Macrophage and T Cell Produced IL-10 Promotes Viral Chronicity

PLoS Pathogens

Volumn 9, Issue 11, 2013, Pages

  Richter, Kirsten ^a   Perriard, Guillaume ^a,g   Behrendt, Rayk ^b   Schwendener, Reto A ^c   Sexl, Veronika ^d   Dunn, Robert ^e,h   Kamanaka, Masahito ^f,i   Flavell, Richard A ^f   Roers, Axel ^c   Oxenius, Annette ^a  

^a ETH ZURICH   (Switzerland)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^e BIOGEN   (United States)

^f HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^g LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^h PFIZER INC   (United States)

ⁱ Arai Hospital   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD4+ T LYMPHOCYTE; CELL ISOLATION; CELLULAR IMMUNITY; CHRONICITY; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; LYMPHOCYTE ACTIVATION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MACROPHAGE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SOUTHERN BLOTTING; T CELL DEPLETION; VIRUS INFECTION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CHRONIC DISEASE; INTERLEUKIN-10; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MACROPHAGES; MICE; MICE, KNOCKOUT; RECEPTORS, INTERLEUKIN-10;

EID: 84888220445     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003735     Document Type: Article

References (67)

1. Frebel H, Richter K, Oxenius A, (2010) How chronic viral infections impact on antigen-specific T-cell responses. Eur J Immunol 40: 654-663.
2. Brooks DG, Trifilo MJ, Edelmann KH, Teyton L, McGavern DB, et al. (2006) Interleukin-10 determines viral clearance or persistence in vivo. Nat Med 12: 1301-1309.
3. Ejrnaes M, Filippi CM, Martinic MM, Ling EM, Togher LM, et al. (2006) Resolution of a chronic viral infection after interleukin-10 receptor blockade. J Exp Med 203: 2461-2472.
4. Brockman MA, Kwon DS, Tighe DP, Pavlik DF, Rosato PC, et al. (2009) IL-10 is up-regulated in multiple cell types during viremic HIV infection and reversibly inhibits virus-specific T cells. Blood 114: 346-356.
5. Flynn JK, Dore GJ, Hellard M, Yeung B, Rawlinson WD, et al. (2011) Early IL-10 predominant responses are associated with progression to chronic hepatitis C virus infection in injecting drug users. J Viral Hepat 18: 549-561.
6. Das A, Ellis G, Pallant C, Lopes AR, Khanna P, et al. (2012) IL-10-producing regulatory B cells in the pathogenesis of chronic hepatitis B virus infection. J Immunol 189: 3925-3935.
7. Clerici M, Wynn TA, Berzofsky JA, Blatt SP, Hendrix CW, et al. (1994) Role of interleukin-10 in T helper cell dysfunction in asymptomatic individuals infected with the human immunodeficiency virus. J Clin Invest 93: 768-775.
8. Landay AL, Clerici M, Hashemi F, Kessler H, Berzofsky JA, et al. (1996) In vitro restoration of T cell immune function in human immunodeficiency virus-positive persons: effects of interleukin (IL)-12 and anti-IL-10. J Infect Dis 173: 1085-1091.
9. Rigopoulou EI, Abbott WG, Haigh P, Naoumov NV, (2005) Blocking of interleukin-10 receptor-a novel approach to stimulate T-helper cell type 1 responses to hepatitis C virus. Clin Immunol 117: 57-64.
10. Wilson EB, Brooks DG, (2011) The role of IL-10 in regulating immunity to persistent viral infections. Curr Top Microbiol Immunol 350: 39-65.
11. Couper KN, Blount DG, Riley EM, (2008) IL-10: the master regulator of immunity to infection. J Immunol 180: 5771-5777.
12. Slobedman B, Barry PA, Spencer JV, Avdic S, Abendroth A, (2009) Virus-encoded homologs of cellular interleukin-10 and their control of host immune function. J Virol 83: 9618-9629.
13. Chang WL, Barry PA, (2010) Attenuation of innate immunity by cytomegalovirus IL-10 establishes a long-term deficit of adaptive antiviral immunity. Proc Natl Acad Sci U S A 107: 22647-22652.
14. Paladino N, Fainboim H, Theiler G, Schroder T, Munoz AE, et al. (2006) Gender susceptibility to chronic hepatitis C virus infection associated with interleukin 10 promoter polymorphism. J Virol 80: 9144-9150.
15. Helminen M, Lahdenpohja N, Hurme M, (1999) Polymorphism of the interleukin-10 gene is associated with susceptibility to Epstein-Barr virus infection. J Infect Dis 180: 496-499.
16. Cheong JY, Cho SW, Hwang IL, Yoon SK, Lee JH, et al. (2006) Association between chronic hepatitis B virus infection and interleukin-10, tumor necrosis factor-alpha gene promoter polymorphisms. J Gastroenterol Hepatol 21: 1163-1169.
17. Shin HD, Park BL, Kim LH, Jung JH, Kim JY, et al. (2003) Interleukin 10 haplotype associated with increased risk of hepatocellular carcinoma. Hum Mol Genet 12: 901-906.
18. Shin HD, Winkler C, Stephens JC, Bream J, Young H, et al. (2000) Genetic restriction of HIV-1 pathogenesis to AIDS by promoter alleles of IL10. Proc Natl Acad Sci U S A 97: 14467-14472.
19. Mandaric S, Walton SM, Rulicke T, Richter K, Girard-Madoux MJ, et al. (2012) IL-10 suppression of NK/DC crosstalk leads to poor priming of MCMV-specific CD4 T cells and prolonged MCMV persistence. PLoS Pathog 8: e1002846.
20. Tang-Feldman YJ, Lochhead GR, Lochhead SR, Yu C, Pomeroy C, (2011) Interleukin-10 repletion suppresses pro-inflammatory cytokines and decreases liver pathology without altering viral replication in murine cytomegalovirus (MCMV)-infected IL-10 knockout mice. Inflamm Res 60: 233-243.
21. Lin MT, Hinton DR, Parra B, Stohlman SA, van der Veen RC, (1998) The role of IL-10 in mouse hepatitis virus-induced demyelinating encephalomyelitis. Virology 245: 270-280.
22. Brooks DG, Teyton L, Oldstone MB, McGavern DB, (2005) Intrinsic functional dysregulation of CD4 T cells occurs rapidly following persistent viral infection. J Virol 79: 10514-10527.
23. Wilson EB, Kidani Y, Elsaesser H, Barnard J, Raff L, et al. (2012) Emergence of distinct multiarmed immunoregulatory antigen-presenting cells during persistent viral infection. Cell Host Microbe 11: 481-491.
24. Ng CT, Oldstone MB, (2012) Infected CD8alpha- dendritic cells are the predominant source of IL-10 during establishment of persistent viral infection. Proc Natl Acad Sci U S A 109: 14116-14121.
25. Frebel H, Oxenius A, (2013) The risks of targeting co-inhibitory pathways to modulate pathogen-directed T cell responses. Trends Immunol 34: 193-199.
26. Richter K, Brocker T, Oxenius A, (2012) Antigen amount dictates CD8+ T-cell exhaustion during chronic viral infection irrespective of the type of antigen presenting cell. Eur J Immunol 42: 2290-2304.
27. Seiler P, Aichele P, Odermatt B, Hengartner H, Zinkernagel RM, et al. (1997) Crucial role of marginal zone macrophages and marginal zone metallophils in the clearance of lymphocytic choriomeningitis virus infection. Eur J Immunol 27: 2626-2633.
28. Zeisberger SM, Odermatt B, Marty C, Zehnder-Fjallman AH, Ballmer-Hofer K, et al. (2006) Clodronate-liposome-mediated depletion of tumour-associated macrophages: a new and highly effective antiangiogenic therapy approach. Br J Cancer 95: 272-281.
29. Jung S, Unutmaz D, Wong P, Sano G, De los Santos K, et al. (2002) In vivo depletion of CD11c+ dendritic cells abrogates priming of CD8+ T cells by exogenous cell-associated antigens. Immunity 17: 211-220.
30. Probst HC, van den Broek M, (2005) Priming of CTLs by lymphocytic choriomeningitis virus depends on dendritic cells. J Immunol 174: 3920-3924.
31. Dudeck A, Dudeck J, Scholten J, Petzold A, Surianarayanan S, et al. (2011) Mast cells are key promoters of contact allergy that mediate the adjuvant effects of haptens. Immunity 34: 973-984.
32. Crawford A, Angelosanto JM, Nadwodny KL, Blackburn SD, Wherry EJ, (2011) A role for the chemokine RANTES in regulating CD8 T cell responses during chronic viral infection. PLoS Pathog 7: e1002098.
33. Penaloza-MacMaster P, Ur Rasheed A, Iyer SS, Yagita H, Blazar BR, et al. (2011) Opposing effects of CD70 costimulation during acute and chronic lymphocytic choriomeningitis virus infection of mice. J Virol 85: 6168-6174.
34. Richter K, Perriard G, Oxenius A, (2013) Reversal of chronic to resolved infection by IL-10 blockade is LCMV strain dependent. Eur J Immunol 43: 649-654.
35. Madan R, Demircik F, Surianarayanan S, Allen JL, Divanovic S, et al. (2009) Nonredundant roles for B cell-derived IL-10 in immune counter-regulation. J Immunol 183: 2312-2320.
36. Siewe L, Bollati-Fogolin M, Wickenhauser C, Krieg T, Muller W, et al. (2006) Interleukin-10 derived from macrophages and/or neutrophils regulates the inflammatory response to LPS but not the response to CpG DNA. Eur J Immunol 36: 3248-3255.
37. Roers A, Siewe L, Strittmatter E, Deckert M, Schluter D, et al. (2004) T cell-specific inactivation of the interleukin 10 gene in mice results in enhanced T cell responses but normal innate responses to lipopolysaccharide or skin irritation. J Exp Med 200: 1289-1297.
38. Saraiva M, O'Garra A, (2010) The regulation of IL-10 production by immune cells. Nat Rev Immunol 10: 170-181.
39. Hagiwara E, Abbasi F, Mor G, Ishigatsubo Y, Klinman DM, (1995) Phenotype and frequency of cells secreting IL-2, IL-4, IL-6, IL-10, IFN and TNF-alpha in human peripheral blood. Cytokine 7: 815-822.
40. Kumar A, Angel JB, Daftarian MP, Parato K, Cameron WD, et al. (1998) 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.
41. Said EA, Dupuy FP, Trautmann L, Zhang Y, Shi Y, et al. (2010) Programmed death-1-induced interleukin-10 production by monocytes impairs CD4+ T cell activation during HIV infection. Nat Med 16: 452-459.
42. Humphreys IR, de Trez C, Kinkade A, Benedict CA, Croft M, et al. (2007) Cytomegalovirus exploits IL-10-mediated immune regulation in the salivary glands. J Exp Med 204: 1217-1225.
43. Stacey MA, Marsden M, Wang EC, Wilkinson GW, Humphreys IR, (2011) IL-10 restricts activation-induced death of NK cells during acute murine cytomegalovirus infection. J Immunol 187: 2944-2952.
44. Belkaid Y, Hoffmann KF, Mendez S, Kamhawi S, Udey MC, et al. (2001) The role of interleukin (IL)-10 in the persistence of Leishmania major in the skin after healing and the therapeutic potential of anti-IL-10 receptor antibody for sterile cure. J Exp Med 194: 1497-1506.
45. Norris BA, Uebelhoer LS, Nakaya HI, Price AA, Grakoui A, et al. (2013) Chronic but Not Acute Virus Infection Induces Sustained Expansion of Myeloid Suppressor Cell Numbers that Inhibit Viral-Specific T Cell Immunity. Immunity 38: 309-321.
46. Fiorentino DF, Bond MW, Mosmann TR, (1989) Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J Exp Med 170: 2081-2095.
47. Maynard CL, Weaver CT, (2008) Diversity in the contribution of interleukin-10 to T-cell-mediated immune regulation. Immunol Rev 226: 219-233.
48. Punkosdy GA, Blain M, Glass DD, Lozano MM, O'Mara L, et al. (2011) Regulatory T-cell expansion during chronic viral infection is dependent on endogenous retroviral superantigens. Proc Natl Acad Sci U S A 108: 3677-3682.
49. Schmitz I, Schneider C, Frohlich A, Frebel H, Christ D, et al. (2013) IL-21 restricts virus-driven Treg cell expansion in chronic LCMV infection. PLoS Pathog 9: e1003362.
50. Eckelhart E, Warsch W, Zebedin E, Simma O, Stoiber D, et al. (2011) A novel Ncr1-Cre mouse reveals the essential role of STAT5 for NK-cell survival and development. Blood 117: 1565-1573.
51. Powell MJ, Thompson SA, Tone Y, Waldmann H, Tone M, (2000) Posttranscriptional regulation of IL-10 gene expression through sequences in the 3′-untranslated region. J Immunol 165: 292-296.
52. Maroof A, Beattie L, Zubairi S, Svensson M, Stager S, et al. (2008) Posttranscriptional regulation of II10 gene expression allows natural killer cells to express immunoregulatory function. Immunity 29: 295-305.
53. Tittel AP, Heuser C, Ohliger C, Llanto C, Yona S, et al. (2012) Functionally relevant neutrophilia in CD11c diphtheria toxin receptor transgenic mice. Nat Methods 9: 385-390.
54. Wilson EB, Yamada DH, Elsaesser H, Herskovitz J, Deng J, et al. (2013) Blockade of chronic type I interferon signaling to control persistent LCMV infection. Science 340: 202-207.
55. Teijaro JR, Ng C, Lee AM, Sullivan BM, Sheehan KC, et al. (2013) Persistent LCMV infection is controlled by blockade of type I interferon signaling. Science 340: 207-211.
56. Aichele P, Unsoeld H, Koschella M, Schweier O, Kalinke U, et al. (2006) CD8 T cells specific for lymphocytic choriomeningitis virus require type I IFN receptor for clonal expansion. J Immunol 176: 4525-4529.
57. Kolumam GA, Thomas S, Thompson LJ, Sprent J, Murali-Krishna K, (2005) Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J Exp Med 202: 637-650.
58. Wiesel M, Crouse J, Bedenikovic G, Sutherland A, Joller N, et al. (2012) Type-I IFN drives the differentiation of short-lived effector CD8+ T cells in vivo. Eur J Immunol 42: 320-329.
59. Gazzinelli RT, Oswald IP, James SL, Sher A, (1992) IL-10 inhibits parasite killing and nitrogen oxide production by IFN-gamma-activated macrophages. J Immunol 148: 1792-1796.
60. O'Farrell AM, Liu Y, Moore KW, Mui AL, (1998) IL-10 inhibits macrophage activation and proliferation by distinct signaling mechanisms: evidence for Stat3-dependent and-independent pathways. EMBO J 17: 1006-1018.
61. Waggoner SN, Cornberg M, Selin LK, Welsh RM, (2012) Natural killer cells act as rheostats modulating antiviral T cells. Nature 481: 394-398.
62. Richter K, Agnellini P, Oxenius A, (2010) On the role of the inhibitory receptor LAG-3 in acute and chronic LCMV infection. Int Immunol 22: 13-23.
63. Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W, (1993) Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75: 263-274.
64. Kamanaka M, Kim ST, Wan YY, Sutterwala FS, Lara-Tejero M, et al. (2006) Expression of interleukin-10 in intestinal lymphocytes detected by an interleukin-10 reporter knockin tiger mouse. Immunity 25: 941-952.
65. Hamel K, Doodes P, Cao Y, Wang Y, Martinson J, et al. (2008) Suppression of proteoglycan-induced arthritis by anti-CD20 B Cell depletion therapy is mediated by reduction in autoantibodies and CD4+ T cell reactivity. J Immunol 180: 4994-5003.
66. Nolte MA, Leibundgut-Landmann S, Joffre O, Reis e Sousa C, (2007) Dendritic cell quiescence during systemic inflammation driven by LPS stimulation of radioresistant cells in vivo. J Exp Med 204: 1487-1501.
67. Rickert RC, Rajewsky K, Roes J, (1995) Impairment of T-cell-dependent B-cell responses and B-1 cell development in CD19-deficient mice. Nature 376: 352-355.