Chlamydia heat shock protein 60 induces trophoblast apoptosis through TLR4

Journal of Immunology

Volumn 177, Issue 2, 2006, Pages 1257-1263

  Equils, Ozlem ^a,b   Lu, Daning ^a   Gatter, Mary ^c   Witkin, Steve S ^e   Bertolotto, Cristina ^a   Arditi, Moshe ^a   McGregor, James A ^d   Simmons, Charles F ^a   Hobel, Calvin J ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CEDARS SINAI MEDICAL CENTER   (United States)

^c Planned Parenthood   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^e WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; HEAT SHOCK PROTEIN 60; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4;

APOPTOSIS; ARTICLE; BACTERIAL INFECTION; CELL LINE; CHLAMYDIA; CHLAMYDIA TRACHOMATIS; CONTROLLED STUDY; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; IN VITRO STUDY; INFERTILITY; INNATE IMMUNITY; INTRAUTERINE GROWTH RETARDATION; INTRAUTERINE INFECTION; NONHUMAN; PATHOGENESIS; PLACENTA; PLACENTA DEVELOPMENT; PLACENTA FUNCTION; PREECLAMPSIA; PREGNANCY COMPLICATION; PREGNANCY OUTCOME; PREMATURE LABOR; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SEXUALLY TRANSMITTED DISEASE; TROPHOBLAST; UNITED STATES;

EID: 33745847809     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.2.1257     Document Type: Article

References (76)

1. Schachter, J., and C. R. Dawson. 1990. The epidemiology of trachoma predicts more blindness in the future. Scand. J. Infect. Dis. Suppl. 69: 55-62.
2. Stamm, W. E. 1999. Chlamydia trachomatis infections: progress and problems. J. Infect. Dis. 179(Suppl. 2): S380-S383.
3. McGregor, J. A., and J. I. French. 1991. Chlamydia trachomatis infection during pregnancy. Am. J. Obstet. Gynecol. 164: 1782-1789.
4. Dean, D., R. J. Suchland, and W. E. Stamm. 2000. Evidence for long-term cervical persistence of Chlamydia trachomatis by omp1 genotyping. J. Infect. Dis. 182: 909-916.
5. Beatty, W. L., R. P. Morrison, and G. I. Byrne. 1994. Persistent chlamydiae: from cell culture to a paradigm for chlamydial pathogenesis. Microbiol. Rev. 58: 686-699.
6. LaVerda, D., M. V. Kalayoglu, and G. I. Byrne. 1999. Chlamydial heat shock proteins and disease pathology: new paradigms for old problems? Infect Dis. Obstet. Gynecol. 7: 64-71.
7. Munoz, M. G., J. Jeremias, and S. S. Witkin. 1996. The 60 kDa heat shock protein in human semen: relationship with antibodies to spermatozoa and Chlamydia trachomatis. Hum. Reprod. 11: 2600-2603.
8. Neuer, A., K. N. Lam, F. W. Tiller, L. Kiesel, and S. S. Witkin. 1997. Humoral immune response to membrane components of Chlamydia trachomatis and expression of human 60 kDa heat shock protein in follicular fluid of in-vitro fertilization patients. Hum. Reprod. 12: 925-929.
9. Neuer, A., S. D. Spandorfer, P. Giraldo, S. Dieterle, Z. Rosenwaks, and S. S. Witkin. 2000. The role of heat shock proteins in reproduction. Hum. Reprod. Update 6: 149-159.
10. Raulston, J. E., C. H. Davis, T. R. Paul, J. D. Hobbs, and P. B. Wyrick. 2002. Surface accessibility of the 70-kilodalton Chlamydia trachomatis heat shock protein following reduction of outer membrane protein disulfide bonds. Infect. Immun. 70: 535-543.
11. Kawai, T., and S. Akira. 2005. Pathogen recognition with Toll-like receptors. Curr. Opin. Immunol. 17: 338-344.
12. Pasare, C., and R. Medzhitov. 2005. Toll-like receptors: linking innate and adaptive immunity. Adv. Exp. Med. Biol. 560: 11-18.
13. Aliprantis, A. O., R. B. Yang, M. R. Mark, S. Suggett, B. Devaux, J. D. Radolf, G. R. Klimpel, P. Godowski, and A. Zychlinsky. 1999. Cell activation and apoptosis by bacterial lipoproteins through Toll-like receptor-2. Science 285: 736-739.
14. Aliprantis, A. O., R. B. Yang, D. S. Weiss, P. Godowski, and A. Zychlinsky. 2000. The apoptotic signaling pathway activated by Toll-like receptor-2. EMBO J. 19: 3325-3336.
15. Lopez, M., L. M. Sly, Y. Luu, D. Young, H. Cooper, and N. E. Reiner. 2003. The 19-kDa Mycobacterium tuberculosis protein induces macrophage apoptosis through Toll-like receptor-2. J. Immunol. 170: 2409-2416.
16. Into, T., K. Kiura, M. Yasuda, H. Kataoka, N. Inoue, A. Hasebe, K. Takeda, S. Akira, and K. Shibata. 2004. Stimulation of human Toll-like receptor (TLR) 2 and TLR6 with membrane lipoproteins of Mycoplasma fermentans induces apoptotic cell death after NF-κB activation. Cell Microbiol. 6: 187-199.
17. Haase, R., C. J. Kirschning, A. Sing, P. Schrottner, K. Fukase, S. Kusumoto, H. Wagner, J. Heesemann, and K. Ruckdeschel. 2003. A dominant role of Toll-like receptor 4 in the signaling of apoptosis in bacteria-faced macrophages. J. Immunol. 171: 4294-4303.
18. 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-β, but not MyD88, in bacteria-infected murine macrophages. J. Immunol. 173: 3320-3328.
19. Hsu, L. C., J. M. Park, K. Zhang, J. L. Luo, S. Maeda, R. J. Kaufman, L. Eckmann, D. G. Guiney, and M. Karin. 2004. The protein kinase PKR is required for macrophage apoptosis after activation of Toll-like receptor 4. Nature 428: 341-345.
20. Pioli, P. A., E. Amiel, T. M. Schaefer, J. E. Connolly, C. R. Wira, and P. M. Guyre. 2004. Differential expression of Toll-like receptors 2 and 4 in tissues of the human female reproductive tract. Infect. Immun. 72: 5799-5806.
21. Fazeli, A., C. Bruce, and D. O. Anumba. 2005. Characterization of Toll-like receptors in the female reproductive tract in humans. Hum. Reprod. 20: 1372-1378.
22. Holmlund, U., G. Gebers, A. R. Dahlfors, B. Sandstedt, K. Bremme, E. S. Ekstrom, and A. Scheynius. 2002. Expression and regulation of the pattern recognition receptors Toll-like receptor-2 and Toll-like receptor-4 in the human placenta. Immunology 107: 145-151.
23. Kumazaki, K., M. Nakayama, I, Yanagihara, N. Suehara, and Y. Wada. 2004. Immunohistochemical distribution of Toll-like receptor 4 in term and preterm human placentas from normal and complicated pregnancy including chorioamnionitis. Hum. Pathol 35: 47-54.
24. Schaefer, T. M., K. Desouza, J. V. Fahey, K. W. Beagley, and C. R. Wira. 2004. Toll-like receptor (TLR) expression and TLR-mediated cytokine/chemokine production by human uterine epithelial cells. Immunology 112: 428-436.
25. Fichorova, R. N., A. O. Cronin, E. Lien, D. J. Anderson, and R. R. Ingalls. 2002. Response to Neisseria gonorrhoeae by cervicovaginal epithelial cells occurs in the absence of Toll-like receptor 4-mediated signaling. J. Immunol. 168: 2424-2432.
26. Schaefer, T. M., J. V. Fahey, J. A. Wright, and C. R. Wira. 2005. Innate immunity in the human female reproductive tract: antiviral response of uterine epithelial cells to the TLR3 agonist poly(I:C). J. Immunol. 174: 992-1002.
27. Abrahams, V. M., P. Bole-Aldo, Y. M. Kim, S. L. Straszewski-Chavez, T. Chaiworapongsa, R. Romero, and G. Mor. 2004. Divergent trophoblast responses to bacterial products mediated by TLRs. J. Immunol. 173: 4286-4296.
28. Varner, M. W., and M. S. Esplin. 2005. Current understanding of genetic factors in preterm birth. Bjog 112(Suppl. 1): 28-31.
29. 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.
30. Tsuchiya, S., M. Yamabe, Y. Yamaguchi, Y. Kobayashi, T. Konno, and K. Tada. 1980. Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int. J. Cancer 26: 171-176.
31. Hogan, M. M., and S. N. Vogel. 1987. Lipid A-associated proteins provide an alternate "second signal" in the activation of recombinant interferon-γ-primed, C3H/HeJ macrophages to a fully tumoricidal state. J. Immunol. 139: 3697-3702.
32. Hogan, M. M., and S. N. Vogel. 1988. Production of tumor necrosis factor by rIFN-γ-primed C3H/HeJ (Lpsd) macrophages requires the presence of lipid A-associated proteins. J. Immunol. 141: 4196-4202.
33. LaVerda, D., L. N. Albanese, P. E. Ruther, S. G. Morrison, R. P. Morrison, K. A. Ault, and G. I. Byrne. 2000. Seroreactivity to Chlamydia trachomatis Hsp10 correlates with severity of human genital tract disease. Infect. Immun. 68: 303-309.
34. Balkundi, D. R., J. A. Ziegler, J. F. Watchko, C. Craven, and M. Trucco. 2003. Regulation of FasL/Fas in human trophoblasts: possible implications for chorioamnionitis. Biol. Reprod. 69: 718-724.
35. Beutler, B. 2002. TLR4 as the mammalian endotoxin sensor. Curr. Top. Microbiol. Immunol. 270: 109-120.
36. Bausinger, H., D. Lipsker, U. Ziylan, S. Manie, J. P. Briand, J. P. Cazenave, S. Muller, J. F. Haeuw, C. Ravanat, H. de la Salle, and D. Hanau. 2002. Endotoxin-free heat-shock protein 70 fails to induce APC activation. Eur. J. Immunol. 32: 3708-3713.
37. Gao, B., and M. F. Tsan. 2003. Endotoxin contamination in recombinant human heat shock protein 70 (Hsp70) preparation is responsible for the induction of tumor necrosis factor α release by murine macrophages. J. Biol. Chem. 278: 174-179.
38. U.S. Department of Health and Human Service. 2003. Prevention, CfDCa, September 2003. Sexually transmitted disease surveillance, 2002. Atlanta, GA: U.S. Department of Health and Human Service.
39. Washington, A. E., and P. Katz. 1991. Cost of and payment source for pelvic inflammatory disease: trends and projections, 1983 through 2000. J. Am. Med. Assoc. 266: 2565-2569.
40. Gene, M., and A. Mardh. 1996. A cost-effectiveness analysis of screening and treatment for Chlamydia trachomatis infection in asymptomatic women. Ann. Intern. Med. 124: 1-7.
41. Miyairi, I., and G. I. Byrne. 2006. Chlamydia and programmed cell death. Curr. Opin. Microbiol. 9: 102-108.
42. Fan, T., H. Lu, H. Hu, L. Shi, G. A. McClarty, D. M. Nance, A. H. Greenberg, and G. Zhong. 1998. Inhibition of apoptosis in chlamydia-infected cells: blockade of mitochondrial cytochrome c release and caspase activation. J. Exp. Med. 187: 487-496.
43. Dean, D., and V. C. Powers. 2001. Persistent Chlamydia trachomatis infections resist apoptotic stimuli. Infect. Immun. 69: 2442-2447.
44. Gibellini, D., R. Panaya, and F. Rumpianesi. 1998. Induction of apoptosis by Chlamydia psittaci and Chlamydia trachomatis infection in tissue culture cells. Zentralbl. Bakteriol. 288: 35-43.
45. Ojcius, D. M., P. Souque, J. L. Perfettini, and A. Dautry-Varsat. 1998. Apoptosis of epithelial cells and macrophages due to infection with the obligate intracellular pathogen Chlamydia psittaci. J. Immunol. 161: 4220-4226.
46. Perfettini, J. L., D. M. Ojcius, C. W. Andrews, Jr., S. J. Korsmeyer, R. G. Rank, and T. Darville. 2003. Role of proapoptotic BAX in propagation of Chlamydia muridarum (the mouse pneumonitis strain of Chlamydia trachomatis) and the host inflammatory response. J. Biol. Chem. 278: 9496-9502.
47. Rajalingam, K., H. Al-Younes, A. Muller, T. F. Meyer, A. J. Szczepek, and T. Rudel. 2001. Epithelial cells infected with Chlamydophila pneumoniae (Chlamydia pneumoniae) are resistant to apoptosis. Infect. Immun. 69: 7880-7888.
48. Schoier, J., K. Ollinger, M. Kvarnstrom, G. Soderlund, and E. Kihlstrom. 2001. Chlamydia trachomatis-induced apoptosis occurs in uninfected McCoy cells late in the developmental cycle and is regulated by the intracellular redox state. Microb. Pathog. 31: 173-184.
49. Greene, W., Y. Xiao, Y. Huang, G. McClarty, and G. Zhong. 2004. Chlamydia-infected cells continue to undergo mitosis and resist induction of apoptosis. Infect. Immun. 72: 451-460.
50. Eley, A., A. A. Pacey, M. Galdiero, M. Galdiero, and F. Galdiero. 2005. Can Chlamydia trachomatis directly damage your sperm? Lancet Infect. Dis. 5: 53-57.
51. Eley, A., S. Hosseinzadeh, H. Hakimi, I. Geary, and A. A. Pacey. 2005. Apoptosis of ejaculated human sperm is induced by co-incubation with Chlamydia trachomatis lipopolysaccharide. Hum. Reprod. 20: 2601-2607.
52. Dumrese, C., C. F. Maurus, D. Gygi, M. K. Schneider, M. Walch, P. Groscurth, and U. Ziegler. 2005. Chlamydia pneumoniae induces aponecrosis in human aortic smooth muscle cells. BMC Microbiol. 5: 2.
53. Yaraei, K., L. A. Campbell, X. Zhu, W. C. Liles, C. C. Kuo, and M. E. Rosenfeld. 2005. Chlamydia pneumoniae augments the oxidized low-density lipoprotein-induced death of mouse macrophages by a caspase-independent pathway. Infect. Immun. 73: 4315-4322.
54. Byrne, G. I., and D. M. Ojcius. 2004. Chlamydia and apoptosis: life and death decisions of an intracellular pathogen. Nat. Rev. Microbiol. 2: 802-808.
55. Jungas, T., P. Verbeke, T. Darville, and D. M. Ojcius. 2004. Cell death, BAX activation, and HMGB1 release during infection with Chlamydia. Microbes Infect. 6: 1145-1155.
56. Thouas, G. A., N. A. Korfiatis, A. J. French, G. M. Jones, and A. O. Trounson. 2001. Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts. Reprod. Biomed. Online 3: 25-29.
57. Smith, S. C., P. N. Baker, and E. M. Symonds. 1997. Increased placental apoptosis in intrauterine growth restriction. Am. J. Obstet. Gynecol. 177: 1395-1401.
58. Allaire, A. D., K. A. Ballenger, S. R. Wells, M. J. McMahon, and B. A. Lessey. 2000. Placental apoptosis in preeclampsia. Obstet. Cynecol. 96: 271-276.
59. Crocker, I. P., S. Cooper, S. C. Ong, and P. N. Baker. 2003. Differences in apoptotic susceptibility of cytotrophoblasts and syncytiotrophoblasts in normal pregnancy to those complicated with preeclampsia and intrauterine growth restriction. Am. J. Pathol. 162: 637-643.
60. Ohashi, K., V. Burkart, S. Flohe, and H. Kolb. 2000. Cutting edge: heat shock protein 60 is a putative endogenous ligand of the Toll-like receptor-4 complex. J. Immunol. 164: 558-561.
61. Kol, A., A. H. Lichtman, R. W. Finberg, P. Libby, and E. A. Kurt-Jones. 2000. Cutting edge: heat shock protein (HSP) 60 activates the innate immune response: CD14 is an essential receptor for HSP60 activation of mononuclear cells. J. Immunol. 164: 13-17.
62. Prebeck, S., H. Brade, C. J. Kirschning, C. P. da Costa, S. Durr, H. Wagner, and T. Miethke. 2003. The Gram-negative bacterium Chlamydia trachomatis L2 stimulates tumor necrosis factor secretion by innate immune cells independently of its endotoxin. Microbes Infect. 5: 463-470.
63. Netea, M. G., B. J. Kullberg, J. M. Galama, A. F. Stalenhoef, C. A. Dinarello, and J. W. Van der Meer. 2002. Non-LPS components of Chlamydia pneumoniae stimulate cytokine production through Toll-like receptor 2-dependent pathways. Eur. J. Immunol. 32: 1188-1195.
64. Prebeck, S., C. Kirschning, S. Durr, C. da Costa, B. Donath, K. Brand, V. Redecke, H. Wagner, and T. Miethke. 2001. Predominant role of Toll-like receptor 2 versus 4 in Chlamydia pneumoniae-induced activation of dendritic cells. J. Immunol. 167: 3316-3323.
65. Everett, K. D., R. M. Bush, and A. A. Andersen. 1999. Emended description of the order Chlamydiales, proposal of Parachlamydiaceae fam. nov. and Simkaniaceae fam. nov., each containing one monotypic genus, revised taxonomy of the family Chlamydiaceae, including a new genus and five new species, and standards for the identification of organisms. Int. J. Syst. Bacteriol. 49: 415-440.
66. 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.
67. Lindquist, S., and E. A. Craig. 1988. The heat-shock proteins. Annu. Rev. Genet. 22: 631-677.
68. Rothman, J. E. 1989. Polypeptide chain binding proteins: catalysts of protein folding and related processes in cells. Cell 59: 591-601.
69. Bavoil, P., R. S. Stephens, and S. Falkow. 1990. A soluble 60 kilodalton antigen of Chlamydia spp. is a homologue of Escherichia coli GroEL. Mol. Microbiol. 4: 461-469.
70. Li, T., J. Hu, J. A. Thomas, and L. Li. 2005. Differential induction of apoptosis by LPS and taxol in monocytic cells. Mol. Immunol. 42: 1049-1055.
71. Yonehara, S. 1999. Effects of anti-Fas antibodies on lymphocytes and other organs: preparation of original and new monoclonal antibodies and amelioration of systemic autoimmune disease. Int. Rev. Immunol. 18: 329-345.
72. Boatright, K. M., and G. S. Salvesen. 2003. Mechanisms of caspase activation. Curr. Opin. Cell Biol. 15: 725-731.
73. Thorburn, A. 2004. Death receptor-induced cell killing. Cell Signal 16: 139-144.
74. Martelli, A. M., M. Zweyer, R. L. Ochs, P. L. Tazzari, G. Tabellini, P. Narducci, and R. Bortul. 2001. Nuclear apoptotic changes: an overview. J. Cell. Biochem. 82: 634-646.
75. Han, K. J., X. Su, L. G. Xu, L. H. Bin, J. Zhang, and H. B. Shu. 2004. Mechanisms of the TRIF-induced interferon-stimulated response element and NF-κB activation and apoptosis pathways. J. Biol. Chem. 279: 15652-15661.
76. Eckert, L. O., D. E. Moore, D. L. Patton, K. J. Agnew, and D. A. Eschenbach. 2003. Relationship of vaginal bacteria and inflammation with conception and early pregnancy loss following in-vitro fertilization. Infect. Dis. Obstet. Gynecol. 11: 11-17.