Host cell responses to Chlamydia pneumoniae in gamma interferon-induced persistence overlap those of productive infection and are linked to genes involved in apoptosis, cell cycle, and metabolism

Infection and Immunity

Volumn 75, Issue 6, 2007, Pages 2853-2863

  Eickhoff, Meike ^a   Thalmann, Jessica ^b   Hess, Simone ^c   Martin, Myriam ^b   Laue, Thomas ^a   Kruppa, Joachim ^d   Brandes, Gudrun ^b   Klos, Andreas ^b  

^a QIAGEN GMBH   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^d UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; RIFAMPICIN; RNA POLYMERASE;

APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; BACTERIAL METABOLISM; CELL ACTIVATION; CELL CYCLE; CELL STRUCTURE; CHLAMYDOPHILA PNEUMONIAE; CONTROLLED STUDY; ENZYME INHIBITION; GENE EXPRESSION; GENETIC TRANSCRIPTION; GIANT CELL ARTERITIS; HELA CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PERSISTENT INFECTION; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION;

APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BACTERIAL PROTEINS; CELL CYCLE; CELL DIVISION; CHLAMYDIA INFECTIONS; CHLAMYDOPHILA PNEUMONIAE; HELA CELLS; HUMANS; INTERFERON TYPE II;

EID: 34249878472     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01045-06     Document Type: Article

References (59)

1. Baetz, D., K. M. Regula, K. Ens, J. Shaw, S. Kothari, N. Yurkova, and L. A. Kirshenbaum. 2005. Nuclear factor-κB-mediated cell survival involves transcriptional silencing of the mitochondrial death gene BNIP3 in ventricular myocytes. Circulation 112:3777-3785.
2. 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.
3. Blythe, M. J., B. P. Katz, B. E. Batteiger, J. A. Ganser, and R. B. Jones. 1992. Recurrent genitourinary chlamydial infections in sexually active female adolescents. J. Pediatr. 121:487-493.
4. Brantjes, H., N. Barker, J. van Es, and H. Clevers. 2002. TCF: Lady Justice casting the final verdict on the outcome of Wnt signalling. Biol. Chem. 383:255-261.
5. Burns, T. F., P. Fei, K. A. Scata, D. T. Dicker, and W. S. El Deiry. 2003. Silencing of the novel p53 target gene Snk/Plk2 leads to mitotic catastrophe in paclitaxel (taxol)-exposed cells. Mol. Cell. Biol. 23:5556-5571.
6. Chen, Y., and X. Y. Du. 2006. Functional properties and intracellular signaling of CCN1/Cyr61. J. Cell Biochem.
7. Dong, F., H. Su, Y. Huang, Y. Zhong, and G. Zhong. 2004. Cleavage of host keratin 8 by a Chlamydia-secreted protease. Infect. Immun. 72:3863-3868.
8. Dorai, T., I. S. Sawczuk, J. Pastorek, P. H. Wiernik, and J. P. Dutcher. 2005. The role of carbonic anhydrase IX overexpression in kidney cancer. Eur. J. Cancer 41:2935-2947.
9. Duhaut, P., S. Bosshard, and J. P. Ducroix. 2004. Is giant cell arteritis an infectious disease? Biological and epidemiological evidence. Presse Med. 33:1403-1408.
10. Eskildsen, S., J. Justesen, M. H. Schierup, and R. Hartmann. 2003. Characterization of the 2′-5′-oligoadenylate synthetase ubiquitin-like family. Nucleic Acids Res. 31:3166-3173.
11. 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 monotypie 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.
12. 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.
13. Fischer, S. F., J. Vier, S. Kirschnek, A. Klos, S. Hess, S. Ying, and G. Hacker. 2004. Chlamydia inhibit host cell apoptosis by degradation of proapoptotic BH3-only proteins. J. Exp. Med. 200:905-916.
14. Fukuda, E. Y., S. P. Lad, D. P. Mikolon, M. Iacobelli-Martinez, and E. Li. 2005. Activation of lipid metabolism contributes to interleukin-8 production during Chlamydia trachomatis infection of cervical epithelial cells. Infect. Immun. 73:4017-4024.
15. Geng, Y., K. Berencsi, Z. Gyulai, T. Valyi-Nagy, E. Gonczol, and G. Trinchieri. 2000. Roles of interleukin-12 and gamma interferon in murine Chlamydia pneumoniae infection. Infect. Immun. 68:2245-2253.
16. Gieffers, J., H. Fullgraf, J. Jahn, M. Klinger, K. Dalhoff, H. A. Katus, W. Solbach, and M. Maass. 2001. Chlamydia pneumoniae infection in circulating human monocytes is refractory to antibiotic treatment. Circulation 103:351- 356.
17. Gieffers, J., J. Rupp, A. Gebert, W. Solbach, and M. Klinger. 2004. First-choice antibiotics at subinhibitory concentrations induce persistence of Chlamydia pneumoniae. Antimicrob. Agents Chemother. 48:1402-1405.
18. Grayston, J. T., C. C. Kuo, S. P. Wang, and J. Altman. 1986. A new Chlamydia psittaci strain, TWAR, isolated in acute respiratory tract infections. N. Engl. J. Med. 315:161-168.
19. Hahn, D. L., R. W. Dodge, and R. Golubjatnikov. 1991. Association of Chlamydia pneumoniae (strain TWAR) infection with wheezing, asthmatic bronchitis, and adult-onset asthma. JAMA 266:225-230.
20. Hammerschlag, M. R. 2003. Advances in the management of Chlamydia pneumoniae infections. Exp. Rev. Anti. Infect. Ther. 1:493-503.
21. Hammerschlag, M. R., K. Chirgwin, P. M. Roblin, M. Gelling, W. Dumornay, L. Mandel, P. Smith, and J. Schachter. 1992. Persistent infection with Chlamydia pneumoniae following acute respiratory illness. Clin. Infect. Dis. 14: 178-182.
22. Hatch, T. P. 1999. Developmental biology 12321, p. 29-68. In R. S. Stephens (ed.), Chlamydia: intracellular biology, pathogenesis, and immunity. ASM Press, Washington, D.C., USA
23. Haupt, Y., R. Maya, A. Kazaz, and M. Oren. 1997. Mdm2 promotes the rapid degradation of p53. Nature 387:296-299.
24. Hess, S., J. Peters, G. Bartling, C. Rheinheimer, P. Hegde, M. Magid-Slav, R. Tal-Singer, and A. Klos. 2003. More than just innate immunity: comparative analysis of Chlamydophila pneumoniae and Chlamydia trachomatis effects on host-cell gene regulation. Cell Microbiol. 5:785-795.
25. Hess, S., C. Rheinheimer, F. Tidow, G. Bartling, C. Kaps, J. Lauber, J. Buer, and A. Klos. 2001. The reprogrammed host: Chlamydia trachomatis-induced up-regulation of glycoprotein 130 cytokines, transcription factors, and antiapoptotic genes. Arthritis Rheum. 44:2392-2401.
26. Hogan, R. J., S. A. Mathews, S. Mukhopadhyay, J. T. Summersgill, and P. Timms. 2004. Chlamydial persistence: beyond the biphasic paradigm. Infect. Immun. 72:1843-1855.
27. Huang, Q., A. Raya, P. DeJesus, S. H. Chao, K. C. Quon, J. S. Caldwell, S. K. Chanda, J. C. Izpisua-Belmonte, and P. G. Schultz. 2004. Identification of p53 regulators by genome-wide functional analysis. Proc. Natl. Acad. Sci. USA 101:3456-3461.
28. Igietseme, J. U., I. M. Uriri, S. N. Kumar, G. A. Ananaba, O. O. Ojior, I. A. Momodu, D. H. Candal, and C. M. Black. 1998. Route of infection that induces a high intensity of gamma interferon-secreting T cells in the genital tract produces optimal protection against Chlamydia trachomatis infection in mice. Infect. Immun. 66:4030-4035.
29. Kim, S., P. Wong, and P. A. Coulombe. 2006. A keratin cytoskeletal protein regulates protein synthesis and epithelial cell growth. Nature 441:362-365.
30. Kitamura, A., K. Takahashi, A. Okajima, and N. Kitamura. 1994. Induction of the human gene for p44, a hepatitis-C-associated microtubular aggregate protein, by interferon-alpha/beta. Eur. J. Biochem. 224:877-883.
31. Kuo, C. C., L. A. Jackson, L. A. Campbell, and J. T. Grayston. 1995. Chlamydia pneumoniae (TWAR). Clin. Microbiol. Rev. 8:451-461.
32. Kuo, C. C., A. Shor, L. A. Campbell, H. Fukushi, D. L. Patton, and J. T. Grayston. 1993. Demonstration of Chlamydia pneumoniae in atherosclerotic lesions of coronary arteries. J. Infect. Dis. 167:841-849.
33. Lucero, H. A., and H. M. Kagan. 2006. Lysyl oxidase: an oxidative enzyme and effector of cell function. Cell Mol. Life Sci. 63:2304-2316.
34. Moulder, J. W. 1966. The relation of the psittacosis group (Chlamydiae) to bacteria and viruses. Annu. Rev. Microbiol. 20:107-130.
35. Moulder, J. W. 1991. Interaction of chlamydiae and host cells in vitro. Microbiol. Rev. 55:143-190.
36. Netea, M. G., B. J. Kullberg, L. E. Jacobs, T. J. Verver-Jansen, D. Van, V., J. M. Galama, A. F. Stalenhoef, C. A. Dinarello, and J. W. Van Der Meer. 2004. Chlamydia pneumoniae stimulates IFN-gamma synthesis through MyD88-dependent, TLR2- and TLR4-independent induction of IL-18 release. J. Immunol. 173:1477-1482.
37. Niehrs, C. 2006. Function and biological roles of the Dickkopf family of Wnt modulators. Oncogene 25:7469-7481.
38. Pantoja, L. G., R. D. Miller, J. A. Ramirez, R. E. Molestina, and J. T. Summersgill. 2000. Inhibition of Chlamydia pneumoniae replication in human aortic smooth muscle cells by gamma interferon-induced indoleamine 2,3-dioxygenase activity. Infect. Immun. 68:6478-6481.
39. Pantoja, L. G., R. D. Miller, J. A. Ramirez, R. E. Molestina, and J. T. Summersgill. 2001. Characterization of Chlamydia pneumoniae persistence in HEp-2 cells treated with gamma interferon. Infect. Immun. 69:7927-7932.
40. Peifer, M., and P. Polakis. 2000. Wnt signaling in oncogenesis and embryo-genesis - a look outside the nucleus. Science 287:1606-1609.
41. Peters, J., S. Hess, K. Endlich, J. Thalmann, D. Holzberg, M. Kracht, M. Schaefer, G. Bartling, and A. Klos. 2005. Silencing or permanent activation: host-cell responses in models of persistent Chlamydia pneumoniae infection. Cell Microbiol. 7:1099-1108.
42. Rothfuchs, A. G., D. Gigliotti, K. Palmblad, U. Andersson, H. Wigzell, and M. E. Rottenberg. 2001. IFN-αβ-dependent, IFN-γ secretion by bone marrow-derived macrophages controls an intracellular bacterial infection. J. Immunol. 167:6453-6461.
43. Rothfuchs, A. G., M. R. Kreuger, H. Wigzell, and M. E. Rottenberg. 2004. Macrophages, CD4+ or CD8+ cells are each sufficient for protection against Chlamydia pneumoniae infection through their ability to secrete IFN-gamma. J. Immunol. 172:2407-2415.
44. 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.
45. Rottenberg, M. E., R. A. Gigliotti, D. Gigliotti, M. Ceausu, C. Une, V. Levitsky, and H. Wigzell. 2000. Regulation and role of IFN-gamma in the innate resistance to infection with Chlamydia pneumoniae. J. Immunol. 164: 4812-4818.
46. Rupp, J., T. Hellwig-Burgel, V. Wobbe, U. Seltzer, E. Brandt, and M. Maass. 2005. Chlamydia pneumoniae infection promotes a proliferative phenotype in the vasculature through Egr-1 activation in vitro and in vivo. Proc. Natl. Acad. Sci. USA.
47. Saikku, P., M. Leinenen, K. Mattila, M. R. Ekman, M. S. Nieminen, P. H. Makela, J. K. 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 2:983-986.
48. Stamm, W. E. 2000. Potential for antimicrobial resistance in Chlamydia pneumoniae. J. Infect. Dis. 181(Suppl 3):S456-S459.
49. Stein, S., E. K. Thomas, B. Herzog, M. D. Westfall, J. V. Rocheleau, R. S. Jackson, M. Wang, and P. Liang. 2004. NDRG1 is necessary for p53-dependent apoptosis. J. Biol. Chem. 279:48930-48940.
50. Thomas, P. D., M. J. Campbell, A. Kejariwal, H. Mi, B. Karlak, R. Daverman, K. Diemer, A. Muruganujan, and A. Narechania. 2003. PANTHER: a library of protein families and subfamilies indexed by function. Genome Res. 13: 2129-2141.
51. Vogelstein, B., D. Lane, and A. J. Levine. 2000. Surfing the p53 network. Nature 408:307-310.
52. Vuola, J. M., V. Puurula, M. Anttila, P. H. Makela, and N. Rautonen. 2000. Acquired immunity to Chlamydia pneumoniae is dependent on gamma interferon in two mouse strains that initially differ in this respect after primary challenge. Infect. Immun. 68:960-964.
53. Wagner, A. D., H. C. Gerard, T. Fresemann, W. A. Schmidt, E. Gromnica-Ihle, A. P. Hudson, and H. Zeidler. 2000. Detection of Chlamydia pneumoniae in giant cell vasculitis and correlation with the topographic arrangement of tissue-infiltrating dendritic cells. Arthritis Rheum. 43:1543-1551.
54. Wolf, K., E. Fischer, and T. Hackstadt. 2000. Ultrastructural analysis of developmental events in Chlamydia pneumoniae-infected cells. Infect. Im- mun. 68:2379-2385.
55. Worm, H. C., G. H. Wirnsberger, A. Mauric, and H. Holzer. 2004. High prevalence of Chlamydia pneumoniae infection in cyclosporin A-induced post-transplant gingival overgrowth tissue and evidence for the possibility of persistent infection despite short-term treatment with azithromycin. Nephrol. Dial. Transplant. 19:1890-1894.
56. Wu, Q., W. Ding, A. Mirza, T. Van Arsdale, I. Wei, W. R. Bishop, A. Basso, T. McClanahan, L. Luo, P. Kirschmeier, E. Gustafson, M. Hernandez, and S. Liu. 2005. Integrative genomics revealed RAI3 is a cell growth-promoting gene and a novel P53 transcriptional target. J. Biol. Chem. 280:12935- 12943.
57. Yang, T., P. J. Espenshade, M. E. Wright, D. Yabe, Y. Gong, R. Aebersold, J. L. Goldstein, and M. S. Brown. 2002. Crucial step in cholesterol homeostasis: sterols promote binding of SCAP to INSIG-1, a membrane protein that facilitates retention of SREBPs in ER. Cell 110:489-500.
58. Yucesan, C., and S. Sriram. 2001. Chlamydia pneumoniae infection of the central nervous system. Curr. Opin. Neurol. 14:355-359.
59. Zhang, H. M., P. Cheung, B. Yanagawa, B. M. McManus, and D. C. Yang. 2003. BNips: a group of pro-apoptotic proteins in the Bcl-2 family. Apoptosis 8:229-236.