Telomere loss, not average telomere length, confers radiosensitivity to TK6-irradiated cells

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 740, Issue 1-2, 2012, Pages 13-20

  Berardinelli, F ^a,b   Nieri, D ^a,b   Sgura, A ^a,b   Tanzarella, C ^a,b   Antoccia, A ^a,b  

^a ROMA TRE UNIVERSITY   (Italy)

^b INFN SEZIONE DI ROMA   (Italy)

Author keywords

Ionizing radiation; Radioresistance; Telomerase; Telomere; Telomere loss; TK6

Indexed keywords

TELOMERASE;

ARTICLE; CELL CLONE; CELL HETEROGENEITY; CHROMOSOME LOSS; CHROMOSOME SIZE; CLONOGENIC ASSAY; CONTROLLED STUDY; DAUDI CELL; ENZYME ACTIVITY; FLUORESCENCE IN SITU HYBRIDIZATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; RADIATION DOSE; RADIATION EXPOSURE; RADIOSENSITIVITY; TELOMERE; TELOMERE HOMEOSTASIS; TELOMERIC REPEAT AMPLIFICATION PROTOCOL; X RAY;

CELL LINE; HUMANS; LYMPHOCYTES; RADIATION TOLERANCE; TELOMERASE; TELOMERE HOMEOSTASIS; TELOMERE SHORTENING;

EID: 84871804251     PISSN: 00275107     EISSN: 09218262     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2012.11.004     Document Type: Article

References (40)

1. Weichselbaum R.R., Beckett M.A., Vokes E.E., Brachman D.G., Haraf D., Hallahan D., Kufe D. Cellular and molecular mechanisms of radioresistance. Cancer Treat. Res. 1995, 74:131-140.
2. Banath J.P., Olive P.L. Expression of phosphorylated histone H2AX as a surrogate of cell killing by drugs that create DNA double-strand breaks. Cancer Res. 2003, 63:4347-4350.
3. Chen X., Shen B., Xia L., Khaletzkiy A., Chu D., Wong J.Y., Li J.J. Activation of nuclear factor kappaB in radioresistance of TP53-inactive human keratinocytes. Cancer Res. 2002, 62:1213-1221.
4. Jameel J.K., Rao V.S., Cawkwell L., Drew P.J. Radioresistance in carcinoma of the breast. Breast 2004, 13:452-460.
5. Morgan W.F., Murnane J.P. A role for genomic instability in cellular radioresistance?. Cancer Metastasis Rev. 1995, 14:49-58.
6. Skinner H.D., Sandulache V.C., Ow T.J., Meyn R.E., Yordy J.S., Beadle B.M., Fitzgerald A.L., Giri U., Ang K.K., Myers J.N. TP53 disruptive mutations lead to head and neck cancer treatment failure through inhibition of radiation-induced senescence. Clin. Cancer Res. 2012, 18:290-300.
7. Ayouaz A., Raynaud C., Heride C., Revaud D., Sabatier L. Telomeres: hallmarks of radiosensitivity. Biochimie 2008, 90:60-72.
8. Fumagalli M., Rossiello F., Clerici M., Barozzi S., Cittaro D., Kaplunov J.M., Bucci G., Dobreva M., Matti V., Beausejour C.M., Herbig U., Longhese M.P., d'Adda F.d. Telomeric DNA damage is irreparable and causes persistent DNA-damage-response activation. Nat. Cell Biol. 2012, 14:355-365.
9. Genesca A., Martin M., Latre L., Soler D., Pampalona J., Tusell L. Telomere dysfunction: a new player in radiation sensitivity. Bioessays 2006, 28:1172-1180.
10. Salin H., Ricoul M., Morat L., Sabatier L. Increased genomic alteration complexity and telomere shortening in B-CLL cells resistant to radiation-induced apoptosis. Cytogenet. Genome Res. 2008, 122:343-349.
11. Wong K.K., Chang S., Weiler S.R., Ganesan S., Chaudhuri J., Zhu C., Artandi S.E., Rudolph K.L., Gottlieb G.J., Chin L., Alt F.W., DePinho R.A. Telomere dysfunction impairs DNA repair and enhances sensitivity to ionizing radiation. Nat. Genet. 2000, 26:85-88.
12. Counter C.M., Avilion A.A., LeFeuvre C.E., Stewart N.G., Greider C.W., Harley C.B., Bacchetti S. Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J. 1992, 11:1921-1929.
13. Morin G.B. The human telomere terminal transferase enzyme is a ribonucleoprotein that synthesizes TTAGGG repeats. Cell 1989, 59:521-529.
14. McIlrath J., Bouffler S.D., Samper E., Cuthbert A., Wojcik A., Szumiel I., Bryant P.E., Riches A.C., Thompson A., Blasco M.A., Newbold R.F., Slijepcevic P. Telomere length abnormalities in mammalian radiosensitive cells. Cancer Res. 2001, 61:912-915.
15. Sharpless N.E., DePinho R.A. How stem cells age and why this makes us grow old. Nat. Rev. Mol. Cell Biol. 2007, 8:703-713.
16. Hemann M.T., Strong M.A., Hao L.Y., Greider C.W. The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell 2001, 107:67-77.
17. Muraki K., Nyhan K., Han L., Murnane J.P. Mechanisms of telomere loss and their consequences for chromosome instability. Front. Oncol. 2012, 2:135.
18. Drissi R., Wu J., Hu Y., Bockhold C., Dome J.S. Telomere shortening alters the kinetics of the DNA damage response after ionizing radiation in human cells. Cancer Prev. Res. (Phila.) 2011, 4:1973-1981.
19. Bai Y., Murnane J.P. Telomere instability in a human tumor cell line expressing NBS1 with mutations at sites phosphorylated by ATM. Mol. Cancer Res. 2003, 1:1058-1069.
20. Bai Y., Murnane J.P. Telomere instability in a human tumor cell line expressing a dominant-negative WRN protein. Hum. Genet. 2003, 113:337-347.
21. Cabuy E., Newton C., Joksic G., Woodbine L., Koller B., Jeggo P.A., Slijepcevic P. Accelerated telomere shortening and telomere abnormalities in radiosensitive cell lines. Radiat. Res. 2005, 164:53-62.
22. Castella M., Puerto S., Creus A., Marcos R., Surralles J. Telomere length modulates human radiation sensitivity in vitro. Toxicol. Lett. 2007, 172:29-36.
23. Goytisolo F.A., Samper E., Martin-Caballero J., Finnon P., Herrera E., Flores J.M., Bouffler S.D., Blasco M.A. Short telomeres result in organismal hypersensitivity to ionizing radiation in mammals. J. Exp. Med. 2000, 192:1625-1636.
24. Latre L., Tusell L., Martin M., Miro R., Egozcue J., Blasco M.A., Genesca A. Shortened telomeres join to DNA breaks interfering with their correct repair. Exp. Cell Res. 2003, 287:282-288.
25. Sprung C.N., Davey D.S., Goh S.K., Radford I.R., McKay M.J. Uncoupling of telomere length and radiosensitivity in mouse lymphoma cell lines of similar genetic background. Int. J. Radiat. Biol. 2007, 83:515-521.
26. Sprung C.N., Davey D.S., Withana N.P., Distel L.V., McKay M.J. Telomere length in lymphoblast cell lines derived from clinically radiosensitive cancer patients. Cancer Biol. Ther. 2008, 7:638-644.
27. 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.
28. Furth E.E., Thilly W.G., Penman B.W., Liber H.L., Rand W.M. Quantitative assay for mutation in diploid human lymphoblasts using microtiter plates. Anal. Biochem. 1981, 110:1-8.
29. Liber H.L., Thilly W.G. Mutation assay at the thymidine kinase locus in diploid human lymphoblasts. Mutat. Res. 1982, 94:467-485.
30. Durante M., Furusawa Y., Gotoh E. A simple method for simultaneous interphase-metaphase chromosome analysis in biodosimetry. Int. J. Radiat. Biol. 1998, 74:457-462.
31. Berardinelli F., Antoccia A., Cherubini R., De N.V., Gerardi S., Cirrone G.A., Tanzarella C., Sgura A. Transient activation of the ALT pathway in human primary fibroblasts exposed to high-LET radiation. Radiat. Res. 2010, 174:539-549.
32. Perner S., Bruderlein S., Hasel C., Waibel I., Holdenried A., Ciloglu N., Chopurian H., Nielsen K.V., Plesch A., Hogel J., Moller P. Quantifying telomere lengths of human individual chromosome arms by centromere-calibrated fluorescence in situ hybridization and digital imaging. Am. J. Pathol. 2003, 163:1751-1756.
33. Wege H., Chui M.S., Le H.T., Tran J.M., Zern M.A. SYBR Green real-time telomeric repeat amplification protocol for the rapid quantification of telomerase activity. Nucleic Acids Res. 2003, 31:E3.
34. Kim N.W., Wu F. Advances in quantification and characterization of telomerase activity by the telomeric repeat amplification protocol (TRAP). Nucleic Acids Res. 1997, 25:2595-2597.
35. Baerlocher G.M., Vulto I., de Jong G., Lansdorp P.M. Flow cytometry and FISH to measure the average length of telomeres (flow FISH). Nat. Protoc. 2006, 1:2365-2376.
36. Neuhof D., Ruess A., Wenz F., Weber K.J. Induction of telomerase activity by irradiation in human lymphoblasts. Radiat. Res. 2001, 155:693-697.
37. Blasco M.A. The epigenetic regulation of mammalian telomeres. Nat. Rev. Genet. 2007, 8:299-309.
38. Berardinelli F., Antoccia A., Cherubini R., De N.V., Gerardi S., Tanzarella C., Sgura A. Telomere alterations and genomic instability in long-term cultures of normal human fibroblasts irradiated with X rays and protons. Radiat. Prot. Dosim. 2011, 143:274-278.
39. Leteurtre F., Li X., Gluckman E., Carosella E.D. Telomerase activity during the cell cycle and in gamma-irradiated hematopoietic cells. Leukemia 1997, 11:1681-1689.
40. Soler D., Pampalona J., Tusell L., Genesca A. Radiation sensitivity increases with proliferation-associated telomere dysfunction in nontransformed human epithelial cells. Aging Cell 2009, 8:414-425.