Chlamydial Hsp60-2 is iron responsive in Chlamydia trachomatis serovar E-infected human endometrial epithelial cells in vitro

Infection and Immunity

Volumn 75, Issue 5, 2007, Pages 2374-2380

  LaRue, Richard W ^a   Dill, Brian D ^a   Giles, David K ^a   Whittimore, Judy D ^a   Raulston, Jane E ^a  

^a East Tennessee State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 20; IRON; PROTEIN SUBUNIT;

ARTICLE; BACTERIAL STRAIN; CHLAMYDIA TRACHOMATIS; CULTURE MEDIUM; ENDOMETRIUM CELL; EPITHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IRON RESTRICTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE HOMOLOGY; SEROTYPE;

CHAPERONIN 60; CHLAMYDIA TRACHOMATIS; ENDOMETRIUM; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; IRON; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; SEROTYPING;

EID: 34248389725     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01465-06     Document Type: Article

References (56)

1. Andrews, N. C. 2000. Iron homeostasis: insights from genetics and animal models. Nat. Rev. 1:208-216.
2. Beatty, W. L., G. I. Byrne, and R. P. Morrison. 1993. Morphologic and antigenic characterization of interferon gamma-mediated persistent Chlamydia trachomatis infection in vitro. Proc. Natl. Acad. Sci. USA 90:3998-4002.
3. Beatty, W. L., G. I. Byrne, and R. P. Morrison. 1994. Repeated and persistent infection with Chlamydia and the development of chronic inflammation and disease. Trends Microbiol. 2:94-98.
4. Belland, R. J., D. E. Nelson, D. Virok, D. D. Crane, D. Hogan, D. Sturdevant, W. L. Beatty, and H. D. Caldwell. 2003. Transcriptome analysis of chlamydial growth during IFN-γ-mediated persistence and reactivation. Proc. Natl. Acad. Sci. USA 100:15971-15976.
5. Belland, R. J., L. Rose, and Y. AbdelRahman. 2006. Promoter mapping of coding and non-coding RNAs using an intergenic microarray for Chlamydia trachomatis, p. 17-20. In M. Chernesky, H. Caldwell, G. Christiansen, I. N. Clarke, B. Kaltenboek, C. Knirsch, C.-C. Kuo, J. Mahony, R. G. Rank, P. Saikku, J. Schachter, W. E. Stamm, R. S. Stephens, J. T. Summersgill, P. Timms, and P. B. Wyrick (ed.), Proceedings of the 11th International Symposium on Human Chlamydial Infections, Niagara-on-the-Lake, Ontario, Canada. International Chlamydia Symposium, San Francisco, CA.
6. Betsou, F., J. M. Sueur, and J. Orfila. 2003. Anti-Chlamydia pneumoniae heat shock protein 10 antibodies in asthmatic adults. FEMS Immunol. Med. Microbiol. 35:107-111.
7. Brunham, R. C., I. W. Maclean, B. Binns, and R. W. Peeling. 1985. Chlamydia trachomatis: its role in tubal infertility. J. Infect. Dis. 152:1275-1282.
8. Bulut, Y., E. Faure, L. Thomas, H. Karahashi, K. S. Michelson, 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.
9. Cohen, C. R., and R. C. Brunham. 1999. Pathogenesis of Chlamydia induced pelvic inflammatory disease. Sex. Transm. Infect. 75:21-24.
10. Cohen, C. R., J. Gichui, Rukaria, S. Sinei, L. K. Gaur, and R. C. Brunham. 2003. Immunogenetic correlates for Chlamydia trachomatis-associated tubal infertility. Obstet. Gynecol. 101:438-444.
11. 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: importance of heat shock protein 60 and interferon-gamma. J. Infect. Dis. 4:591-599.
12. Conway, D. J., M. J. Holland, A. E. Campbell, R. L. Bailey, P. Krausa, R. W. Peeling, H. C. Whittle, and D. C. Mabey. 1996. HLA class I and II polymorphisms and trachomatous scarring in a Chlamydia trachomatis- endemic population. J. Infect. Dis. 174:643-646.
13. Darville, T. 2000. Chlamydia spp., p. 229-261. In J. P. Nataro, M. J. Blaser, and S. Cunningham-Rundles (ed.), Persistent bacterial infections. ASM Press, Washington, DC.
14. Debattista, J., P. Timms, J. Allan, and J. Allan. 2003. Immunopathogenesis of Chlamydia trachomatis infections in women. Fertil. Steril. 79:1273-1287.
15. den Hartog, J. E., J. A. Land, F. R. M. Stassen, A. G. H. Kessels, and C. A. Bruggeman. 2005. Serological markers of persistent C. trachomatis infections in women with tubal factor subfertility. Hum. Reprod. 20:986-990.
16. Di Felice, V., S. David, F. Cappello, F. Farina, and G. Zummo. 2005. Is chlamydial heat shock protein 60 a risk factor for oncogenesis? Cell. Mol. Life Sci. 62:4-9.
17. Dreses-Werringloer, U., I. Padubrin, B. Jurgens-Saathoff, A. P. Hudson, H. Zeidler, and L. Kohler. 2000. Persistence of Chlamydia trachomatis is induced by ciprofloxacin and ofloxacin in vitro. Antimicrob. Agents Chemother. 44:3288-3297.
18. Equils, O., D. Lu, M. Gatter, S. S. Witkin, C. Bertolotto, M. Arditi, J. A. McGregor, C. F. Simmons, and C. J. Hobel. 2006. Chlamydia heat shock protein 60 induces trophoblast apoptosis through TLR4. J. Immunol. 177:1257-1263.
19. Gerard, H. C., L. Kohler, P. J. Branigan, H. Zeilder, H. R. Schumacher, and A. P. Hudson. 1998. Viability and gene expression in Chlamydia trachomatis during persistent infection of cultured human monocytes. Med. Microbiol. Immunol. 187:115-120.
20. Gerard, H. C., J. A. Whittum-Hudson, H. R. Schumacher, and A. P. Hudson. 2004. Differential expression of three Chlamydia trachomatis Hsp60-encoding genes in active vs. persistent infections. Microb. Pathog. 36:35-39.
21. Giles, D. K., J. D. Whittimore, R. W. LaRue, J. E. Raulston, and P. B. Wyrick. 2006. Ultrastructural analysis of chlamydial antigen-containing vesicles everting from the Chlamydia trachomatis inclusion. Microb. Infect. 8:1579-1591.
22. Goellner, S., E. Schubert, E. Liebler-Tenorio, H. Hotzel, H. P. Saluz, and K. Sachse. 2006. Transcriptional response patterns of Chlamydia psittaci in different in vitro models of persistent infection. Infect. Immun. 74:4801-4808.
23. Higgins, D. P., S. Hemsley, and P. J. Canfield. 2005. Association of uterine and salpingeal fibrosis with chlamydial Hsp60 and Hsp10 antigen-specific antibodies in Chlamydia-infected koalas. Clin. Diag. Lab. Immunol. 12:632-639.
24. Jackson, M., N. White, P. Giffard, and P. Timms. 1999. Epizootiology of Chlamydia infections in two free-range koala populations. Vet. Microbiol. 65:255-264.
25. Kadner, R. J. 2005. Regulation by iron: RNA rules the rust. J. Bacteriol. 187:6870-6873.
26. Kalayoglu, M. V., Indrawati, R. P. Morrison, S. G. Morrison, Y. Yuan, and G. I. Byrne. 2000. Chlamydial virulence determinants in atherogenesis: the role of chlamydial lipopolysaccharide and heat shock protein 60 in macrophage-lipoprotein interactions. J. Infect. Dis. 181:S483-S489.
27. Karinen, L., A. Pouta, A. L. Hartikainen, A. Bloigu, M. Paldanius, M. Leinonen, P. Saikku, and M. R. Jarvelin. 2004. Antibodies to Chlamydia trachomatis heat shock proteins Hsp60 and Hsp10 and subfertility in general population at age 31. Am. J. Reprod. Immunol. 52:291-297.
28. Karunakaran, K. P., Y. Noguchi, T. D. Read, A. Cherkasov, J. Kwee, C. Shen, C. C. Nelson, and R. C. Brunham. 2003. Molecular analysis of the multiple GroEL proteins of chlamydiae. J. Bacteriol. 185:1958-1966.
29. Kelver, M. E., A. Kaul, B. Nowicki, W. E. Findley, T. W. Hutchens, and N. Nagamani. 1996. Estrogen regulation of lactoferrin expression in human endometrium. Am. J. Reprod. Immunol. 36:243-247.
30. Kinnunen, A., J. Paavonen, and H. M. Surcel. 2001. Heat shock protein 60 specific T-cell response in chlamydial infections. Scand. J. Immunol. 54:76-81.
31. Kol, A., G. K. Suhkova, A. H. Lichtman, and P. Libby. 1998. Chlamydial heat shock protein 60 localizes in human atheroma and regulates macrophage tumor necrosis factor-α and matrix metalloproteinase expression. Circulation 98:300-307.
32. 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. I. Immunol. 164:13-17.
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. 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.
35. Lipman, D. J., and W. R. Pearson. 1985. Rapid and sensitive protein similarity searches. Science 227:1435-1441.
36. Melkani, G. C., G. Zardeneta, and J. A. Mendoza. 2005. On the chaperone activity of GroEL at heat-shock temperature. Int. J. Biochem. Cell. Biol. 37:1375-1385.
37. Morrison, R. P., K. Lyng, and H. D. Caldwell. 1989. Chlamydial disease pathogenesis. Ocular hypersensitivity elicited by a genus-specific 57-kDa protein. J. Exp. Med. 169:663-675.
38. Mozzato-Chamay, N., O. S. Madhi, O. Jallow, D. C. Mabey, R. L. Bailey, and D. J. Conway. 2000. Polymorphisms in candidate genes and risk of scarring trachoma in a Chlamydia trachomatis-endemic population. J. Infect. Dis. 182:1545-1548.
39. Mukhopadhyay, S., R. D. Miller, E. D. Sullivan, C. Theodoropoulos, S. A. Mathews, P. Timms, and J. T. Summersgill. 2006. Protein expression profiles of Chlamydia pneumoniae in models of persistence versus those of heat shock stress response. Infect. Immun. 74:3853-3863.
40. Peeling, R. W., and D. C. Mabey. 1999. Heat shock protein expression and immunity in chlamydial infections. Infect. Dis. Obstet. Gynecol. 7:72-79.
41. Qazi, K. R., M. R. Qazi, E. Julian, M. Singh, M. Abedi-Valugerdi, and C. Fernandez. 2005. Exposure to mycobacteria primes the immune system for evolutionarily diverse heat shock proteins. Infect. Immun. 73:7687-7696.
42. Rau, A., S. Wyllie, J. Whittimore, and J. E. Raulston. 2005. Identification of Chlamydia trachomatis genomic sequences recognized by chlamydial divalent cation-dependent regulator A (DcrA). J. Bacteriol. 187:443-448.
43. Raulston, J. E. 1997. Response of Chlamydia trachomatis serovar E to iron restriction in vitro and evidence for iron-regulated chlamydial proteins. Infect. Immun. 65:4539-4547.
44. Raulston, J. E., T. R. Paul, S. T. Knight, and P. B. Wyrick. 1998. Localization of Chlamydia trachomatis heat shock proteins 60 and 70 during infection of a human endometrial epithelial cell line in vitro. Infect. Immun. 66:2323-2329.
45. Saikku, P., M. Leinonen, K. Mattila, M. R. Ekman, M. S. Nieminen, P. H. Huttunen, and V. Valtonen. 1988. Serological evidence of an association of a novel Chlamydia, TWAR, with chronic coronary heart disease and acute myocardial infarction. Lancet ii:983-986.
46. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.
47. Sasu, S., D. LaVerda, N. Qureshi, D. T. Golenbock, and D. Beasley. 2001. Chlamydia pneumoniae and chlamydial heat shock protein 60 stimulate proliferation of human vascular smooth muscle cells via Toll-like receptor 4 and p44/p42 mitogen-activated protein kinase activation. Circ. Res. 89:244-250.
48. Sharma, J., F. Dong, M. Pirbhai, and G. Zhong. 2005. Inhibition of proteolytic activity of a chlamydial proteosome/protease-like factor by antibodies from humans infected with Chlamydia trachomatis. Infect. Immun. 73:4414-4419.
49. Stephens, R. S., S. Kalman, C. Lammel, J. Fan, R. Marathe, L. Aravind, W. Mitchell, L. Olinger, R. L. Tatusov, Q. Zhao, E. V. Koonin, and R. W. Davis. 1998. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282:754-759.
50. Sziller, I., S. S. Witkin, M. Zeigert, Z. Csapo, A. Ujhazy, and Z. Papp. 1998. Serological responses of patients with ectopic pregnancy to epitopes of the Chlamydia trachomatis 60kDa heat shock protein. Hum. Reprod. 13:1088-1093.
51. Tiitinen, A., H. M. Surcel, M. Halttunen, S. Birkelund, A. Bloigu, G. Christiansen, P. Koskela, S. G. Morrison, R. P. Morrison, and J. Paavonen. 2006. Chlamydia trachomatis and chlamydial heat shock protein 60-specific antibody and cell-mediated responses predict tubal factor infertility. Hum. Reprod. 21:1533-1538.
52. Toye, B., C. Laferrie, P. Claman, P. Jessamine, and R. Peeling. 1993. Association between antibody to the chlamydial heat shock protein and tubal infertility. J. Infect. Dis. 168:1236-1240.
53. Wilson, A. C., C. C. Wu, J. R. Yates III, and M. Tan. 2005. Chlamydial GroEL autoregulates its own expression through direct interactions with the HrcA repressor protein. J. Bacteriol. 187:7535-7542.
54. Witkin, S. S., M. Askienazy-Elbhar, J. Henry-Suchet, J. Belaisch-Allart, J. Tort-Grumbacj, and K. Sarjdine. 1998. Circulating antibodies to a conserved epitope of the Chlamydia trachomatis 60 kDa heat shock protein (hsp60) in infertile couples and its relationship to antibodies to C. trachomatis surface antigens and the Escherichia coli and human Hsp60. Hum. Reprod. 13:1175-1179.
55. Wyllie, S., and J. E. Raulston. 2001. Identifying regulators of transcription in an obligate intracellular pathogen: a metal-dependent repressor in Chlamydia trachomatis. Mol. Microbiol. 40:1027-1036.
56. Young, R. A., and T. J. Elliot. 1989. Stress proteins, infection, and immune surveillance. Cell 59:5-8.