Regulatory CD4+ CD25+ T cells dampen inflammatory disease in murine mycoplasma pneumonia and promote IL-17 and IFN-γ Responses

PLoS ONE

Volumn 11, Issue 5, 2016, Pages

  Odeh, Adam N ^a   Simecka, Jerry W ^a  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 4; TRANSFORMING GROWTH FACTOR BETA; CYTOKINE; INTERLEUKIN 2 RECEPTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; BAGG ALBINO MOUSE; CD25+ T LYMPHOCYTE; CD4+ CD25+ FOXP3+ REGULATORY T CELL; CD4+ CD25+ REGULATORY T CELL; CD4+ CD25+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DEPLETION; DISEASE SEVERITY; FEMALE; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LYMPH NODE; LYMPHOCYTE SUBPOPULATION; LYMPHOCYTIC INFILTRATION; MOUSE; MYCOPLASMA PNEUMONIA; NONHUMAN; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; TH2 CELL; ANIMAL; ANTIBODY PRODUCTION; BLOOD; COMPLICATION; IMMUNOLOGY; LUNG; LYMPHOCYTE COUNT; LYMPHOCYTE DEPLETION; METABOLISM; MICROBIOLOGY; MYCOPLASMA PULMONIS; PATHOLOGY; PHENOTYPE; PHYSIOLOGY; SEVERITY OF ILLNESS INDEX;

ANIMALS; ANTIBODY FORMATION; CYTOKINES; FEMALE; INFLAMMATION; INTERFERON-GAMMA; INTERLEUKIN-17; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LUNG; LYMPH NODES; LYMPHOCYTE COUNT; LYMPHOCYTE DEPLETION; MICE, INBRED BALB C; MYCOPLASMA PULMONIS; PHENOTYPE; PNEUMONIA, MYCOPLASMA; SEVERITY OF ILLNESS INDEX; T-LYMPHOCYTES, REGULATORY; TH2 CELLS;

EID: 84971221964     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0155648     Document Type: Article

References (91)

1. Krause DC, Taylor-Robinson D. Mycoplasmas which infect humans. In: Maniloff J, McElhaney RN, Finch LR, Baseman JB, editors. Mycoplasmas: Molecular biology and pathogenesis. Washington, D. C.: American Society of Microbiology; 1993. p. 417-44.
2. Freymuth F, Vabret A, Brouard J, Toutain F, Verdon R, Petitjean J, et al. Detection of viral, Chlamydia pneumoniae and Mycoplasma pneumoniae infections in exacerbations of asthma in children. J Clin Virol. 1999; 13(3):131-9. PMID: 10443789
3. Kraft M, Cassell GH, Henson JE, Watson H, Williamson J, Marmion BP, et al. Detection of Mycoplasma pneumoniae in the airways of adults with chronic asthma. Am J Respir Crit Care Med. 1998; 158 (3):998-1001. PMID: 9731038
4. Seggev JS, Lis I, Siman-Tov R, Gutman R, Abu-Samara H, Schey G, et al. Mycoplasma pneumoniae is a frequent cause of exacerbation of bronchial asthma in adults. Ann Allergy. 1986; 57(4):263-5. PMID: 3094410.
5. Cartner SC, Lindsey JR, Gibbs-Erwin J, Cassell GH, Simecka JW. Roles of innate and adaptive immunity in respiratory mycoplasmosis. Infect Immun. 1998; 66(8):3485-91. PMID: 9673224
6. Denny FW, Taylor-Robinson D, Allison AC. The role of thymus-dependent immunity in Mycoplasma pulmonis infections of mice. J Med Microbiol. 1972; 5(3):327-36. PMID: 4560750.
7. Jones H, Tabor L, Sun X, Woolard M, Simecka J. Depletion of CD8+ T cells exacerbates CD4+ Th cell associated inflammatory lesions during murine mycoplasma respiratory disease. J Immunol. 2002; 168:3493-501. PMID: 11907110
8. Jones HP, Simecka JW. T lymphocyte responses are critical determinants in the pathogenesis and resistance to Mycoplasma respiratory disease. Front Biosci. 2003; 8:D930-45. PMID: 12700085.
9. Dobbs NA, Odeh AN, Sun X, Simecka JW. The multifaceted role of T cell-mediated immunity in pathogenesis and resistance to mycoplasma respiratory disease. Current trends in immunology. 2009; 10:1-19. Epub 2009/01/01. PMID: 21743780; PubMed Central PMCID: PMC3131222.
10. Bodhankar S, Sun X, Woolard MD, Simecka JW. Interferon gamma and interleukin 4 have contrasting effects on immunopathology and the development of protective adaptive immunity against mycoplasma respiratory disease. J Infect Dis. 2010; 202(1):39-51. Epub 2010/05/28. doi: 10.1086/653121 PMID: 20504237.
11. Bodhankar S, Woolard MD, Sun X, Simecka JW. NK cells interfere with the generation of resistance against mycoplasma respiratory infection following nasal-pulmonary immunization. J Immunol. 2009; 183(4):2622-31. Epub 2009/07/25. doi: 10.4049/jimmunol.0802180 PMID: 19625649; PubMed Central PMCID: PMC2811958.
12. Woolard MD, Hudig D, Tabor L, Ivey JA, Simecka JW. NK cells in gamma-interferon-deficient mice suppress lung innate immunity against Mycoplasma spp. Infection and immunity. 2005; 73(10):6742-51.Epub 2005/09/24. doi: 10.1128/IAI.73.10.6742-6751.2005 PMID: 16177352; PubMed Central PMCID: PMC1230952.
13. Shevach EM. From vanilla to 28 flavors: multiple varieties of T regulatory cells. Immunity. 2006; 25 (2):195-201. doi: 10.1016/j.immuni.2006.08.003 PMID: 16920638.
14. Bluestone JA, Abbas AK. Natural versus adaptive regulatory T cells. Nature reviews. 2003; 3(3):253-7.Epub 2003/03/27. doi: 10.1038/nri1032 PMID: 12658273.
15. Groux H, O'Garra A, Bigler M, Rouleau M, Antonenko S, de Vries JE, et al. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature. 1997; 389(6652):737-42. Epub 1997/ 10/24 21:29. doi: 10.1038/39614 PMID: 9338786.
16. Tran DQ. TGF-beta: the sword, the wand, and the shield of FOXP3(+) regulatory T cells. Journal of molecular cell biology. 2012; 4(1):29-37. Epub 2011/12/14. doi: 10.1093/jmcb/mjr033 PMID: 22158907.
17. Kochetkova I, Thornburg T, Callis G, Pascual DW. Segregated regulatory CD39+CD4+ T cell function: TGF-beta-producing Foxp3- and IL-10-producing Foxp3+ cells are interdependent for protection against collagen-induced arthritis. J Immunol. 2011; 187(9):4654-66. Epub 2011/10/05. doi: 10.4049/ jimmunol.1100530 PMID: 21967895; PubMed Central PMCID: PMC3237119.
18. Hussain SF, Paterson Y. CD4+CD25+ regulatory T cells that secrete TGFbeta and IL-10 are preferentially induced by a vaccine vector. J Immunother. 2004; 27(5):339-46. Epub 2004/08/18. PMID: 15314542.
19. Marshall NA, Vickers MA, Barker RN. Regulatory T cells secreting IL-10 dominate the immune response to EBV latent membrane protein 1. J Immunol. 2003; 170(12):6183-9. Epub 2003/06/10. PMID: 12794149.
20. Stohlman SA, Pei L, Cua DJ, Li Z, Hinton DR. Activation of regulatory cells suppresses experimental allergic encephalomyelitis via secretion of IL-10. J Immunol. 1999; 163(11):6338-44. Epub 1999/11/26. PMID: 10570329.
21. Zhang X, Koldzic DN, Izikson L, Reddy J, Nazareno RF, Sakaguchi S, et al. IL-10 is involved in the suppression of experimental autoimmune encephalomyelitis by CD25+CD4+ regulatory T cells. Int Immunol. 2004; 16(2):249-56. Epub 2004/01/22. PMID: 14734610.
22. Fowler S, Powrie F. Control of immune pathology by IL-10-secreting regulatory T cells. Springer Semin Immunopathol. 1999; 21(3):287-94. PMID: 10666774.
23. Beriou G, Costantino CM, Ashley CW, Yang L, Kuchroo VK, Baecher-Allan C, et al. IL-17-producing human peripheral regulatory T cells retain suppressive function. Blood. 2009; 113(18):4240-9. Epub 2009/01/28. doi: 10.1182/blood-2008-10-183251 PMID: 19171879; PubMed Central PMCID: PMC2676084.
24. Ranjbar M, Solgi G, Mohammadnia M, Nikbin B, Pourmand G, Ansaripour B, et al. Regulatory T-cell subset analysis and profile of interleukin (IL)-10, IL-17 and interferon-gamma cytokine-producing cells in kidney allograft recipients with donor cells infusion. Clinical and experimental nephrology. 2012; 16 (4):636-46. Epub 2012/02/09. doi: 10.1007/s10157-012-0591-9 PMID: 22314659.
25. Kryczek I, Wu K, Zhao E, Wei S, Vatan L, Szeliga W, et al. IL-17+ regulatory T cells in the microenvironments of chronic inflammation and cancer. J Immunol. 2011; 186(7):4388-95. Epub 2011/03/02. doi: 10.4049/jimmunol.1003251 PMID: 21357259.
26. Voo KS, Wang YH, Santori FR, Boggiano C, Wang YH, Arima K, et al. Identification of IL-17-producing FOXP3+ regulatory T cells in humans. Proc Natl Acad Sci USA. 2009; 106(12):4793-8. Epub 2009/03/11. doi: 10.1073/pnas.0900408106 PMID: 19273860; PubMed Central PMCID: PMC2653560.
27. Xu L, Kitani A, Fuss I, Strober W. Cutting edge: regulatory T cells induce CD4+CD25-Foxp3- T cells or are self-induced to become Th17 cells in the absence of exogenous TGF-beta. J Immunol. 2007; 178 (11):6725-9. Epub 2007/05/22. PMID: 17513718.
28. Esposito M, Ruffini F, Bergami A, Garzetti L, Borsellino G, Battistini L, et al. IL-17- and IFN-gammasecreting Foxp3+ T cells infiltrate the target tissue in experimental autoimmunity. J Immunol. 2010; 185 (12):7467-73. Epub 2010/11/26. doi: 10.4049/jimmunol.1001519 PMID: 21098230.
29. Daniel V, Sadeghi M, Wang H, Opelz G. CD4+CD25+Foxp3+IFN-gamma+ human induced T regulatory cells are induced by interferon-gamma and suppress alloresponses nonspecifically. Hum Immunol. 2011; 72(9):699-707. Epub 2011/06/15. doi: 10.1016/j.humimm.2011.05.020 PMID: 21664396.
30. Haringer B, Lozza L, Steckel B, Geginat J. Identification and characterization of IL-10/IFN-gamma-producing effector-like T cells with regulatory function in human blood. J Exp Med. 2009; 206(5):1009-17. Epub 2009/05/06. doi: 10.1084/jem.20082238 PMID: 19414553; PubMed Central PMCID: PMC2715038.
31. Koenecke C, Lee CW, Thamm K, Fohse L, Schafferus M, Mittrucker HW, et al. IFN-gamma production by allogeneic Foxp3+ regulatory T cells is essential for preventing experimental graft-versus-host disease. J Immunol. 2012; 189(6):2890-6. Epub 2012/08/08. doi: 10.4049/jimmunol.1200413 PMID: 22869903.
32. Zheng J, Liu Y, Qin G, Lam KT, Guan J, Xiang Z, et al. Generation of human Th1-like regulatory CD4+ T cells by an intrinsic IFN-gamma- and T-bet-dependent pathway. Eur J Immunol. 2011; 41(1):128-39. Epub 2010/12/25. doi: 10.1002/eji.201040724 PMID: 21182084.
33. Rouse BT, Suvas S. Regulatory cells and infectious agents: detentes cordiale and contraire. J Immunol. 2004; 173(4):2211-5. Epub 2004/08/06. PMID: 15294929.
34. Belkaid Y. Regulatory T cells and infection: a dangerous necessity. Nature reviews. 2007; 7(11):875-88. Epub 2007/10/20. doi: 10.1038/nri2189 PMID: 17948021.
35. Odeh AN, Simecka JW. The Contrasting Roles of T Regulatory Cells in Bacterial Lung Diseases: Intech; 2012. Available from: http://www.intechopen.com/books/respiratory-diseases/the-contrastingroles-of-t-regulatory-cells-in-bacterial-lung-diseases.
36. Suvas S, Azkur AK, Kim BS, Kumaraguru U, Rouse BT. CD4+CD25+ regulatory T cells control the severity of viral immunoinflammatory lesions. J Immunol. 2004; 172(7):4123-32. PMID: 15034024.
37. Hesse M, Piccirillo CA, Belkaid Y, Prufer J, Mentink-Kane M, Leusink M, et al. The pathogenesis of schistosomiasis is controlled by cooperating IL-10-producing innate effector and regulatory T cells. J Immunol. 2004; 172(5):3157-66. Epub 2004/02/24. PMID: 14978122.
38. Shafiani S, Tucker-Heard G, Kariyone A, Takatsu K, Urdahl KB. Pathogen-specific regulatory T cells delay the arrival of effector T cells in the lung during early tuberculosis. J Exp Med. 2010; 207(7):1409-20. Epub 2010/06/16. doi: 10.1084/jem.20091885 PMID: 20547826; PubMed Central PMCID: PMC2901066.
39. Mendez S, Reckling SK, Piccirillo CA, Sacks D, Belkaid Y. Role for CD4(+) CD25(+) regulatory T cells in reactivation of persistent leishmaniasis and control of concomitant immunity. J Exp Med. 2004; 200 (2):201-10. PMID: 15263027.
40. Abel S, Luckheide N, Westendorf AM, Geffers R, Roers A, Muller W, et al. Strong impact of CD4+ Foxp3+ regulatory T cells and limited effect of T cell-derived IL-10 on pathogen clearance during Plasmodium yoelii infection. J Immunol. 2012; 188(11):5467-77. Epub 2012/05/01. doi: 10.4049/jimmunol.1102223 PMID: 22544931.
41. Walther M, Tongren JE, Andrews L, Korbel D, King E, Fletcher H, et al. Upregulation of TGF-beta, FOXP3, and CD4+CD25+ regulatory T cells correlates with more rapid parasite growth in human malaria infection. Immunity. 2005; 23(3):287-96. Epub 2005/09/20. doi: 10.1016/j.immuni.2005.08.006 PMID: 16169501.
42. Johanns TM, Ertelt JM, Rowe JH, Way SS. Regulatory T cell suppressive potency dictates the balance between bacterial proliferation and clearance during persistent Salmonella infection. PLoS pathogens. 2010; 6(8):e1001043. Epub 2010/08/18. doi: 10.1371/journal.ppat.1001043 PMID: 20714351; PubMed Central PMCID: PMC2920851.
43. Davidson MK, Ross SE, Lindsey JR, Cassell GH. Colony opacity, hemadsorption, hemolysis, and mitogenicity are not associated with virulence of Mycoplasma pulmonis. Infect Immun. 1988; 56(8):2169-73. PMID: 3397189
44. Simecka JW, Cassell GH. Serum antibody and cellular responses in LEW and F344 rats after immunization with Mycoplasma pulmonis antigens. Infect Immun. 1987; 55(3):731-5. PMID: 3493221
45. Davidson MK, Lindsey JR, Parker RF, Tully JG, Cassell GH. Differences in virulence for mice among strains of Mycoplasma pulmonis. Infect Immun. 1988; 56:2156-62. PMID: 3397187
46. Overcash RG, Lindsey JR, Cassel GH, Baker HJ. Enhancement of natural and experimental respiratory mycoplasmosis in rats by hexamethylphosphoramide. Am J Pathol. 1976; 82(01):171-89. PMID: 1247084.
47. Pinson DM, Schoeb TR, Lindsey JR, Davis JK. Evaluation by scoring and computerized morphometry of lesions of early Mycoplasma pulmonis infection and ammonia exposure in F344/N rats. Vet Pathol. 1986; 23(5):550-5. PMID: 3776012.
48. Jones H, Hodge L, Fujihashi K, Kiyono H, McGhee JR, Simecka JW. The pulmonary environment promotes Th2 cell responses after nasal-pulmonary immunization with antigen alone, but Th1 responses are induced during instances of intense immune stimulation. J Immunol. 2001; 167:4518-26. PMID: 11591779
49. Jackson RJ, Fujihashi K, Xu-Amano J, Kiyono H, Elson CO, McGhee JR. Optimizing oral vaccines: induction of systemic and mucosal B-cell and antibody responses to tetanus toxoid by use of cholera toxin as an adjuvant. Infect Immun. 1993; 61(10):4272-9. PMID: 8406816
50. Hodge LM, Marinaro M, Jones HP, McGhee JR, Kiyono H, Simecka JW. Immunoglobulin A (IgA) responses and IgE-associated inflammation along the respiratory tract after mucosal but not systemic immunization. Infect Immun. 2001; 69(4):2328-38. PMID: 11254590
51. Liang SC, Schoeb TR, Davis JK, Simecka JW, Cassell GH, Lindsey JR. Comparative severity of respiratory lesions of sialodacryoadenitis virus and Sendai virus infections in LEW and F344 rats. Vet Pathol. 1995; 32(6):661-7. PMID: 8592801
52. Shimizu J, Yamazaki S, Takahashi T, Ishida Y, Sakaguchi S. Stimulation of CD25(+)CD4(+) regulatory T cells through GITR breaks immunological self-tolerance. Nat Immunol. 2002; 3(2):135-42. Epub 2002/01/29. doi: 10.1038/ni759 PMID: 11812990.
53. Wing K, Onishi Y, Prieto-Martin P, Yamaguchi T, Miyara M, Fehervari Z, et al. CTLA-4 control over Foxp3+ regulatory T cell function. Science. 2008; 322(5899):271-5. Epub 2008/10/11. doi: 10.1126/ science.1160062 PMID: 18845758.
54. Takahashi T, Tagami T, Yamazaki S, Uede T, Shimizu J, Sakaguchi N, et al. Immunologic self-tolerance maintained by CD25(+)CD4(+) regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4. J Exp Med. 2000; 192(2):303-10. Epub 2000/07/19. PMID: 10899917; PubMed Central PMCID: PMC2193248.
55. McHugh RS, Whitters MJ, Piccirillo CA, Young DA, Shevach EM, Collins M, et al. CD4(+)CD25(+) immunoregulatory T cells: gene expression analysis reveals a functional role for the glucocorticoidinduced TNF receptor. Immunity. 2002; 16(2):311-23. Epub 2002/03/01. PMID: 11869690.
56. Lehmann J. Huehn J. de la Rosa M Maszyna F Kretschmer U , Krenn Vet al.Expression of the integrin alpha Ebeta 7 identifies unique subsets of CD25+ as well as CD25- regulatory T cellsProc Natl Acad Sci USA2002992013031-13036Epub 2002/09/21 PMID: 12242333; PubMed Central PMCID: PMC13058110.1073/pnas.192162899
57. Yu N, Li X, Song W, Li D, Yu D, Zeng X, et al. CD4(+)CD25 (+)CD127 (low/-) T cells: a more specific Treg population in human peripheral blood. Inflammation. 2012; 35(6):1773-80. Epub 2012/07/04. doi: 10.1007/s10753-012-9496-8 PMID: 22752562.
58. Bremm M, Huenecke S, Lehrnbecher T, Ponstingl E, Mueller R, Heinze A, et al. Advanced flowcytometric analysis of regulatory T cells: CD127 downregulation early post stem cell transplantation and altered Treg/CD3(+)CD4(+)-ratio in severe GvHD or relapse. J Immunol Methods. 2011; 373(1-2):36-44. Epub 2011/08/16. doi: 10.1016/j.jim.2011.07.018 PMID: 21839739.
59. Lee SK, Choi BK, Kim YH, Kang WJ, Kim KH, Sakaguchi S, et al. Glucocorticoid-induced tumour necrosis factor receptor family-related receptor signalling exacerbates hapten-induced colitis by CD4+ T cells. Immunology. 2006; 119(4):479-87. Epub 2006/12/21. doi: 10.1111/j.1365-2567.2006.02459.x PMID: 17177830; PubMed Central PMCID: PMC2265816.
60. Namangala B, Yokoyama N, Ikehara Y, Taguchi O, Tsujimura K, Sugimoto C, et al. Effect of CD4 +CD25+ T cell-depletion on acute lethal infection of mice with Trypanosoma congolense. J Vet Med Sci. 2008; 70(8):751-9. Epub 2008/09/06. PMID: 18772548.
61. Morgan ME, Sutmuller RP, Witteveen HJ, van Duivenvoorde LM, Zanelli E, Melief CJ, et al. CD25+ cell depletion hastens the onset of severe disease in collagen-induced arthritis. Arthritis Rheum. 2003; 48 (5):1452-60. Epub 2003/05/15. doi: 10.1002/art.11063 PMID: 12746920.
62. Josefowicz SZ, Niec RE, Kim HY, Treuting P, Chinen T, Zheng Y, et al. Extrathymically generated regulatory T cells control mucosal TH2 inflammation. Nature. 2012; 482(7385):395-9. Epub 2012/02/10. doi: 10.1038/nature10772 PMID: 22318520; PubMed Central PMCID: PMC3485072.
63. Faustino L, Mucida D, Keller AC, Demengeot J, Bortoluci K, Sardinha LR, et al. Regulatory T cells accumulate in the lung allergic inflammation and efficiently suppress T-cell proliferation but not Th2 cytokine production. Clinical & developmental immunology. 2012; 2012:721817. Epub 2011/12/14. doi: 10. 1155/2012/721817 PMID: 22162718; PubMed Central PMCID: PMC3227414.
64. Turner JD, Jenkins GR, Hogg KG, Aynsley SA, Paveley RA, Cook PC, et al. CD4+CD25+ regulatory cells contribute to the regulation of colonic Th2 granulomatous pathology caused by schistosome infection. PLoS neglected tropical diseases. 2011; 5(8):e1269. Epub 2011/08/23. doi: 10.1371/journal.pntd. 0001269 PMID: 21858239; PubMed Central PMCID: PMC3153428.
65. Hussain S, Kirwin SJ, Stohlman SA. Increased T regulatory cells lead to development of Th2 immune response in male SJL mice. Autoimmunity. 2011; 44(3):219-28. Epub 2010/10/05. doi: 10.3109/ 08916934.2010.519746 PMID: 20883149.
66. Girtsman T, Jaffar Z, Ferrini M, Shaw P, Roberts K. Natural Foxp3(+) regulatory T cells inhibit Th2 polarization but are biased toward suppression of Th17-driven lung inflammation. J Leukoc Biol. 2010; 88 (3):537-46. Epub 2010/05/25. doi: 10.1189/jlb.0110044 PMID: 20495073; PubMed Central PMCID: PMC2924601.
67. Taams LS, Vukmanovic-Stejic M, Smith J, Dunne PJ, Fletcher JM, Plunkett FJ, et al. Antigen-specific T cell suppression by human CD4+CD25+ regulatory T cells. Eur J Immunol. 2002; 32(6):1621-30. Epub 2002/07/13. doi: 10.1002/1521-4141(200206)32:6<1621::AID-IMMU1621>3.0.CO;2-Q PMID: 12115645.
68. Couper KN, Lanthier PA, Perona-Wright G, Kummer LW, Chen W, Smiley ST, et al. Anti-CD25 antibody-mediated depletion of effector T cell populations enhances susceptibility of mice to acute but not chronic Toxoplasma gondii infection. J Immunol. 2009; 182(7):3985-94. doi: 10.4049/jimmunol. 0803053 PMID: 19299696; PubMed Central PMCID: PMCPMC3942880.
69. Cartner SC, Simecka JW, Briles DE, Cassell GH, Lindsey JR. Resistance to mycoplasmal lung disease in mice is a complex genetic trait. Infect Immun. 1996; 64(12):5326-31. PMID: 8945584
70. Chen X, Oppenheim JJ, Howard OM. BALB/c mice have more CD4+CD25+ T regulatory cells and show greater susceptibility to suppression of their CD4+CD25- responder T cells than C57BL/6 mice. J Leukoc Biol. 2005; 78(1):114-21. doi: 10.1189/jlb.0604341 PMID: 15845645.
71. Cartner SC, Simecka JW, Lindsey JR, Cassell GH, Davis JK. Chronic respiratory mycoplasmosis in C3H/HeN and C57BL/6N mice: lesion severity and antibody response. Infect Immun. 1995; 63 (10):4138-42. PMID: 7558330
72. Hickman-Davis JM. Role of innate immunity in respiratory mycoplasma infection. Front Biosci. 2002; 7: d1347-55. PMID: 11991835.
73. Hickman-Davis JM, Michalek SM, Gibbs-Erwin J, Lindsey JR. Depletion of alveolar macrophages exacerbates respiratory mycoplasmosis in mycoplasma-resistant C57BL mice but not mycoplasma-susceptible C3H mice. Infect Immun. 1997; 65(6):2278-82. PMID: 9169764
74. Belkaid Y, Hoffmann KF, Mendez S, Kamhawi S, Udey MC, Wynn TA, 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. 2001; 194(10):1497-506. PMID: 11714756.
75. Kane MM, Mosser DM. The role of IL-10 in promoting disease progression in leishmaniasis. J Immunol. 2001; 166(2):1141-7. PMID: 11145695.
76. Murray HW, Lu CM, Mauze S, Freeman S, Moreira AL, Kaplan G, et al. Interleukin-10 (IL-10) in experimental visceral leishmaniasis and IL-10 receptor blockade as immunotherapy. Infect Immun. 2002; 70 (11):6284-93. PMID: 12379707.
77. Yang X, Gartner J, Zhu L, Wang S, Brunham RC. IL-10 gene knockout mice show enhanced Th1-like protective immunity and absent granuloma formation following Chlamydia trachomatis lung infection. J Immunol. 1999; 162(2):1010-7. PMID: 9916727.
78. Hiura T, Kagamu H, Miura S, Ishida A, Tanaka H, Tanaka J, et al. Both regulatory T cells and antitumor effector T cells are primed in the same draining lymph nodes during tumor progression. J Immunol. 2005; 175(8):5058-66. Epub 2005/10/08. PMID: 16210609.
79. Carson WFt Guernsey LA, Singh A Vella AT, Schramm CM Thrall RS. Accumulation of regulatory T cells in local draining lymph nodes of the lung correlates with spontaneous resolution of chronic asthma in a murine model. Int Arch Allergy Immunol. 2008; 145(3):231-43. Epub 2007/10/05. doi: 10.1159/000109292 PMID: 17914275; PubMed Central PMCID: PMC2576511.
80. Zhang N, Schroppel B, Lal G, Jakubzick C, Mao X, Chen D, et al. Regulatory T cells sequentially migrate from inflamed tissues to draining lymph nodes to suppress the alloimmune response. Immunity. 2009; 30(3):458-69. Epub 2009/03/24. doi: 10.1016/j.immuni.2008.12.022 PMID: 19303390; PubMed Central PMCID: PMC2737741.
81. Deng L, Zhang H, Luan Y, Zhang J, Xing Q, Dong S, et al. Accumulation of foxp3+ T regulatory cells in draining lymph nodes correlates with disease progression and immune suppression in colorectal cancer patients. Clinical cancer research: an official journal of the American Association for Cancer Research. 2010; 16(16):4105-12. Epub 2010/08/05. doi: 10.1158/1078-0432.CCR-10-1073 PMID: 20682706.
82. Jones HP, Tabor L, Sun X, Woolard MD, Simecka JW. Depletion of CD8+ T cells exacerbates CD4+ Th cell-associated inflammatory lesions during murine mycoplasma respiratory disease. J Immunol. 2002; 168(7):3493-501. Epub 2002/03/22. PMID: 11907110.
83. Stassen M, Jonuleit H, Muller C, Klein M, Richter C, Bopp T, et al. Differential regulatory capacity of CD25+ T regulatory cells and preactivated CD25+ T regulatory cells on development, functional activation, and proliferation of Th2 cells. J Immunol. 2004; 173(1):267-74. PMID: 15210784.
84. Sawant DV, Gravano DM, Vogel P, Giacomin P, Artis D, Vignali DA. Regulatory T cells limit induction of protective immunity and promote immune pathology following intestinal helminth infection. J Immunol. 2014; 192(6):2904-12. doi: 10.4049/jimmunol.1202502 PMID: 24532574; PubMed Central PMCID: PMC3955731.
85. Schulze B, Piehler D, Eschke M, von Buttlar H, Kohler G, Sparwasser T, et al. CD4(+) FoxP3(+) regulatory T cells suppress fatal T helper 2 cell immunity during pulmonary fungal infection. Eur J Immunol. 2014; 44(12):3596-604. doi: 10.1002/eji.201444963 PMID: 25187063.
86. Moore-Connors JM, Fraser R, Halperin SA, Wang J. CD4(+)CD25(+)Foxp3(+) regulatory T cells promote Th17 responses and genital tract inflammation upon intracellular Chlamydia muridarum infection. J Immunol. 2013; 191(6):3430-9. doi: 10.4049/jimmunol.1301136 PMID: 23956419.
87. Pandiyan P, Conti HR, Zheng L, Peterson AC, Mathern DR, Hernandez-Santos N, et al. CD4(+)CD25 (+)Foxp3(+) regulatory T cells promote Th17 cells in vitro and enhance host resistance in mouse Candida albicans Th17 cell infection model. Immunity. 2011; 34(3):422-34. doi: 10.1016/j.immuni.2011.03.002 PMID: 21435589; PubMed Central PMCID: PMC3258585.
88. Wang Z, Friedrich C, Hagemann SC, Korte WH, Goharani N, Cording S, et al. Regulatory T cells promote a protective Th17-associated immune response to intestinal bacterial infection with C. rodentium. Mucosal Immunol. 2014; 7(6):1290-301. doi: 10.1038/mi.2014.17 PMID: 24646939.
89. Whibley N, Maccallum DM, Vickers MA, Zafreen S, Waldmann H, Hori S, et al. Expansion of Foxp3(+) T-cell populations by Candida albicans enhances both Th17-cell responses and fungal dissemination after intravenous challenge. Eur J Immunol. 2014; 44(4):1069-83. doi: 10.1002/eji.201343604 PMID: 24435677; PubMed Central PMCID: PMC3992851.
90. Bai H, Cheng J, Gao X, Joyee AG, Fan Y, Wang S, et al. IL-17/Th17 promotes type 1 T cell immunity against pulmonary intracellular bacterial infection through modulating dendritic cell function. J Immunol. 2009; 183(9):5886-95. Epub 2009/10/09. doi: 10.4049/jimmunol.0901584 PMID: 19812198.
91. Nakagome K, Okunishi K, Imamura M, Harada H, Matsumoto T, Tanaka R, et al. IFN-gamma attenuates antigen-induced overall immune response in the airway as a Th1-type immune regulatory cytokine. J Immunol. 2009; 183(1):209-20. Epub 2009/06/23. doi: 10.4049/jimmunol.0802712 PMID: 19542432.