Locally Produced IL-10 Limits Cutaneous Vaccinia Virus Spread

PLoS Pathogens

Volumn 12, Issue 3, 2016, Pages

  Cush, Stephanie S ^a   Reynoso, Glennys V ^a   Kamenyeva, Olena ^a   Bennink, Jack R ^a   Yewdell, Jonathan W ^a   Hickman, Heather D ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; CYTOKINE; IL10 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; FLOW CYTOMETRY; IMAGE ANALYSIS; MICROSCOPY; MOUSE; MULTIPHOTON INTRAVITAL MICROSCOPY; NONHUMAN; POLYMERASE CHAIN REACTION; REAL TIME POLYMERASE CHAIN REACTION; SKIN INFECTION; VACCINIA VIRUS; VACCINIA VIRUS INFECTION; VIROGENESIS; VIRUS INFECTION; VIRUS REPLICATION; VIRUS TRANSMISSION; ANIMAL; C57BL MOUSE; FEMALE; GENETICS; GERMFREE ANIMAL; IMMUNOLOGY; METABOLISM; MONOCYTE; SKIN; T LYMPHOCYTE; TRANSGENIC MOUSE; VACCINIA; VIROLOGY;

ANIMALS; CYTOKINES; FEMALE; INTERLEUKIN-10; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MONOCYTES; SKIN; SPECIFIC PATHOGEN-FREE ORGANISMS; T-LYMPHOCYTES; VACCINIA; VACCINIA VIRUS; VIRUS REPLICATION;

EID: 84962408966     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005493     Document Type: Article

References (64)

1. Baskin CR, Bielefeldt-Ohmann H, Tumpey TM, Sabourin PJ, Long JP, Garcia-Sastre A, et al. Early and sustained innate immune response defines pathology and death in nonhuman primates infected by highly pathogenic influenza virus. Proc Natl Acad Sci U S A. 2009;106(9):3455–60. Epub 2009/02/17. doi: 10.1073/pnas.081323410619218453; PubMed Central PMCID: PMC2642661.
2. Taubenberger JK, Morens DM, The pathology of influenza virus infections. Annual review of pathology. 2008;3:499–522. Epub 2007/11/28. doi: 10.1146/annurev.pathmechdis.3.121806.15431618039138; PubMed Central PMCID: PMC2504709.
3. Iacono KT, Kazi L, Weiss SR, Both spike and background genes contribute to murine coronavirus neurovirulence. J Virol. 2006;80(14):6834–43. Epub 2006/07/01. doi: 10.1128/JVI.00432-0616809289; PubMed Central PMCID: PMC1489045.
4. Johnson JE, Gonzales RA, Olson SJ, Wright PF, Graham BS, The histopathology of fatal untreated human respiratory syncytial virus infection. Modern pathology: an official journal of the United States and Canadian Academy of Pathology, Inc. 2007;20(1):108–19. Epub 2006/12/05. doi: 10.1038/modpathol.380072517143259.
5. Olson MR, Varga SM, Pulmonary immunity and immunopathology: lessons from respiratory syncytial virus. Expert review of vaccines. 2008;7(8):1239–55. Epub 2008/10/11. doi: 10.1586/14760584.7.8.123918844597; PubMed Central PMCID: PMC2630464.
6. de Waal Malefyt R, Abrams J, Bennett B, Figdor CG, de Vries JE, Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J Exp Med. 1991;174(5):1209–20. Epub 1991/11/01. 1940799; PubMed Central PMCID: PMC2119001.
7. Ding L, Linsley PS, Huang LY, Germain RN, Shevach EM, IL-10 inhibits macrophage costimulatory activity by selectively inhibiting the up-regulation of B7 expression. J Immunol. 1993;151(3):1224–34. Epub 1993/08/01. 7687627.
8. Fiorentino DF, Zlotnik A, Mosmann TR, Howard M, O'Garra A, IL-10 inhibits cytokine production by activated macrophages. J Immunol. 1991;147(11):3815–22. Epub 1991/12/01. 1940369.
9. Couper KN, Blount DG, Riley EM, IL-10: the master regulator of immunity to infection. J Immunol. 2008;180(9):5771–7. Epub 2008/04/22. 18424693.
10. Puissant-Lubrano B, Bossi P, Gay F, Crance JM, Bonduelle O, Garin D, et al. Control of vaccinia virus skin lesions by long-term-maintained IFN-gamma+TNF-alpha+ effector/memory CD4+ lymphocytes in humans. J Clin Invest. 2010;120(5):1636–44. Epub 2010/04/07. doi: 10.1172/JCI3850620364089; PubMed Central PMCID: PMC2860918.
11. Ito S, Ansari P, Sakatsume M, Dickensheets H, Vazquez N, Donnelly RP, et al. Interleukin-10 inhibits expression of both interferon alpha- and interferon gamma- induced genes by suppressing tyrosine phosphorylation of STAT1. Blood. 1999;93(5):1456–63. Epub 1999/02/25. 10029571.
12. Trandem K, Zhao J, Fleming E, Perlman S, Highly activated cytotoxic CD8 T cells express protective IL-10 at the peak of coronavirus-induced encephalitis. J Immunol. 2011;186(6):3642–52. Epub 2011/02/15. doi: 10.4049/jimmunol.100329221317392; PubMed Central PMCID: PMC3063297.
13. Weiss KA, Christiaansen AF, Fulton RB, Meyerholz DK, Varga SM, Multiple CD4+ T cell subsets produce immunomodulatory IL-10 during respiratory syncytial virus infection. J Immunol. 2011;187(6):3145–54. Epub 2011/08/17. doi: 10.4049/jimmunol.110076421844390; PubMed Central PMCID: PMC3304096.
14. Zou Q, Wu B, Xue J, Fan X, Feng C, Geng S, et al. CD8+ Treg cells suppress CD8+ T cell-responses by IL-10-dependent mechanism during H5N1 influenza virus infection. European journal of immunology. 2014;44(1):103–14. Epub 2013/10/12. doi: 10.1002/eji.20134358324114149.
15. Brooks DG, Trifilo MJ, Edelmann KH, Teyton L, McGavern DB, Oldstone MB, Interleukin-10 determines viral clearance or persistence in vivo. Nat Med. 2006;12(11):1301–9. Epub 2006/10/17. doi: 10.1038/nm149217041596; PubMed Central PMCID: PMC2535582.
16. Brooks DG, Lee AM, Elsaesser H, McGavern DB, Oldstone MB, IL-10 blockade facilitates DNA vaccine-induced T cell responses and enhances clearance of persistent virus infection. J Exp Med. 2008;205(3):533–41. Epub 2008/03/12. doi: 10.1084/jem.2007194818332180; PubMed Central PMCID: PMC2275377.
17. Mandaric S, Walton SM, Rulicke T, Richter K, Girard-Madoux MJ, Clausen BE, et al. IL-10 suppression of NK/DC crosstalk leads to poor priming of MCMV-specific CD4 T cells and prolonged MCMV persistence. PLoS Pathog. 2012;8(8):e1002846. Epub 2012/08/10. doi: 10.1371/journal.ppat.100284622876184; PubMed Central PMCID: PMC3410900.
18. Hughes AL, Origin and evolution of viral interleukin-10 and other DNA virus genes with vertebrate homologues. Journal of molecular evolution. 2002;54(1):90–101. Epub 2001/12/06. doi: 10.1007/s00239-001-0021-111734902.
19. Bartlett NW, Dumoutier L, Renauld JC, Kotenko SV, McVey CE, Lee HJ, et al. A new member of the interleukin 10-related cytokine family encoded by a poxvirus. The Journal of general virology. 2004;85(Pt 6):1401–12. Epub 2004/05/29. 15166422.
20. Hsu DH, de Waal Malefyt R, Fiorentino DF, Dang MN, Vieira P, de Vries J, et al. Expression of interleukin-10 activity by Epstein-Barr virus protein BCRF1. Science. 1990;250(4982):830–2. Epub 1990/11/09. 2173142.
21. Sun J, Madan R, Karp CL, Braciale TJ, Effector T cells control lung inflammation during acute influenza virus infection by producing IL-10. Nat Med. 2009;15(3):277–84. Epub 2009/02/24. doi: 10.1038/nm.192919234462; PubMed Central PMCID: PMC2693210.
22. Loebbermann J, Schnoeller C, Thornton H, Durant L, Sweeney NP, Schuijs M, et al. IL-10 regulates viral lung immunopathology during acute respiratory syncytial virus infection in mice. PLoS One. 2012;7(2):e32371. Epub 2012/03/07. doi: 10.1371/journal.pone.003237122393401; PubMed Central PMCID: PMC3290561.
23. Sun J, Cardani A, Sharma AK, Laubach VE, Jack RS, Muller W, et al. Autocrine regulation of pulmonary inflammation by effector T-cell derived IL-10 during infection with respiratory syncytial virus. PLoS Pathog. 2011;7(8):e1002173. Epub 2011/08/11. doi: 10.1371/journal.ppat.100217321829368; PubMed Central PMCID: PMC3150291.
24. Puntambekar SS, Bergmann CC, Savarin C, Karp CL, Phares TW, Parra GI, et al. Shifting hierarchies of interleukin-10-producing T cell populations in the central nervous system during acute and persistent viral encephalomyelitis. J Virol. 2011;85(13):6702–13. Epub 2011/04/29. doi: 10.1128/JVI.00200-1121525347; PubMed Central PMCID: PMC3126516.
25. Saraiva M, O'Garra A, The regulation of IL-10 production by immune cells. Nat Rev Immunol. 2010;10(3):170–81. Epub 2010/02/16. doi: 10.1038/nri271120154735.
26. Hickman HD, Reynoso GV, Ngudiankama BF, Rubin EJ, Magadan JG, Cush SS, et al. Anatomically restricted synergistic antiviral activities of innate and adaptive immune cells in the skin. Cell Host Microbe. 2013;13(2):155–68. Epub 2013/02/19. doi: 10.1016/j.chom.2013.01.00423414756; PubMed Central PMCID: PMC3591514.
27. Kamanaka M, Kim ST, Wan YY, Sutterwala FS, Lara-Tejero M, Galan JE, et al. Expression of interleukin-10 in intestinal lymphocytes detected by an interleukin-10 reporter knockin tiger mouse. Immunity. 2006;25(6):941–52. Epub 2006/12/02. doi: 10.1016/j.immuni.2006.09.01317137799.
28. Madan R, Demircik F, Surianarayanan S, Allen JL, Divanovic S, Trompette A, et al. Nonredundant roles for B cell-derived IL-10 in immune counter-regulation. J Immunol. 2009;183(4):2312–20. Epub 2009/07/22. doi: 10.4049/jimmunol.090018519620304; PubMed Central PMCID: PMC2772089.
29. Bouabe H, Cytokine reporter mice: the special case of IL-10. Scandinavian journal of immunology. 2012;75(6):553–67. Epub 2012/03/21. doi: 10.1111/j.1365-3083.2012.02695.x22429026.
30. Sanchez AM, Zhu J, Huang X, Yang Y, The development and function of memory regulatory T cells after acute viral infections. J Immunol. 2012;189(6):2805–14. Epub 2012/08/03. doi: 10.4049/jimmunol.120064522855712; PubMed Central PMCID: PMC3436958.
31. Szabo SJ, Kim ST, Costa GL, Zhang X, Fathman CG, Glimcher LH, A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell. 2000;100(6):655–69. Epub 2000/04/13. 10761931.
32. Sullivan BM, Juedes A, Szabo SJ, von Herrath M, Glimcher LH, Antigen-driven effector CD8 T cell function regulated by T-bet. Proc Natl Acad Sci U S A. 2003;100(26):15818–23. Epub 2003/12/16. doi: 10.1073/pnas.263693810014673093; PubMed Central PMCID: PMC307651.
33. Li JL, Goh CC, Keeble JL, Qin JS, Roediger B, Jain R, et al. Intravital multiphoton imaging of immune responses in the mouse ear skin. Nature protocols. 2012;7(2):221–34. Epub 2012/01/14. doi: 10.1038/nprot.2011.43822240584.
34. Hickman HD, Reynoso GV, Ngudiankama BF, Rubin EJ, Magadan JG, Cush SS, et al. Anatomically restricted synergistic antiviral activities of innate and adaptive immune cells in the skin. Cell Host Microbe. 2013;13(2):155–68. doi: 10.1016/j.chom.2013.01.00423414756; PubMed Central PMCID: PMC3591514.
35. Lee KH, Holdorf AD, Dustin ML, Chan AC, Allen PM, Shaw AS, T cell receptor signaling precedes immunological synapse formation. Science. 2002;295(5559):1539–42. Epub 2002/02/23. doi: 10.1126/science.106771011859198.
36. Saederup N, Cardona AE, Croft K, Mizutani M, Cotleur AC, Tsou CL, et al. Selective chemokine receptor usage by central nervous system myeloid cells in CCR2-red fluorescent protein knock-in mice. PLoS One. 2010;5(10):e13693. doi: 10.1371/journal.pone.001369321060874; PubMed Central PMCID: PMCPMC2965160.
37. Domenico J, Lucas JJ, Fujita M, Gelfand EW, Susceptibility to vaccinia virus infection and spread in mice is determined by age at infection, allergen sensitization and mast cell status. International archives of allergy and immunology. 2012;158(2):196–205. Epub 2012/01/31. doi: 10.1159/00033064722286752; PubMed Central PMCID: PMC3291886.
38. Muller AJ, Filipe-Santos O, Eberl G, Aebischer T, Spath GF, Bousso P, CD4+ T cells rely on a cytokine gradient to control intracellular pathogens beyond sites of antigen presentation. Immunity. 2012;37(1):147–57. Epub 2012/06/26. doi: 10.1016/j.immuni.2012.05.01522727490.
39. Ariotti S, Beltman JB, Chodaczek G, Hoekstra ME, van Beek AE, Gomez-Eerland R, et al. Tissue-resident memory CD8+ T cells continuously patrol skin epithelia to quickly recognize local antigen. Proc Natl Acad Sci U S A. 2012;109(48):19739–44. Epub 2012/11/15. doi: 10.1073/pnas.120892710923150545; PubMed Central PMCID: PMC3511734.
40. Ariotti S, Beltman JB, Borsje R, Hoekstra ME, Halford WP, Haanen JB, et al. Subtle CXCR3-Dependent Chemotaxis of CTLs within Infected Tissue Allows Efficient Target Localization. J Immunol. 2015. doi: 10.4049/jimmunol.150085326525288.
41. Karupiah G, Xie QW, Buller RM, Nathan C, Duarte C, MacMicking JD, Inhibition of viral replication by interferon-gamma-induced nitric oxide synthase. Science. 1993;261(5127):1445–8. 7690156.
42. Wynn TA, Chawla A, Pollard JW, Macrophage biology in development, homeostasis and disease. Nature. 2013;496(7446):445–55. doi: 10.1038/nature1203423619691; PubMed Central PMCID: PMCPMC3725458.
43. Tiemessen MM, Jagger AL, Evans HG, van Herwijnen MJ, John S, Taams LS, CD4+CD25+Foxp3+ regulatory T cells induce alternative activation of human monocytes/macrophages. Proc Natl Acad Sci U S A. 2007;104(49):19446–51. Epub 2007/11/29. doi: 10.1073/pnas.070683210418042719; PubMed Central PMCID: PMC2148309.
44. Liu G, Ma H, Qiu L, Li L, Cao Y, Ma J, et al. Phenotypic and functional switch of macrophages induced by regulatory CD4+CD25+ T cells in mice. Immunology and cell biology. 2011;89(1):130–42. Epub 2010/06/02. doi: 10.1038/icb.2010.7020514074.
45. Shirey KA, Pletneva LM, Puche AC, Keegan AD, Prince GA, Blanco JC, et al. Control of RSV-induced lung injury by alternatively activated macrophages is IL-4R alpha-, TLR4-, and IFN-beta-dependent. Mucosal immunology. 2010;3(3):291–300. Epub 2010/04/21. doi: 10.1038/mi.2010.620404812; PubMed Central PMCID: PMC2875872.
46. Pesce JT, Ramalingam TR, Mentink-Kane MM, Wilson MS, El Kasmi KC, Smith AM, et al. Arginase-1-expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis. PLoS Pathog. 2009;5(4):e1000371. Epub 2009/04/11. doi: 10.1371/journal.ppat.100037119360123; PubMed Central PMCID: PMC2660425.
47. Novak ML, Koh TJ, Phenotypic transitions of macrophages orchestrate tissue repair. The American journal of pathology. 2013;183(5):1352–63. Epub 2013/10/05. doi: 10.1016/j.ajpath.2013.06.03424091222; PubMed Central PMCID: PMC3969506.
48. Novak ML, Koh TJ, Macrophage phenotypes during tissue repair. Journal of leukocyte biology. 2013;93(6):875–81. Epub 2013/03/19. doi: 10.1189/jlb.101251223505314; PubMed Central PMCID: PMC3656331.
49. Vellozzi C, Lane JM, Averhoff F, Maurer T, Norton S, Damon I, et al. Generalized vaccinia, progressive vaccinia, and eczema vaccinatum are rare following smallpox (vaccinia) vaccination: United States surveillance, 2003. Clinical infectious diseases: an official publication of theInfectious Diseases Society of America. 2005;41(5):689–97. Epub 2005/08/05. doi: 10.1086/43258416080092.
50. Schneider L, Weinberg A, Boguniewicz M, Taylor P, Oettgen H, Heughan L, et al. Immune response to varicella vaccine in children with atopic dermatitis compared with nonatopic controls. The Journal of allergy and clinical immunology. 2010;126(6):1306–7 e2. Epub 2010/10/05. doi: 10.1016/j.jaci.2010.08.01020889193; PubMed Central PMCID: PMC2998561.
51. Darling AR, Freyschmidt EJ, Burton OT, Koleoglou KJ, Oyoshi MK, Oettgen HC, IL-10 suppresses IL-17-mediated dermal inflammation and reduces the systemic burden of Vaccinia virus in a mouse model of eczema vaccinatum. Clin Immunol. 2014;150(2):153–60. Epub 2014/01/15. doi: 10.1016/j.clim.2013.11.01024412909; PubMed Central PMCID: PMC3946343.
52. Kurilla MG, Swaminathan S, Welsh RM, Kieff E, Brutkiewicz RR, Effects of virally expressed interleukin-10 on vaccinia virus infection in mice. J Virol. 1993;67(12):7623–8. Epub 1993/12/01. 8230481; PubMed Central PMCID: PMC238230.
53. Zhao Y, Adams YF, Croft M, Preferential replication of vaccinia virus in the ovaries is independent of immune regulation through IL-10 and TGF-beta. Viral Immunol. 2011;24(5):387–96. Epub 2011/10/01. doi: 10.1089/vim.2011.002021958373; PubMed Central PMCID: PMC3189386.
54. van Den Broek M, Bachmann MF, Kohler G, Barner M, Escher R, Zinkernagel R, et al. IL-4 and IL-10 antagonize IL-12-mediated protection against acute vaccinia virus infection with a limited role of IFN-gamma and nitric oxide synthetase 2. J Immunol. 2000;164(1):371–8. Epub 1999/12/22. 10605032.
55. Broder CC, Kennedy PE, Michaels F, Berger EA, Expression of foreign genes in cultured human primary macrophages using recombinant vaccinia virus vectors. Gene. 1994;142(2):167–74. Epub 1994/05/16. 8194748.
56. Liu L, Xu Z, Fuhlbrigge RC, Pena-Cruz V, Lieberman J, Kupper TS, Vaccinia virus induces strong immunoregulatory cytokine production in healthy human epidermal keratinocytes: a novel strategy for immune evasion. J Virol. 2005;79(12):7363–70. Epub 2005/05/28. doi: 10.1128/JVI.79.12.7363–7370.200515919891; PubMed Central PMCID: PMC1143660.
57. Byrd D, Shepherd N, Lan J, Hu N, Amet T, Yang K, et al. Primary human macrophages serve as vehicles for vaccinia virus replication and dissemination. J Virol. 2014. Epub 2014/04/04. doi: 10.1128/JVI.03726-1324696488.
58. Honda T, Egen JG, Lammermann T, Kastenmuller W, Torabi-Parizi P, Germain RN, Tuning of antigen sensitivity by T cell receptor-dependent negative feedback controls T cell effector function in inflamed tissues. Immunity. 2014;40(2):235–47. Epub 2014/01/21. doi: 10.1016/j.immuni.2013.11.01724440150.
59. Filipe-Santos O, Pescher P, Breart B, Lippuner C, Aebischer T, Glaichenhaus N, et al. A dynamic map of antigen recognition by CD4 T cells at the site of Leishmania major infection. Cell host & microbe. 2009;6(1):23–33. Epub 2009/07/21. doi: 10.1016/j.chom.2009.04.01419616763.
60. Hickman HD, Reynoso GV, Ngudiankama BF, Cush SS, Gibbs J, Bennink JR, et al. CXCR3 chemokine receptor enables local CD8(+) T cell migration for the destruction of virus-infected cells. Immunity. 2015;42(3):524–37. doi: 10.1016/j.immuni.2015.02.00925769612; PubMed Central PMCID: PMCPMC4365427.
61. Willis KL, Langland JO, Shisler JL, Viral double-stranded RNAs from vaccinia virus early or intermediate gene transcripts possess PKR activating function, resulting in NF-kappaB activation, when the K1 protein is absent or mutated. J Biol Chem. 2011;286(10):7765–78. Epub 2010/12/25. doi: 10.1074/jbc.M110.19470421183678; PubMed Central PMCID: PMC3048664.
62. Hickman HD, Li L, Reynoso GV, Rubin EJ, Skon CN, Mays JW, et al. Chemokines control naive CD8+ T cell selection of optimal lymph node antigen presenting cells. The Journal of experimental medicine. 2011;208(12):2511–24. Epub 2011/11/02. doi: 10.1084/jem.2010254522042976; PubMed Central PMCID: PMC3256957.
63. Hickman HD, Takeda K, Skon CN, Murray FR, Hensley SE, Loomis J, et al. Direct priming of antiviral CD8+ T cells in the peripheral interfollicular region of lymph nodes. Nature immunology. 2008;9(2):155–65. Epub 2008/01/15. ni1557 [pii] doi: 10.1038/ni155718193049.
64. Pieri L, Sassoli C, Romagnoli P, Domenici L, Use of periodate-lysine-paraformaldehyde for the fixation of multiple antigens in human skin biopsies. European journal of histochemistry: EJH. 2002;46(4):365–75. Epub 2003/02/25. 12597622.