Differential transcriptional regulation of human telomerase in a cellular model representing important genetic alterations in esophageal squamous carcinogenesis

Carcinogenesis

Volumn 26, Issue 11, 2005, Pages 1879-1889

  Quante, Michael ^a   Heeg, Steffen ^a   von Werder, Alexander ^a   Goessel, Gitta ^a   Fulda, Christine ^a   Doebele, Michaela ^a   Nakagawa, Hiroshi ^b   Beijersbergen, Roderick ^c   Blum, Hubert E ^a   Opitz, Oliver G ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; MYC PROTEIN; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; TRANSCRIPTION FACTOR E2F; TRANSCRIPTION FACTOR SP1;

ARTICLE; CANCER CELL; CARCINOGENESIS; CONTROLLED STUDY; DNA METHYLATION; ENZYME ACTIVITY; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; HUMAN TISSUE; MALIGNANT TRANSFORMATION; ONCOGENE C MYC; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; TELOMERE; TRANSCRIPTION REGULATION;

BLOTTING, WESTERN; CARCINOMA, SQUAMOUS CELL; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; DNA METHYLATION; DNA-BINDING PROTEINS; E2F TRANSCRIPTION FACTORS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EPITHELIAL CELLS; ESOPHAGEAL NEOPLASMS; ESOPHAGUS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; PROMOTER REGIONS (GENETICS); PROTO-ONCOGENE PROTEINS C-MYC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SP1 TRANSCRIPTION FACTOR; TELOMERASE; TELOMERE; TRANS-ACTIVATION (GENETICS); TRANSFECTION;

EID: 27744529808     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgi153     Document Type: Article

References (56)

1. Hahn,W.C. and Weinberg,R.A. (2002) Rules for making human tumor cells [Erratum (2003) N. Engl. J. Med., 348, 674]. N. Engl. J. Med., 347, 1593-1603.
2. Lundberg,A.S., Hahn,W.C., Gupta,P. and Weinberg,R.A. (2000) Genes involved in senescence and immortalization. Curr. Opin. Cell. Biol., 12, 705-709.
3. Blackburn,E.H. (1991) Structure and function of telomeres. Nature, 350, 569-573.
4. Kim,N.W., Piatyszek,M.A., Prowse,K.R., Harley,C.B., West,M.D., Ho,P.L., Coviello,G.M., Wright,W.E., Weinrich,S.L. and Shay,J.W. (1994) Specific association of human telomerase activity with immortal cells and cancer. Science, 266, 2011-2015.
5. Harley,C.B., Kim,N.W., Prowse,K.R. et al. (1994) Telomerase, cell immortality, and cancer. Cold Spring Harb. Symp. Quant. Biol., 59, 307-15.
6. Harada,H., Nakagawa,H., Oyama,K., Takaoka,M., Andl,C.D., Jacobmeier,B., von Werder,A., Enders,G.H., Opitz,O.G. and Rustgi,A.K. (2003) Telomerase induces immortalization of human esophageal keratinocytes without p16INK4a inactivation. Mol. Cancer Res., 1, 729-738.
7. Nakagawa,H., Zukerberg,L., Togawa,K., Meltzer,S.J., Nishihara,T. and Rustgi,A.K. (1995) Human cyclin D1 oncogene and esophageal squamous cell carcinoma. Cancer, 76, 541-549.
8. Nakagawa,H., Wang,T.C., Zukerberg,L., Odze,R., Togawa,K., May,G.H., Wilson,J. and Rustgi,A.K. (1997) The targeting of the cyclin D1 oncogene by an Epstein-Barr virus promoter in transgenic mice causes dysplasia in the tongue, esophagus and forestomach. Oncogene, 14, 1185-1190.
9. Okamoto,A., Demetrick,D.J., Spillare,E.A. et al. (1994) Mutations and altered expression of p16INK4 in human cancer. Proc. Natl Acad. Sci. USA, 91, 11045-11049.
10. Bradley,G., Irish,J., MacMillan,C., Mancer,K., Witterick,I., Hartwick,W., Gullane,P., Kamel-Reid,S. and Benchimol,S. (2001) Abnormalities of the ARF-p53 pathway in oral squamous cell carcinoma. Oncogene, 20, 654-658.
11. Masutomi,K., Yu,E.Y., Khurts,S. et al. (2003) Telomerase maintains telomere structure in normal human cells. Cell, 114, 241-253.
12. Meyerson,M., Counter,C.M., Eaton,E.N. et al. (1997) hEST2, the putative human telomerase catalytic subunit gene, is up-regulated in tumor cells and during immortalization. Cell, 90, 785-795.
13. Nakamura,T.M., Morin,G.B., Chapman,K.B., Weinrich,S.L., Andrews,W.H., Lingner,J., Harley,C.B. and Cech,T.R. (1997) Telomerase catalytic subunit homologs from fission yeast and human. Science, 277, 955-959.
14. Bodnar,A.G., Ouellette,M., Frolkis,M., Holt,S.E., Chiu,C.P., Morin,G.B., Harley,C.B., Shay,J.W., Lichtsteiner,S. and Wright,W.E. (1998) Extension of life-span by introduction of telomerase into normal human cells. Science, 279, 349-352.
15. Takakura,M., Kyo,S., Kanaya,T., Tanaka,M. and Inoue,M. (1998) Expression of human telomerase subunits and correlation with telomerase activity in cervical cancer. Cancer Res., 58, 1558-1561.
16. Horikawa,I. and Barrett,J.C. (2003) Transcriptional regulation of the telomerase hTERT gene as a target for cellular and viral oncogenic mechanisms. Carcinogenesis, 24, 1167-1176.
17. Ulaner,G.A., Hu,J.F., Vu,T.H., Giudice,L.C. and Hoffman,A.R. (2001) Tissue-specific alternate splicing of human telomerase reverse transcriptase (hTERT) influences telomere lengths during human development. Int. J. Cancer, 91, 644-649.
18. Cerezo,A., Kalthoff,H., Schuermann,M., Schafer,B. and Boukamp,P. (2002) Dual regulation of telomerase activity through c-Myc-dependent inhibition and alternative splicing of hTERT. J. Cell. Sci., 115, 1305-1312.
19. Aisner,D.L., Wright,W.E. and Shay,J.W. (2002) Telomerase regulation: Not just flipping the switch. Curr. Opin. Genet. Dev., 12, 80-85.
20. Liu,K., Hodes,R.J. and Weng,N. (2001) Cutting edge: Telomerase activation in human T lymphocytes does not require increase in telomerase reverse transcriptase (hTERT) protein but is associated with hTERT phosphorylation and nuclear translocation. J. Immunol., 166, 4826-4830.
21. Poole,J.C., Andrews,L.G. and Tollefsbol,T.O. (2001) Activity, function, and gene regulation of the catalytic subunit of telomerase (hTERT). Gene, 269, 1-12.
22. Ducrest,A.L., Szutorisz,H., Lingner,J. and Nabholz,M. (2002) Regulation of the human telomerase reverse transcriptase gene. Oncogene, 21, 541-552.
23. Horikawa,I., Cable,P.L., Afshari,C. and Barrett,J.C. (1999) Cloning and characterization of the promoter region of human telomerase reverse transcriptase gene. Cancer Res., 59, 826-830.
24. Kyo,S. and Inoue,M. (2002) Complex regulatory mechanisms of telomerase activity in normal and cancer cells: How can we apply them for cancer therapy? Oncogene, 21, 688-697.
25. Takakura,M., Kyo,S., Kanaya,T., Hirano,H., Takeda,J., Yutsudo,M. and Inoue,M. (1999) 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., 59, 551-557.
26. Greenberg,R.A., O'Hagan,R.C., Deng,H., Xiao,Q., Hann,S.R., Adams,R.R., Lichtsteiner,S., Chin,L., Morin,G.B. and DePinho,R.A. (1999) Telomerase reverse transcriptase gene is a direct target of c-Myc but is not functionally equivalent in cellular transformation. Oncogene, 18, 1219-1226.
27. Kyo,S., Takakura,M., Taira,T., Kanaya,T., Itoh,H., Yutsudo,M., Ariga,H. and Inoue,M. (2000) Sp1 cooperates with c-Myc to activate transcription of the human telomerase reverse transcriptase gene (hTERT). Nucleic Acids Res., 28, 669-677.
28. Xiang,H., Wang,J., Mao,Y., Liu,M., Reddy,V.N. and Li,D.W. (2002) Human telomerase accelerates growth of lens epithelial cells through regulation of the genes mediating RB/E2F pathway. Oncogene, 21, 3784-3791.
29. Xu,D., Popov,N., Hou,M., Wang,Q., Bjorkholm,M., Gruber,A., Menkel,A.R. and Henriksson,M. (2001) Switch from Myc/Max to Mad1/Max binding and decrease in histone acetylation at the telomerase reverse transcriptase promoter during differentiation of HL60 cells. Proc. Natl Acad. Sci. USA, 98, 3826-3831.
30. Gunes,C., Lichtsteiner,S., Vasserot,A.P. and Englert,C. (2000) Expression of the hTERT gene is regulated at the level of transcriptional initiation and repressed by Mad1. Cancer Res., 60, 2116-2121.
31. Oh,S., Song,Y.H., Yim,J. and Kim,T.K. (2000) Identification of Mad as a repressor of the human telomerase (hTERT) gene. Oncogene, 19, 1485-1490.
32. Hiyama,H., Iavarone,A., LaBaer,J. and Reeves,S.A. (1997) Regulated ectopic expression of cyclin D1 induces transcriptional activation of the cdk inhibitor p21 gene without altering cell cycle progression. Oncogene, 14, 2533-2542.
33. Opitz,O.G., Suliman,Y., Hahn,W.C., Harada,H., Blum,H.E. and Rustgi,A.K. (2001) Cyclin D1 overexpression and p53 inactivation immortalize primary oral keratinocytes by a telomerase-independent mechanism. J. Clin. Invest., 108, 725-732.
34. Andl,C.D., Mizushima,T., Nakagawa,H., Oyama,K., Harada,H., Chruma,K., Herlyn,M. and Rustgi,A.K. (2003) Epidermal growth factor receptor mediates increased cell proliferation, migration, and aggregation in esophageal keratinocytes in vitro and in vivo. J. Biol. Chem., 278, 1824-1830.
35. Hahn,W.C., Stewart,S.A., Brooks,M.W., York,S.G., Eaton,E., Kurachi,A., Beijersbergen,R.L., Knoll,J.H., Meyerson,M. and Weinberg,R.A. (1999) Inhibition of telomerase limits the growth of human cancer cells. Nat. Med., 5, 1164-1170.
36. Jenkins,T.D., Opitz,O.G., Okano,J. and Rustgi,A.K. (1998) Transactivation of the human keratin 4 and Epstein-Barr virus ED-L2 promoters by gut-enriched Kruppel-like factor. J. Biol. Chem., 273, 10747-10754.
37. Herman,J.G., Graff,J.R., Myohanen,S., Nelkin,B.D. and Baylin,S.B. (1996) Methylation-specific PCR: A novel PCR assay for methylation status of CpG islands. Proc. Natl Acad. Sci. USA, 93, 9821-9826.
38. Nakagawa,H., Inomoto,T. and Rustgi,A.K. (1997) A CACCC box-like cis-regulatory element of the Epstein-Barr virus ED-L2 promoter interacts with a novel transcriptional factor in tissue-specific squamous epithelia. J. Biol. Chem., 272, 16688-16699.
39. Schreiber,E., Matthias,P., Muller,M.M. and Schaffner,W. (1989) Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res., 17, 6419.
40. Opitz,O.G., Jenkins,T.D. and Rustgi,A.K. (1998) Transcriptional regulation of the differentiation-linked human K4 promoter is dependent upon esophageal-specific nuclear factors. J. Biol. Chem., 273, 23912-23921.
41. Hanahan,D. and Weinberg,R.A. (2000) The hallmarks of cancer. Cell, 100, 57-70.
42. Meyerson,M. (1998) Telomerase enzyme activation and human cell immortalization. Toxicol. Lett., 102-103, 41-45.
43. Casillas,M.A., Brotherton,S.L., Andrews,L.G., Ruppert,J.M. and Tollefsbol,T.O. (2003) Induction of endogenous telomerase (hTERT) by c-Myc in WI-38 fibroblasts transformed with specific genetic elements. Gene, 316, 57-65.
44. Cong,Y.S., Wen,J. and Bacchetti,S. (1999) The human telomerase catalytic subunit hTERT: Organization of the gene and characterization of the promoter. Hum. Mol. Genet., 8, 137-142.
45. Horikawa,I., Cable,P.L., Mazur,S.J., Appella,E., Afshari,C.A. and Barrett,J.C. (2002) Downstream E-box-mediated regulation of the human telomerase reverse transcriptase (hTERT) gene transcription: Evidence for an endogenous mechanism of transcriptional repression. Mol. Biol. Cell., 13, 2585-2597.
46. Pugh,B.F. and Tjian,R. (1991) Transcription from a TATA-less promoter requires a multisubunit TFIID complex. Genes Dev., 5, 1935-1945.
47. Kanaya,T., Kyo,S., Hamada,K., Takakura,M., Kitagawa,Y., Harada,H. and Inoue,M. (2000) Adenoviral expression of p53 represses telomerase activity through down-regulation of human telomerase reverse transcriptase transcription. Clin. Cancer Res., 6, 1239-1247.
48. Won,J., Yim,J. and Kim,T.K. (2002) Sp1 and Sp3 recruit histone deacetylase to repress transcription of human telomerase reverse transcriptase (hTERT) promoter in normal human somatic cells. J. Biol. Chem., 277, 38230-38238.
49. Xu,D., Wang,Q., Gruber,A., Bjorkholm,M., Chen,Z., Zaid,A., Selivanova,G., Peterson,C., Wiman,K.G. and Pisa,P. (2000) Downregulation of telomerase reverse transcriptase mRNA expression by wild type p53 in human tumor cells. Oncogene, 19, 5123-5133.
50. Wang,J., Xie,L.Y., Allan,S., Beach,D. and Hannon,G.J. (1998) Myc activates telomerase. Genes Dev., 12, 1769-1774.
51. Veldman,T., Horikawa,I., Barrett,J.C. and Schlegel,R. (2001) Transcriptional activation of the telomerase hTERT gene by human papillomavirus type 16 E6 oncoprotein. J. Virol., 75, 4467-4472.
52. Gewin,L. and Galloway,D.A. (2001) E box-dependent activation of telomerase by human papillomavirus type 16 E6 does not require induction of c-myc. J. Virol., 75, 7198-7201.
53. Crowe,D.L., Nguyen,D.C., Tsang,K.J. and Kyo,S. (2001) E2F-1 represses transcription of the human telomerase reverse transcriptase gene. Nucleic Acids Res., 29, 2789-2794.
54. Won,J., Yim,J. and Kim,T.K. (2002) Opposing regulatory roles of E2F in human telomerase reverse transcriptase (hTERT) gene expression in human tumor and normal somatic cells. FASEB J., 16, 1943-1945.
55. Dessain,S.K., Yu,H., Reddel,R.R., Beijersbergen,R.L. and Weinberg,R.A. (2000) Methylation of the human telomerase gene CpG island. Cancer Res., 60, 537-541.
56. Guilleret,I. and Benhattar,J. (2004) Unusual distribution of DNA methylation within the hTERT CpG island in tissues and cell lines. Biochem. Biophys. Res. Commun., 325, 1037-1043.