Dual role of DNA methylation inside and outside of CTCF-binding regions in the transcriptional regulation of the telomerase hTERT gene

Nucleic Acids Research

Volumn 35, Issue 4, 2007, Pages 1245-1256

  Renaud, S ^a,b   Loukinov, D ^b   Abdullaev, Z ^b   Guilleret, I ^a   Bosman, F T ^a   Lobanenkov, V ^b   Benhattar, J ^a  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; NUCLEAR FACTOR; TELOMERASE REVERSE TRANSCRIPTASE;

ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CPG ISLAND; DEMETHYLATION; DNA METHYLATION; DOWN REGULATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; EXON; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; TRANSCRIPTION REGULATION;

AZACITIDINE; BINDING SITES; CELL LINE; DNA METHYLATION; DNA-BINDING PROTEINS; DOWN-REGULATION; EXONS; GENE EXPRESSION REGULATION; HUMANS; PROMOTER REGIONS (GENETICS); REPRESSOR PROTEINS; TELOMERASE; TRANSCRIPTION, GENETIC;

EID: 34047137148     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkl1125     Document Type: Article

References (45)

1. Blackburn,E.H. (1997) The telomere and telomerase: Nucleic acid-protein complexes acting in a telomere homeostasis system. A review. Biochemistry (Mosc.), 62, 1196-1201.
2. Greider,C.W. (1996) Telomere length regulation. Annu. Rev. Biochem., 65, 337-365.
3. 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.
4. Yasumoto,S., Kunimura,C., Kikuchi,K., Tahara,H., Ohji,H., Yamamoto,H., Ide,T. and Utakoji,T. (1996) Telomerase activity in normal human epithelial cells. Oncogene, 13, 433-439.
5. 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.
6. Feng,J., Funk,W.D., Wang,S.S., Weinrich,S.L., Avilion,A.A., Chiu,C.P., Adams,R.R., Chang,E., Allsopp,R.C., Yu,J. et al. (1995) The RNA component of human telomerase. Science, 269, 1236-1241.
7. Weinrich,S.L., Pruzan,R., Ma,L., Ouellette,M., Tesmer,V.M., Holt,S.E., Bodnar,A.G., Lichtsteiner,S., Kim,N.W., Trager,J.B. et al. (1997) Reconstitution of human telomerase with the template RNA component hTR and the catalytic protein subunit hTRT. Nat. Genet., 17, 498-502.
8. 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.
9. 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.
10. 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.
11. Wick,M., Zubov,D. and Hagen,G. (1999) Genomic organization and promoter characterization of the gene encoding the human telomerase reverse transcriptase (hTERT). Gene, 232, 97-106.
12. Goueli,B.S. and Janknecht,R. (2003) Regulation of telomerase reverse transcriptase gene activity by upstream stimulatory factor. Oncogene, 22, 8042-8047.
13. Goueli,B.S. and Janknecht,R. (2004) Upregulation of the catalytic Telomerase Subunit by the Transcription Factor ER81 and Oncogenic HER2/ Neu, Ras, or Raf. Mol. Cell. Biol., 24, 25-35.
14. Lv,J., Liu,H., Wang,Q., Tang,Z., Hou,L. and Zhang,B. (2003) Molecular cloning of a novel human gene encoding histone acetyltransferase-like protein involved in transcriptional activation of hTERT. Biochem. Biophys. Res. Commun., 311, 506-513.
15. Nishi,H., Nakada,T., Kyo,S., Inoue,M., Shay,J.W. and Isaka,K. (2004) Hypoxia-inducible factor 1 mediates upregulation of telomerase (hTERT). Mol. Cell. Biol., 24, 6076-6083.
16. Pardal,R., Clarke,M.F. and Morrison,S.J. (2003) Applying the principles of stem-cell biology to cancer. Nat. Rev. Cancer, 3, 895-902.
17. 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.
18. Renaud,S., Loukinov,D., Bosman,F.T., Lobanenkov,V. and Benhattar,J. (2005) CTCF binds the proximal exonic region of hTERT and inhibits its transcription. Nucleic Acids Res., 33, 6850-6860.
19. Valk-Lingbeek,M.E., Bruggeman,S.W. and van Lohuizen,M. (2004) Stem cells and cancer; the polycomb connection. Cell, 118, 409-418.
20. Yatabe,N., Kyo,S., Maida,Y., Nishi,H., Nakamura,M., Kanaya,T., Tanaka,M., Isaka,K., Ogawa,S. and Inoue,M. (2004) HIF-1-mediated activation of telomerase in cervical cancer cells. Oncogene, 23, 3708-3715.
21. Horikawa,I., Chiang,Y.J., Patterson,T., Feigenbaum,L., Leem,S.H., Michishita,E., Larionov,V., Hodes,R.J. and Barrett,J.C. (2005) Differential cis-regulation of human versus mouse TERT gene expression in vivo: Identification of a human-specific repressive element. Proc. Natl. Acad. Sci. U.S.A., 102, 18437-18442.
22. Renaud,S., Bosman,F.T. and Benhattar,J. (2003) Implication of the exon region in the regulation of the human telomerase reverse transcriptase gene promoter. Biochem. Biophys. Res. Commun., 300, 47-54.
23. Klenova,E.M., Nicolas,R.H., Paterson,H.F., Carne,A.F., Heath,C.M., Goodwin,G.H., Neiman,P.E. and Lobanenkov,V.V. (1993) CTCF, a conserved nuclear factor required for optimal transcriptional activity of the chicken c-myc gene, is an 11-Zn-finger protein differentially expressed in multiple forms. Mol. Cell. Biol., 13, 7612-7624.
24. Lutz,M., Burke,L.J., Barreto,G., Goeman,F., Greb,H., Arnold,R., Schultheiss,H., Brehm,A., Kouzarides,T., Lobanenkov,V. et al. (2000) Transcriptional repression by the insulator protein CTCF involves histone deacetylases. Nucleic Acids Res., 28, 1707-1713.
25. 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.
26. Devereux,T.R., Horikawa,I., Anna,C.H., Annab,L.A., Afshari,C.A. and Barrett,J.C. (1999) DNA methylation analysis of the promoter region of the human telomerase reverse transcriptase (hTERT) gene. Cancer Res., 59, 6087-6090.
27. Guilleret,I., Yan,P., Grange,F., Braunschweig,R., Bosman,F.T. and Benhattar,J. (2002) Hypermethylation of the human telomerase catalytic subunit (hTERT) gene correlates with telomerase activity. Int. J. Cancer, 101, 335-341.
28. Robertson,K.D. and Jones,P.A. (2000) DNA methylation: Past, present and future directions. Carcinogenesis, 21, 461-467.
29. 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.
30. Baisse,B., Bian,Y.S. and Benhattar,J. (2000) Microdissection by exclusion and DNA extraction for multiple PCR analyses from archival tissue sections. Biotechniques, 28, 856-858, 860, 862.
31. Benhattar,J. and Clement,G. (2004) Methylation-sensitive single-strand conformation analysis: A rapid method to screen for and analyze DNA methylation. Methods Mol. Biol., 287, 181-193.
32. Kanduri,C., Pant,V., Loukinov,D., Pugacheva,E., Qi,C.F., Wolffe,A., Ohlsson,R. and Lobanenkov,V.V. (2000) Functional association of CTCF with the insulator upstream of the H19 gene is parent of origin-specific and methylation-sensitive. Curr. Biol., 10, 853-856.
33. Guilleret,I. and Benhattar,J. (2003) Demethylation of the human telomerase catalytic subunit (hTERT) gene promoter reduced hTERT expression and telomerase activity and shortened telomeres. Exp. Cell Res., 289, 326-334.
34. Kitagawa,Y., Kyo,S., Takakura,M., Kanaya,T., Koshida,K., Namiki,M. and Inoue,M. (2000) Demethylating reagent 5-azacytidine inhibits telomerase activity in human prostate cancer cells through transcriptional repression of hTERT. Clin. Cancer Res., 6, 2868-2875.
35. Kumakura,S., Tsutsui,T.W., Yagisawa,J., Barrett,J.C. and Tsutsui,T. (2005) Reversible conversion of immortal human cells from telomerase-positive to telomerase-negative cells. Cancer Res., 65, 2778-2786.
36. Ducrest,A.L., Amacker,M., Mathieu,Y.D., Cuthbert,A.P., Trott,D.A., Newbold,R.F., Nabholz,M. and Lingner,J. (2001) Regulation of human telomerase activity: Repression by normal chromosome 3 abolishes nuclear telomerase reverse transcriptase transcripts but does not affect c-Myc activity. Cancer Res., 61, 7594-7602.
37. Yi,X., Shay,J.W. and Wright,W.E. (2001) Quantitation of telomerase components and hTERT mRNA splicing patterns in immortal human cells. Nucleic Acids Res., 29, 4818-4825.
38. Robertson,K.D. and Ambinder,R.F. (1997) Methylation of the Epstein-Barr virus genome in normal lymphocytes. Blood, 90, 4480-4484.
39. Filippova,G.N., Fagerlie,S., Klenova,E.M., Myers,C., Dehner,Y., Goodwin,G., Neiman,P.E., Collins,S.J. and Lobanenkov,V.V. (1996) An exceptionally conserved transcriptional repressor, CTCF, employs different combinations of zinc fingers to bind diverged promoter sequences of avian and mammalian c-myc oncogenes. Mol. Cell Biol., 16, 2802-2813.
40. Nomoto,K., Maekawa,M., Sugano,K., Ushiama,M., Fukayama,N., Fujita,S. and Kakizoe,T. (2002) Methylation status and expression of human telomerase reverse transcriptase mRNA in relation to hypermethylation of the p16 gene in colorectal cancers as analyzed by bisulfite PCR-SSCP. Jpn. J. Clin. Oncol., 32, 3-8.
41. Widschwendter,A., Muller,H.M., Hubalek,M.M., Wiedemair,A., Fiegl,H., Goebel,G., Mueller-Holzner,E., Marth,C. and Widschwendter,M. (2004) Methylation status and expression of human telomerase reverse transcriptase in ovarian and cervical cancer. Gynecol. Oncol., 93, 407-416.
42. Bechter,O.E., Eisterer,W., Dlaska,M., Kuhr,T. and Thaler,J. (2002) CpG island methylation of the hTERT promoter is associated with lower telomerase activity in B-cell lymphocytic leukemia. Exp. Hematol., 30, 26-33.
43. Lopatina,N.G., Poole,J.C., Saldanha,S.N., Hansen,N.J., Key,J.S., Pita,M.A., Andrews,L.G. and Tollefsbol,T.O. (2003) Control mechanisms in the regulation of telomerase reverse transcriptase expression in differentiating human teratocarcinoma cells. Biochem. Biophys. Res. Commun., 306, 650-659.
44. Ritz,J.M., Kuhle,O., Riethdorf,S., Sipos,B., Deppert,W., Englert,C. and Gunes,C. (2005) A novel transgenic mouse model reveals humanlike regulation of an 8-kbp human TERT gene promoter fragment in normal and tumor tissues. Cancer Res., 65, 1187-1196.
45. Loukinov,D.I., Pugacheva,E., Vatolin,S., Pack,S.D., Moon,H., Chernukhin,I., Mannan,P., Larsson,E., Kanduri,C., Vostrov,A.A. et al. (2002) BORIS, a novel male germ-line-specific protein associated with epigenetic reprogramming events, shares the same 11-zinc-finger domain with CTCF, the insulator protein involved in reading imprinting marks in the soma. Proc. Natl. Acad. Sci. U.S.A., 99, 6806-6811.