Chlamydia trachomatis inhibits telomeric DNA damage signaling via transient hTERT upregulation

International Journal of Medical Microbiology

Volumn 303, Issue 8, 2013, Pages 463-474

  Padberg, Inken ^a,b   Janßen, Sabrina ^a   Meyer, Thomas F ^a  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^b Metanomics GmbH   (Germany)

Author keywords

Apoptosis; Cell transformation; Chlamydia trachomatis; Neoplastic; Telomerase; Telomere

Indexed keywords

CERAMIDE; DOXYCYCLINE; ETOPOSIDE; HISTONE H2AX; MESSENGER RNA; PROTEIN P53; TELOMERASE;

ARTICLE; BACTERIAL CLEARANCE; CELL AGING; CELL CYCLE CHECKPOINT; CELL SURVIVAL; CELL TRANSFORMATION; CHLAMYDIA TRACHOMATIS; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVE SITE; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; NONHUMAN; PATHOGEN CLEARANCE; PHENOTYPE; PROTEIN BINDING; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; STAINING; TELOMERE; UPREGULATION;

APOPTOSIS; CELL TRANSFORMATION; CHLAMYDIA TRACHOMATIS; CTR; EB; ELEMENTARY BODY; GCA; GOLGICIDE A; HTERT; HUMAN TELOMERASE REVERSE TRANSCRIPTASE; MOI; MULTIPLICITY OF INFECTION; NEOPLASTIC; P.I.; PELVIC INFLAMMATORY DISEASE; PEPTIDE NUCLEIC ACID; PID; PNA; POST INFECTION; QRT-PCR; QUANTITATIVE REAL-TIME PCR; RB; RETICULATE BODY; TELOMERASE; TELOMERE; TELOMERE REPEAT AMPLIFICATION PROTOCOL; TRAP; Γ-PHOSPHO-H2A.X; ΓH2A.X;

CELL LINE; CELL SURVIVAL; CELL TRANSFORMATION, NEOPLASTIC; CHLAMYDIA TRACHOMATIS; DNA DAMAGE; HOST-PATHOGEN INTERACTIONS; HUMANS; SIGNAL TRANSDUCTION; TELOMERASE; UP-REGULATION;

EID: 84887611781     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2013.06.001     Document Type: Article

References (111)

1. Abdul-Sater A.A., Said-Sadier N., Lam V.M., Singh B., Pettengill M.A., Soares F., Tattoli I., Lipinski S., Girardin S.E., Rosenstiel P., Ojcius D.M. Enhancement of reactive oxygen species production and chlamydial infection by the mitochondrial nod-like family member NLRX1. J. Biol. Chem. 2010, 285:41637-41645.
2. Artandi S.E., Attardi L.D. Pathways connecting telomeres and p53 in senescence, apoptosis, and cancer. Biochem. Biophys. Res. Commun. 2005, 331:881-890.
3. Artandi S.E., DePinho R.A. Telomeres and telomerase in cancer. Carcinogenesis 2010, 31:9-18.
4. Beatty W.L., Morrison R.P., Byrne G.I. Persistent chlamydiae - from cell-culture to a paradigm for chlamydial pathogenesis. Microbiol. Rev. 1994, 58:686-699.
5. Beatty W.L., Morrison R.P., Byrne G.I. Reactivation of persistent chlamydia-trachomatis infection in cell-culture. Infect. Immun. 1995, 63:199-205.
6. Berk A.J. Recent lessons in gene expression, cell cycle control, and cell biology from adenovirus. Oncogene 2005, 24:7673-7685.
7. Bjorge T., Gunbjorud A.B., Haugen O.A., Skare G.B., Trope C., Thoresen S.O. Mass-screening for cervical-cancer in norway - evaluation of the pilot project. Cancer Causes Control 1995, 6:477-484.
8. Bjorge T., Gunbjorud A.B., Langmark F., Skare G.B., Thoresen S.O. Mass screening for cervical cancer. A one-year registration of cervical cytological tests. Tidsskr. Nor. Laegeforen. 1994, 114:341-345.
9. Bosch-Presegue L., Vaquero A. The dual role of sirtuins in cancer. Genes Cancer 2011, 2:648-662.
10. Braithwaite A.W., Cheetham B.F., Li P., Parish C.R., Waldron-Stevens L.K., Bellett A.J. Adenovirus-induced alterations of the cell growth cycle: a requirement for expression of E1A but not of E1B. J. Virol. 1983, 45:192-199.
11. Brown L., Boswell S., Raj L., Lee S.W. Transcriptional targets of p53 that regulate cellular proliferation. Crit. Rev. Eukar. Gene 2007, 17:73-85.
12. Buchholz K.R., Stephens R.S. The extracellular signal-regulated kinase/mitogen-activated protein kinase pathway induces the inflammatory factor interleukin-8 following Chlamydia trachomatis infection. Infect. Immun. 2007, 75:5924-5929.
13. Chiodi I., Mondello C. Telomere-independent functions of telomerase in nuclei, cytoplasm, and mitochondria. Front. Oncol. 2012, 2:133.
14. Cmielova J., Havelek R., Jiroutova A., Kohlerova R., Seifrtova M., Muthna D., Vavrova J., Rezacova M. DNA damage caused by ionizing radiation in embryonic diploid fibroblasts WI-38 induces both apoptosis and senescence. Physiol. Res. 2011, 60:667-677.
15. Cong Y.S., Wen J., Bacchetti S. The human telomerase catalytic subunit hTERT: organization of the gene and characterization of the promoter. Hum. Mol. Genet. 1999, 8:137-142.
16. Cukusic A., Skrobot V.N., Sopta M., Rubelj I. Telomerase regulation at the crossroads of cell fate. Cytogenet. Genome Res. 2008, 122:263-272.
17. d'Adda di Fagagna F., Reaper P.M., Clay-Farrace L., Fiegler H., Carr P., Von Zglinicki T., Saretzki G., Carter N.P., Jackson S.P. A DNA damage checkpoint response in telomere-initiated senescence. Nature 2003, 426:194-198.
18. Dai C., Tang Y., Jung S.Y., Qin J., Aaronson S.A., Gu W. Differential effects on p53-mediated cell cycle arrest vs. apoptosis by p90. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:18937-18942.
19. Daniel M., Peek G.W., Tollefsbol T.O. Regulation of the human catalytic subunit of telomerase (hTERT). Gene 2012, 498:135-146.
20. Dazard J.E., Zhang K., Sha J., Yasin O., Cai L., Nguyen C., Ghosh M., Bongorno J., Harter M.L. The dynamics of E1A in regulating networks and canonical pathways in quiescent cells. BMC Res. Notes 2011, 4:160.
21. de Stanchina E., McCurrach M.E., Zindy F., Shieh S.Y., Ferbeyre G., Samuelson A.V., Prives C., Roussel M.F., Sherr C.J., Lowe S.W. E1A signaling to p53 involves the p19(ARF) tumor suppressor. Genes Dev. 1998, 12:2434-2442.
22. Deluca G.D., Basiletti J., Schelover E., Vasquez N.D., Alonso J.M., Marin H.M., Lucero R.H., Picconi M.A. Chlamydia trachomatis as a probable cofactor in human papillomavirus infection in aboriginal women from northeastern Argentina. Braz. J. Infect. Dis. 2011, 15:567-572.
23. Ding Z., Wu C.J., Jaskelioff M., Ivanova E., Kost-Alimova M., Protopopov A., Chu Gerald C., Wang G., Lu X., Labrot Emma S., et al. Telomerase reactivation following telomere dysfunction yields murine prostate tumors with bone metastases. Cell 2012, 148:896-907.
24. Doms R.W., Russ G., Yewdell J.W. Brefeldin A redistributes resident and itinerant Golgi proteins to the endoplasmic reticulum. J. Cell Biol. 1989, 109:61-72.
25. Duelli D.M., Lazebnik Y.A. Primary cells suppress oncogene-dependent apoptosis. Nat. Cell Biol. 2000, 2:859-862.
26. Evan G.I., d'Adda di F.F. Cellular senescence: hot or what?. Curr. Opin. Genet. Dev. 2009, 19:25-31.
27. Fearnhead H.O., Rodriguez J., Govek E.E., Guo W., Kobayashi R., Hannon G., Lazebnik Y.A. Oncogene-dependent apoptosis is mediated by caspase-9. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:13664-13669.
28. Feng Z., Lin M., Wu R. The regulation of aging and longevity: a new and complex role of p53. Genes Cancer 2011, 2:443-452.
29. Ferrari R., Pellegrini M., Horwitz G.A., Xie W., Berk A.J., Kurdistani S.K. Epigenetic reprogramming by adenovirus e1a. Science 2008, 321:1086-1088.
30. Fumagalli M., Rossiello F., Clerici M., Barozzi S., Cittaro D., Kaplunov J.M., Bucci G., Dobreva M., Matti V., Beausejour C.M., et al. Telomeric DNA damage is irreparable and causes persistent DNA-damage-response activation. Nat. Cell Biol. 2012, 14:355-365.
31. Gopalakrishnan S., Quinlan M.P. Modulation of E-cadherin localization in cells expressing wild-type E1A 12S or hypertransforming mutants. Cell Growth Differ. 1995, 6:985-998.
32. Greenblatt M.S., Bennett W.P., Hollstein M., Harris C.C. Mutations in the p53 tumor suppressor gene: clues to cancer etiology and molecular pathogenesis. Cancer Res. 1994, 54:4855-4878.
33. Grieshaber S.S., Grieshaber N.A., Miller N., Hackstadt T. Chlamydia trachomatis causes centrosomal defects resulting in chromosomal segregation abnormalities. Traffic 2006, 7:940-949.
34. Gu B., Zhu W.G. Surf the post-translational modification network of p53 regulation. Int. J. Biol. Sci. 2012, 8:672-684.
35. Hackstadt T., Rockey D.D., Heinzen R.A., Scidmore M.A. Chlamydia trachomatis interrupts an exocytic pathway to acquire endogenously synthesized sphingomyelin in transit from the Golgi apparatus to the plasma membrane. EMBO J. 1996, 15:964-977.
36. Hackstadt T., Scidmore M.A., Rockey D.D. Lipid metabolism in Chlamydia trachomatis-infected cells: directed trafficking of Golgi-derived sphingolipids to the chlamydial inclusion. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:4877-4881.
37. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
38. Haupt S., Berger M., Goldberg Z., Haupt Y. Apoptosis - the p53 network. J. Cell Sci. 2003, 116:4077-4085.
39. Heisig P. Type II topoisomerases - inhibitors, repair mechanisms and mutations. Mutagenesis 2009, 24:465-469.
40. Herbig U., Jobling W.A., Chen B.P., Chen D.J., Sedivy J.M. Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21(CIP1), but not p16(INK4a). Mol. Cell 2004, 14:501-513.
41. Heuer D., Rejman L.A., Machuy N., Karlas A., Wehrens A., Siedler F., Brinkmann V., Meyer T.F. Chlamydia causes fragmentation of the Golgi compartment to ensure reproduction. Nature 2009, 457:731-735.
42. Hill R., Madureira P.A., Waisman D.M., Lee P.W. DNA-PKCS binding to p53 on the p21WAF1/CIP1 promoter blocks transcription resulting in cell death. Oncotarget 2011, 2:1094-1108.
43. Hogan R.J., Mathews S.A., Mukhopadhyay S., Summersgill J.T., Timms P. Chlamydial persistence: beyond the biphasic paradigm. Infect. Immun. 2004, 72:1843-1855.
44. Hollstein M., Sidransky D., Vogelstein B., Harris C.C. p53 mutations in human cancers. Science 1991, 253:49-53.
45. Hosenfeld C.B., Workowski K.A., Berman S., Zaidi A., Dyson J., Mosure D., Bolan G., Bauer H.M. Repeat infection with Chlamydia and gonorrhea among females: a systematic review of the literature. Sex. Transm. Dis. 2009, 36:478-489.
46. Howe J.A., Bayley S.T. Effects of Ad5 E1A mutant viruses on the cell cycle in relation to the binding of cellular proteins including the retinoblastoma protein and cyclin A. Virology 1992, 186:15-24.
47. Hsia R., Ohayon H., Gounon P., Dautry-Varsat A., Bavoil P.M. Phage infection of the obligate intracellular bacterium, Chlamydia psittaci strain guinea pig inclusion conjunctivitis. Microbes Infect. 2000, 2:761-772.
48. Johnson K.A., Tan M., Sutterlin C. Centrosome abnormalities during a Chlamydia trachomatis infection are caused by dysregulation of the normal duplication pathway. Cell. Microbiol. 2009, 11:1064-1073.
49. Jones C.H., Pepper C., Baird D.M. Telomere dysfunction and its role in haematological cancer. Br. J. Haematol. 2012, 156:573-587.
50. Jullien L., Mestre M., Roux P., Gire V. Eroded human telomeres are more prone to remain uncapped and to trigger a G2 checkpoint response. Nucleic Acids Res. 2013, 41:900-911.
51. Kahane S., Friedman M.G. Reversibility of heat shock in Chlamydia trachomatis. FEMS Microbiol. Lett. 1992, 76:25-30.
52. Kanaya T., Kyo S., Hamada K., Takakura M., Kitagawa Y., Harada H., Inoue M. Adenoviral expression of p53 represses telomerase activity through down-regulation of human telomerase reverse transcriptase transcription. Clin. Cancer Res. 2000, 6:1239-1247.
53. Karpinich N.O., Tafani M., Rothman R.J., Russo M.A., Farber J.L. The course of etoposide-induced apoptosis from damage to DNA and p53 activation to mitochondrial release of cytochrome c. J. Biol. Chem. 2002, 277:16547-16552.
54. Kessler M., Zielecki J., Thieck O., Mollenkopf H.J., Fotopoulou C., Meyer T.F. Chlamydia trachomatis disturbs epithelial tissue homeostasis in fallopian tubes via paracrine Wnt signaling. Am. J. Pathol. 2012, 180:186-198.
55. Koehler L., Nettelnbreker E., Hudson A.P., Ott N., Gerard H.C., Branigan P.J., Schumacher H.R., Drommer W., Zeidler H. Ultrastructural and molecular analyses of the persistence of Chlamydia trachomatis (serovarK) in human monocytes. Microb Pathog. 1997, 22:133-142.
56. Kolli S., Buchmann A.M., Williams J., Weitzman S., Thimmapaya B. Antisense-mediated depletion of p300 in human cells leads to premature G1 exit and up-regulation of c-MYC. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:4646-4651.
57. Kusumoto M., Ogawa T., Mizumoto K., Ueno H., Niiyama H., Sato N., Nakamura M., Tanaka M. Adenovirus-mediated p53 gene transduction inhibits telomerase activity independent of its effects on cell cycle arrest and apoptosis in human pancreatic cancer cells. Clin. Cancer Res. 1999, 5:2140-2147.
58. Lee Y.L., Peng Q., Fong S.W., Chen A.C., Lee K.F., Ng E.H., Nagy A., Yeung W.S. Sirtuin 1 facilitates generation of induced pluripotent stem cells from mouse embryonic fibroblasts through the miR-34a and p53 pathways. PLoS ONE 2012, 7:e45633.
59. Lin T.T., Letsolo B.T., Jones R.E., Rowson J., Pratt G., Hewamana S., Fegan C., Pepper C., Baird D.M. Telomere dysfunction and fusion during the progression of chronic lymphocytic leukemia: evidence for a telomere crisis. Blood 2010, 116:1899-1907.
60. Majerska J., Sykorova E., Fajkus J. Non-telomeric activities of telomerase. Mol. Biosyst. 2011, 7:1013-1023.
61. Manning A.L., Dyson N.J. pRB, a tumor suppressor with a stabilizing presence. Trends Cell Biol. 2011, 21:433-441.
62. Masutomi K., Possemato R., Wong J.M., Currier J.L., Tothova Z., Manola J.B., Ganesan S., Lansdorp P.M., Collins K., Hahn W.C. The telomerase reverse transcriptase regulates chromatin state and DNA damage responses. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:8222-8227.
63. Matsumoto A., Manire G.P. Electron microscopic observations on the effects of penicillin on the morphology of Chlamydia psittaci. J. Bacteriol. 1970, 101:278-285.
64. Mazzucchelli G.D., Gabelica V., Smargiasso N., Fleron M., Ashimwe W., Rosu F., De Pauw-Gillet M.C., Riou J.F., De P.E. Proteome alteration induced by hTERT transfection of human fibroblast cells. Proteome Sci. 2008, 6:12.
65. Mehlitz A., Banhart S., Maurer A.P., Kaushansky A., Gordus A.G., Zielecki J., Macbeath G., Meyer T.F. Tarp regulates early Chlamydia-induced host cell survival through interactions with the human adaptor protein SHC1. J. Cell Biol. 2010, 190:143-157.
66. Meyerson M., Counter C.M., Eaton E.N., Ellisen L.W., Steiner P., Caddle S.D., Ziaugra L., Beijersbergen R.L., Davidoff M.J., Liu Q., et al. hEST2, the putative human telomerase catalytic subunit gene, is up-regulated in tumor cells and during immortalization. Cell 1997, 90:785-795.
67. Millau J.F., Bastien N., Bouchard E.F., Drouin R. p53 Pre- and post-binding event theories revisited: stresses reveal specific and dynamic p53-binding patterns on the p21 gene promoter. Cancer Res. 2009, 69:8463-8471.
68. Moore E.R., Fischer E.R., Mead D.J., Hackstadt T. The chlamydial inclusion preferentially intercepts basolaterally directed sphingomyelin-containing exocytic vacuoles. Traffic 2008, 9:2130-2140.
69. Moulder J.W. Interaction of chlamydiae and host cells in vitro. Microbiol. Rev. 1991, 55:143-190.
70. Moulder J.W., Levy N.J., Schulman L.P. Persistent infection of mouse fibroblasts (L cells) with Chlamydia psittaci: evidence for a cryptic chlamydial form. Infect. Immun. 1980, 30:874-883.
71. Mukherjee S., Firpo E.J., Wang Y., Roberts J.M. Separation of telomerase functions by reverse genetics. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:E1363-E1371.
72. Nakamura A.J., Redon C.E., Bonner W.M., Sedelnikova O.A. Telomere-dependent and telomere-independent origins of endogenous DNA damage in tumor cells. Aging 2009, 1:212-218.
73. Nakamura A.J., Redon C.E., Sedelnikova O.A. Where did they come from? The origin of endogenous gamma-H2AX foci in tumor cells. Cell Cycle 2009, 8:2324.
74. Ngok-Ngam P., Watcharasit P., Thiantanawat A., Satayavivad J. Pharmacological inhibition of GSK3 attenuates DNA damage-induced apoptosis via reduction of p53 mitochondrial translocation and Bax oligomerization in neuroblastoma SH-SY5Y cells. Cell. Mol. Biol. Lett. 2013, 18:58-74.
75. Nozell S., Chen X. p21B, a variant of p21(Waf1/Cip1), is induced by the p53 family. Oncogene 2002, 21:1285-1294.
76. Oda K., Arakawa H., Tanaka T., Matsuda K., Tanikawa C., Mori T., Nishimori H., Tamai K., Tokino T., Nakamura Y., Taya Y. p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell 2000, 102:849-862.
77. Ogretmen B., Schady D., Usta J., Wood R., Kraveka J.M., Luberto C., Birbes H., Hannun Y.A., Obeid L.M. Role of ceramide in mediating the inhibition of telomerase activity in A549 human lung adenocarcinoma cells. J. Biol. Chem. 2001, 276:24901-24910.
78. Paba P., Bonifacio D., Di Bonito L., Ombres D., Favalli C., Syrjanen K., Ciotti M. Co-expression of HSV2 and Chlamydia trachomatis in HPV-positive cervical cancer and cervical intraepithelial neoplasia lesions is associated with aberrations in key intracellular pathways. Intervirology 2008, 51:230-234.
79. Pantoja L.G., Miller R.D., Ramirez J.A., Molestina R.E., Summersgill J.T. Characterization of Chlamydia pneumoniae persistence in HEp-2 cells treated with gamma interferon. Infect. Immun. 2001, 69:7927-7932.
80. Peck B., Chen C.Y., Ho K.K., Di F.P., Myatt S.S., Coombes R.C., Fuchter M.J., Hsiao C.D., Lam E.W. SIRT inhibitors induce cell death and p53 acetylation through targeting both SIRT1 and SIRT2. Mol. Cancer Ther. 2010, 9:844-855.
81. Rajalingam K., Sharma M., Lohmann C., Oswald M., Thieck O., Froelich C.J., Rudel T. Mcl-1 is a key regulator of apoptosis resistance in Chlamydia trachomatis-infected cells. PLoS ONE 2008, 3:e3102.
82. Rampazzo E., Bertorelle R., Serra L., Terrin L., Candiotto C., Pucciarelli S., Del B.P., Nitti D., De R.A. Relationship between telomere shortening, genetic instability, and site of tumour origin in colorectal cancers. Br. J. Cancer 2010, 102:1300-1305.
83. Raulston J.E. Response of Chlamydia trachomatis serovar E to iron restriction in vitro and evidence for iron-regulated chlamydial proteins. Infect. Immun. 1997, 65:4539-4547.
84. Riccardi C., Nicoletti I. Analysis of apoptosis by propidium iodide staining and flow cytometry. Nat. Protoc. 2006, 1:1458-1461.
85. Rich T., Allen R.L., Wyllie A.H. Defying death after DNA damage. Nature 2000, 407:777-783.
86. Rivera J., Walduck A.K., Strugnell R.A., Sobey C.G., Drummond G.R. Chlamydia pneumoniae induces a pro-inflammatory phenotype in murine vascular smooth muscle cells independently of elevating reactive oxygen species. Clin. Exp. Pharmacol. Physiol. 2012, 39:218-226.
87. Rodel J., Grosse C., Yu H., Wolf K., Otto G.P., Liebler-Tenorio E., Forsbach-Birk V., Straube E. Persistent Chlamydia trachomatis infection of HeLa cells mediates apoptosis resistance through a Chlamydia protease-like activity factor-independent mechanism and induces high mobility group box 1 release. Infect. Immun. 2012, 80:195-205.
88. Sasaki T., Maier B., Bartke A., Scrable H. Progressive loss of SIRT1 with cell cycle withdrawal. Aging Cell 2006, 5:413-422.
89. Shanmughapriya S., Senthilkumar G., Vinodhini K., Das B.C., Vasanthi N., Natarajaseenivasan K. Viral and bacterial aetiologies of epithelial ovarian cancer. Eur. J. Clin. Microbiol. Infect. Dis. 2012, 31:2311-2317.
90. Sharma M., Machuy N., Bohme L., Karunakaran K., Maurer A.P., Meyer T.F., Rudel T. HIF-1alpha is involved in mediating apoptosis resistance to Chlamydia trachomatis-infected cells. Cell. Microbiol. 2011, 13:1573-1585.
91. Shay J.W., Wright W.E., Werbin H. Defining the molecular mechanisms of human cell immortalization. Biochim. Biophys. Acta 1991, 1072:1-7.
92. Smith J.S., Bosetti C., Munoz N., Herrero R., Bosch F.X., Eluf-Neto J., Meijer C.J., Van Den Brule A.J., Franceschi S., Peeling R.W. Chlamydia trachomatis and invasive cervical cancer: a pooled analysis of the IARC multicentric case-control study. Int. J. Cancer 2004, 111:431-439.
93. Son K., Fujioka S., Iida T., Furukawa K., Fujita T., Yamada H., Chiao P.J., Yanaga K. Doxycycline induces apoptosis in PANC-1 pancreatic cancer cells. Anticancer Res. 2009, 29:3995-4003.
94. Southern E.M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol. Biol. 1975, 98:503-517.
95. Spencer V.A., Sun J.M., Li L., Davie J.R. Chromatin immunoprecipitation: a tool for studying histone acetylation and transcription factor binding. Methods 2003, 31:67-75.
96. Spindler K.R., Eng C.Y., Berk A.J. An adenovirus early region 1A protein is required for maximal viral DNA replication in growth-arrested human cells. J. Virol. 1985, 53:742-750.
97. Stadler G., Wieser M., Streubel B., Stift A., Friedl J., Gnant M., Niederle B., Beham A., Katinger H., Pfragner R., et al. Low telomerase activity: possible role in the progression of human medullary thyroid carcinoma. Eur. J. Cancer 2008, 44:866-875.
98. Szaszak M., Steven P., Shima K., Orzekowsky-Schroder R., Huttmann G., Konig I.R., Solbach W., Rupp J. Fluorescence lifetime imaging unravels C. trachomatis metabolism and its crosstalk with the host cell. PLoS Pathog. 2011, 7:e1002108.
99. Takai H., Smogorzewska A., de Lange T. DNA damage foci at dysfunctional telomeres. Curr. Biol. 2003, 13:1549-1556.
100. Takakura M., Kyo S., Kanaya T., Hirano H., Takeda J., Yutsudo M., Inoue M. Cloning of human telomerase catalytic subunit (hTERT) gene promoter and identification of proximal core promoter sequences essential for transcriptional activation in immortalized and cancer cells. Cancer Res. 1999, 59:551-557.
101. Vasa M., Breitschopf K., Zeiher A.M., Dimmeler S. Nitric oxide activates telomerase and delays endothelial cell senescence. Circ. Res. 2000, 87:540-542.
102. Vaziri H., West M.D., Allsopp R.C., Davison T.S., Wu Y.S., Arrowsmith C.H., Poirier G.G., Benchimol S. ATM-dependent telomere loss in aging human diploid fibroblasts and DNA damage lead to the post-translational activation of p53 protein involving poly(ADP-ribose) polymerase. EMBO J. 1997, 16:6018-6033.
103. Veloso M., Wrba F., Kaserer K., Heinze G., Magalhaes A., Herbst F., Teleky B. p53 gene status and expression of p53, mdm2, and p21Waf1/Cip1 proteins in colorectal cancer. Virchows Arch. 2000, 437:241-247.
104. Verbeke P., Welter-Stahl L., Ying S., Hansen J., Hacker G., Darville T., Ojcius D.M. Recruitment of BAD by the Chlamydia trachomatis vacuole correlates with host-cell survival. PLoS Pathog. 2006, 2:e45.
105. Verdun R.E., Crabbe L., Haggblom C., Karlseder J. Functional human telomeres are recognized as DNA damage in G2 of the cell cycle. Mol. Cell 2005, 20:551-561.
106. Westrom L. Incidence, prevalence, and trends of acute pelvic inflammatory disease and its consequences in industrialized countries. Am. J. Obstet. Gynecol. 1980, 138:880-892.
107. Wilson J.S., Honey E., Templeton A., Paavonen J., Mårdh P.A., Stary A., Stray-Pedersen B., Group f.t.E.B.C.A. A systematic review of the prevalence of Chlamydia trachomatis among European women. Hum. Reprod. Update 2002, 8:385-394.
108. Wooten-Blanks L.G., Song P., Senkal C.E., Ogretmen B. Mechanisms of ceramide-mediated repression of the human telomerase reverse transcriptase promoter via deacetylation of Sp3 by histone deacetylase 1. FASEB J. 2007, 21:3386-3397.
109. Wright H.R., Turner A., Taylor H.R. Trachoma. Lancet 2008, 371:1945-1954.
110. Yang Q. Cellular senescence, telomere recombination and maintenance. Cytogenet. Genome Res. 2008, 122:211-218.
111. Zerler B., Roberts R.J., Mathews M.B., Moran E. Different functional domains of the adenovirus E1A gene are involved in regulation of host cell cycle products. Mol. Cell. Biol. 1987, 7:821-829.