclonal antibody b12 has enhanced Fcgamma RIIIa-mediated antiviral activity in vitro but does not improve protection against mucosal SHIV challenge in macaques. J Virol 86, 6189-6196 (2012).
15. Moog, C. et al. Protective effect of vaginal application of neutralizing and nonneutralizing inhibitory antibodies against vaginal SHIV challenge in macaques. Mucosal Immunol 7, 46-56 (2014).
16. Forthal, D., Hope, T. J. & Alter, G. New paradigms for functional HIV-specific nonneutralizing antibodies. Curr Opin HIV AIDS 8, 393-401 (2013).
17. Holl, V. et al. Efficient inhibition of HIV-1 replication in human immature monocyte-derived dendritic cells by purified anti-HIV-1 IgG without induction of maturation. Blood 107, 4466-4474 (2006). (Pubitemid 43801374)
18. Holl, V. et al. Nonneutralizing antibodies are able to inhibit human immunodeficiency virus type 1 replication in macrophages and immature dendritic cells. J Virol 80, 6177-6181 (2006). (Pubitemid 43849196)
19. Holl, V. 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 173, 6274-6283 (2004). (Pubitemid 39487786)
20. Peressin, M. et al. HIV-1 replication in Langerhans and interstitial dendritic cells is inhibited by neutralizing and Fc-mediated inhibitory antibodies. J Virol 85, 1077-1085 (2011).
21. Su, B. et al. Neutralizing antibodies inhibit HIV-1 transfer from primary dendritic cells to autologous CD4 T lymphocytes. Blood 120, 3708-3717 (2012).
22. Bloch, N. et al. HIV type 1 infection of plasmacytoid and myeloid dendritic cells is restricted by high levels of SAMHD1 and cannot be counteracted by Vpx. AIDS Res Hum Retroviruses 30, 195-203 (2014).
23. Patterson, S., Rae, A., Hockey, N., Gilmour, J. & Gotch, F. Plasmacytoid dendritic cells are highly susceptible to human immunodeficiency virus type 1 infection and release infectious virus. J Virol 75, 6710-6713 (2001). (Pubitemid 32578192)
24. Smed-Sorensen, A. et al. Differential susceptibility to human immunodeficiency virus type 1 infection of myeloid and plasmacytoid dendritic cells. J Virol 79, 8861-8869 (2005). (Pubitemid 40934796)
25. Bave, U. et al. Fc gamma RIIa is expressed on natural IFN-alpha-producing cells (plasmacytoid dendritic cells) and is required for the IFN-alpha production induced by apoptotic cells combined with lupus IgG. J Immunol 171, 3296-3302 (2003). (Pubitemid 37093557)
26. Beignon, A. S. et al. Endocytosis of HIV-1 activates plasmacytoid dendritic cells via Toll-like receptor-viral RNA interactions. J Clin Invest 115, 3265-3275 (2005).
27. Liu, Y. J. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu Rev Immunol 23, 275-306 (2005).
28. Gilliet, M., Cao, W. & Liu, Y. J. Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat Rev Immunol 8, 594-606 (2008).
29. Miller, E. & Bhardwaj, N. Dendritic cell dysregulation during HIV-1 infection. Immunol Rev 254, 170-189 (2013).
30. O'Brien, M., Manches, O. & Bhardwaj, N. Plasmacytoid dendritic cells in HIV infection. Adv Exp Med Biol 762, 71-107 (2013).
31. Moog, C., Fleury, H. J., Pellegrin, I., Kirn, A. & Aubertin, A. M. Autologous and heterologous neutralizing antibody responses following initial seroconversion in human immunodeficiency virus type 1-infected individuals. J Virol 71, 3734-3741 (1997). (Pubitemid 27172386)
32. Perez, L.G., Costa, M. R., Todd, C. A., Haynes, B. F. & Montefiori, D. C. Utilization of immunoglobulin G Fc receptors by human immunodeficiency virus type 1: a specific role for antibodies against the membrane-proximal external region of gp41. J Virol 83, 7397-7410 (2009).
33. Moody, M. A. et al. Anti-phospholipid human monoclonal antibodies inhibit CCR5-tropic HIV-1 and induce beta-chemokines. J Exp Med 207, 763-776 (2010).
34. Haynes, B. F. et al. Cardiolipin polyspecific autoreactivity in two broadly neutralizing HIV-1 antibodies. Science 308, 1906-1908 (2005). (Pubitemid 40941873)
35. Malbec, M. et al. Broadly neutralizing antibodies that inhibit HIV-1 cell to cell transmission. J Exp Med 210, 2813-2821 (2013).
36. Schmidt, B., Ashlock, B.M., Foster, H., Fujimura, S. H. & Levy, J. A. HIV-infected cells are major inducers of plasmacytoid dendritic cell interferon production, maturation, and migration. Virology 343, 256-266 (2005). (Pubitemid 41598365)
37. Barblu, L. et al. Plasmacytoid dendritic cells (pDCs) from HIV controllers produce interferon-alpha and differentiate into functional killer pDCs under HIV activation. J Infect Dis 206, 790-801 (2012).
38. Zhou, T. et al. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329, 811-817 (2010).
39. Lynch, R.M. et al. The development of CD4 binding site antibodies during HIV-1 infection. J Virol 86, 7588-7595 (2012).
40. Li, Y. et al. Mechanism of neutralization by the broadly neutralizing HIV-1 monoclonal antibody VRC01. J Virol 85, 8954-8967 (2011).
41. Zhou, D., Kang, K. H. & Spector, S. A. Production of interferon alpha by human immunodeficiency virus type 1 in human plasmacytoid dendritic cells is dependent on induction of autophagy. J Infect Dis 205, 1258-1267 (2012).
42. Green, D. S., Lum, T. & Green, J. A. IgG-derived Fc down-regulates virus-induced plasmacytoid dendritic cell (pDC) IFNalpha production. Cytokine 26, 209-216 (2004). (Pubitemid 38639749)
43. Wiedeman, A. E. et al. Contrasting mechanisms of interferon-alpha inhibition by intravenous immunoglobulin after induction by immune complexes versus Tolllike receptor agonists. Arthritis Rheum 65, 2713-2723 (2013).
44. Takahashi, K. et al. Plasmacytoid dendritic cells sense hepatitis C virus-infected cells, produce interferon, and inhibit infection. Proc Natl Acad Sci U S A 107, 7431-7436 (2010).
45. Schijf, M. A. et al. Respiratory Syncytial Virus Induced Type I IFN Production by pDC Is Regulated by RSV-Infected Airway Epithelial Cells, RSV-Exposed Monocytes and Virus Specific Antibodies. PLoS One 8, e81695 (2013).
46. Palmer, P., Charley, B., Rombaut, B., Daeron, M. & Lebon, P. Antibody-dependent induction of type I interferons by poliovirus in human mononuclear blood cells requires the type II fcgamma receptor (CD32). Virology 278, 86-94 (2000). (Pubitemid 32002597)
47. Bruel, T. et al. Plasmacytoid dendritic cell dynamics tune interferon-alfa production in SIV-infected cynomolgus macaques. PLoS Pathog 10, e1003915 (2014).
48. Kader, M. et al. Blocking TLR7-and TLR9-mediated IFN-alpha production by plasmacytoid dendritic cells does not diminish immune activation in early SIV infection. PLoS Pathog 9, e1003530 (2013).
49. Harris, L. D. et al. Downregulation of robust acute type I interferon responses distinguishes nonpathogenic simian immunodeficiency virus (SIV) infection of natural hosts from pathogenic SIV infection of rhesus macaques. J Virol 84, 7886-7891 (2010).
50. Lehmann, C. et al. Plasmacytoid dendritic cells accumulate and secrete interferon alpha in lymph nodes of HIV-1 patients. PLoS One 5, e11110 (2010).
51. Benitez-Ribas, D. et al. Plasmacytoid dendritic cells of melanoma patients present exogenous proteins to CD41+T cells after Fc gamma RII-mediated uptake. J Exp Med 203, 1629-1635 (2006). (Pubitemid 44036266)
52. Burrer, R. et al. Immunoglobulin G (IgG) and IgA, but also nonantibody factors, account for in vitro neutralization of human immunodeficiency virus (HIV) type 1 primary isolates by serum and plasma of HIV-infected patients. J Virol 75, 5421-5424 (2001). (Pubitemid 32448569)