Programmed death-1-induced interleukin-10 production by monocytes impairs CD4 + T cell activation during HIV infection

Nature Medicine

Volumn 16, Issue 4, 2010, Pages 452-459

  Said, Elias A ^a,b,c   Dupuy, Franck P ^a,b,c   Trautmann, Lydie ^a,b,c,d   Zhang, Yuwei ^a,b,c   Shi, Yu ^a,b,c   El Far, Mohamed ^a,b,c   Hill, Brenna J ^e   Noto, Alessandra ^a,b,c   Ancuta, Petronela ^a,b,c   Peretz, Yoav ^a,b,c   Fonseca, Simone G ^a,b,c   Van Grevenynghe, Julien ^a,b,c   Boulassel, Mohamed R ^f   Bruneau, Julie ^a,g   Shoukry, Naglaa H ^a,b   Routy, Jean Pierre ^c,f   Douek, Daniel C ^e   Haddad, Elias K ^a,b,c,h   Sekaly, Rafick Pierre ^a,b,c,d,h  

^a UNIVERSITY OF MONTREAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^d Vaccine and Gene Therapy Institute of Florida   (United States)

^e NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^f ROYAL VICTORIA HOSPITAL   (Canada)

^g Département de Médecine Familiale   (Canada)

^h MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; INTERLEUKIN 10; PROGRAMMED DEATH 1; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CELL EXPANSION; CELL FUNCTION; CELL TYPE; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MOLECULAR INTERACTION; MONOCYTE; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; UPREGULATION;

ANIMALIA;

EID: 77950525439     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.2106     Document Type: Article

References (50)

1. El-Far, M. et al. T-cell exhaustion in HIV infection. Curr. HIV/AIDS Rep. 5, 13-19 (2008). (Pubitemid 351480776)
2. Klenerman, P. & Hill, A. T cells and viral persistence: lessons from diverse infections. Nat. Immunol. 6, 873-879 (2005). (Pubitemid 43090441)
3. Brenchley, J.M. et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med. 12, 1365-1371 (2006).
4. Breen, E.C. et al. Infection with HIV is associated with elevated IL-6 levels and production. J. Immunol. 144, 480-484 (1990).
5. Chollet-Martin, S. et al. Comparison of plasma cytokine levels in African patients with HIV-1 and HIV-2 infection. AIDS 8, 879-884 (1994). (Pubitemid 24206596)
6. Ketlinskii, S.A. et al. Tumor necrosis factor-a and interleukin-1p in the blood plasma of patients with HIV infection. Vestn. Ross. Akad. Med. Nauk. 9-10, 36-41 (1992).
7. Norris, P.J. et al. Elevations in IL-10, TNF-a, and IFN-yfrom the earliest point of HIV Type 1 infection. AIDS Res. Hum. Retroviruses 22, 757-762 (2006).
8. Salazar-Gonzalez, J.F. et al. Relationship of plasma HIV-RNA levels and levels of TNF-a and immune activation products in HIV infection. Clin. Immunol. Immunopathol. 84, 36-45 (1997).
9. Than, S. et al. Cytokine pattern in relation to disease progression in human immunodefciency virus-infected children. J. Infect. Dis. 175, 47-56 (1997). (Pubitemid 27020823)
10. + T cells during chronic viral infection. Nature 439, 682-687 (2006).
11. Day, C.L. et al. PD-1 expression on HIV-specifc T cells is associated with T cell exhaustion and disease progression. Nature 443, 350-354 (2006).
12. + T cells leads to reversible immune dysfunction. Nat. Med. 12, 1198-1202 (2006). (Pubitemid 44527357)
13. + T cell survival in HIV infection. J. Exp. Med. 203, 2281-2292 (2006). (Pubitemid 44498363)
14. Velu, V. et al. Enhancing SIV-specifc immunity in vivo by PD-1.blockade. Nature 458, 206-210 (2009).
15. Brooks, D.G. et al. Interleukin-10 determines viral clearance or persistence in vivo. Nat. Med. 12, 1301-1309 (2006).
16. Ejrnaes, M. et al. Resolution of a chronic viral infection after interleukin-10 receptor blockade. J. Exp. Med. 203, 2461-2472 (2006). (Pubitemid 44664616)
17. Clerici, M. et al. Human immunodefciency virus (HIV) phenotype and interleukin-2/interleukin-10 ratio are associated markers of protection and progression in HIV infection. Blood 88, 574-579 (1996). (Pubitemid 26240389)
18. Stylianou, E., Aukrust, P., Kvale, D., Muller, F. & Froland, S.S. IL-10 in HIV infection: increasing serum IL-10 levels with disease progression-down-regulatory effect of potent anti-retroviral therapy. Clin. Exp. Immunol. 116, 115-120 (1999). (Pubitemid 29170013)
19. Orsilles, M.A., Pieri, E., Cooke, P. & Caula, C. IL-2 and IL-10 serum levels in HIV-1-infected patients with or without active antiretroviral therapy. APMIS 114, 55-60 (2006). (Pubitemid 43356835)
20. Clerici, M. et al. Role of interleukin-10 in T helper cell dysfunction in asymptomatic individuals infected with the human immunodefciency virus. J. Clin. Invest. 93, 768-775 (1994). (Pubitemid 24072820)
21. Hagiwara, E., Sacks, T., Leitman-Klinman, S.F. & Klinman, D.M. Effect of HIV infection on the frequency of cytokine-secreting cells in human peripheral blood. AIDS Res. Hum. Retroviruses 12, 127-133 (1996). (Pubitemid 26039711)
22. Kumar, A. et al. Differential production of IL-10 by T cells and monocytes of HIV-infected individuals: association of IL-10 production with CD28-mediated immune responsiveness. Clin. Exp. Immunol. 114, 78-86 (1998). (Pubitemid 28442817)
23. Gröschel, S. et al. TLR-mediated induction of negative regulatory ligands on dendritic cells. J. Mol. Med. 86, 443-455 (2008).
24. Meier, A. et al. Upregulation of PD-L1 on monocytes and dendritic cells by HIV-1 derived TLR ligands. AIDS 22, 655-658 (2008). (Pubitemid 351640601)
25. Keir, M.E., Butte, M.J., Freeman, G.J. & Sharpe, A.H. PD-1 and its ligands in tolerance and immunity. Annu. Rev. Immunol. 26, 677-704 (2008). (Pubitemid 351600389)
26. Lin, D.Y. et al. The PD-1/PD-L1 complex resembles the antigen-binding Fv domains of antibodies and T cell receptors. Proc. Natl. Acad. Sci. USA 105, 3011-3016 (2008).
27. Gordon, S. et al. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5, 953-964 (2005). (Pubitemid 41746764)
28. Heil, F. et al. Species-specifc recognition of single-stranded RNA via Toll-like receptor 7 and 8. Science 303, 1526-1529 (2004). (Pubitemid 38314424)
29. Frankenberger, M., Sternsdorf, T., Pechumer, H., Pforte, A. & Ziegler-Heitbrock, H.W. Differential cytokine expression in human blood monocyte subpopulations: a polymerase chain reaction analysis. Blood 87, 373-377 (1996). (Pubitemid 26011852)
30. de Waal Malefyt, R. et al. Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specifc human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression. J. Exp. Med. 174, 915-924 (1991).
31. Younes, S.A. et al. HIV-1 viremia prevents the establishment of interleukin 2-producing HIV-specifc memory CD4 T cells endowed with proliferative capacity. J. Exp. Med. 198, 1909-1922 (2003).
32. Niemand, C. et al. Activation of STAT3 by IL-6 and IL-10 in primary human macrophages is differentially modulated by suppressor of cytokine signaling 3. J. Immunol. 170, 3263-3272 (2003). (Pubitemid 36302204)
33. Trabattoni, D. et al. B7-H1 is up-regulated in HIV infection and is a novel surrogate marker of disease progression. Blood 101, 2514-2520 (2003). (Pubitemid 36857606)
34. Zhong, Z. et al. Stat3: a STAT family member activated by tyrosine phosphorylation in response to epidermal growth factor and interleukin-6. Science 264, 95-98 (1994). (Pubitemid 24144493)
35. Bright, J.J. et al. TGF-β inhibits IL-12-induced activation of Jak-STAT pathway in T lymphocytes. J. Immunol. 161, 1772-1777 (1998).
36. H17 phenotype. Proc. Natl. Acad. Sci. USA 105, 20846-20851 (2008).
37. El Kasmi, K.C. et al. General nature of the STAT3-activated anti-infammatory response. J. Immunol. 177, 7880-7888 (2006).
38. Williams, L. et al. Signal transducer and activator of transcription 3 is the dominant mediator of the anti-infammatory effects of IL-10 in human macrophages. J. Immunol. 172, 567-576 (2004). (Pubitemid 38020514)
39. Berlato, C. et al. Involvement of suppressor of cytokine signaling-3 as a mediator of the inhibitory effects of IL-10 on lipopolysaccharide-induced macrophage activation. J. Immunol. 168, 6404-6411 (2002). (Pubitemid 34620065)
40. Urbani, S. et al. PD-1 expression in acute hepatitis C virus (HCV) infection is associated with HCV-specifc CD8 exhaustion. J. Virol. 80, 11398-11403 (2006). (Pubitemid 44706581)
41. + monocytes of patients with chronic hepatitis B virus infection, which correlates with higher serum IL-10 levels. J. Viral Hepat. 13, 725-733 (2006). (Pubitemid 44583497)
42. Shrestha, S. et al. Interleukin-10 gene (IL-10) polymorphisms and human papillomavirus clearance among immunosuppressed adolescents. Cancer Epidemiol. Biomarkers Prev. 16, 1626-1632 (2007). (Pubitemid 47294829)
43. Swaminathan, S. Molecular biology of Epstein-Barr virus and Kaposi's sarcoma-associated herpesvirus. Semin. Hematol. 40, 107-115 (2003). (Pubitemid 36461088)
44. + T cell population in chronic hepatitis C virus infection. J. Clin. Invest. 113, 963-972 (2004). (Pubitemid 38544117)
45. Yao, S. et al. PD-1 on dendritic cells impedes innate immunity against bacterial infection. Blood 113, 5811-5818 (2009).
46. Boasso, A. et al. PDL-1 upregulation on monocytes and T cells by HIV via type I interferon: restricted expression of type I interferon receptor by CCR5-expressing leukocytes. Clin. Immunol. 129, 132-144 (2008).
47. + T cells is a typical feature of natural SIV hosts. Blood 109, 1069-1076 (2007). (Pubitemid 46220653)
48. Huang, X. et al. PD-1 expression by macrophages plays a pathologic role in altering microbial clearance and the innate infammatory response to sepsis. Proc. Natl. Acad. Sci. USA 106, 6303-6308 (2009).
49. Nelson, D.R. et al. Long-term interleukin 10 therapy in chronic hepatitis C patients has a proviral and anti-infammatory effect. Hepatology 38, 859-868 (2003).
50. Xiao, Y. et al. Cell-surface processing of extracellular human immunodefciency virus type 1 Vpr by proprotein convertases. Virology 372, 384-397 (2008). (Pubitemid 351273749)