Super-telomeres in transformed human fibroblasts

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 8, 2013, Pages 1885-1893

  Chiodi, Ilaria ^a   Belgiovine, Cristina ^a   Zongaro, Samantha ^a,f   Ricotti, Roberta ^a   Horard, Beatrice ^b,g   Lossani, Andrea ^a   Focher, Federico ^a   Gilson, Eric ^b,c,d   Giulotto, Elena ^e   Mondello, Chiara ^a  

^a CNR   (Italy)

^b UNIVERSITÉ DE LYON   (France)

^c UNIVERSITY OF NICE SOPHIA ANTIPOLIS   (France)

^d CENTRE HOSPITALIER UNIVERSITAIRE DE NICE   (France)

^e UNIVERSITY OF PAVIA   (Italy)

^f INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^g CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

DNA methylation; Telomerase; Telomere; Telomere positioning effect; Telomeric protein

Indexed keywords

HEAT SHOCK PROTEIN 90; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; TELOMERIC REPEAT BINDING FACTOR 1; TELOMERIC REPEAT BINDING FACTOR 2;

ARTICLE; CARCINOGENESIS; CATALYSIS; CELL CULTURE; CELL ELONGATION; CELL GROWTH; CELL IMMORTALIZATION; CELL LEVEL; CELL TRANSFORMATION; CONTROLLED STUDY; DNA METHYLATION; ENZYME ACTIVITY; ENZYME REGULATION; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN CELL; MALIGNANT TRANSFORMATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; TELOMERE;

CELL LINE, TRANSFORMED; CELL TRANSFORMATION, NEOPLASTIC; DNA METHYLATION; FIBROBLASTS; HUMANS; NUCLEAR PROTEINS; RNA; TELOMERASE; TELOMERE; TELOMERE HOMEOSTASIS; TELOMERIC REPEAT BINDING PROTEIN 1; TELOMERIC REPEAT BINDING PROTEIN 2;

EID: 84877824666     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.03.030     Document Type: Article

References (52)

1. Blackburn E.H., Greider C.W., Szostak J.W. Telomeres and telomerase: the path from maize, Tetrahymena and yeast to human cancer and aging. Nat. Med. 2006, 12:1133-1138.
2. Makarov V.L., Hirose Y., Langmore J.P. Long G tails at both ends of human chromosomes suggest a C strand degradation mechanism for telomere shortening. Cell 1997, 88:657-666.
3. Gilson E., Geli V. How telomeres are replicated. Nat. Rev. Mol. Cell Biol. 2007, 8:825-838.
4. Palm W., de Lange T. How shelterin protects mammalian telomeres. Annu. Rev. Genet. 2008, 42:301-334.
5. van Steensel B., de Lange T. Control of telomere length by the human telomeric protein TRF1. Nature 1997, 385:740-743.
6. Ancelin K., Brunori M., Bauwens S., Koering C.E., Brun C., Ricoul M., Pommier J.P., Sabatier L., Gilson E. Targeting assay to study the cis functions of human telomeric proteins: evidence for inhibition of telomerase by TRF1 and for activation of telomere degradation by TRF2. Mol. Cell. Biol. 2002, 22:3474-3487.
7. Takai K.K., Hooper S., Blackwood S., Gandhi R., de Lange T. In vivo stoichiometry of shelterin components. J. Biol. Chem. 2010, 285:1457-1467.
8. Loayza D., De Lange T. POT1 as a terminal transducer of TRF1 telomere length control. Nature 2003, 423:1013-1018.
9. Blackburn E.H., Collins K. Telomerase: an RNP enzyme synthesizes DNA. Cold Spring Harb. Perspect. Biol. 2011, 3.
10. Cohen S.B., Graham M.E., Lovrecz G.O., Bache N., Robinson P.J., Reddel R.R. Protein composition of catalytically active human telomerase from immortal cells. Science 2007, 315:1850-1853.
11. Masutomi K., Yu E.Y., Khurts S., Ben-Porath I., Currier J.L., Metz G.B., Brooks M.W., Kaneko S., Murakami S., DeCaprio J.A., Weinberg R.A., Stewart S.A., Hahn W.C. Telomerase maintains telomere structure in normal human cells. Cell 2003, 114:241-253.
12. Rodier F., Campisi J. Four faces of cellular senescence. J. Cell Biol. 2011, 192:547-556.
13. 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. (Epub 2003 Nov 2005).
14. Harley C.B. Telomere loss: mitotic clock or genetic time bomb?. Mutat. Res. 1991, 256:271-282.
15. Shay J.W., Bacchetti S. A survey of telomerase activity in human cancer. Eur. J. Cancer 1997, 33:787-791.
16. Bryan T.M., Englezou A., Dalla-Pozza L., Dunham M.A., Reddel R.R. Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nat. Med. 1997, 3:1271-1274.
17. Cesare A.J., Reddel R.R. Alternative lengthening of telomeres: models, mechanisms and implications. Nat. Rev. Genet. 2010, 11:319-330.
18. Belgiovine C., Chiodi I., Mondello C. Telomerase: cellular immortalization and neoplastic transformation. Multiple functions of a multifaceted complex. Cytogenet. Genome Res. 2008, 122:255-262.
19. Bodnar A.G., Ouellette M., Frolkis M., Holt S.E., Chiu C.P., Morin G.B., Harley C.B., Shay J.W., Lichtsteiner S., Wright W.E. Extension of life-span by introduction of telomerase into normal human cells. Science 1998, 279:349-352.
20. Ouellette M.M., Aisner D.L., Savre-Train I., Wright W.E., Shay J.W. Telomerase activity does not always imply telomere maintenance. Biochem. Biophys. Res. Commun. 1999, 254:795-803.
21. Zongaro S., Verri A., Giulotto E., Mondello C. Telomere length and radiosensitivity in human fibroblast clones immortalized by ectopic telomerase expression. Oncol. Rep. 2008, 19:1605-1609.
22. Cristofari G., Lingner J. Telomere length homeostasis requires that telomerase levels are limiting. EMBO J. 2006, 25:565-574.
23. Vidale P., Magnani E., Nergadze S.G., Santagostino M., Cristofari G., Smirnova A., Mondello C., Giulotto E. The catalytic and the RNA subunits of human telomerase are required to immortalize equid primary fibroblasts. Chromosoma 2012, 121:475-488.
24. Belgiovine C., Frapolli R., Bonezzi K., Chiodi I., Favero F., Mello-Grand M., Dei Tos A.P., Giulotto E., Taraboletti G., D'Incalci M., Mondello C. Reduced expression of the ROCK inhibitor Rnd3 is associated with increased invasiveness and metastatic potential in mesenchymal tumor cells. PLoS One 2010, 5:e14154.
25. Mondello C., Chiesa M., Rebuzzini P., Zongaro S., Verri A., Colombo T., Giulotto E., D'Incalci M., Franceschi C., Nuzzo F. Karyotype instability and anchorage-independent growth in telomerase-immortalized fibroblasts from two centenarian individuals. Biochem. Biophys. Res. Commun. 2003, 308:914-921.
26. Ostano P., Bione S., Belgiovine C., Chiodi I., Ghimenti C., Scovassi A.I., Chiorino G., Mondello C. Cross-analysis of gene and miRNA genome-wide expression profiles in human fibroblasts at different stages of transformation. OMICS 2012, 16:24-36.
27. Zongaro S., de Stanchina E., Colombo T., D'Incalci M., Giulotto E., Mondello C. Stepwise neoplastic transformation of a telomerase immortalized fibroblast cell line. Cancer Res. 2005, 65:11411-11418.
28. Harley C.B., Futcher A.B., Greider C.W. Telomeres shorten during ageing of human fibroblasts. Nature 1990, 345:458-460.
29. Lansdorp P.M., Verwoerd N.P., van de Rijke F.M., Dragowska V., Little M.T., Dirks R.W., Raap A.K., Tanke H.J. Heterogeneity in telomere length of human chromosomes. Hum. Mol. Genet. 1996, 5:685-691.
30. Yi X., Tesmer V.M., Savre-Train I., Shay J.W., Wright W.E. Both transcriptional and posttranscriptional mechanisms regulate human telomerase template RNA levels. Mol. Cell. Biol. 1999, 19:3989-3997.
31. Gilson E., Horard B. Comprehensive DNA methylation profiling of human repetitive DNA elements using an MeDIP-on-RepArray assay. Methods Mol. Biol. 2012, 859:267-291.
32. Horard B., Eymery A., Fourel G., Vassetzky N., Puechberty J., Roizes G., Lebrigand K., Barbry P., Laugraud A., Gautier C., Simon E.B., Devaux F., Magdinier F., Vourc'h C., Gilson E. Global analysis of DNA methylation and transcription of human repetitive sequences. Epigenetics 2009, 4:339-350.
33. Benetti R., Garcia-Cao M., Blasco M.A. Telomere length regulates the epigenetic status of mammalian telomeres and subtelomeres. Nat. Genet. 2007, 39:243-250.
34. van Deutekom J.C., Wijmenga C., van Tienhoven E.A., Gruter A.M., Hewitt J.E., Padberg G.W., van Ommen G.J., Hofker M.H., Frants R.R. FSHD associated DNA rearrangements are due to deletions of integral copies of a 3.2kb tandemly repeated unit. Hum. Mol. Genet. 1993, 2:2037-2042.
35. Gabellini D., D'Antona G., Moggio M., Prelle A., Zecca C., Adami R., Angeletti B., Ciscato P., Pellegrino M.A., Bottinelli R., Green M.R., Tupler R. Facioscapulohumeral muscular dystrophy in mice overexpressing FRG1. Nature 2006, 439:973-977.
36. Pickett H.A., Cesare A.J., Johnston R.L., Neumann A.A., Reddel R.R. Control of telomere length by a trimming mechanism that involves generation of t-circles. EMBO J. 2009, 28:799-809.
37. Donà F., Chiodi I., Belgiovine C., Raineri T., Ricotti R., Mondello C., Scovassi A.I. Poly(ADP-ribosylation) and neoplastic transformation: effect of PARP inhibitors. Curr. Pharm. Biotechnol. Mar. 20 2012, (Epub ahead of print).
38. Chang J.T., Lu Y.C., Chen Y.J., Tseng C.P., Chen Y.L., Fang C.W., Cheng A.J. hTERT phosphorylation by PKC is essential for telomerase holoprotein integrity and enzyme activity in head neck cancer cells. Br. J. Cancer 2006, 94:870-878.
39. DeZwaan D.C., Freeman B.C. HSP90 manages the ends. Trends Biochem. Sci. 2010, 35:384-391.
40. Trepel J., Mollapour M., Giaccone G., Neckers L. Targeting the dynamic HSP90 complex in cancer. Nat. Rev. Cancer 2010, 10:537-549.
41. Matsutani N., Yokozaki H., Tahara E., Tahara H., Kuniyasu H., Haruma K., Chayama K., Yasui W., Tahara E. Expression of telomeric repeat binding factor 1 and 2 and TRF1-interacting nuclear protein 2 in human gastric carcinomas. Int. J. Oncol. 2001, 19:507-512.
42. Oh B.K., Kim Y.J., Park C., Park Y.N. Up-regulation of telomere-binding proteins, TRF1, TRF2, and TIN2 is related to telomere shortening during human multistep hepatocarcinogenesis. Am. J. Pathol. 2005, 166:73-80.
43. Nijjar T., Bassett E., Garbe J., Takenaka Y., Stampfer M.R., Gilley D., Yaswen P. Accumulation and altered localization of telomere-associated protein TRF2 in immortally transformed and tumor-derived human breast cells. Oncogene 2005, 24:3369-3376.
44. Nakanishi K., Kawai T., Kumaki F., Hiroi S., Mukai M., Ikeda E., Koering C.E., Gilson E. Expression of mRNAs for telomeric repeat binding factor (TRF)-1 and TRF2 in atypical adenomatous hyperplasia and adenocarcinoma of the lung. Clin. Cancer Res. 2003, 9:1105-1111.
45. Munoz P., Blanco R., Blasco M.A. Role of the TRF2 telomeric protein in cancer and ageing. Cell Cycle 2006, 5:718-721.
46. Biroccio A., Rizzo A., Elli R., Koering C.E., Belleville A., Benassi B., Leonetti C., Stevens M.F., D'Incalci M., Zupi G., Gilson E. TRF2 inhibition triggers apoptosis and reduces tumourigenicity of human melanoma cells. Eur. J. Cancer 2006, 42:1881-1888.
47. Blanco R., Munoz P., Flores J.M., Klatt P., Blasco M.A. Telomerase abrogation dramatically accelerates TRF2-induced epithelial carcinogenesis. Genes Dev. 2007, 21:206-220.
48. Simonet T., Zaragosi L.E., Philippe C., Lebrigand K., Schouteden C., Augereau A., Bauwens S., Ye J., Santagostino M., Giulotto E., Magdinier F., Horard B., Barbry P., Waldmann R., Gilson E. The human TTAGGG repeat factors 1 and 2 bind to a subset of interstitial telomeric sequences and satellite repeats. Cell Res. 2011, 21:1028-1038.
49. Blasco M.A. The epigenetic regulation of mammalian telomeres. Nat. Rev. Genet. 2007, 8:299-309.
50. Oh B.K., Um T.H., Choi G.H., Park Y.N. Frequent changes in subtelomeric DNA methylation patterns and its relevance to telomere regulation during human hepatocarcinogenesis. Int. J. Cancer 2011, 128:857-868.
51. Vera E., Canela A., Fraga M.F., Esteller M., Blasco M.A. Epigenetic regulation of telomeres in human cancer. Oncogene 2008, 27:6817-6833.
52. Gadalla S.M., Katki H.A., Shebl F.M., Giri N., Alter B.P., Savage S.A. The relationship between DNA methylation and telomere length in dyskeratosis congenita. Aging Cell 2012, 11:24-28.