The role of IL-10 in immune regulation during M. tuberculosis infection

Mucosal Immunology

Volumn 4, Issue 3, 2011, Pages 261-270

  Redford, P S ^a   Murray, P J ^b   O'Garra, A ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTING CELL; ARTICLE; CELL FUNCTION; CELLULAR IMMUNITY; DISEASE COURSE; HUMAN; IMMUNOPATHOGENESIS; IMMUNOREGULATION; INFECTION RESISTANCE; INNATE IMMUNITY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; TH1 CELL; TUBERCULOSIS;

EID: 79955102870     PISSN: 19330219     EISSN: None     Source Type: Journal    
DOI: 10.1038/mi.2011.7     Document Type: Article

References (167)

1. WHO. World Health Organisation: Global'Tuberculosis Control 2010 http://www.who.int/tb/country/en/index.html (2010).
2. Flynn, J.L. & Chan, J. What's good forthe host is good forthe bug. Trends Microbiol. 13, 98-102 (2005). (Pubitemid 40311891)
3. Ulrichs, T. & Kaufmann, S.H. New insights into the function of granulomas in human tuberculosis. J. Pathol. 208, 261-269 (2006). (Pubitemid 43126118)
4. Davis, J.M. & Ramakrishnan, L. The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell 136, 37-49 (2009).
5. Volkman, H.E., Pozos, T.C., Zheng, J., Davis, J.M., Rawls, J.F. & Ramakrishnan, L. Tuberculous granuloma induction via interaction of a bacterial secreted protein with host epithelium. Science 327, 466-469 (2010).
6. Tobin, D.M. & Ramakrishnan, L. Comparative pathogenesis of Mycobacterium marinum and Mycobacterium tuberculosis. Cell Microbiol. 10, 1027-1039 (2008). (Pubitemid 351540503)
7. Zhang, S.Y. et al. Inborn errors of interferon (IFN)-mediated immunity in humans: insights into the respective roles of IFN-alpha/beta, IFN-gamma, and IFN-lambda in host defense. Immunol. Rev. 226, 29-40 (2008).
8. Altare, F. et al. Impairment of mycobacterial immunity in human interleukin-12 receptor deficiency. Science 280, 1432-1435 (1998). (Pubitemid 28264836)
9. Casanova, J.L. & Abel, L. Genetic dissection of immunity to mycobacteria: the human model. Annu. Rev. Immunol. 20, 581-620 (2002). (Pubitemid 34293435)
10. Dorman, S.E. & Holland, S.M. Interferon-gamma and interleukin-12 pathway defects and human disease. Cytokine Growth Factor Rev. 11, 321-333(2000).
11. Remus, N. et al. Association of IL12RB1 polymorphisms with pulmonary tuberculosis in adults in Morocco. J. Infect. Dis. 190, 580-587 (2004). (Pubitemid 38982099)
12. Newport, M.J., Awomoyi, A.A. & Blackwell, J.M. Polymorphism in the interferon-gamma receptor-1 gene and susceptibility to pulmonary tuberculosis in The Gambia. Scand. J. Immunol. 58, 383-385 (2003). (Pubitemid 37215050)
13. Jouanguy, E. et al. Partial interferon-gamma receptor 1 deficiency in a child with tuberculoid bacillus Calmette-Guerin infection and a sibling with clinical tuberculosis. J. Clin. Invest. 100, 2658-2664 (1997). (Pubitemid 28007532)
14. Jouanguy, E. et al. A human IFNGR1 small deletion hotspot associated with dominant susceptibility to mycobacterial infection. Nat. Genet. 21, 370-378(1999). (Pubitemid 29159572)
15. Dorman, S.E. & Holland, S.M. Mutation in the signal-transducing chain of the interferon-gamma receptor and susceptibility to mycobacterial infection. J. Clin. Invest. 101, 2364-2369 (1998). (Pubitemid 28270430)
16. Dupuis, S. et al. Impairment of mycobacterial but not viral immunity by a germline human STAT1 mutation. Science 293, 300-303 (2001). (Pubitemid 32694746)
17. Holland, S.M. Interferon gamma, IL-12, IL-12R and STAT-1 immunodeficiency diseases: disorders of the interface of innate and adaptive immunity. Immunol. Res. 38, 342-346 (2007). (Pubitemid 47574918)
18. Dorman, S. E. et al. Clinical features of dominant and recessive interferon gamma receptor 1 deficiencies. Lancet 364, 2113-2121 (2004). (Pubitemid 39626807)
19. Selwyn, P.A. et al. A prospective study of the risk of tuberculosis among intravenous drug users with human immunodeficiency virus infection. N. Engl. J. Med. 320, 545-550 (1989). (Pubitemid 19070537)
20. Post, F.A., Wood, R. & Pillay, G.P. Pulmonary tuberculosis in HIV infection: radiographic appearance is related to CD4+ T-lymphocyte count. Tuber. Lung Dis. 76, 518-521 (1995). (Pubitemid 26008707)
21. Nunn, P., Williams, B., Floyd, K., Dye, C., Elzinga, G. & Raviglione, M. Tuberculosis control in the era of HIV Nat. Rev. Immunol. 5, 819-826 (2005). (Pubitemid 41400855)
22. Diedrich, C.R. et al. Reactivation of latent tuberculosis in cynomolgus macaques infected with SIV is associated with early peripheral T cell depletion and not virus load. PLoS One 5, e9611 (2010).
23. Caruso, A.M., Serbina, N., Klein, E., Triebold, K., Bloom, B.R. & Flynn, J.L. Mice deficient in CD4T cells have only transiently diminished levels of IFN-gamma, yet succumb to tuberculosis. J. Immunol. 162, 5407-5416 (1999). (Pubitemid 29307149)
24. Mogues, T., Goodrich, M.E., Ryan, L., LaCourse, R. & North, R.J. The relative importance of T cell subsets in immunity and immunopathology of airborne Mycobacterium tuberculosis infection in mice. J. Exp. Med. 193, 271-280(2001). (Pubitemid 32524511)
25. Scanga, C.A. et al. Depletion of CD4(+) T cells causes reactivation of murine persistent tuberculosis despite continued expression of interferon gamma and nitric oxide synthase 2. J. Exp. Med. 192, 347-358 (2000). (Pubitemid 30629160)
26. Keane, J. et al. Tuberculosis associated with infliximab, a tumor necrosis factor alpha-neutralizing agent. N. Engl. J. Med. 345, 1098-1104 (2001).
27. Lin, P.L. et al. Tumor necrosis factor neutralization results in disseminated disease in acute and latent Mycobacterium tuberculosis infection with normal granuloma structure in a cynomolgus macaque model. Arthritis Rheum. 62, 340-350 (2010).
28. Mohan, V.P. et al. Effects of tumor necrosis factor alpha on host immune response in chronic persistent tuberculosis: possible role for limiting pathology. Infect. Immun. 69, 1847-1855 (2001). (Pubitemid 32187645)
29. Scanga, C.A., Mohan, V.P., Joseph, H., Yu, K., Chan, J. & Flynn, J.L. Reactivation of latent tuberculosis: variations on the Cornell murine model. Infect. Immun. 67, 4531-4538 (1999). (Pubitemid 29400429)
30. Cooper, A.M., Dalton, D.K., Stewart, T.A., Griffin, J.P., Russell, D.G. & Orme, I.M. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J. Exp. Med. 178, 2243-2247 (1993). (Pubitemid 23344885)
31. Flynn, J.L, Chan, J., Triebold, K.J., Dalton, D.K., Stewart, T.A. & Bloom, B.R. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J. Exp. Med. 178, 2249-2254 (1993). (Pubitemid 23344886)
32. Cooper, A.M., Magram, J., Ferrante, J. & Orme, I.M. Interleukin 12 (IL-12) is crucial to the development of protective immunity in mice intravenously infected with mycobacterium tuberculosis. J. Exp. Med. 186, 39-45(1997). (Pubitemid 27304845)
33. Cooper, A.M., Roberts, A.D., Rhoades, E.R., Callahan, J.E., Getzy, D.M. & Orme, I.M. The role of interleukin-12 in acquired immunity to Mycobacterium tuberculosis infection. Immunology 84, 423-432 (1995).
34. Flynn, J.L., Goldstein, M.M., Triebold, K.J., Sypek, J., Wolf, S. & Bloom, B.R. IL-12 increases resistance of BALB/c mice to Mycobacterium tuberculosis infection. J. Immunol. 155, 2515-2524 (1995).
35. Bean, A.G. et al. Structural deficiencies in granuloma formation in TNF gene-targeted mice underlie the heightened susceptibility to aerosol Mycobacterium tuberculosis infection, which is not compensated for by lymphotoxin. J. Immunol. 162, 3504-3511 (1999). (Pubitemid 29313602)
36. Flynn, J.L. et al. Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 2, 561-572 (1995).
37. Fiorentino, D.F, Bond, M.W. & Mosmann, T.R. 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 (1989).
38. Moore, K.W., de Waal Malefyt, R., Coffman, R.L. & O'Garra, A. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19, 683-765(2001). (Pubitemid 32368050)
39. Saraiva, M. & O'Garra, A. The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 10, 170-181 (2010).
40. O'Garra, A., Vieira, P.L., Vieira, P. & Goldfeld, A.E. IL-10-producing and naturally occurring CD4+ Tregs: limiting collateral damage. J. Clin. Invest. 114, 1372-1378 (2004). (Pubitemid 40385564)
41. Belkaid, Y. & Chen, W. Regulatory ripples. Nat. Immunol. 11, 1077-1078 (2010).
42. Barnes, M.J. & Powrie, F. Regulatory T cells reinforce intestinal homeostasis. Immunity 31, 401-411 (2009).
43. Scott-Browne, J.P. et al. Expansion and function of Foxp3-expressing T regulatory cells during tuberculosis. J. Exp. Med. 204, 2159-2169 (2007). (Pubitemid 47360876)
44. Shafiani, S., Tucker-Heard, G., Kariyone, A., Takatsu, K. & Urdahl, K.B. Pathogen-specific regulatory T cells delay the arrival of effector T cells in the lung during early tuberculosis. J. Exp. Med. 207, 1409-1420 (2010).
45. Anderson, C.F., Oukka, M., Kuchroo, V.J. & Sacks, D. CD4(+)CD25(-) Foxp3(-)Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. J. Exp. Med. 204, 285-297 (2007). (Pubitemid 46294545)
46. Jankovic, D. et al. Conventional T-bet(+)Foxp3(-)Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. J. Exp. Med. 204, 273-283 (2007). (Pubitemid 46294544)
47. Williams, L., Bradley, L., Smith, A. & Foxwell, B. Signal transducer and activator of transcription 3 is the dominant mediator of the antiinflammatory effects of IL-10 in human macrophages. J. Immunol. 172, 567-576 (2004). (Pubitemid 38020514)
48. ElKasmi, K.C. et al. General nature of the STAT3-activated antiinflammatory response. J. Immunol. 177, 7880-7888 (2006). (Pubitemid 44846303)
49. Holland, S.M. et al. STAT3 mutations in the hyper-IgE syndrome. N Engl. J. Med. 357, 1608-1619 (2007). (Pubitemid 47598403)
50. Kaiser, F. et al. TPL-2 negatively regulates interferon-beta production in macrophages and myeloid dendritic cells. J. Exp. Med. 206, 1863-1871 (2009).
51. Boonstra, A. et al. Macrophages and myeloid dendritic cells, but not plasmacytoid dendritic cells, produce IL-10 in response to MyD88- and TRIF-dependent TLR signals, and TLR-independent signals. J. Immunol. 177, 7551-7558(2006). (Pubitemid 44846270)
52. Chang, E.Y, Guo, B., Doyle, S.E. & Cheng, G. Cutting edge: involvement of the type IIFN production and signaling pathway in lipopolysaccharide-induced IL-10 production. J. Immunol. 178, 6705-6709 (2007). (Pubitemid 46847391)
53. Iyer, S.S., Ghaffari, A.A. & Cheng, G. Lipopolysaccharide-mediated IL-10 transcriptional regulation requires sequential induction of type I IFNs and IL-27 in macrophages. J. Immunol. 185, 6599-6607 (2010).
54. Fremond, C.M., Yeremeev, V., Nicolle, D.M., Jacobs, M., Quesniaux, V.F. & Ryffel, B. Fatal Mycobacterium tuberculosis infection despite adaptive immune response in the absence of MyD88. J. Clin. Invest. 114, 1790-1799(2004). (Pubitemid 40385535)
55. Scanga, C.A., Bafica, A., Feng, C.G., Cheever, A.W., Hieny, S. & Sher, A. MyD88-deficient mice display a profound loss in resistance to Mycobacterium tuberculosis associated with partially impaired Th1 cytokine and nitric oxide synthase 2 expression. Infect. Immun. 72, 2400-2404 (2004). (Pubitemid 38419959)
56. Reiling, N., Ehlers, S. & Holscher, C. MyDths and un-TOLLed truths: sensor, instructive and effector immunity to tuberculosis. Immunol. Lett. 116, 15-23(2008).
57. Mayer-Barber, K.D. et al. Caspase-1 independent IL-1beta production is critical for host resistance to mycobacterium tuberculosis and does not require TLR signaling in vivo. J. Immunol. 184, 3326-3330 (2010).
58. Rogers, N.C. et al. Syk-dependent cytokine induction by Dectin-1 reveals a novel pattern recognition pathway for C type lectins. Immunity 22, 507-517 (2005). (Pubitemid 40545115)
59. Dorhoi, A. et al. The adaptor molecule CARD9 is essential for tuberculosis control. J. Exp. Med. 207, 777-792 (2010).
60. Zhang, X., Majlessi, L., Deriaud, E., Leclerc, C. & Lo-Man, R. Coactivation of syk kinase and MyD88 adaptor protein pathways by bacteria promotes regulatory properties of neutrophils. Immunity 31, 761-771 (2009).
61. Geijtenbeek, T.B. et al. Mycobacteria target DC-SIGN to suppress dendritic cell function. J. Exp. Med. 197, 7-17 (2003). (Pubitemid 36110253)
62. Gerber, J.S. & Mosser, D.M. Reversing lipopolysaccharide toxicity by ligating the macrophage Fc gamma receptors. J. Immunol. 166, 6861-6868(2001). (Pubitemid 32467232)
63. Edwards, A.D. et al. Microbial recognition via Toll-like receptor-dependent and -independent pathways determines the cytokine response of murine dendritic cell subsets to CD40 triggering. J. Immunol. 169, 3652-3660 (2002).
64. Saraiva, M., Christensen, J.R., Veldhoen, M., Murphy, T.L., Murphy, K.M. & O'Garra, A. Interleukin-10 production by Th1 cells requires interleukin-12-induced STAT4 transcription factor and ERK MAP kinase activation by high antigen dose. Immunity 31, 209-219 (2009).
65. Fiorentino, D.F, Zlotnik, A., Mosmann, T.R., Howard, M. & O'Garra, A. IL-10 inhibits cytokine production by activated macrophages. J. Immunol. 147, 3815-3822 (1991).
66. Fiorentino, D.F. et al. IL-10 acts on the antigen-presenting cell to inhibit cytokine production by Th1 cells. J. Immunol. 146, 3444-3451 (1991).
67. Gazzinelli, R.T., Oswald, I.P., James, S.L. & Sher, A. IL-10 inhibits parasite killing and nitrogen oxide production by IFN-gamma-activated macrophages. J. Immunol. 148, 1792-1796 (1992).
68. Redpath, S., Ghazal, P. & Gascoigne, N.R. Hijacking and exploitation of IL-10 by intracellular pathogens. Trends Microbiol. 9, 86-92 (2001). (Pubitemid 32155327)
69. Barrat, F.J. et al. In vitro generation of interleukin 10-producing regulatory CD4(+) T cells is induced by immunosuppressive drugs and inhibited by T helper type 1 (Th1)- and Th2-inducing cytokines. J. Exp. Med. 195, 603-616(2002). (Pubitemid 34461505)
70. Murai, M. et al. 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 (2009).
71. Pils, M.C. et al. Monocytes/macrophages and/or neutrophils are the target of IL-10 in the LPS endotoxemia model. Eur. J. Immunol. 40, 443-448(2010).
72. Kuhn, R., Lohler, J., Rennick, D., Rajewsky K. & Muller, W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75, 263-274(1993). (Pubitemid 23320290)
73. Sellon, R.K. et al. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect. Immun. 66, 5224-5231 (1998). (Pubitemid 29044613)
74. Dai, W.J., Kohler, G. & Brombacher, F. Both innate and acquired immunity to Listeria monocytogenes infection are increased in IL-10-deficient mice. J. Immunol. 158, 2259-2267 (1997). (Pubitemid 127470010)
75. Silva, R.A. & Appelberg, R. Blocking the receptor for interleukin 10 protects mice from lethal listeriosis. Antimicrob. Agents Chemother. 45, 1312-1314(2001). (Pubitemid 32231020)
76. Wagner, R.D., Maroushek, N.M., Brown, J.F. & Czuprynski, C.J. Treatment with anti-interleukin-10 monoclonal antibody enhances early resistance to but impairs complete clearance of Listeria monocytogenes infection in mice. Infect. Immun. 62, 2345-2353 (1994). (Pubitemid 24157062)
77. Brooks, D.G., Trifilo, M.J., Edelmann, K.H., Teyton, L., McGavern, D.B. & Oldstone, M.B. Interleukin-10 determines viral clearance or persistence in vivo. Nat. Med. 12, 1301-1309 (2006). (Pubitemid 44706933)
78. Brooks, D.G., Lee, A.M., Elsaesser, H., McGavern, D.B. & Oldstone, M.B. IL-10 blockade facilitates DNA vaccine-induced T cell responses and enhances clearance of persistent virus infection. J. Exp. Med. 205, 533-541 (2008). (Pubitemid 351439301)
79. Belkaid, Y. et al. 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(2001). (Pubitemid 33081524)
80. Belkaid, Y., Piccirillo, C.A., Mendez, S., Shevach, E.M. & Sacks, D.L. CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 420, 502-507 (2002). (Pubitemid 35477041)
81. Murray, H.W. et al. Interleukin-10 (IL-10) in experimental visceral leishmaniasis and IL-10 receptor blockade as immunotherapy. Infect. Immun. 70, 6284-6293 (2002). (Pubitemid 35192720)
82. Mege, J.L, Meghari, S., Honstettre, A., Capo, C. & Raoult, D. The two faces of interleukin 10 in human infectious diseases. Lancet Infect. Dis. 6, 557-569 (2006). (Pubitemid 44262343)
83. Gazzinelli, R.J. et al. In the absence of endogenous IL-10, mice acutely infected with Toxoplasma gondii succumb to a lethal immune response dependent on CD4+ T cells and accompanied by overproduction of IL-12, IFN-gamma and TNF-alpha. J. Immunol. 157, 798-805 (1996).
84. Reise Sousa, C. et al. Paralysis of dendritic cell IL-12 production by microbial products prevents infection-induced immunopathology Immunity 11, 637-647 (1999).
85. Suzuki, Y. et al. IL-10 is required for prevention of necrosis in the small intestine and mortality in both genetically resistant BALB/c and susceptible C57BL/6 mice following peroral infection with Toxoplasma gondii. J. Immunol. 164, 5375-5382 (2000). (Pubitemid 30305218)
86. Hunter, C.A. et al. IL-10 is required to prevent immune hyperactivity during infection with Trypanosoma cruzi. J. Immunol. 158, 3311-3316 (1997). (Pubitemid 127484048)
87. Li, C., Corraliza, I. & Langhorne, J. A defect in interleukin-10 leads to enhanced malarial disease in Plasmodium chabaudi chabaudi infection in mice. Infect. Immun. 67, 4435-4442 (1999). (Pubitemid 29400417)
88. Shaw, T.C., Thomas, L.H. & Friedland, J.S. Regulation of IL-10 secretion after phagocytosis of Mycobacterium tuberculosis by human monocytic cells. Cytokine 12, 483-486 (2000). (Pubitemid 30449847)
89. Giacomini, E. et al. Infection of human macrophages and dendritic cells with Mycobacterium tuberculosis induces a differential cytokine gene expression that modulates T cell response. J. Immunol. 166, 7033-7041 (2001). (Pubitemid 32525572)
90. Bodnar, K.A., Serbina, N.V. & Flynn, J.L. Fate of Mycobacterium tuberculosis within murine dendritic cells. Infect. Immun. 69, 800-809 (2001). (Pubitemid 32109542)
91. Hickman, S.P., Chan, J. & Salgame, P. Mycobacterium tuberculosis induces differential cytokine production from dendritic cells and macrophages with divergent effects on naive T cell polarization. J. Immunol. 168, 4636-4642 (2002). (Pubitemid 34441370)
92. Armstrong, J. A. & Hart, P.D. Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes. J. Exp. Med. 134, 713-740 (1971).
93. Sturgill-Koszycki, S., Schaible, U.E. & Russell, D.G. Mycobacterium-containing phagosomes are accessible to early endosomes and reflect a transitional state in normal phagosome biogenesis. EMBO J. 15, 6960-6968(1996). (Pubitemid 27023267)
94. Collins, H.L., Kaufmann, S.H. & Schaible, U.E. Iron chelation via deferoxamine exacerbates experimental salmonellosis via inhibition of the nicotinamide adenine dinucleotide phosphate oxidase-dependent respiratory burst. J. Immunol. 168, 3458-3463 (2002). (Pubitemid 34250411)
95. O'Leary, S., O'Sullivan, M.P. & Keane, J. IL-10 blocks phagosome maturation in Mycobacterium tuberculosis-infected human macrophages. Am. J. Respir. Cell Mol. Biol. doi:10.1165/rcmb.2010-03190C (2010).
96. Chan, J., Tanaka, K., Carroll, D., Flynn, J. & Bloom, B.R. Effects of nitric oxide synthase inhibitors on murine infection with Mycobacterium tuberculosis. Infect. Immun. 63, 736-740 (1995).
97. Chan, J., Xing, Y., Magliozzo, R.S. & Bloom, B.R. Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages. J. Exp. Med. 175, 1111-1122(1992).
98. Flynn, J.L., Scanga, C.A., Tanaka, K.E. & Chan, J. Effects of aminoguanidine on latent murine tuberculosis. J. Immunol. 160, 1796-1803(1998). (Pubitemid 28106466)
99. MacMicking, J.D., North, R.J., LaCourse, R., Mudgett, J.S., Shah, S.K. & Nathan, C.F. Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc. Natl. Acad. Sci. USA 94, 5243-5248 (1997). (Pubitemid 27214768)
100. Shi, S. et al. MyD88 primes macrophages for full-scale activation by interferon-gamma yet mediates few responses to Mycobacterium tuberculosis. J. Exp. Med. 198, 987-997 (2003). (Pubitemid 37248615)
101. Murray, P. J., Wang, L., Onufryk, C., Tepper, R.I. & Young, R.A. T cell-derived IL-10 antagonizes macrophage function in mycobacterial infection. J. Immunol. 158, 315-321 (1997). (Pubitemid 127483871)
102. Schreiber, T. et al. Autocrine IL-10 induces hallmarks of alternative activation in macrophages and suppresses antituberculosis effector mechanisms without compromising T cell immunity. J. Immunol. 183, 1301-1312(2009).
103. Garcia-Romo, G.S. et al. Airways infection with virulent Mycobacterium tuberculosis delays the influx of dendritic cells and the expression of costimulatory molecules in mediastinal lymph nodes. Immunology 112, 661-668(2004). (Pubitemid 39061492)
104. Wolf, A.J. et al. Mycobacterium tuberculosis infects dendritic cells with high frequency and impairs their function in vivo. J. Immunol. 179, 2509-2519(2007).
105. Tailleux, L et al. Constrained intracellular survival of Mycobacterium tuberculosis in human dendritic cells. J. Immunol. 170, 1939-1948 (2003). (Pubitemid 36197413)
106. Khader, S.A. et al. Interleukin 12p40 is required for dendritic cell migration and T cell priming after Mycobacterium tuberculosis infection. J. Exp. Med. 203, 1805-1815 (2006). (Pubitemid 44036285)
107. Demangel, C., Bertolino, P. & Britton, W.J. Autocrine IL-10 impairs dendritic cell (DC)-derived immune responses to mycobacterial infection by suppressing DC trafficking to draining lymph nodes and local IL-12 production. Eur. J. Immunol. 32, 994-1002 (2002). (Pubitemid 34428814)
108. Reiley W.W. et al. ESAT-6-specific CD4T cell responses to aerosol Mycobacterium tuberculosis infection are initiated in the mediastinal lymph nodes. Proc. Natl. Acad. Sci. USA 105, 10961-10966 (2008).
109. Wolf, A.J. et al. Initiation of the adaptive immune response to Mycobacterium tuberculosis depends on antigen production in the local lymph node, not the lungs. J. Exp. Med. 205, 105-115 (2008). (Pubitemid 351185719)
110. Redford, RS. et al. Enhanced protection to Mycobacterium tuberculosis infection in IL-10-deficient mice is accompanied by early and enhanced Th1 responses in the lung. Eur. J. Immunol. 40, 2200-2210 (2010).
111. Tian, T., Woodworth, J., Skold, M. & Behar, S.M. In vivo depletion of CD11C+ cells delays the CD4+ T cell response to Mycobacterium tuberculosis and exacerbates the outcome of infection. J. Immunol. 175, 3268-3272 (2005). (Pubitemid 41170548)
112. Barnes, P.F., Lu, S., Abrams, J.S., Wang, E., Yamamura, M. & Modlin, R.L. Cytokine production at the site of disease in human tuberculosis. Infect. Immun. 61, 3482-3489 (1993). (Pubitemid 23223442)
113. Huard, R.C. et al. The Mycobacterium tuberculosis complex-restricted gene cfp32 encodes an expressed protein that is detectable in tuberculosis patients and is positively correlated with pulmonary interleukin-10. Infect. Immun. 71, 6871-6883 (2003). (Pubitemid 37475317)
114. Almeida, A.S. et al. Tuberculosis is associated with a down-modulatory lung immune response that impairs Th1 -type immunity. J. Immunol. 183, 718-731 (2009).
115. Verbon, A., Juffermans, N., Van Deventer, S.J., Speelman, P., Van Deutekom, H. & Van Der Poll, T. Serum concentrations of cytokines in patients with active tuberculosis (TB) and after treatment. Clin. Exp. Immunol. 115, 110-113(1999). (Pubitemid 29030371)
116. Zhang, M., Gong, J., Iyer, D.V, Jones, B.E., Modlin, R.L. & Barnes, P.F. T cell cytokine responses in persons with tuberculosis and human immunodeficiency virus infection. J. Clin. Invest. 94, 2435-2442 (1994). (Pubitemid 24379619)
117. Gong, J.H. et al. Interleukin-10 downregulates Mycobacterium tuberculosis-induced Th1 responses and CTLA-4 expression. Infect. Immun. 64, 913-918(1996).
118. Boussiotis, V.A. et al. IL-10-producing T cells suppress immune responses in anergic tuberculosis patients. J. Clin. Invest. 105, 1317-1325(2000). (Pubitemid 30266085)
119. Bonecini-Almeida, M.G. et al. Down-modulation of lung immune responses by interleukin-10 and transforming growth factor beta (TGF-beta) and analysis of TGF-beta receptors I and II in active tuberculosis. Infect. Immun. 72, 2628-2634 (2004). (Pubitemid 38542389)
120. Rojas, R.E., Balaji, K.N., Subramanian, A. & Boom, W.H. Regulation of human CD4(+) alphabeta T-cell-receptor-positive (TCR(+)) and gammadelta TCR(+) T-cell responses to Mycobacterium tuberculosis by interleukin-10 and transforming growth factor beta. Infect. Immun. 67, 6461-6472(1999).
121. Gerosa, F. et al. CD4(+) T cell clones producing both interferon-gamma and interleukin-10 predominate in bronchoalveolar lavages of active pulmonary tuberculosis patients. Clin. Immunol. 92, 224-234 (1999). (Pubitemid 29439669)
122. Turner, J. et al. In vivo IL-10 production reactivates chronic pulmonary tuberculosis in C57BL/6 mice. J. Immunol. 169, 6343-6351 (2002). (Pubitemid 36903482)
123. Awomoyi, A.A., Marchant, A., Howson, J.M., McAdam, K.P., Blackwell, J.M. & Newport, M.J. Interleukin-10, polymorphism in SLC11A1 (formerly NRAMP1), and susceptibility to tuberculosis. J. Infect. Dis. 186, 1808-1814(2002). (Pubitemid 35463514)
124. Quails, J.E. et al. Arginine usage in mycobacteria-infected macrophages depends on autocrine-paracrine cytokine signaling. Sci. Signal. 3, ra62 (2010).
125. Bellamy, R., Ruwende, C., Corrah, T, McAdam, K.P., Whittle, H.C. & Hill, A.V. Assessment of the interleukin 1 gene cluster and other candidate gene polymorphisms in host susceptibility to tuberculosis. Tuber. Lung Dis. 79, 83-89(1998). (Pubitemid 29078276)
126. Delgado, J.C., Baena, A., Thim, S. & Goldfeld, A.E. Ethnic-specific genetic associations with pulmonary tuberculosis. J. Infect. Dis. 186, 1463-1468(2002). (Pubitemid 35286114)
127. Lopez-Maderuelo, D. et al. Interferon-gamma and interleukin-10 gene polymorphisms in pulmonary tuberculosis. Am. J. Respir. Crit. Care Med. 167, 970-975(2003). (Pubitemid 36408162)
128. Fitness, J. et al. Large-scale candidate gene study of tuberculosis susceptibility in the Karonga district of northern Malawi. Am. J. Trop. Med. Hyg. 71, 341-349 (2004). (Pubitemid 39223512)
129. Shin, H.D., Park, B.L, Kim, Y.H., Cheong, H.S., Lee, I.H. & Park, S.K. Common interleukin 10 polymorphism associated with decreased risk of tuberculosis. Exp. Mol. Med. 37, 128-132 (2005). (Pubitemid 40676922)
130. Henao, M.I., Montes, C., Paris, S.C. & Garcia, L.F. Cytokine gene polymorphisms in Colombian patients with different clinical presentations oftuberculosis. Tuberculosis (Edinb) 86, 11-19 (2006). (Pubitemid 41797654)
131. Oral, H.B. et al. Interleukin-10 (IL-10) gene polymorphism as a potential host susceptibility factor in tuberculosis. Cytokine 35, 143-147 (2006). (Pubitemid 44666429)
132. Oh, J.H. et al. Polymorphisms of interleukin-10 and tumour necrosis factor-alpha genes are associated with newly diagnosed and recurrent pulmonary tuberculosis. Respirology 12, 594-598 (2007).
133. Prabhu Anand, S., Selvaraj, P., Jawahar, M.S., Adhilakshmi, A.R. & Narayanan, P.R. Interleukin-12B & interleukin-10 gene polymorphisms in pulmonary tuberculosis. Indian J. Med. Res. 126, 135-138 (2007). (Pubitemid 350028047)
134. Ates, O., Musellim, B., Ongen, G. & Topal-Sarikaya, A. Interleukin-10 and tumor necrosis factor-alpha gene polymorphisms in tuberculosis. J. Clin. Immunol. 28, 232-236 (2008).
135. Pacheco, A.G., Cardoso, C.C. & Moraes, M.O. IFNG+874T/A, IL10-1082G/A and TNF -308G/A polymorphisms in association with tuberculosis susceptibility: a meta-analysis study. Hum. Genet. 123, 477-484 (2008).
136. Bermudez, L.E. & Champsi, J. Infection with Mycobacterium avium induces production of interleukin-10 (IL-10), and administration of anti-IL-10 antibody is associated with enhanced resistance to infection in mice. Infect. Immun. 61, 3093-3097 (1993). (Pubitemid 23182316)
137. Roach, D.R., Martin, E., Bean, A.G., Rennick, D.M., Briscoe, H. & Britton, W.J. Endogenous inhibition of antimycobacterial immunity by IL-10 varies between mycobacterial species. Scand. J. Immunol. 54, 163-170(2001). (Pubitemid 32592342)
138. Roque, S., Nobrega, C., Appelberg, R. & Correia-Neves, M. IL-10 underlies distinct susceptibility of BALB/c and C57BL/6 mice to Mycobacterium avium infection and influences efficacy of antibiotic therapy. J. Immunol. 178, 8028-8035 (2007). (Pubitemid 46898074)
139. Murray, P.J. & Young, R.A. Increased antimycobacterial immunity in interleukin-10-deficient mice. Infect. Immun. 67, 3087-3095 (1999). (Pubitemid 29244734)
140. Jacobs, M., Brown, N., Allie, N., Gulert, R. & Ryffel, B. Increased resistance to mycobacterial infection in the absence of interleukin-10. Immunology 100, 494-501 (2000). (Pubitemid 30608503)
141. Jacobs, M., Fick, L., Allie, N., Brown, N. & Ryffel, B. Enhanced immune response in Mycobacterium bovis Bacille Calmette Guerin (BCG)-infected IL-10-deficient mice. Clin. Chem. Lab. Med. 40, 893-902 (2002). (Pubitemid 35277415)
142. Roberts, M.T, Stober, C.B., McKenzie, A.N. & Blackwell, J.M. Interleukin-4 (IL-4) and IL-10 collude in vaccine failure for novel exacerbatory antigens in murine Leishmania major infection. Infect. Immun. 73, 7620-7628 (2005). (Pubitemid 41587668)
143. Stober, C.B., Lange, U.G., Roberts, M.T., Alcami, A. & Blackwell, J.M. IL-10 from regulatory T cells determines vaccine efficacy in murine Leishmania major infection. J. Immunol. 175, 2517-2524 (2005). (Pubitemid 41113863)
144. Tabbara, K.S. et al. Conditions influencing the efficacy of vaccination with live organisms against Leishmania major infection. Infect. Immun. 73, 4714-4722(2005). (Pubitemid 41105627)
145. Silva, R.A., Pais, T.F. & Appelberg, R. Blocking the receptor for IL-10 improves antimycobacterial chemotherapy and vaccination. J. Immunol. 167, 1535-1541 (2001). (Pubitemid 32703153)
146. O'Garra, A., Barrat, F.J., Castro, A.G., Vicari, A. & Hawrylowicz, C. Strategies for use of IL-10 or its antagonists in human disease. Immunol. Rev. 223, 114-131 (2008). (Pubitemid 351986180)
147. Jung, Y.J., Ryan, L., LaCourse, R. & North, R.J. Increased interleukin-10 expression is not responsible for failure of T helper 1 immunity to resolve airborne Mycobacterium tuberculosis infection in mice. Immunology 109, 295-299(2003). (Pubitemid 36683621)
148. North, R.J. Mice incapable of making IL-4 or IL-10 display normal resistance to infection with Mycobacterium tuberculosis. Clin. Exp. Immunol. 113, 55-58 (1998). (Pubitemid 28329065)
149. Higgins, D.M., Sanchez-Campillo, J., Rosas-Taraco, A.G., Lee, E.J., Orme, I.M. & Gonzalez-Juarrero, M. Lack of IL-10 alters inflammatory and immune responses during pulmonary Mycobacterium tuberculosis infection. Tuberculosis (Edinb) 89, 149-157 (2009).
150. Rosas-Taraco, A.G., Higgins, D.M., Sanchez-Campillo, J., Lee, E.J., Orme, I.M. & Gonzalez-Juarrero, M. Local pulmonary immunotherapy with siRNA targeting TGFbetal enhances antimicrobial capacity in Mycobacterium tuberculosis infected mice. Tuberculosis (Edinb) 91, 98-106(2010).
151. Beamer, G.L. et al. Interleukin-10 promotes Mycobacterium tuberculosis disease progression in CBA/J mice. J. Immunol. 181, 5545-5550 (2008).
152. Yahagi, A. et al. Suppressed induction of mycobacterial antigen-specific Th1 -type CD4+ T cells in the lung after pulmonary mycobacterial infection. Int. Immunol. 22, 307-318 (2010).
153. Ioerger, T. R. et al. Variation among genome sequences of H37Rv strains of Mycobacterium tuberculosis from multiple laboratories. J. Bacteriol. 192, 3645-3653(2010).
154. Manca, C. et al. Virulence of a Mycobacterium tuberculosis clinical isolate in mice is determined by failure to induce Th1 type immunity and is associated with induction of IFN-alpha/beta. Proc. Natl. Acad. Sci. USA 98, 5752-5757 (2001). (Pubitemid 32435714)
155. Reed, M.B. et al. A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 431, 84-87 (2004). (Pubitemid 39215112)
156. Manca, C. et al. Hypervirulent M. tuberculosis W/Beijing strains upregulate type I IFNs and increase expression of negative regulators of the Jak-Stat pathway. J. Interferon Cytokine Res. 25, 694-701 (2005). (Pubitemid 43010524)
157. Ordway D. et al. The hypervirulent Mycobacterium tuberculosis strain HN878 induces a potent TH1 response followed by rapid down-regulation. J. Immunol. 179, 522-531 (2007). (Pubitemid 46986569)
158. Newton, S.M. et al. A deletion defining a common Asian lineage of Mycobacterium tuberculosis associates with immune subversion. Proc. Natl. Acad. Sci. USA 103, 15594-15598 (2006). (Pubitemid 44625637)
159. Torrado, E. & Cooper, A.M. IL-17 and Th17 cells in tuberculosis. Cytokine Growth Factor Rev. 21, 455-462 (2010).
160. Eruslanov, E.B. et al. Neutrophil responses to Mycobacterium tuberculosis infection in genetically susceptible and resistant mice. Infect. Immun. 73, 1744-1753 (2005). (Pubitemid 40470763)
161. Keller, C., Hoffmann, R., Lang, R., Brandau, S., Hermann, C. & Ehlers, S. Genetically determined susceptibility to tuberculosis in mice causally involves accelerated and enhanced recruitment of granulocytes. Infect. Immun. 74, 4295-4309 (2006). (Pubitemid 43993363)
162. Cruz, A. et al. Pathological role of interleukin 17 in mice subjected to repeated BCG vaccination after infection with Mycobacterium tuberculosis. J. Exp. Med. 207, 1609-1616 (2010).
163. Aujla, S.J., Dubin, P.J. & Kolls, J.K. Th17 cells and mucosal host defense. Semin. Immunol. 19, 377-382 (2007). (Pubitemid 351274047)
164. Aujla, S.J. et al. IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nat. Med. 14, 275-281 (2008). (Pubitemid 351347908)
165. Okamoto Yoshida, Y. et al. Essential role of IL-17A in the formation of a mycobacterial infection-induced granuloma in the lung. J. Immunol. 184, 4414-4422(2010).
166. Khader, S.A. et al. IL-23and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat. Immunol. 8, 369-377 (2007). (Pubitemid 46745412)
167. Khader, S.A. & Cooper, A.M. IL-23 and IL-17 in tuberculosis. Cytokine 41, 79-83(2008).