Unexpected Role for IL-17 in Protective Immunity against Hypervirulent Mycobacterium tuberculosis HN878 Infection

PLoS Pathogens

Volumn 10, Issue 5, 2014, Pages

  Gopal, Radha ^a   Monin, Leticia ^a   Slight, Samantha ^a   Uche, Uzodinma ^a   Blanchard, Emmeline ^a   A Fallert Junecko, Beth ^b   Ramos Payan, Rosalio ^c,d   Stallings, Christina L ^e   Reinhart, Todd A ^b   Kolls, Jay K ^f   Kaushal, Deepak ^g   Nagarajan, Uma ^h   Rangel Moreno, Javier ^d   Khader, Shabaana A ^a,e  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIVERSIDAD AUTÓNOMA DE SINALOA   (Mexico)

^d UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^g TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^h UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IL17A PROTEIN, MOUSE; IL1R1 PROTEIN, MOUSE; INTERLEUKIN 1 RECEPTOR TYPE I; INTERLEUKIN 17; INTERLEUKIN 1BETA; TLR2 PROTEIN, MOUSE; TOLL LIKE RECEPTOR 2;

ANIMAL; C57BL MOUSE; CELL CULTURE; CELL PROTECTION; COMMUNICABLE DISEASE; FEMALE; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; KNOCKOUT MOUSE; MALE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; PATHOGENICITY; PHYSIOLOGY; TUBERCULOSIS;

ANIMALS; CELLS, CULTURED; COMMUNICABLE DISEASES, EMERGING; CYTOPROTECTION; FEMALE; IMMUNITY, INNATE; INTERLEUKIN-17; INTERLEUKIN-1BETA; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYCOBACTERIUM TUBERCULOSIS; RECEPTORS, INTERLEUKIN-1 TYPE I; TOLL-LIKE RECEPTOR 2; TUBERCULOSIS;

EID: 84901659079     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004099     Document Type: Article

References (42)

1. Bifani PJ, Mathema B, Kurepina NE, Kreiswirth BN, (2002) Global dissemination of the Mycobacterium tuberculosis W-Beijing family strains. Trends Microbiol 10: 45-52.
2. Kremer K, Glynn JR, Lillebaek T, Niemann S, Kurepina NE, et al. (2004) Definition of the Beijing/W lineage of Mycobacterium tuberculosis on the basis of genetic markers. J Clin Microbiol 42: 4040-4049.
3. van Soolingen D, Qian L, de Haas PE, Douglas JT, Traore H, et al. (1995) Predominance of a single genotype of Mycobacterium tuberculosis in countries of east Asia. J Clin Microbiol 33: 3234-3238.
4. Ordway DJ, Shang S, Henao-Tamayo M, Obregon-Henao A, Nold L, et al. (2011) Mycobacterium bovis BCG-mediated protection against W-Beijing strains of Mycobacterium tuberculosis is diminished concomitant with the emergence of regulatory T cells. Clin Vaccine Immunol 18: 1527-1535.
5. Kruuner A, Hoffner SE, Sillastu H, Danilovits M, Levina K, et al. (2001) Spread of drug-resistant pulmonary tuberculosis in Estonia. J Clin Microbiol 39: 3339-3345.
6. Glynn JR, Whiteley J, Bifani PJ, Kremer K, van Soolingen D, (2002) Worldwide occurrence of Beijing/W strains of Mycobacterium tuberculosis: a systematic review. Emerg Infect Dis 8: 843-849.
7. Caws M, Thwaites G, Stepniewska K, Nguyen TN, Nguyen TH, et al. (2006) Beijing genotype of Mycobacterium tuberculosis is significantly associated with human immunodeficiency virus infection and multidrug resistance in cases of tuberculous meningitis. J Clin Microbiol 44: 3934-3939.
8. Manca C, Tsenova L, Bergtold A, Freeman S, Tovey M, et al. (2001) 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 U S A 98: 5752-5757.
9. Ordway D, Henao-Tamayo M, Harton M, Palanisamy G, Troudt J, et al. (2007) The hypervirulent Mycobacterium tuberculosis strain HN878 induces a potent TH1 response followed by rapid down-regulation. J Immunol 179: 522-531.
10. Manca C, Tsenova L, Freeman S, Barczak AK, Tovey M, et al. (2005) 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.
11. Reed MB, Domenech P, Manca C, Su H, Barczak AK, et al. (2004) A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 431: 84-87.
12. Kolls JK, Khader SA, (2010) The role of Th17 cytokines in primary mucosal immunity. Cytokine Growth Factor Rev 21: 443-448.
13. Khader SA, Pearl JE, Sakamoto K, Gilmartin L, Bell GK, et al. (2005) IL-23 compensates for the absence of IL-12p70 and is essential for the IL-17 response during tuberculosis but is dispensable for protection and antigen-specific IFN-gamma responses if IL-12p70 is available. J Immunol 175: 788-795.
14. Aujla SJ, Chan YR, Zheng M, Fei M, Askew DJ, et al. (2008) IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nat Med 14: 275-281.
15. Khader SA, Guglani L, Rangel-Moreno J, Gopal R, Fallert Junecko BA, et al. (2011) IL-23 Is Required for Long-Term Control of Mycobacterium tuberculosis and B Cell Follicle Formation in the Infected Lung. J Immunol 187: 5402-5407.
16. Khader SA, Bell GK, Pearl JE, Fountain JJ, Rangel-Moreno J, et al. (2007) IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat Immunol 8: 369-377.
17. Gopal R, Rangel-Moreno J, Slight S, Lin Y, Nawar HF, et al. (2013) Interleukin-17-dependent CXCL13 mediates mucosal vaccine-induced immunity against tuberculosis. Mucosal Immunol 6: 972-984.
18. Nakae S, Komiyama Y, Nambu A, Sudo K, Iwase M, et al. (2002) Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17: 375-387.
19. Zheng M, Shellito JE, Marrero L, Zhong Q, Julian S, et al. (2001) CD4+ T cell-independent vaccination against Pneumocystis carinii in mice. J Clin Invest 108: 1469-1474.
20. Slight SR, Rangel-Moreno J, Gopal R, Lin Y, Fallert Junecko BA, et al. (2013) CXCR5+ T helper cells mediate protective immunity against tuberculosis. J Clin Invest 123: 712-26.
21. Reiley WW, Calayag MD, Wittmer ST, Huntington JL, Pearl JE, et al. (2008) ESAT-6-specific CD4 T cell responses to aerosol Mycobacterium tuberculosis infection are initiated in the mediastinal lymph nodes. Proc Natl Acad Sci U S A 105: 10961-10966.
22. Khader SA, Partida-Sanchez S, Bell G, Jelley-Gibbs DM, Swain S, et al. (2006) Interleukin 12p40 is required for dendritic cell migration and T cell priming after Mycobacterium tuberculosis infection. J Exp Med 203: 1805-1815.
23. Khader SA, Rangel-Moreno J, Fountain JJ, Martino CA, Reiley WW, et al. (2009) In a murine tuberculosis model, the absence of homeostatic chemokines delays granuloma formation and protective immunity. J Immunol 183: 8004-8014.
24. Nurieva RI, Chung Y, Hwang D, Yang XO, Kang HS, et al. (2008) Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity 29: 138-149.
25. Sutton C, Brereton C, Keogh B, Mills KH, Lavelle EC, (2006) A crucial role for interleukin (IL)-1 in the induction of IL-17-producing T cells that mediate autoimmune encephalomyelitis. J Exp Med 203: 1685-1691.
26. Yoshida A, Inagawa H, Kohchi C, Nishizawa T, Soma G, (2009) The role of toll-like receptor 2 in survival strategies of Mycobacterium tuberculosis in macrophage phagosomes. Anticancer Res 29: 907-910.
27. Kleinnijenhuis J, Joosten LA, van de Veerdonk FL, Savage N, van Crevel R, et al. (2009) Transcriptional and inflammasome-mediated pathways for the induction of IL-1beta production by Mycobacterium tuberculosis. Eur J Immunol 39: 1914-1922.
28. Lin Y, Ritchea S, Logar A, Slight S, Messmer M, et al. (2009) Interleukin-17 Is Required for T Helper 1 Cell Immunity and Host Resistance to the Intracellular Pathogen Francisella tularensis. Immunity 31: 799-810.
29. Bai H, Cheng J, Gao X, Joyee AG, Fan Y, et al. (2009) IL-17/Th17 promotes type 1 T cell immunity against pulmonary intracellular bacterial infection through modulating dendritic cell function. J Immunol 183: 5886-5895.
30. Gopal R, Rangel-Moreno J, Slight S, Lin Y, Nawar HF, et al. (2013) Interleukin-17-dependent CXCL13 mediates mucosal vaccine-induced immunity against tuberculosis. Mucosal Immunol 6: 972-84.
31. Agerton TB, Valway SE, Blinkhorn RJ, Shilkret KL, Reves R, et al. (1999) Spread of strain W, a highly drug-resistant strain of Mycobacterium tuberculosis, across the United States. Clin Infect Dis 29: 85-92 discussion 93-85.
32. Sinsimer D, Huet G, Manca C, Tsenova L, Koo MS, et al. (2008) The phenolic glycolipid of Mycobacterium tuberculosis differentially modulates the early host cytokine response but does not in itself confer hypervirulence. Infect Immun 76: 3027-3036.
33. Cambier CJ, Takaki KK, Larson RP, Hernandez RE, Tobin DM, et al. (2014) Mycobacteria manipulate macrophage recruitment through coordinated use of membrane lipids. Nature 505: 218-222.
34. Rangel-Moreno J, Carragher DM, de la Luz Garcia-Hernandez M, Hwang JY, Kusser K, et al. (2011) The development of inducible bronchus-associated lymphoid tissue depends on IL-17. Nat Immunol 12: 639-646.
35. Umemura M, Yahagi A, Hamada S, Begum MD, Watanabe H, et al. (2007) IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection. J Immunol 178: 3786-3796.
36. Schulz SM, Kohler G, Schutze N, Knauer J, Straubinger RK, et al. (2008) Protective immunity to systemic infection with attenuated Salmonella enterica serovar enteritidis in the absence of IL-12 is associated with IL-23-dependent IL-22, but not IL-17. J Immunol 181: 7891-7901.
37. Gopal R, Khader SA, (2013) Vaccines against tuberculosis: moving forward with new concepts. Expert Rev Vaccines 12: 829-831.
38. Jurado JO, Pasquinelli V, Alvarez IB, Pena D, Rovetta AI, et al. (2012) IL-17 and IFN-gamma expression in lymphocytes from patients with active tuberculosis correlates with the severity of the disease. J Leukoc Biol 91: 991-1002.
39. Peng MY, Wang ZH, Yao CY, Jiang LN, Jin QL, et al. (2008) Interleukin 17-producing gamma delta T cells increased in patients with active pulmonary tuberculosis. Cell Mol Immunol 5: 203-208.
40. Stern JN, Keskin DB, Romero V, Zuniga J, Encinales L, et al. (2009) Molecular signatures distinguishing active from latent tuberculosis in peripheral blood mononuclear cells, after in vitro antigenic stimulation with purified protein derivative of tuberculin (PPD) or Candida: a preliminary report. Immunol Res 45: 1-12.
41. Chen X, Zhang M, Liao M, Graner MW, Wu C, et al. (2010) Reduced Th17 response in patients with tuberculosis correlates with IL-6R expression on CD4+ T Cells. Am J Respir Crit Care Med 181: 734-742.
42. Scriba TJ, Kalsdorf B, Abrahams DA, Isaacs F, Hofmeister J, et al. (2008) Distinct, Specific IL-17- and IL-22-Producing CD4+ T Cell Subsets Contribute to the Human Anti-Mycobacterial Immune Response. J Immunol 180: 1962-1970.