Imbalanced Oxidative Stress Causes Chlamydial Persistence during Non-Productive Human Herpes Virus Co-Infection

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Prusty, Bhupesh K ^a   Böhme, Linda ^a   Bergmann, Birgit ^a   Siegl, Christine ^a   Krause, Eva ^b   Mehlitz, Adrian ^a   Rudel, Thomas ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE; GLUTATHIONE REDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ARTICLE; BIOACCUMULATION; CHLAMYDIA TRACHOMATIS; CHLAMYDIASIS; CONTROLLED STUDY; CYTOMEGALOVIRUS; ENZYME ACTIVITY; HERPES SIMPLEX VIRUS 1; HERPES VIRUS INFECTION; HOST CELL; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 6; MICROBIAL ACTIVITY; MIXED INFECTION; NONHUMAN; ORGANISMAL INTERACTION; OXIDATIVE STRESS; VIRUS CELL INTERACTION;

BIOLOGICAL EVOLUTION; CHLAMYDIA INFECTIONS; CHLAMYDIA TRACHOMATIS; COINFECTION; HELA CELLS; HERPESVIRUS 6, HUMAN; HUMANS; OXIDATIVE STRESS; ROSEOLOVIRUS INFECTIONS;

EID: 84867540341     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047427     Document Type: Article

References (57)

1. Carter JD, Inman RD, Whittum-Hudson J, Hudson AP (2011) Chlamydia and chronic arthritis. Annals of medicine EPub.
2. Zhan P, Suo L-j, Qian Q, Shen X-k, Qiu L-X, et al. (2011) Chlamydia pneumoniae infection and lung cancer risk: a meta-analysis. Eur J Cancer 47: 742-747.
3. Shima K, Kuhlenbäumer G, Rupp J, (2010) Chlamydia pneumoniae infection and Alzheimer's disease: a connection to remember? Med Microbiol Immunol 199: 283-289.
4. Dean D, Powers V, (2001) Persistent Chlamydia trachomatis infections resist apoptotic stimuli. Infection and immunity 69: 2442.
5. Wyrick PB, (2010) Chlamydia trachomatis persistence in vitro: an overview. J Infect Dis 201 (Suppl 2): S88-95.
6. Vanover J, Kintner J, Whittimore J, Schoborg RV (2010) Interaction of HSV-2 glycoprotein D with the host cell surface is sufficient to induce Chlamydia trachomatis persistence. Microbiology: 1-28.
7. Vanover J, Sun J, Deka S, Kintner J, Duffourc M, et al. (2008) Herpes simplex virus co-infection-induced Chlamydia trachomatis persistence is not mediated by any known persistence inducer or anti-chlamydial pathway. Microbiology 154: 971.
8. Deka S, Vanover J, Sun J, Kintner J, Whittimore J, et al. (2007) An early event in the herpes simplex virus type-2 replication cycle is sufficient to induce Chlamydia trachomatis persistence. Cellular Microbiology 9: 725-737.
9. Deka S, Vanover J, Dessus-Babus S, Whittimore J, Howett MK, et al. (2006) Chlamydia trachomatis enters a viable but non-cultivable (persistent) state within herpes simplex virus type 2 (HSV-2) co-infected host cells. Cellular Microbiology 8: 149-162.
10. Lusso P, (2006) HHV-6 and the immune system: mechanisms of immunomodulation and viral escape. Journal of clinical virology: the official publication of the Pan American Society for Clinical Virology 37 (Suppl 1): S4-10.
11. Paavonen J, Stevens CE, Wølner-Hanssen P, Critchlow CW, Derouen T, et al. (1988) Colposcopic manifestations of cervical and vaginal infections. Obstet Gynecol Surv 43: 373-381.
12. Caselli E, Boni M, Bracci A, Rotola A, Cermelli C, et al. (2002) Detection of antibodies directed against human herpesvirus 6 U94/REP in sera of patients affected by multiple sclerosis. Journal of Clinical Microbiology 40: 4131-4137.
13. Nicolson GL, Gan R, Haier J, (2003) Multiple co-infections (Mycoplasma, Chlamydia, human herpes virus-6) in blood of chronic fatigue syndrome patients: association with signs and symptoms. APMIS 111: 557-566.
14. Beatty WL, Morrison RP, Byrne GI, (1994) Persistent chlamydiae: from cell culture to a paradigm for chlamydial pathogenesis. Microbiol Rev 58: 686-699.
15. Luppi M, Torelli G, (1996) The new lymphotropic herpesviruses (HHV-6, HHV-7, HHV-8) and hepatitis C virus (HCV) in human lymphoproliferative diseases: an overview. Haematologica 81: 265-281.
16. Manor E, Sarov I, (1986) Fate of Chlamydia trachomatis in human monocytes and monocyte-derived macrophages. Infection and Immunity 54: 90-95.
17. Hogan RJ, Mathews SA, Mukhopadhyay S, Summersgill JT, Timms P, (2004) Chlamydial persistence: beyond the biphasic paradigm. Infection and Immunity 72: 1843-1855.
18. Yoshikawa T, Asano Y, Akimoto S, Ozaki T, Iwasaki T, et al. (2002) Latent infection of human herpesvirus 6 in astrocytoma cell line and alteration of cytokine synthesis. J Med Virol 66: 497-505.
19. Rotola A, Ravaioli T, Gonelli A, Dewhurst S, Cassai E, et al. (1998) U94 of human herpesvirus 6 is expressed in latently infected peripheral blood mononuclear cells and blocks viral gene expression in transformed lymphocytes in culture. Proceedings of the National Academy of Sciences of the United States of America 95: 13911.
20. Mori Y, Akkapaiboon P, Yang X, Yamanishi K, (2003) The human herpesvirus 6 U100 gene product is the third component of the gH-gL glycoprotein complex on the viral envelope. Journal of Virology 77: 2452-2458.
21. Caruso A, Favilli F, Rotola A, Comar M, Horejsh D, et al. (2003) Human herpesvirus-6 modulates RANTES production in primary human endothelial cell cultures. J Med Virol 70: 451-458.
22. Wu C, Shanley J, (1998) Chronic infection of human umbilical vein endothelial cells by human herpesvirus-6. Journal of General Virology 79: 1247.
23. Ojcius D, Degani H, Mispelter J, Dautry-Varsat A, (1998) Enhancement of ATP levels and glucose metabolism during an infection by Chlamydia. NMR studies of living cells. Journal of Biological Chemistry 273: 7052.
24. Chen F-H, Zhang L-B, Qiang L, Yang Z, Wu T, et al. (2010) Reactive oxygen species-mitochondria pathway involved in LYG-202-induced apoptosis in human hepatocellular carcinoma HepG(2) cells. Cancer Lett 296: 96-105.
25. Dai D-F, Rabinovitch P, (2011) Mitochondrial oxidative stress mediates induction of autophagy and hypertrophy in angiotensin-II treated mouse hearts. Autophagy 7: 917-918.
26. Boncompain G, Schneider B, Delevoye C, Kellermann O, Dautry-Varsat A, et al. (2010) Production of Reactive Oxygen Species Is Turned On and Rapidly Shut Down in Epithelial Cells Infected with Chlamydia trachomatis. Infection and Immunity 78: 80-87.
27. Fukuda R, Zhang H, Kim J-w, Shimoda L, Dang CV, et al. (2007) HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell 129: 111-122.
28. Semenza GL, (1999) Perspectives on oxygen sensing. Cell 98: 281-284.
29. Sharma M, Machuy N, Bohme L, Karunakaran K, Maurer AP, et al. (2011) HIF-1alpha is involved in mediating apoptosis resistance to Chlamydia trachomatis-infected cells. Cellular Microbiology 13: 1573-1585.
30. Bedard K, Krause KH, (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiological reviews 87: 245-313.
31. Geiszt M, Lekstrom K, Brenner S, Hewitt SM, Dana R, et al. (2003) NAD(P)H oxidase 1, a product of differentiated colon epithelial cells, can partially replace glycoprotein 91phox in the regulated production of superoxide by phagocytes. Journal of immunology 171: 299-306.
32. Winkler BS, DeSantis N, Solomon F, (1986) Multiple NADPH-producing pathways control glutathione (GSH) content in retina. Exp Eye Res 43: 829-847.
33. Skilton R, Cutcliffe L, Barlow D, Wang Y, Salim O, (2009) Penicillin induced persistence in Chlamydia trachomatis: high quality time lapse video analysis of the developmental cycle. PLoS ONE 4: e7723.
34. Matsumoto A, Manire GP, (1970) Electron microscopic observations on the effects of penicillin on the morphology of Chlamydia psittaci. Journal of Bacteriology 101: 278-285.
35. Kahane S, Dvoskin B, Mathias M, Friedman MG, (2001) Infection of Acanthamoeba polyphaga with Simkania negevensis and S. negevensis survival within amoebal cysts. Appl Environ Microbiol 67: 4789-4795.
36. Kuipers JG, Jurgens-Saathoff B, Bialowons A, Wollenhaupt J, Kohler L, et al. (1998) Detection of Chlamydia trachomatis in peripheral blood leukocytes of reactive arthritis patients by polymerase chain reaction. Arthritis and rheumatism 41: 1894-1895.
37. Cirino F, Webley WC, West C, Croteau NL, Andrzejewski C Jr, et al. (2006) Detection of Chlamydia in the peripheral blood cells of normal donors using in vitro culture, immunofluorescence microscopy and flow cytometry techniques. BMC infectious diseases 6: 23.
38. Kondo K, Kondo T, Okuno T, Takahashi M, Yamanishi K, (1991) Latent human herpesvirus 6 infection of human monocytes/macrophages. Journal of General Virology 72: 1401.
39. Stuedli A, Grest P, Schiller I, Pospischil A, (2005) Mixed infections in vitro with different Chlamydiaceae strains and a cell culture adapted porcine epidemic diarrhea virus. Veterinary microbiology 106: 209-223.
40. Borel N, Dumrese C, Ziegler U, Schifferli A, Kaiser C, et al. (2010) Mixed infections with Chlamydia and porcine epidemic diarrhea virus- a new in vitro model of chlamydial persistence. BMC microbiology 10: 201.
41. Santoro F, Kennedy P, Locatelli G, Malnati M, Berger E, et al. (1999) CD46 is a cellular receptor for human herpesvirus 6. Cell 99: 817-827.
42. Lau ATY, Wang Y, Chiu J-F, (2008) Reactive oxygen species: current knowledge and applications in cancer research and therapeutic. J Cell Biochem 104: 657-667.
43. Abdul-Sater AA, Said-Sadier N, Lam VM, Singh B, Pettengill MA, et al. (2010) Enhancement of Reactive Oxygen Species Production and Chlamydial Infection by the Mitochondrial Nod-like Family Member NLRX1. Journal of Biological Chemistry 285: 41637-41645.
44. Denko NC, (2008) Hypoxia, HIF1 and glucose metabolism in the solid tumour. Nature reviews Cancer 8: 705-713.
45. Lum JJ, Bui T, Gruber M, Gordan JD, DeBerardinis RJ, et al. (2007) The transcription factor HIF-1alpha plays a critical role in the growth factor-dependent regulation of both aerobic and anaerobic glycolysis. Genes & Development 21: 1037-1049.
46. Delgado T, Carroll PA, Punjabi AS, Margineantu D, Hockenbery DM, et al. (2010) Induction of the Warburg effect by Kaposi's sarcoma herpesvirus is required for the maintenance of latently infected endothelial cells. Proceedings of the National Academy of Sciences of the United States of America 107: 10696-10701.
47. Torii S, Goto Y, Ishizawa T, Hoshi H, Goryo K, et al. (2011) Pro-apoptotic activity of inhibitory PAS domain protein (IPAS), a negative regulator of HIF-1, through binding to pro-survival Bcl-2 family proteins. Cell death and differentiation 18: 1711-1725.
48. Ishikawa K, Takenaga K, Akimoto M, Koshikawa N, Yamaguchi A, et al. (2008) ROS-generating mitochondrial DNA mutations can regulate tumor cell metastasis. Science 320: 661-664.
49. Hackstadt T, Todd WJ, Caldwell HD, (1985) Disulfide-mediated interactions of the chlamydial major outer membrane protein: role in the differentiation of chlamydiae? Journal of Bacteriology 161: 25-31.
50. Lazarev VN, Borisenko GG, Shkarupeta MM, Demina IA, Serebryakova MV, et al. (2010) The role of intracellular glutathione in the progression of Chlamydia trachomatis infection. Free Radical Biology and Medicine 49: 1947-1955.
51. Hatch TP, Miceli M, Sublett JE, (1986) Synthesis of disulfide-bonded outer membrane proteins during the developmental cycle of Chlamydia psittaci and Chlamydia trachomatis. J Bacteriol 165: 379-385.
52. Mukhopadhyay S, Good D, Miller RD, Graham JE, Mathews SA, et al. (2006) Identification of Chlamydia pneumoniae Proteins in the Transition from Reticulate to Elementary Body Formation. Molecular & Cellular Proteomics 5: 2311-2318.
53. Wang Y, (2006) Identification of surface-exposed components of MOMP of Chlamydia trachomatis serovar F. Protein Science. 15: 122-134.
54. Beydemir S, Ciftci M, Kufrevioglu OI, (2002) Purification and characterization of glucose 6-phosphate dehydrogenase from sheep erythrocytes and inhibitory effects of some antibiotics on enzyme activity. Journal of enzyme inhibition and medicinal chemistry 17: 271-277.
55. Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ, (2007) A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130: 797-810.
56. Prusty BK, zur Hausen H, Schmidt R, Kimmel R, de Villiers EM, (2008) Transcription of HERV-E and HERV-E-related sequences in malignant and non-malignant human haematopoietic cells. Virology 382: 37-45.
57. Bohme L, Albrecht M, Riede O, Rudel T, (2010) Chlamydia trachomatis-infected host cells resist dsRNA-induced apoptosis. Cellular Microbiology 12: 1340-1351.