MyD88 deficiency leads to decreased NK cell gamma interferon production and T cell recruitment during chlamydia muridarum genital tract infection, but a predominant Th1 response and enhanced monocytic inflammation are associated with infection resolution

Infection and Immunity

Volumn 79, Issue 1, 2011, Pages 486-498

  Nagarajan, Uma M ^a   Sikes, James ^a   Prantner, Daniel ^a   Andrews Jr , Charles W ^b   Frazer, Lauren ^c   Goodwin, Anna ^a,d   Snowden, Jessica N ^a,e   Darville, Toni ^a,d  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b Milstead Pathology   (United States)

^c UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^d CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^e UNIVERSITY OF NEBRASKA AT OMAHA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 12P70; INTERLEUKIN 17; INTERLEUKIN 18; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHLAMYDIA; CHLAMYDIASIS; CYTOKINE PRODUCTION; FEMALE; FEMALE GENITAL TRACT INFECTION; MONOCYTE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; TH1 CELL;

ANIMALS; CHLAMYDIA INFECTIONS; CHLAMYDIA MURIDARUM; FALLOPIAN TUBES; FEMALE; GENE EXPRESSION REGULATION; INFLAMMATION; INTERFERON-GAMMA; INTERLEUKINS; KILLER CELLS, NATURAL; MICE; MICE, KNOCKOUT; MONOCYTES; MYELOID DIFFERENTIATION FACTOR 88; RNA, MESSENGER; T-LYMPHOCYTES; TH1 CELLS; TOLL-LIKE RECEPTOR 4; UTERUS; VAGINITIS;

EID: 78650879482     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00843-10     Document Type: Article

References (32)

1. Adachi, O., T. Kawai, K. Takeda, M. Matsumoto, H. Tsutsui, M. Sakagami, K. Nakanishi, and S. Akira. 1998. Targeted disruption of the MyD88 gene results in loss of IL-1-and IL-18-mediated function. Immunity 9:143-150.
2. Caldwell, H. D., J. Kromhout, and J. Schachter. 1981. Purification and partial characterization of the major outer membrane protein of Chlamydia trachomatis. Infect. Immun. 31:1161-1176.
3. Chen, L., L. Lei, X. Chang, Z. Li, C. Lu, X. Zhang, Y. Wu, I. T. Yeh, and G. Zhong. 2010. Mice deficient in MyD88 develop a Th2-dominant response and severe pathology in the upper genital tract following Chlamydia muri-darum infection. J. Immunol. 184:2602-2610.
4. Cohen, C. R., K. M. Koochesfahani, A. S. Meier, C. Shen, K. Karunakaran, B. Ondondo, T. Kinyari, N. R. Mugo, R. Nguti, and R. C. Brunham. 2005. Immunoepidemiologic profile of Chlamydia trachomatis infection: impor tance of heat-shock protein 60 and interferon-gamma. J. Infect. Dis. 192: 591-599.
5. Darville, T., C. W. Andrews, Jr., K. K. Laffoon, W. Shymasani, L. R. Kishen, and R. G. Rank. 1997. Mouse strain-dependent variation in the course and outcome of chlamydial genital tract infection is associated with differences in host response. Infect. Immun. 65:3065-3073.
6. Darville, T., C. W. Andrews, Jr., J. D. Sikes, P. L. Fraley, L. Braswell, and R. G. Rank. 2001. Mouse strain-dependent chemokine regulation of the genital tract T helper cell type 1 immune response. Infect. Immun. 69:7419-7424.
7. Darville, T., C. W. Andrews, Jr., J. D. Sikes, P. L. Fraley, and R. G. Rank. 2001. Early local cytokine profiles in strains of mice with different outcomes from chlamydial genital tract infection. Infect. Immun. 69:3556-3561.
8. Darville, T., J. M. O'Neill, C. W. Andrews, Jr., U. M. Nagarajan, L. Stahl, and D. M. Ojcius. 2003. Toll-like receptor-2, but not toll-like receptor-4, is essential for development of oviduct pathology in chlamydial genital tract infection. J. Immunol. 171:6187-6197.
9. Fehniger, T. A., M. H. Shah, M. J. Turner, J. B. VanDeusen, S. P. Whitman, M. A. Cooper, K. Suzuki, M. Wechser, F. Goodsaid, and M. A. Caligiuri. 1999. Differential cytokine and chemokine gene expression by human NK cells following activation with IL-18 or IL-15 in combination with IL-12: implications for the innate immune response. J. Immunol. 162:4511-4520.
10. Fremond, C. M., V. Yeremeev, D. M. Nicolle, M. Jacobs, V. F. Quesniaux, and B. Ryffel. 2004. Fatal Mycobacterium tuberculosis infection despite adaptive immune response in the absence of MyD88. J. Clin. Invest. 114: 1790-1799.
11. Hvid, M., A. Baczynska, B. Deleuran, J. Fedder, H. J. Knudsen, G. Christiansen, and S. Birkelund. 2007. Interleukin-1 is the initiator of fallopian tube destruction during Chlamydia trachomatis infection. Cell. Microbiol. 12:2795-2803.
12. Jia, T., I. Leiner, G. Dorothee, K. Brandl, and E. G. Pamer. 2009. MyD88 and type I interferon receptor-mediated chemokine induction and monocyte recruitment during Listeria monocytogenes infection. J. Immunol. 183:1271-1278.
13. Kawai, T., O. Adachi, T. Ogawa, K. Takeda, and S. Akira. 1999. Unrespon-siveness of MyD88-deficient mice to endotoxin. Immunity 11:115-122.
14. Kelly, K. A., E. A. Robinson, and R. G. Rank. 1996. Initial route of antigen administration alters the T-cell cytokine profile produced in response to the mouse pneumonitis biovar of Chlamydia trachomatis following genital infection. Infect. Immun. 64:4976-4983.
15. Erratum, 65:2508, 1997.
16. Kupfer, A., S. J. Singer, C. A. Janeway, Jr., and S. L. Swain. 1987. Coclus-tering of CD4 (L3T4) molecule with the T-cell receptor is induced by specific direct interaction of helper T cells and antigen-presenting cells. Proc. Natl. Acad. Sci. U.S.A. 84:5888-5892.
17. LaRosa, D. F., J. S. Stumhofer, A. E. Gelman, A. H. Rahman, D. K. Taylor, C. A. Hunter, and L. A. Turka. 2008. T cell expression of MyD88 is required for resistance to Toxoplasma gondii. Proc. Natl. Acad. Sci. U.S.A. 105: 3855-3860.
18. Lin, Y., S. Ritchea, A. Logar, S. Slight, M. Messmer, J. Rangel-Moreno, L. Guglani, J. F. Alcorn, H. Strawbridge, S. M. Park, R. Onishi, N. Nyugen, M. J. Walter, D. Pociask, T. D. Randall, S. L. Gaffen, Y. Iwakura, J. K. Kolls, and S. A. Khader. 2009. Interleukin-17 is required for T helper 1 cell immunity and host resistance to the intracellular pathogen Francisella tula-rensis. Immunity 31:799-810.
19. Murthy, A. K., J. P. Chambers, P. A. Meier, G. Zhong, and B. P. Arulanan-dam. 2007. Intranasal vaccination with a secreted chlamydial protein enhances resolution of genital Chlamydia muridarum infection, protects against oviduct pathology, and is highly dependent upon endogenous gamma interferon production. Infect. Immun. 75:666-676.
20. Nagarajan, U. M., D. M. Ojcius, L. Stahl, R. G. Rank, and T. Darville. 2005. Chlamydia trachomatis induces expression of IFN-gamma-inducible protein 10 and IFN-beta independent of TLR2 and TLR4, but largely dependent on MyD88. J. Immunol. 175:450-460.
21. Naiki, Y., K. S. Michelsen, N. W. Schroder, R. Alsabeh, A. Slepenkin, W. Zhang, S. Chen, B. Wei, Y. Bulut, M. H. Wong, E. M. Peterson, and M. Arditi. 2005. MyD88 is pivotal for the early inflammatory response and subsequent bacterial clearance and survival in a mouse model of Chlamydia pneumoniae pneumonia. J. Biol. Chem. 280:29242-29249.
22. Natividad, A., M. J. Holland, K. A. Rockett, J. Forton, N. Faal, H. M. Joof, D. C. Mabey, R. L. Bailey, and D. P. Kwiatkowski. 2008. Susceptibility to sequelae of human ocular chlamydial infection associated with allelic variation in IL10 cis-regulation. Hum. Mol. Genet. 17:323-329.
23. O'Connell, C. M., I. A. Ionova, A. J. Quayle, A. Visintin, and R. R. Ingalls. 2006. Localization of TLR2 and MyD88 to Chlamydia trachomatis inclusions. Evidence for signaling by intracellular TLR2 during infection with an obligate intracellular pathogen. J. Biol. Chem. 281:1652-1659.
24. Prantner, D., T. Darville, and U. M. Nagarajan. 2010. Stimulator of IFN gene is critical for induction of IFN-beta during Chlamydia muridarum infection. J. Immunol. 184:2551-2560.
25. Prantner, D., T. Darville, J. D. Sikes, C. W. Andrews, Jr., H. Brade, R. G. Rank, and U. M. Nagarajan. 2009. Critical role for interleukin-1beta (IL-1beta) during Chlamydia muridarum genital infection and bacterial replication-independent secretion of IL-1beta in mouse macrophages. Infect. Im-mun. 77:5334-5346.
26. Ramsey, K. H., L. S. Soderberg, and R. G. Rank. 1988. Resolution of chlamydial genital infection in B-cell-deficient mice and immunity to reinfection. Infect. Immun. 56:1320-1325.
27. Ruckdeschel, K., G. Pfaffinger, R. Haase, A. Sing, H. Weighardt, G. Hacker, B. Holzmann, and J. Heesemann. 2004. Signaling of apoptosis through TLRs critically involves toll/IL-1 receptor domain-containing adapter inducing IFN-beta, but not MyD88, in bacteria-infected murine macrophages. J. Immunol. 173:3320-3328.
28. Su, H., R. Messer, W. Whitmire, E. Fischer, J. C. Portis, and H. D. Caldwell. 1998. Vaccination against chlamydial genital tract infection after immunization with dendritic cells pulsed ex vivo with nonviable chlamydiae. J. Exp. Med. 188:809-818.
29. Tseng, C. K., and R. G. Rank. 1998. Role of NK cells in the early host response to chlamydial genital infection. Infect. Immun. 66:5867-5875.
30. Welter-Stahl, L., D. M. Ojcius, G. Viale, S. Girardin, W. Liu, C. Delarbre, D. Philpott, K. A. Kelly, and T. Darville. 2006. Stimulation of the cytosolic receptor for peptidoglycan, Nod1, by infection with Chlamydia trachomatis or Chlamydia muridarum. Cell. Microbiol. 8:1047-1057.
31. Wherry, J. C., R. D. Schreiber, and E. R. Unanue. 1991. Regulation of gamma interferon production by natural killer cells in scid mice: roles of tumor necrosis factor and bacterial stimuli. Infect. Immun. 59:1709-1715.
32. Zhang, X., L. Gao, L. Lei, Y. Zhong, P. Dube, M. T. Berton, B. Arulanandam, J. Zhang, and G. Zhong. 2009. A MyD88-dependent early IL-17 production protects mice against airway infection with the obligate intracellular pathogen Chlamydia muridarum. J. Immunol. 183:1291-1300.