T-bet regulates immunity to Francisella tularensis live vaccine strain infection, particularly in lungs

Infection and Immunity

Volumn 82, Issue 4, 2014, Pages 1477-1490

  Melillo, Amanda A ^a,d   Foreman, Oded ^b   Bosio, Catharine M ^c   Elkins, Karen L ^a  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^b GENENTECH INC   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 17; TRANSCRIPTION FACTOR T BET; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GROWTH; BACTERIAL IMMUNITY; BACTERIAL LOAD; CONTROLLED STUDY; CYTOKINE RELEASE; FRANCISELLA TULARENSIS LIVE VACCINE STRAIN INFECTION; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; LETHAL DOSE; LUNG ALVEOLUS MACROPHAGE; LUNG INFECTION; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL; T LYMPHOCYTE; TULAREMIA; UPREGULATION; VACCINATION; WILD TYPE;

ANIMALS; ANTIBODIES, BACTERIAL; BACTERIAL VACCINES; CYTOKINES; DISEASE MODELS, ANIMAL; FRANCISELLA TULARENSIS; IMMUNITY, CELLULAR; INTERFERON-GAMMA; LUNG; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHILS; NITRITES; SPLEEN; T-BOX DOMAIN PROTEINS; T-LYMPHOCYTES; TULAREMIA;

EID: 84896471373     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01545-13     Document Type: Article

References (42)

1. Elkins KL, Cowley SC, Bosio CM. 2007. Innate and adaptive immunity to Francisella. Ann. N. Y. Acad. Sci. 1105:284-324. http://dx.doi.org/10.1196/annals.1409.014.
2. Rick Lyons C, Wu TH. 2007. Animal models of Francisella tularensis infection. Ann. N. Y. Acad. Sci. 1105:238-265. http://dx.doi.org/10.1196/annals.1409.003.
3. De Pascalis R, Chou AY, Bosio CM, Huang CY, Follmann DA, Elkins KL. 2012. Development of functional and molecular correlates of vaccineinduced protection for a model intracellular pathogen, F. tularensis LVS. PLoS Pathog. 8:e1002494. http://dx.doi.org/10.1371/journal.ppat.1002494.
4. Cowley SC, Myltseva SV, Nano FE. 1996. Phase variation in Francisella tularensis affecting intracellular growth, lipopolysaccharide antigenicity, and nitric oxide production. Mol. Microbiol. 20:867-874. http://dx.doi.org/10.1111/j.1365-2958.1996.tb02524.x.
5. Eigelsbach HT, Downs CM. 1961. Prophylactic effectiveness of live and killed tularemia vaccines. J. Immunol. 87:415-425.
6. Chen W, KuoLee R, Shen H, Conlan JW. 2004. Susceptibility of immunodeficient mice to aerosol and systemic infection with virulent strains of Francisella tularensis. Microb. Pathog. 36:311-318. http://dx.doi.org/10.1016/j.micpath.2004.02.003.
7. Zhang D, Kuolee R, Harris G, Zhang Q, Conlan JW, Chen W. 2008. Lymphotoxin-alpha plays only a minor role in host resistance to respiratory infection with virulent typeAFrancisella tularensis in mice. Mediators Inflamm. 2008:239740. http://dx.doi.org/10.1155/2008/239740.
8. Lindgren H, Stenmark S, Chen W, Tarnvik A, Sjostedt A. 2004. Distinct roles of reactive nitrogen and oxygen species to control infection with the facultative intracellular bacterium Francisella tularensis. Infect. Immun. 72:7172-7182. http://dx.doi.org/10.1128/IAI.72.12.7172-7182.2004.
9. De Pascalis R, Taylor BC, Elkins KL. 2008. Diverse myeloid and lymphoid cell subpopulations produce gamma interferon during early innate immune responses to Francisella tularensis live vaccine strain. Infect. Immun. 76:4311-4321. http://dx.doi.org/10.1128/IAI.00514-08.
10. Szabo SJ, Kim ST, Costa GL, Zhang X, Fathman CG, Glimcher LH. 2000. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100:655-669. http://dx.doi.org/10.1016/S0092-8674(00)80702-3.
11. Szabo SJ, Sullivan BM, Stemmann C, Satoskar AR, Sleckman BP, Glimcher LH. 2002. Distinct effects of T-bet in TH1 lineage commitment and IFN-gamma production in CD4 and CD8 T cells. Science 295:338-342. http://dx.doi.org/10.1126/science.1065543.
12. Mayer KD, Mohrs K, Reiley W, Wittmer S, Kohlmeier JE, Pearl JE, Cooper AM, Johnson LL, Woodland DL, Mohrs M. 2008. Cutting edge: T-bet and IL-27R are critical for in vivo IFN-gamma production by CD8 T cells during infection. J. Immunol. 180:693-697.
13. Sullivan BM, Juedes A, Szabo SJ, von Herrath M, Glimcher LH. 2003. Antigen-driven effector CD8 T cell function regulated by T-bet. Proc. Natl. Acad. Sci. U. S. A. 100:15818-15823. http://dx.doi.org/10.1073/pnas.2636938100.
14. Townsend MJ, Weinmann AS, Matsuda JL, Salomon R, Farnham PJ, Biron CA, Gapin L, Glimcher LH. 2004. T-bet regulates the terminal maturation and homeostasis of NK and Valpha14i NKT cells. Immunity 20:477-494. http://dx.doi.org/10.1016/S1074-7613(04)00076-7.
15. Esensten JH, Lee MR, Glimcher LH, Bluestone JA. 2009. T-bet-deficient NOD mice are protected from diabetes due to defects in both T cell and innate immune system function. J. Immunol. 183:75-82. http://dx.doi.org/10.4049/jimmunol.0804154.
16. Peng SL, Szabo SJ, Glimcher LH. 2002. T-bet regulates IgG class switching and pathogenic autoantibody production. Proc. Natl. Acad. Sci. U. S. A. 99:5545-5550. http://dx.doi.org/10.1073/pnas.082114899.
17. Rosas LE, Snider HM, Barbi J, Satoskar AA, Lugo-Villarino G, Keiser T, Papenfuss T, Durbin JE, Radzioch D, Glimcher LH, Satoskar AR. 2006. Cutting edge: STAT1 and T-bet play distinct roles in determining outcome of visceral leishmaniasis caused by Leishmania donovani. J. Immunol. 177:22-25.
18. Sullivan BM, Jobe O, Lazarevic V, Vasquez K, Bronson R, Glimcher LH, Kramnik I. 2005. Increased susceptibility of mice lacking T-bet to infection with Mycobacterium tuberculosis correlates with increased IL-10 and decreased IFN-gamma production. J. Immunol. 175:4593-4602.
19. Ravindran R, Foley J, Stoklasek T, Glimcher LH, McSorley SJ. 2005. Expression of T-bet by CD4 T cells is essential for resistance to Salmonella infection. J. Immunol. 175:4603-4610.
20. Bakshi CS, Malik M, Carrico PM, Sellati TJ. 2006. T-bet deficiency facilitates airway colonization by Mycoplasma pulmonis in a murine model of asthma. J. Immunol. 177:1786-1795.
21. Bosio CM, Elkins KL. 2001. Susceptibility to secondary Francisella tularensis LVS infection in B cell deficient mice is associated with neutrophilia but not with defects in specific T cell mediated immunity. Infect. Immun. 69:194-203. http://dx.doi.org/10.1128/IAI.69.1.194-203.2001.
22. Cowley SC, Elkins KL. 2003. Multiple T cell subsets control Francisella tularensis LVS intracellular growth without stimulation through macrophage interferon gamma receptors. J. Exp. Med. 198:379-389. http://dx.doi.org/10.1084/jem.20030687.
23. Rhinehart-Jones TR, Fortier AH, Elkins KL. 1994. Transfer of immunity against lethal murine Francisella infection by specific antibody depends on host gamma interferon and T cells. Infect. Immun. 62:3129-3137.
24. Reed LJ, Muench H. 1938. A simple method of estimating fifty per cent endpoints. Am. J. Hyg. 25:493-497.
25. - double-negative T cells are prominent producers of IL-17A and IFN-gamma during primary respiratory murine infection with Francisella tularensis live vaccine strain. J. Immunol. 184:5791-5801. http://dx.doi.org/10.4049/jimmunol.1000362.
26. Elkins KL, Rhinehart-Jones TR, Culkin SJ, Yee D, Winegar RK. 1996. Minimal requirements for murine resistance to infection with Francisella tularensis LVS. Infect. Immun. 64:3288-3293.
27. Leiby DA, Fortier AH, Crawford RM, Schreiber RD, Nacy CA. 1992. In vivo modulation of the murine immune response to Francisella tularensis LVS by administration of anticytokine antibodies. Infect. Immun. 60:84-89.
28. Cobb D, Hambright D, Smeltz RB. 2010. T-bet-independent effects of IL-12 family cytokines on regulation of Th17 responses to experimental T. cruzi infection. J. Leukoc. Biol. 88:965-971. http://dx.doi.org/10.1189/jlb.0410238.
29. Pearce EL, Mullen AC, Martins GA, Krawczyk CM, Hutchins AS, Zediak VP, Banica M, DiCioccio CB, Gross DA, Mao CA, Shen H, Cereb N, Yang SY, Lindsten T, Rossant J, Hunter CA, Reiner SL. 2003. Control of effector CD8+ T cell function by the transcription factor eomesodermin. Science 302:1041-1043. http://dx.doi.org/10.1126/science.1090148.
30. Yang Y, Xu J, Niu Y, Bromberg JS, Ding Y. 2008. T-bet and eomesodermin play critical roles in directing T cell differentiation to Th1 versus Th17. J. Immunol. 181:8700-8710.
31. Lin Y, Ritchea S, Logar A, Slight S, Messmer M, Rangel-Moreno J, Guglani L, Alcorn JF, Strawbridge H, Park SM, Onishi R, Nyugen N, Walter MJ, Pociask D, Randall TD, Gaffen SL, Iwakura Y, Kolls JK, Khader SA. 2009. Interleukin-17 is required for T helper 1 cell immunity and host resistance to the intracellular pathogen Francisella tularensis. Immunity 31:799-810. http://dx.doi.org/10.1016/j.immuni.2009.08.025.
32. Conlan JW, KuoLee R, Shen H, Webb A. 2002. Different host defences are required to protect mice from primary systemic vs pulmonary infection with the facultative intracellular bacterial pathogen, Francisella tularensis LVS. Microb. Pathog. 32:127-134. http://dx.doi.org/10.1006/mpat.2001.0489.
33. Sjöstedt A, Conlan JW, North RJ. 1994. Neutrophils are critical for host defense against primary infection with the facultative intracellular bacterium Francisella tularensis in mice and participate in defense against reinfection. Infect. Immun. 62:2779-2783.
34. McCaffrey RL, Allen LA. 2006. Francisella tularensis LVS evades killing by human neutrophils via inhibition of the respiratory burst and phagosome escape. J. Leukoc. Biol. 80:1224-1230. http://dx.doi.org/10.1189/jlb.0406287.
35. McCaffrey RL, Schwartz JT, Lindemann SR, Moreland JG, Buchan BW, Jones BD, Allen LA. 2010. Multiple mechanisms of NADPH oxidase inhibition by type A and type B Francisella tularensis. J. Leukoc. Biol. 88:791-805. http://dx.doi.org/10.1189/jlb.1209811.
36. Malik M, Bakshi CS, McCabe K, Catlett SV, Shah A, Singh R, Jackson PL, Gaggar A, Metzger DW, Melendez JA, Blalock JE, Sellati TJ. 2007. Matrix metalloproteinase 9 activity enhances host susceptibility to pulmonary infection with type A and B strains of Francisella tularensis. J. Immunol. 178:1013-1020.
37. Henry T, Kirimanjeswara GS, Ruby T, Jones JW, Peng K, Perret M, Ho L, Sauer JD, Iwakura Y, Metzger DW, Monack DM. 2010. Type I IFN signaling constrains IL-17A/F secretion by gammadelta T cells during bacterial infections. J. Immunol. 184:3755-3767. http://dx.doi.org/10.4049/jimmunol.0902065.
38. Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM, Weaver CT. 2005. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6:1123-1132. http://dx.doi.org/10.1038/ni1254.
39. Mathur AN, Chang HC, Zisoulis DG, Kapur R, Belladonna ML, Kansas GS, Kaplan MH. 2006. T-bet is a critical determinant in the instability of the IL-17-secreting T-helper phenotype. Blood 108:1595-1601. http://dx.doi.org/10.1182/blood-2006-04-015016.
40. Park IK, Shultz LD, Letterio JJ, Gorham JD. 2005. TGF-beta1 inhibits T-bet induction by IFN-gamma in murine CD4+ T cells through the protein tyrosine phosphatase Src homology region 2 domain-containing phosphatase-1. J. Immunol. 175:5666-5674.
41. Markel G, Bar-Haim E, Zahavy E, Cohen H, Cohen O, Shafferman A, Velan B. 2010. The involvement of IL-17A in the murine response to sub-lethal inhalational infection with Francisella tularensis. PLoS One 5:e11176. http://dx.doi.org/10.1371/journal.pone.0011176.
42. Hall JD, Woolard MD, Gunn BM, Craven RR, Taft-Benz S, Frelinger JA, Kawula TH. 2008. Infected-host-cell repertoire and cellular response in the lung following inhalation of Francisella tularensis Schu S4, LVS, or U112. Infect Immun. 76:5843-5852. http://dx.doi.org/10.1128/IAI.01176-08.