IL-10 regulates viral lung immunopathology during acute respiratory syncytial virus infection in mice

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Loebbermann, Jens ^a   Schnoeller, Corinna ^a   Thornton, Hannah ^a   Durant, Lydia ^a   Sweeney, Nathan P ^a   Schuijs, Martijn ^a   O'Garra, Anne ^b   Johansson, Cecilia ^a   Openshaw, Peter J ^a  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CCL1 CHEMOKINE; CXCL1 CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 10; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; INTERLEUKIN 1 RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOCRINE EFFECT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL COUNT; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; IMMUNE RESPONSE; IMMUNOREGULATION; LUNG LAVAGE; MOUSE; NATURAL KILLER CELL; NEUTROPHILIA; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RESPIRATORY SYNCYTIAL VIRUS INFECTION; T LYMPHOCYTE ACTIVATION; TH1 CELL; VIRUS LOAD; WEIGHT REDUCTION; ANIMAL; BAGG ALBINO MOUSE; CYTOLOGY; INFLAMMATION; METABOLISM; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TRANSGENIC MOUSE;

MUS; RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

ANIMALS; BRONCHOALVEOLAR LAVAGE; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; INFLAMMATION; INTERFERON-GAMMA; INTERLEUKIN-10; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; RECEPTORS, INTERLEUKIN-1; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUSES; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84857682575     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032371     Document Type: Article

References (39)

1. Saraiva M, O'Garra A, (2010) The regulation of IL-10 production by immune cells. Nat Rev Immunol 10: 170-181.
2. O'Garra A, Vieira P, (2004) Regulatory T cells and mechanisms of immune system control. Nat Med 10: 801-805.
3. Lloyd CM, Hawrylowicz CM, (2009) Regulatory T cells in asthma. Immunity 31: 438-449.
4. Maloy KJ, Powrie F, (2011) Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature (London) 474: 298-306.
5. O'Garra A, Murphy KM, (2009) From IL-10 to IL-12: how pathogens and their products stimulate APCs to induce T(H)1 development. Nat Immunol 10: 929-932.
6. Sabat R, Grutz G, Warszawska K, Kirsch S, Witte E, et al. (2010) Biology of interleukin-10. Cytokine Growth Factor Rev 21: 331-344.
7. 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.
8. Mege JL, Meghari S, Honstettre A, Capo C, Raoult D, (2006) The two faces of interleukin 10 in human infectious diseases. Lancet Infect Dis 6: 557-569.
9. Couper KN, Blount DG, Riley EM, (2008) IL-10: the master regulator of immunity to infection. J Immunol 180: 5771-5777.
10. Nagamatsu K, Kuwae A, Konaka T, Nagai S, Yoshida S, et al. (2009) Bordetella evades the host immune system by inducing IL-10 through a type III effector, BopN. J Exp Med 206: 3073-3088.
11. Hall CB, (2001) Respiratory syncytial virus and parainfluenza virus. N Engl J Med 344: 1917-1928.
12. Smyth RL, Openshaw PJ, (2006) Bronchiolitis. Lancet 368: 312-322.
13. Sigurs N, Bjarnason R, Sigurbergsson F, Kjellman B, (2000) Respiratory syncytial virus bronchiolitis in infancy is an important risk factor for asthma and allergy at age 7. American Journal of Respiratory and Critical Care Medicine 161: 1501-1507.
14. Falsey AR, Hennessey PA, Formica MA, Cox C, Walsh EE, (2005) Respiratory syncytial virus infection in elderly and high-risk adults. N Engl J Med 352: 1749-1759.
15. Freymuth F, Vabret A, Gouarin S, Petitjean J, Charbonneau P, et al. (2004) [Epidemiology and diagnosis of respiratory syncitial virus in adults]. Rev Mal Respir 21: 35-42.
16. Legg JP, Hussain IR, Warner JA, Johnston SL, Warner JO, (2003) Type 1 and type 2 cytokine imbalance in acute respiratory syncytial virus bronchiolitis. Am J Respir Crit Care Med 168: 633-639.
17. Murai H, Terada A, Mizuno M, Asai M, Hirabayashi Y, et al. (2007) IL-10 and RANTES are elevated in nasopharyngeal secretions of children with respiratory syncytial virus infection. Allergol Int 56: 157-163.
18. Schuurhof A, Janssen R, de GH, Hodemaekers HM, de KA, et al. (2011) Local interleukin-10 production during respiratory syncytial virus bronchiolitis is associated with post-bronchiolitis wheeze. Respir Res 12: 121.
19. Hoebee B, Bont L, Rietveld E, van OM, Hodemaekers HM, et al. (2004) Influence of promoter variants of interleukin-10, interleukin-9, and tumor necrosis factor-alpha genes on respiratory syncytial virus bronchiolitis. J Infect Dis 189: 239-247.
20. Sun J, Madan R, Karp CL, Braciale TJ, (2009) Effector T cells control lung inflammation during acute influenza virus infection by producing IL-10. Nat Med 15: 277-284.
21. McKinstry KK, Strutt TM, Buck A, Curtis JD, Dibble JP, et al. (2009) IL-10 deficiency unleashes an influenza-specific Th17 response and enhances survival against high-dose challenge. J Immunol 182: 7353-7363.
22. Weiss KA, Christiaansen AF, Fulton RB, Meyerholz DK, Varga SM, (2011) Multiple CD4+ T cell subsets produce immunomodulatory IL-10 during respiratory syncytial virus infection. J Immunol 187: 3145-3154.
23. Sun J, Cardani A, Sharma AK, Laubach VE, Jack RS, et al. (2011) Autocrine regulation of pulmonary inflammation by effector T-cell derived IL-10 during infection with respiratory syncytial virus. PLoS Pathog 7 (8): e1002173.
24. Pribul PK, Harker J, Wang B, Wang H, Tregoning JS, et al. (2008) Alveolar macrophages are a major determinant of early responses to viral lung infection but do not influence subsequent disease development. J Virol 82: 4441-4448.
25. Jankovic D, Kugler DG, Sher A, (2010) IL-10 production by CD4+ effector T cells: a mechanism for self-regulation. Mucosal Immunol 3: 239-246.
26. Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W, (1993) Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75: 263-274.
27. Zeng R, Li C, Li N, Wei L, Cui Y, (2011) The role of cytokines and chemokines in severe respiratory syncytial virus infection and subsequent asthma. Cyto 53: 1-7.
28. Bem RA, Bos AP, Bots M, Wolbink AM, van Ham SM, et al. (2008) Activation of the granzyme pathway in children with severe respiratory syncytial virus infection. Pediatr Res 63: 650-655.
29. Roncarolo MG, Gregori S, Battaglia M, Bacchetta R, Fleischhauer K, et al. (2006) Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunol Rev 212: 28-50.
30. Cardone J, Le FG, Vantourout P, Roberts A, Fuchs A, et al. (2010) Complement regulator CD46 temporally regulates cytokine production by conventional and unconventional T cells. Nat Immunol 11: 862-871.
31. Chaudhry A, Samstein RM, Treuting P, Liang Y, Pils MC, et al. (2011) Interleukin-10 signaling in regulatory T cells is required for suppression of Th17 cell-mediated inflammation. Immunity 34: 566-578.
32. Hawrylowicz CM, O'Garra A, (2005) Potential role of interleukin-10-secreting regulatory T cells in allergy and asthma. Nat Rev Immunol 5: 271-283.
33. Joetham A, Takeda K, Taube C, Miyahara N, Matsubara S, et al. (2007) Naturally occurring lung CD4(+)CD25(+) T cell regulation of airway allergic responses depends on IL-10 induction of TGF-beta. J Immunol 178: 1433-1442.
34. Rubtsov YP, Rasmussen JP, Chi EY, Fontenot J, Castelli L, et al. (2008) Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity 28: 546-558.
35. 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.
36. Pils MC, Pisano F, Fasnacht N, Heinrich JM, Groebe L, et al. (2010) Monocytes/macrophages and/or neutrophils are the target of IL-10 in the LPS endotoxemia model. Eur J Immunol 40: 443-448.
37. Castilow EM, Olson MR, Meyerholz DK, Varga SM, (2008) Differential role of gamma interferon in inhibiting pulmonary eosinophilia and exacerbating systemic disease in fusion protein-immunized mice undergoing challenge infection with respiratory syncytial virus. J Virol 82: 2196-2207.
38. Lee DC, Harker JA, Tregoning JS, Atabani SF, Johansson C, et al. (2010) CD25+ natural regulatory T cells are critical in limiting innate and adaptive immunity and resolving disease following respiratory syncytial virus infection. J Virol.
39. Grossman WJ, Verbsky JW, Tollefsen BL, Kemper C, Atkinson JP, et al. (2004) Differential expression of granzymes A and B in human cytotoxic lymphocyte subsets and T regulatory cells. Blood 104: 2840-2848.