Mice deficient in MyD88 develop a Th2-dominant response and severe pathology in the upper genital tract following Chlamydia muridarum infection

Journal of Immunology

Volumn 184, Issue 5, 2010, Pages 2602-2610

  Chen, Lili ^a,b   Lei, Lei ^a   Chang, Xiaotong ^a   Li, Zhihong ^a   Lu, Chunxue ^a,b   Zhang, Xiaoyun ^a   Wu, Yimou ^b   Yeh, I Tien ^a   Zhong, Guangming ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b UNIVERSITY OF SOUTH CHINA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MYELOID DIFFERENTIATION FACTOR 88; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; MYD88 PROTEIN, MOUSE; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHLAMYDIA; CHLAMYDIASIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE DURATION; DISEASE SEVERITY; FEMALE; FEMALE GENITAL TRACT INFECTION; HELA CELL; HOST; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INFECTION RESISTANCE; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SAMPLING; SIGNAL TRANSDUCTION; TH17 CELL; TH2 CELL; UROGENITAL TRACT INFECTION; WILD TYPE; ANIMAL; C57BL MOUSE; GENETICS; HELPER CELL; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; TH1 CELL; UROGENITAL SYSTEM; VAGINA;

ADAPTIVE IMMUNITY; ANIMALS; CHLAMYDIA INFECTIONS; CHLAMYDIA MURIDARUM; FEMALE; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERLEUKIN-17; INTERLEUKIN-1ALPHA; INTERLEUKIN-6; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; T-LYMPHOCYTES, HELPER-INDUCER; TH1 CELLS; TH2 CELLS; TUMOR NECROSIS FACTOR-ALPHA; UROGENITAL SYSTEM; VAGINA;

EID: 77951913183     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901593     Document Type: Article

References (51)

1. Grayston, J. T. 1992. Chlamydia pneumoniae, strain TWAR pneumonia. Annu. Rev. Med. 43: 317-323.
2. Hu, H., G. N. Pierce, and G. Zhong. 1999. The atherogenic effects of chlamydia are dependent on serum cholesterol and specific to Chlamydia pneumoniae. J. Clin. Invest. 103: 747-753.
3. Sherman, K. J., J. R. Daling, A. Stergachis, N. S. Weiss, H. M. Foy, S. P. Wang, and J. T. Grayston. 1990. Sexually transmitted diseases and tubal pregnancy. Sex. Transm. Dis. 17: 115-121.
4. Stephens, R. S. 2003. The cellular paradigm of chlamydial pathogenesis. Trends Microbiol. 11: 44-51.
5. Cotter, T. W., Q. Meng, Z. L. Shen, Y. X. Zhang, H. Su, and H. D. Caldwell. 1995. Protective efficacy of major outer membrane protein-specific immunoglobulin A (IgA) and IgG monoclonal antibodies in a murine model of Chlamydia trachomatis genital tract infection. Infect. Immun. 63: 4704-4714.
6. Pal, S., E. M. Peterson, and L. M. de la Maza. 2005. Vaccination with the Chlamydia trachomatis major outer membrane protein can elicit an immune response as protective as that resulting from inoculation with live bacteria. Infect. Immun. 73: 8153-8160.
7. Lu, H., and G. Zhong. 1999. Interleukin-12 production is required for chlamydial antigen-pulsed dendritic cells to induce protection against live Chlamydia trachomatis infection. Infect. Immun. 67: 1763-1769.
8. Murthy, A. K., J. Sharma, J. J. Coalson, G. Zhong, and B. P. Arulanandam. 2004. Chlamydia trachomatis pulmonary infection induces greater inflammatory pathology in immunoglobulin A deficient mice. Cell. Immunol. 230: 56-64.
9. Morrison, S. G., and R. P. Morrison. 2005. A predominant role for antibody in acquired immunity to chlamydial genital tract reinfection. J. Immunol. 175: 7536-7542.
10. Shah, A. A., J. H. Schripsema, M. T. Imtiaz, I. M. Sigar, J. Kasimos, P. G. Matos, S. Inouye, and K. H. Ramsey. 2005. Histopathologic changes related to fibrotic oviduct occlusion after genital tract infection of mice with Chlamydia muridarum. Sex. Transm. Dis. 32: 49-56.
11. Bulut, Y., E. Faure, L. Thomas, H. Karahashi, K. S. Michelsen, O. Equils, S. G. Morrison, R. P. Morrison, and M. Arditi. 2002. Chlamydial heat shock protein 60 activates macrophages and endothelial cells through Toll-like receptor 4 and MD2 in a MyD88-dependent pathway. J. Immunol. 168: 1435-1440.
12. Arancibia, S. A., C. J. Beltrán, I. M. Aguirre, P. Silva, A. L. Peralta, F. Malinarich, and M. A. Hermoso. 2007. Toll-like receptors are key participants in innate immune responses. Biol. Res. 40: 97-112.
13. Zhao, Y., C. De Trez, R. Flynn, C. F. Ware, M. Croft, and S. Salek-Ardakani. 2009. The adaptor molecule MyD88 directly promotes CD8 T cell responses to vaccinia virus. J. Immunol. 182: 6278-6286.
14. Muraille, E., C. De Trez, M. Brait, P. De Baetselier, O. Leo, and Y. Carlier. 2003. Genetically resistant mice lacking MyD88-adapter protein display a high susceptibility to Leishmania major infection associated with a polarized Th2 response. J. Immunol. 170: 4237-4241. (Pubitemid 36428190)
15. Debus, A., J. Gläsner, M. Röllinghoff, and A. Gessner. 2003. High levels of susceptibility and T helper 2 response in MyD88-deficient mice infected with Leishmania major are interleukin-4 dependent. Infect. Immun. 71: 7215-7218.
16. Kenny, E. F., and L. A. O'Neill. 2008. Signalling adaptors used by Toll-like receptors: an update. Cytokine 43: 342-349.
17. Kopp, E., and R. Medzhitov. 2003. Recognition of microbial infection by Toll-like receptors. Curr. Opin. Immunol. 15: 396-401.
18. O'Neill, L. A. 2006. How Toll-like receptors signal: what we know and what we don't know. Curr. Opin. Immunol. 18: 3-9.
19. De Luca, A., C. Montagnoli, T. Zelante, P. Bonifazi, S. Bozza, S. Moretti, C. D'Angelo, C. Vacca, L. Boon, F. Bistoni, et al. 2007. Functional yet balanced reactivity to Candida albicans requires TRIF, MyD88, and IDO-dependent inhibition of Rorc. J. Immunol. 179: 5999-6008.
20. Takeda, K., and S. Akira. 2005. Toll-like receptors in innate immunity. Int. Immunol. 17: 1-14.
21. Yamamoto, M., S. Sato, H. Hemmi, K. Hoshino, T. Kaisho, H. Sanjo, O. Takeuchi, M. Sugiyama, M. Okabe, K. Takeda, and S. Akira. 2003. Role of adaptor TRIF in the MyD88-independent Toll-like receptor signaling pathway. Science 301: 640-643. (Pubitemid 36927946)
22. Wieland, C. W., S. Florquin, N. A. Maris, K. Hoebe, B. Beutler, K. Takeda, S. Akira, and T. van der Poll. 2005. The MyD88-dependent, but not the MyD88-independent, pathway of TLR4 signaling is important in clearing nontypeable Haemophilus influenzae from the mouse lung. J. Immunol. 175: 6042-6049.
23. Wiersinga, W. J., C. W. Wieland, J. J. Roelofs, and T. van der Poll. 2008. MyD88 dependent signaling contributes to protective host defense against Burkholderia pseudomallei. PLoS One 3: e3494.
24. Skerrett, S. J., H. D. Liggitt, A. M. Hajjar, and C. B. Wilson. 2004. Cutting edge: myeloid differentiation factor 88 is essential for pulmonary host defense against Pseudomonas aeruginosa but not Staphylococcus aureus. J. Immunol. 172: 3377-3381.
25. Macedo, G. C., D. M. Magnani, N. B. Carvalho, O. Bruna-Romero, R. T. Gazzinelli, and S. C. Oliveira. 2008. Central role of MyD88-dependent dendritic cell maturation and proinflammatory cytokine production to control Brucella abortus infection. J. Immunol. 180: 1080-1087.
26. Oliveira, S. C., F. S. de Oliveira, G. C. Macedo, L. A. de Almeida, and N. B. Carvalho. 2008. The role of innate immune receptors in the control of Brucella abortus infection: Toll-like receptors and beyond. Microbes Infect. 10: 1005-1009.
27. Mun, H. S., F. Aosai, K. Norose, M. Chen, L. X. Piao, O. Takeuchi, S. Akira, H. Ishikura, and A. Yano. 2003. TLR2 as an essential molecule for protective immunity against Toxoplasma gondii infection. Int. Immunol. 15: 1081-1087.
28. + T cell priming during respiratory fungal infection. Immunity 25: 665-675.
29. von Bernuth, H., C. Picard, Z. Jin, R. Pankla, H. Xiao, C. L. Ku, M. Chrabieh, I. B. Mustapha, P. Ghandil, Y. Camcioglu, et al. 2008. Pyogenic bacterial infections in humans with MyD88 deficiency. Science 321: 691-696.
30. Naiki, Y., K. S. Michelsen, N. W. Schröder, R. Alsabeh, A. Slepenkin, W. Zhang, S. Chen, B. Wei, Y. Bulut, M. H. Wong, et al. 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.
31. Rodriguez, N., F. Fend, L. Jennen, M. Schiemann, N. Wantia, C. U. Prazeres da Costa, S. Dürr, U. Heinzmann, H. Wagner, and T. Miethke. 2005. Polymorphonuclear neutrophils improve replication of Chlamydia pneumoniae in vivo upon MyD88-dependent attraction. J. Immunol. 174: 4836-4844. (Pubitemid 40504567)
32. Netea, M. G., B. J. Kullberg, L. E. Jacobs, T. J. Verver-Jansen, J. van der Ven-Jongekrijg, J. M. Galama, A. F. Stalenhoef, C. A. Dinarello, and J. W. Van der Meer. 2004. Chlamydia pneumoniae stimulates IFN-γ synthesis throughMyD88-dependent, TLR2- and TLR4-independent induction of IL-18 release. J. Immunol. 173: 1477-1482.
33. Rothfuchs, A. G., C. Trumstedt, H. Wigzell, and M. E. Rottenberg. 2004. Intracellular bacterial infection-induced IFN-γ is critically but not solely dependent on Toll-like receptor 4-myeloid differentiation factor 88-IFN-αβ-STAT1 signaling. J. Immunol. 172: 6345-6353.
34. Derbigny, W. A., M. S. Kerr, and R. M. Johnson. 2005. Pattern recognition molecules activated by Chlamydia muridarum infection of cloned murine oviduct epithelial cell lines. J. Immunol. 175: 6065-6075.
35. Nagarajan, U. M., D. M. Ojcius, L. Stahl, R. G. Rank, and T. Darville. 2005. Chlamydia trachomatis induces expression of IFN-γ-inducible protein 10 and IFN-β independent of TLR2 and TLR4, but largely dependent on MyD88. J. Immunol. 175: 450-460.
36. Mackern-Oberti, J. P., M. Maccioni, C. Cuffini, G. Gatti, and V. E. Rivero. 2006. Susceptibility of prostate epithelial cells to Chlamydia muridarum infection and their role in innate immunity by recruitment of intracellular Toll-like receptors 4 and 2 and MyD88 to the inclusion. Infect. Immun. 74: 6973-6981.
37. 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.
38. 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. (Pubitemid 37467242)
39. Chen, C., D. Chen, J. Sharma, W. Cheng, Y. Zhong, K. Liu, J. Jensen, R. Shain, B. Arulanandam, and G. Zhong. 2006. The hypothetical protein CT813 is localized in the Chlamydia trachomatis inclusion membrane and is immunogenic in women urogenitally infected with C. trachomatis. Infect. Immun. 74: 4826-4840.
40. Cheng, W., P. Shivshankar, Z. Li, L. Chen, I. T. Yeh, and G. Zhong. 2008. Caspase-1 contributes to Chlamydia trachomatis-induced upper urogenital tract inflammatory pathologies without affecting the course of infection. Infect. Immun. 76: 515-522.
41. Peterson, E. M., G. M. Zhong, E. Carlson, and L. M. de la Maza. 1988. Protective role of magnesium in the neutralization by antibodies of Chlamydia trachomatis infectivity. Infect. Immun. 56: 885-891.
42. Li, W., M. N. Guentzel, J. Seshu, G. Zhong, A. K. Murthy, and B. P. Arulanandam. 2007. Induction of cross-serovar protection against genital chlamydial infection by a targeted multisubunit vaccination approach. Clin. Vaccine Immunol. 14: 1537-1544.
43. Imtiaz, M. T., J. H. Schripsema, I. M. Sigar, J. N. Kasimos, and K. H. Ramsey. 2006. Inhibition of matrix metalloproteinases protects mice from ascending infection and chronic disease manifestations resulting from urogenital Chlamydia muridarum infection. Infect. Immun. 74: 5513-5521.
44. Zhong, G., I. Toth, R. Reid, and R. C. Brunham. 1993. Immunogenicity evaluation of a lipidic amino acid-based synthetic peptide vaccine for Chlamydia trachomatis. J. Immunol. 151: 3728-3736. (Pubitemid 23282685)
45. Zhong, G. M., and R. C. Brunham. 1990. Immunoaccessible peptide sequences of the major outer membrane protein from Chlamydia trachomatis serovar C. Infect. Immun. 58: 3438-3441.
46. Sharma, J., A. M. Bosnic, J. M. Piper, and G. Zhong. 2004. Human antibody responses to a Chlamydia-secreted protease factor. Infect. Immun. 72: 7164-7171.
47. Chen, L., W. Cheng, P. Shivshankar, L. Lei, X. Zhang, Y. Wu, I. T. Yeh, and G. Zhong. 2009. Distinct roles of CD28- and CD40L-mediated costimulation in the development of protective immunity and pathology during Chlamydia muridarum urogenital infection in mice. Infect. Immun. 77: 3080-3089.
48. Yang, X., K. T. HayGlass, and R. C. Brunham. 1996. Genetically determined differences in IL-10 and IFN-gamma responses correlate with clearance of Chlamydia trachomatis mouse pneumonitis infection. J. Immunol. 156: 4338-4344. (Pubitemid 26165833)
49. + T cells. Cell. Immunol. 242: 110-117.
50. Wang, S., Y. Fan, R. C. Brunham, and X. Yang. 1999. IFN-γ knockout mice show Th2-associated delayed-type hypersensitivity and the inflammatory cells fail to localize and control chlamydial infection. Eur. J. Immunol. 29: 3782-3792.
51. Yang, X. 2001. Distinct function of Th1 and Th2 type delayed type hypersensitivity: protective and pathological reactions to chlamydial infection. Microsc. Res. Tech. 53: 273-277.