IL-17 contributes to cell-mediated defense against pulmonary Yersinia pestis infection

Journal of Immunology

Volumn 186, Issue 3, 2011, Pages 1675-1684

  Lin Jr , Shiuan ^a   Kummer, Lawrence W ^a   Szaba, Frank M ^a   Smiley, Stephen T ^a  

^a TRUDEAU INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL VACCINE; D27 PLPXL VACCINE; GAMMA INTERFERON; INTERLEUKIN 17; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; BACTERIAL CLEARANCE; CD4+ T LYMPHOCYTE; CELL PROTECTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; IMMUNIZATION; LUNG; MOUSE; NEUTROPHIL; NONHUMAN; PLAGUE; PRIORITY JOURNAL; SURVIVAL; VACCINATION; YERSINIA PESTIS;

ACYLTRANSFERASES; ADJUVANTS, IMMUNOLOGIC; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; ESCHERICHIA COLI PROTEINS; IMMUNITY, CELLULAR; IMMUNIZATION SCHEDULE; IMMUNIZATION, SECONDARY; INTERLEUKIN-17; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, MUTANT STRAINS; PLAGUE; PLAGUE VACCINE; VACCINES, DNA; YERSINIA PESTIS;

EID: 79251561235     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1003303     Document Type: Article

References (47)

1. Pollitzer, R. 1954. Plague. World Health Organization, Geneva, Switzerland.
2. Perry, R. D., and J. D. Fetherston. 1997. Yersinia pestis - etiologic agent of plague. Clin. Microbiol. Rev. 10: 35-66.
3. Butler, T. 1983. Plague and Other Yersinia Infections. Plenum Press, New York.
4. Galimand, M., A. Guiyoule, G. Gerbaud, B. Rasoamanana, S. Chanteau, E. Carniel, and P. Courvalin. 1997. Multidrug resistance in Yersinia pestis mediated by a transferable plasmid. N. Engl. J. Med. 337: 677-680.
5. Zilinskas, R. A. 2006. The anti-plague system and the Soviet biological warfare program. Crit. Rev. Microbiol. 32: 47-64.
6. Inglesby, T. V., D. T. Dennis, D. A. Henderson, J. G. Bartlett, M. S. Ascher, E. Eitzen, A. D. Fine, A. M. Friedlander, J. Hauer, J. F. Koerner, et al; Working Group on Civilian Biodefense. 2000. Plague as a biological weapon: medical and public health management. JAMA 283: 2281-2290.
7. Titball, R. W., and E. D. Williamson. 2004. Yersinia pestis (plague) vaccines. Expert Opin. Biol. Ther. 4: 965-973.
8. Smiley, S. T. 2008. Current challenges in the development of vaccines for pneumonic plague. Expert Rev. Vaccines 7: 209-221.
9. Bashaw, J., S. Norris, S. Weeks, S. Trevino, J. J. Adamovicz, and S. Welkos. 2007. Development of in vitro correlate assays of immunity to infection with Yersinia pestis. Clin. Vaccine Immunol. 14: 605-616.
10. Elvin, S. J., and E. D. Williamson. 2004. Stat 4 but not Stat 6 mediated immune mechanisms are essential in protection against plague. Microb. Pathog. 37: 177-184.
11. Parent, M. A., K. N. Berggren, L. W. Kummer, L. B. Wilhelm, F. M. Szaba, I. K. Mullarky, and S. T. Smiley. 2005. Cell-mediated protection against pulmonary Yersinia pestis infection. Infect. Immun. 73: 7304-7310.
12. Szaba, F. M., L. W. Kummer, L. B. Wilhelm, J. S. Lin, M. A. Parent, S. W. Montminy-Paquette, E. Lien, L. L. Johnson, and S. T. Smiley. 2009. D27-pLpxL, an avirulent strain of Yersinia pestis, primes T cells that protect against pneumonic plague. Infect. Immun. 77: 4295-4304.
13. Lin, J. S., S. Park, J. J. Adamovicz, J. Hill, J. B. Bliska, C. K. Cote, D. S. Perlin, K. Amemiya, and S. T. Smiley. 2010. TNFα and IFNα contribute to F1/LcrV-targeted immune defense in mouse models of fully virulent pneumonic plague. Vaccine. 29: 357-362.
14. Kummer, L. W., F. M. Szaba, M. A. Parent, J. J. Adamovicz, J. Hill, L. L. Johnson, and S. T. Smiley. 2008. Antibodies and cytokines independently protect against pneumonic plague. Vaccine 26: 6901-6907.
15. Parent, M. A., L. B. Wilhelm, L. W. Kummer, F. M. Szaba, I. K. Mullarky, and S. T. Smiley. 2006. Gamma interferon, tumor necrosis factor alpha, and nitric oxide synthase 2, key elements of cellular immunity, perform critical protective functions during humoral defense against lethal pulmonary Yersinia pestis infection. Infect. Immun. 74: 3381-3386.
16. Philipovskiy, A. V., and S. T. Smiley. 2007. Vaccination with live Yersinia pestis primes CD4 and CD8 T cells that synergistically protect against lethal pulmonary Y. pestis infection. Infect. Immun. 75: 878-885.
17. Korn, T., E. Bettelli, M. Oukka, and V. K. Kuchroo. 2009. IL-17 and Th17 Cells. Annu. Rev. Immunol. 27: 485-517.
18. Gaffen, S. L. 2009. Structure and signalling in the IL-17 receptor family. Nat. Rev. Immunol. 9: 556-567.
19. O'Connor, W., Jr., L. A. Zenewicz, and R. A. Flavell. 2010. The dual nature of T(H)17 cells: shifting the focus to function. Nat. Immunol. 11: 471-476.
20. Dubin, P. J., and J. K. Kolls. 2008. Th17 cytokines and mucosal immunity. Immunol. Rev. 226: 160-171.
21. Ouyang, W., J. K. Kolls, and Y. Zheng. 2008. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28: 454-467.
22. Infante-Duarte, C., H. F. Horton, M. C. Byrne, and T. Kamradt. 2000. Microbial lipopeptides induce the production of IL-17 in Th cells. J. Immunol. 165: 6107-6115.
23. Pène, J., S. Chevalier, L. Preisser, E. Vénéreau, M. H. Guilleux, S. Ghannam, J. P. Molès, Y. Danger, E. Ravon, S. Lesaux, et al. 2008. Chronically inflamed human tissues are infiltrated by highly differentiated Th17 lymphocytes. J. Immunol. 180: 7423-7430.
24. Langrish, C. L., Y. Chen, W. M. Blumenschein, J. Mattson, B. Basham, J. D. Sedgwick, T. McClanahan, R. A. Kastelein, and D. J. Cua. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201: 233-240.
25. Aujla, S. J., Y. R. Chan, M. Zheng, M. Fei, D. J. Askew, D. A. Pociask, T. A. Reinhart, F. McAllister, J. Edeal, K. Gaus, et al. 2008. IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nat. Med. 14: 275-281.
26. Lin, Y., S. Ritchea, A. Logar, S. Slight, M. Messmer, J. Rangel-Moreno, L. Guglani, J. F. Alcorn, H. Strawbridge, S. M. Park, 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.
27. Khader, S. A., G. K. Bell, J. E. Pearl, J. J. Fountain, J. Rangel-Moreno, G. E. Cilley, F. Shen, S. M. Eaton, S. L. Gaffen, S. L. Swain, 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.
28. Schulz, S. M., G. Köhler, N. Schütze, J. Knauer, R. K. Straubinger, A. A. Chackerian, E. Witte, K. Wolk, R. Sabat, Y. Iwakura, 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.
29. Meeks, K. D., A. N. Sieve, J. K. Kolls, N. Ghilardi, and R. E. Berg. 2009. IL-23 is required for protection against systemic infection with Listeria monocytogenes. J. Immunol. 183: 8026-8034.
30. Johnson, L. L., K. N. Berggren, F. M. Szaba, W. Chen, and S. T. Smiley. 2003. Fibrin-mediated protection against infection-stimulated immunopathology. J. Exp. Med. 197: 801-806.
31. Montminy, S. W., N. Khan, S. McGrath, M. J. Walkowicz, F. Sharp, J. E. Conlon, K. Fukase, S. Kusumoto, C. Sweet, K. Miyake, et al. 2006. Virulence factors of Yersinia pestis are overcome by a strong lipopolysaccharide response. Nat. Immunol. 7: 1066-1073.
32. Lukaszewski, R. A., D. J. Kenny, R. Taylor, D. G. Rees, M. G. Hartley, and P. C. Oyston. 2005. Pathogenesis of Yersinia pestis infection in BALB/c mice: effects on host macrophages and neutrophils. Infect. Immun. 73: 7142-7150.
33. Laws, T. R., M. S. Davey, R. W. Titball, and R. Lukaszewski. 2010. Neutrophils are important in early control of lung infection by Yersinia pestis. Microbes Infect. 12: 331-335.
34. Cowan, C., A. V. Philipovskiy, C. R. Wulff-Strobel, Z. Ye, and S. C. Straley. 2005. Anti-LcrV antibody inhibits delivery of Yops by Yersinia pestis KIM5 by directly promoting phagocytosis. Infect. Immun. 73: 6127-6137.
35. Umemura, M., A. Yahagi, S. Hamada, M. D. Begum, H. Watanabe, K. Kawakami, T. Suda, K. Sudo, S. Nakae, Y. Iwakura, and G. Matsuzaki. 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. Okamoto Yoshida, Y., M. Umemura, A. Yahagi, R. L. O'Brien, K. Ikuta, K. Kishihara, H. Hara, S. Nakae, Y. Iwakura, and G. Matsuzaki. 2010. Essential role of IL-17A in the formation of a mycobacterial infection-induced granuloma in the lung. J. Immunol. 184: 4414-4422.
37. Nakajima, R., V. L. Motin, and R. R. Brubaker. 1995. Suppression of cytokines in mice by protein A-V antigen fusion peptide and restoration of synthesis by active immunization. Infect. Immun. 63: 3021-3029.
38. Straley, S. C., and M. L. Cibull. 1989. Differential clearance and host-pathogen interactions of YopE- and YopK- YopL- Yersinia pestis in BALB/c mice. Infect. Immun. 57: 1200-1210.
39. Liang, S. C., X. Y. Tan, D. P. Luxenberg, R. Karim, K. Dunussi-Joannopoulos, M. Collins, and L. A. Fouser. 2006. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J. Exp. Med. 203: 2271-2279.
40. Zenewicz, L. A., G. D. Yancopoulos, D. M. Valenzuela, A. J. Murphy, M. Karow, and R. A. Flavell. 2007. Interleukin-22 but not interleukin-17 provides protection to hepatocytes during acute liver inflammation. Immunity 27: 647-659.
41. Zenewicz, L. A., G. D. Yancopoulos, D. M. Valenzuela, A. J. Murphy, S. Stevens, and R. A. Flavell. 2008. Innate and adaptive interleukin-22 protects mice from inflammatory bowel disease. Immunity 29: 947-957.
42. Muñoz, M., M. M. Heimesaat, K. Danker, D. Struck, U. Lohmann, R. Plickert, S. Bereswill, A. Fischer, I. R. Dunay, K. Wolk, et al. 2009. Interleukin (IL)-23 mediates Toxoplasma gondii-induced immunopathology in the gut via matrixmetalloproteinase-2 and IL-22 but independent of IL-17. J. Exp. Med. 206: 3047-3059.
43. Ma, H. L., S. Liang, J. Li, L. Napierata, T. Brown, S. Benoit, M. Senices, D. Gill, K. Dunussi-Joannopoulos, M. Collins, et al. 2008. IL-22 is required for Th17 cell-mediated pathology in a mouse model of psoriasis-like skin inflammation. J. Clin. Invest. 118: 597-607.
44. Sonnenberg, G. F., M. G. Nair, T. J. Kirn, C. Zaph, L. A. Fouser, and D. Artis. 2010. Pathological versus protective functions of IL-22 in airway inflammation are regulated by IL-17A. J. Exp. Med. 207: 1293-1305.
45. Chan, Y. R., J. S. Liu, D. A. Pociask, M. Zheng, T. A. Mietzner, T. Berger, T.W. Mak, M. C. Clifton, R. K. Strong, P. Ray, and J. K. Kolls. 2009. Lipocalin 2 is required for pulmonary host defense against Klebsiella infection. J. Immunol. 182: 4947-4956.
46. Karlsen, J. R., N. Borregaard, and J. B. Cowland. 2010. Induction of neutrophil gelatinase-associated lipocalin expression by co-stimulation with interleukin-17 and tumor necrosis factor-alpha is controlled by IkappaB-zeta but neither by C/EBP-beta nor C/EBP-delta. J. Biol. Chem. 285: 14088-14100.
47. Pepper, M., J. L. Linehan, A. J. Pagán, T. Zell, T. Dileepan, P. P. Cleary, and M. K. Jenkins. 2010. Different routes of bacterial infection induce long-lived TH1 memory cells and short-lived TH17 cells. Nat. Immunol. 11: 83-89.