Multiple CD4+ T cell subsets produce immunomodulatory IL-10 during respiratory syncytial virus infection

Journal of Immunology

Volumn 187, Issue 6, 2011, Pages 3145-3154

  Weiss, Kayla A ^a   Christiaansen, Allison F ^a   Fulton, Ross B ^a,c   Meyerholz, David K ^b   Varga, Steven M ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c UNIVERSITY OF MINNESOTA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 10 RECEPTOR; INTERLEUKIN 17; TRANSCRIPTION FACTOR FOXP3;

ADAPTIVE IMMUNITY; AIRWAY RESISTANCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; DISEASE SEVERITY; FEMALE; HUMAN; HUMAN CELL; IMMUNOMODULATION; LUNG ALVEOLUS CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; RECEPTOR BLOCKING; REGULATORY T LYMPHOCYTE; RESPIRATORY SYNCYTIAL VIRUS INFECTION; T LYMPHOCYTE SUBPOPULATION; WEIGHT REDUCTION;

ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CD4-POSITIVE T-LYMPHOCYTES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; IMMUNOLOGIC FACTORS; INTERLEUKIN-10; MICE; MICE, INBRED BALB C; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUSES; T-LYMPHOCYTE SUBSETS;

EID: 80053085640     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100764     Document Type: Article

References (68)

1. Falsey, A. R., P. A. Hennessey, M. A. Formica, C. Cox, and E. E. Walsh. 2005. Respiratory syncytial virus infection in elderly and high-risk adults. N. Engl. J. Med. 352: 1749-1759. (Pubitemid 40570923)
2. Falsey, A. R., and E. E. Walsh. 2005. Respiratory syncytial virus infection in elderly adults. Drugs Aging 22: 577-587. (Pubitemid 41214551)
3. Heilman, C. A. 1990. From the National Institute of Allergy and Infectious Diseases and the World Health Organization. Respiratory syncytial and parainfluenza viruses. J. Infect. Dis. 161: 402-406.
4. Ebbert, J. O., and A. H. Limper. 2005. Respiratory syncytial virus pneumonitis in immunocompromised adults: clinical features and outcome. Respiration 72: 263-269. (Pubitemid 40981085)
5. Shay, D. K., R. C. Holman, R. D. Newman, L. L. Liu, J. W. Stout, and L. J. Anderson. 1999. Bronchiolitis-associated hospitalizations among US children, 1980-1996. JAMA 282: 1440-1446. (Pubitemid 29493797)
6. Shay, D. K., R. C. Holman, G. E. Roosevelt, M. J. Clarke, and L. J. Anderson. 2001. Bronchiolitis-associated mortality and estimates of respiratory syncytial virus-associated deaths among US children, 1979-1997. J. Infect. Dis. 183: 16-22. (Pubitemid 32043037)
7. Collins, P. L., and B. S. Graham. 2008. Viral and host factors in human respiratory syncytial virus pathogenesis. J. Virol. 82: 2040-2055. (Pubitemid 351293507)
8. La Gruta, N. L., K. Kedzierska, J. Stambas, and P. C. Doherty. 2007. A question of self-preservation: immunopathology in influenza virus infection. Immunol. Cell Biol. 85: 85-92. (Pubitemid 46398724)
9. Perlman, S., and A. A. Dandekar. 2005. Immunopathogenesis of coronavirus infections: implications for SARS. Nat. Rev. Immunol. 5: 917-927. (Pubitemid 41746761)
10. Holt, P. G., D. H. Strickland, M. E. Wikström, and F. L. Jahnsen. 2008. Regulation of immunological homeostasis in the respiratory tract. Nat. Rev. Immunol. 8: 142-152. (Pubitemid 351161302)
11. Saraiva, M., and A. O'Garra. 2010. The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 10: 170-181.
12. Kotenko, S. V., C. D. Krause, L. S. Izotova, B. P. Pollack, W. Wu, and S. Pestka. 1997. Identification and functional characterization of a second chain of the interleukin-10 receptor complex. EMBO J. 16: 5894-5903. (Pubitemid 27427285)
13. Liu, Y., S. H. Wei, A. S. Ho, R. De Waal Malefyt, and K. W. Moore. 1994. Expression cloning and characterization of a human IL-10 receptor. J. Immunol. 152: 1821-1829.
14. Tan, J. C., S. R. Indelicato, S. K. Narula, P. J. Zavodny, and C. C. Chou. 1993. Characterization of interleukin-10 receptors on human and mouse cells. J. Biol. Chem. 268: 21053-21059. (Pubitemid 23292289)
15. Moore, K. W., R. De Waal Malefyt, R. L. Coffman, and A. O'Garra. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19: 683-765. (Pubitemid 32368050)
16. De Waal Malefyt, R., J. Haanen, H. Spits, M. G. Roncarolo, A. te Velde, C. Figdor, K. Johnson, R. Kastelein, H. Yssel, and J. E. De Vries. 1991. Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific 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.
17. Ding, L., P. S. Linsley, L. Y. Huang, R. N. Germain, and E. M. Shevach. 1993. IL-10 inhibits macrophage costimulatory activity by selectively inhibiting the up-regulation of B7 expression. J. Immunol. 151: 1224-1234. (Pubitemid 23219258)
18. Allavena, P., L. Piemonti, D. Longoni, S. Bernasconi, A. Stoppacciaro, L. Ruco, and A. Mantovani. 1998. IL-10 prevents the differentiation of monocytes to dendritic cells but promotes their maturation to macrophages. Eur. J. Immunol. 28: 359-369. (Pubitemid 28048306)
19. Schandené, L., C. Alonso-Vega, F. Willems, C. Gérard, A. Delvaux, T. Velu, R. Devos, M. De Boer, and M. Goldman. 1994. B7/CD28-dependent IL-5 production by human resting T cells is inhibited by IL-10. J. Immunol. 152: 4368-4374.
20. Taga, K., H. Mostowski, and G. Tosato. 1993. Human interleukin-10 can directly inhibit T-cell growth. Blood 81: 2964-2971. (Pubitemid 23162114)
21. + T cell clones and resting T cells. Specific inhibition of IL-2 production and proliferation. J. Immunol. 150: 4754-4765.
22. Couper, K. N., D. G. Blount, and E. M. Riley. 2008. IL-10: the master regulator of immunity to infection. J. Immunol. 180: 5771-5777.
23. Graham, B. S., L. A. Bunton, P. F. Wright, and D. T. Karzon. 1991. Role of T lymphocyte subsets in the pathogenesis of primary infection and rechallenge with respiratory syncytial virus in mice. J. Clin. Invest. 88: 1026-1033.
24. Peebles, R. S., Jr., and B. S. Graham. 2005. Pathogenesis of respiratory syncytial virus infection in the murine model. Proc. Am. Thorac. Soc. 2: 110-115.
25. Berg, D. J., N. Davidson, R. Kühn, W. Müller, S. Menon, G. Holland, L. Thompson-Snipes, M. W. Leach, and D. Rennick. 1996. Enterocolitis and colon cancer in interleukin-10-deficient mice are associated with aberrant cytokine production and CD4(+) TH1-like responses. J. Clin. Invest. 98: 1010-1020. (Pubitemid 26293320)
26. Kühn, R., J. Löhler, D. Rennick, K. Rajewsky, and W. Müller. 1993. Interleukin- 10-deficient mice develop chronic enterocolitis. Cell 75: 263-274. (Pubitemid 23320290)
27. Madan, R., F. Demircik, S. Surianarayanan, J. L. Allen, S. Divanovic, A. Trompette, N. Yogev, Y. Gu, M. Khodoun, D. Hildeman, et al. 2009. Nonredundant roles for B cell-derived IL-10 in immune counter-regulation. J. Immunol. 183: 2312-2320.
28. Castilow, E. M., K. L. Legge, and S. M. Varga. 2008. Cutting edge: Eosinophils do not contribute to respiratory syncytial virus vaccine-enhanced disease. J. Immunol. 181: 6692-6696.
29. + CD4 regulatory T cells limit pulmonary immunopathology by modulating the CD8 T cell response during respiratory syncytial virus infection. J. Immunol. 185: 2382-2392.
30. Hamelmann, E., J. Schwarze, K. Takeda, A. Oshiba, G. L. Larsen, C. G. Irvin, and E. W. Gelfand. 1997. Noninvasive measurement of airway responsiveness in allergic mice using barometric plethysmography. Am. J. Respir. Crit. Care Med. 156: 766-775. (Pubitemid 27396413)
31. Fulton, R. B., M. R. Olson, and S. M. Varga. 2008. Regulation of cytokine production by virus-specific CD8 T cells in the lungs. J. Virol. 82: 7799-7811.
32. Olson, M. R., S. M. Hartwig, and S. M. Varga. 2008. The number of respiratory syncytial virus (RSV)-specific memory CD8 T cells in the lung is critical for their ability to inhibit RSV vaccine-enhanced pulmonary eosinophilia. J. Immunol. 181: 7958-7968.
33. Castilow, E. M., D. K. Meyerholz, and S. M. Varga. 2008. IL-13 is required for eosinophil entry into the lung during respiratory syncytial virus vaccineenhanced disease. J. Immunol. 180: 2376-2384.
34. Rai, D., N. L. Pham, J. T. Harty, and V. P. Badovinac. 2009. Tracking the total CD8 T cell response to infection reveals substantial discordance in magnitude and kinetics between inbred and outbred hosts. J. Immunol. 183: 7672-7681.
35. + natural regulatory T cells revealed by DNA microarray analysis. Int. Immunol. 18: 1197-1209.
36. Thornton, A. M., P. E. Korty, D. Q. Tran, E. A. Wohlfert, P. E. Murray, Y. Belkaid, and E. M. Shevach. 2010. Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3+ T regulatory cells. J. Immunol. 184: 3433-3441.
37. + T-cell memory in the respiratory tract. Nat. Med. 8: 54-60.
38. + T cells during experimental virus infection. J. Immunol. 167: 4254-4260.
39. - Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. J. Exp. Med. 204: 285-297.
40. + T cell clones producing both interferon-gamma and interleukin-10 predominate in bronchoalveolar lavages of active pulmonary tuberculosis patients. Clin. Immunol. 92: 224-234.
41. - Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. J. Exp. Med. 204: 273-283.
42. Pohl-Koppe, A., K. E. Balashov, A. C. Steere, E. L. Logigian, and D. A. Hafler. 1998. Identification of a T cell subset capable of both IFN-γ and IL-10 secretion in patients with chronic Borrelia burgdorferi infection. J. Immunol. 160: 1804- 1810.
43. McKinstry, K. K., T. M. Strutt, A. Buck, J. D. Curtis, J. P. Dibble, G. Huston, M. Tighe, H. Hamada, S. Sell, R. W. Dutton, and S. L. Swain. 2009. IL-10 deficiency unleashes an influenza-specific Th17 response and enhances survival against high-dose challenge. J. Immunol. 182: 7353-7363.
44. Maynard, C. L., and C. T. Weaver. 2008. Diversity in the contribution of interleukin-10 to T-cell-mediated immune regulation. Immunol. Rev. 226: 219-233.
45. H 1 cells control themselves by producing interleukin-10. Nat. Rev. Immunol. 7: 425-428.
46. Shaw, M. H., G. J. Freeman, M. F. Scott, B. A. Fox, D. J. Bzik, Y. Belkaid, and G. S. Yap. 2006. Tyk2 negatively regulates adaptive Th1 immunity by mediating IL-10 signaling and promoting IFN-gamma-dependent IL-10 reactivation. J. Immunol. 176: 7263-7271. (Pubitemid 43849026)
47. + effector cells acquire the ability to produce IL-10 as a result of entry into the infected lung environment. Virology 404: 225-230.
48. Sun, J., R. Madan, C. L. Karp, and T. J. Braciale. 2009. Effector T cells control lung inflammation during acute influenza virus infection by producing IL-10. Nat. Med. 15: 277-284.
49. + T cell help and innate-derived IL-27 induce Blimp-1-dependent IL-10 production by antiviral CTLs. Nat. Immunol.12: 327-334.
50. Haeberle, H. A., A. Casola, Z. Gatalica, S. Petronella, H. J. Dieterich, P. B. Ernst, A. R. Brasier, and R. P. Garofalo. 2004. IkappaB kinase is a critical regulator of chemokine expression and lung inflammation in respiratory syncytial virus infection. J. Virol. 78: 2232-2241. (Pubitemid 38228916)
51. Tekkanat, K. K., H. Maassab, A. Miller, A. A. Berlin, S. L. Kunkel, and N. W. Lukacs. 2002. RANTES (CCL5) production during primary respiratory syncytial virus infection exacerbates airway disease. Eur. J. Immunol. 32: 3276-3284. (Pubitemid 35414885)
52. De Jong, M. D., C. P. Simmons, T. T. Thanh, V. M. Hien, G. J. Smith, T. N. Chau, D. M. Hoang, N. V. Chau, T. H. Khanh, V. C. Dong, et al. 2006. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat. Med. 12: 1203-1207. (Pubitemid 44527358)
53. Peiris, J. S., W. C. Yu, C. W. Leung, C. Y. Cheung, W. F. Ng, J. M. Nicholls, T. K. Ng, K. H. Chan, S. T. Lai, W. L. Lim, et al. 2004. Re-emergence of fatal human influenza A subtype H5N1 disease. Lancet 363: 617-619. (Pubitemid 38264181)
54. To, K. F., P. K. Chan, K. F. Chan, W. K. Lee, W. Y. Lam, K. F. Wong, N. L. Tang, D. N. Tsang, R. Y. Sung, T. A. Buckley, et al. 2001. Pathology of fatal human infection associated with avian influenza A H5N1 virus. J. Med. Virol. 63: 242-246.
55. Beigel, J. H., J. Farrar, A. M. Han, F. G. Hayden, R. Hyer, M. D. De Jong, S. Lochindarat, T. K. Nguyen, T. H. Nguyen, T. H. Tran, et al; Writing Committee of the World Health Organization (WHO) Consultation on Human Influenza A/H5. 2005. Avian influenza A (H5N1) infection in humans. N. Engl. J. Med. 353: 1374-1385. (Pubitemid 41362705)
56. Cameron, M. J., L. Ran, L. Xu, A. Danesh, J. F. Bermejo-Martin, C. M. Cameron, M. P. Muller, W. L. Gold, S. E. Richardson, S. M. Poutanen, et al Canadian SARS Research Network. 2007. Interferon-mediated immunopathological events are associated with atypical innate and adaptive immune responses in patients with severe acute respiratory syndrome. J. Virol. 81: 8692-8706. (Pubitemid 47242843)
57. Wong, C. K., C. W. Lam, A. K. Wu, W. K. Ip, N. L. Lee, I. H. Chan, L. C. Lit, D. S. Hui, M. H. Chan, S. S. Chung, and J. J. Sung. 2004. Plasma inflammatory cytokines and chemokines in severe acute respiratory syndrome. Clin. Exp. Immunol. 136: 95-103. (Pubitemid 38437770)
58. Zhang, Y., J. Li, Y. Zhan, L. Wu, X. Yu, W. Zhang, L. Ye, S. Xu, R. Sun, Y. Wang, and J. Lou. 2004. Analysis of serum cytokines in patients with severe acute respiratory syndrome. Infect. Immun. 72: 4410-4415. (Pubitemid 38989297)
59. + natural regulatory T cells are critical in limiting innate and adaptive immunity and resolving disease following respiratory syncytial virus infection. J. Virol. 84: 8790-8798.
60. Murai, M., O. Turovskaya, G. Kim, R. Madan, C. L. Karp, H. Cheroutre, and M. Kronenberg. 2009. Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat. Immunol. 10: 1178-1184.
61. Wilson, J., K. Rowlands, K. Rockett, C. Moore, E. Lockhart, M. Sharland, D. Kwiatkowski, and J. Hull. 2005. Genetic variation at the IL10 gene locus is associated with severity of respiratory syncytial virus bronchiolitis. J. Infect. Dis. 191: 1705-1709. (Pubitemid 40656759)
62. Hoebee, B., L. Bont, E. Rietveld, M. Van Oosten, H. M. Hodemaekers, N. J. Nagelkerke, H. J. Neijens, J. L. Kimpen, and T. G. Kimman. 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. (Pubitemid 38147247)
63. Asadullah, K., W. D. Döcke, M. Ebeling, M. Friedrich, G. Belbe, H. Audring, H. D. Volk, and W. Sterry. 1999. Interleukin 10 treatment of psoriasis: clinical results of a phase 2 trial. Arch. Dermatol. 135: 187-192. (Pubitemid 29098366)
64. Braat, H., P. Rottiers, D. W. Hommes, N. Huyghebaert, E. Remaut, J. P. Remon, S. J. Van Deventer, S. Neirynck, M. P. Peppelenbosch, and L. Steidler. 2006. A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn's disease. Clin. Gastroenterol. Hepatol. 4: 754-759. (Pubitemid 43841860)
65. Fedorak, R. N., A. Gangl, C. O. Elson, P. Rutgeerts, S. Schreiber, G. Wild, S. B. Hanauer, A. Kilian, M. Cohard, A. LeBeaut, and B. Feagan. 2000. Recombinant human interleukin 10 in the treatment of patients with mild to moderately active Crohn's disease. The Interleukin 10 Inflammatory Bowel Disease Cooperative Study Group. Gastroenterology 119: 1473-1482. (Pubitemid 32198672)
66. Nelson, D. R., G. Y. Lauwers, J. Y. Lau, and G. L. Davis. 2000. Interleukin 10 treatment reduces fibrosis in patients with chronic hepatitis C: a pilot trial of interferon nonresponders. Gastroenterology 118: 655-660. (Pubitemid 30171614)
67. Opal, S. M., J. C. Wherry, and P. Grint. 1998. Interleukin-10: potential benefits and possible risks in clinical infectious diseases. Clin. Infect. Dis. 27: 1497-1507. (Pubitemid 29242428)
68. Schreiber, S., R. N. Fedorak, O. H. Nielsen, G. Wild, C. N. Williams, S. Nikolaus, M. Jacyna, B. A. Lashner, A. Gangl, P. Rutgeerts, et al. 2000. Safety and efficacy of recombinant human interleukin 10 in chronic active Crohn's disease. Crohn's Disease IL-10 Cooperative Study Group. Gastroenterology 119: 1461-1472. (Pubitemid 32198671)