Telomere dysfunction is related to the intrinsic radio-resistance of human oral cancer cells

Oral Oncology

Volumn 44, Issue 3, 2008, Pages 261-269

  McCaul, James A ^a   Gordon, Katrina E ^a   Minty, Fay ^a   Fleming, Janis ^a   Parkinson, E Kenneth ^a  

^a BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

Author keywords

Keratinocyte; Oral; Radiotherapy; Squamous cell carcinoma; Telomere

Indexed keywords

DNA FRAGMENT; TELOMERASE REPEAT FRAGMENT; TELOMERASE REVERSE TRANSCRIPTASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASSAY; CANCER CELL; CANCER CELL CULTURE; CANCER RADIOTHERAPY; CELL MEMBRANE RESISTANCE; GAMMA IRRADIATION; MOUSE; MOUTH CANCER; NONHUMAN; PRIORITY JOURNAL; RADIOSENSITIZATION; REGRESSION ANALYSIS; SQUAMOUS CELL CARCINOMA; STATISTICAL ANALYSIS; STRUCTURAL CHROMOSOME ABERRATION; VIRUS INFECTION;

ANAPHASE; CARCINOMA, SQUAMOUS CELL; CELL AGING; CELL LINE, TUMOR; CELL SURVIVAL; GAMMA RAYS; HUMANS; MOUTH NEOPLASMS; RADIATION TOLERANCE; REGRESSION ANALYSIS; STATISTICS, NONPARAMETRIC; TELOMERASE; TELOMERE; TREATMENT FAILURE;

EID: 39149092358     PISSN: 13688375     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.oraloncology.2007.02.010     Document Type: Article

References (58)

1. de Lange T. Protection of mammalian telomeres. Oncogene 21 (2002) 532-540
2. Holt S.E., Shay J.W., and Wright W.E. Refining the telomere-telomerase hypothesis of aging and cancer. Nat Biotechnol 14 (1996) 836-839
3. Olovnikov A.M. A theory of marginotomy. The incomplete copying of template margin in enzymic synthesis of polynucleotides and biological significance of the phenomenon. J Theor Biol 41 (1973) 181-190
4. von Zglinicki T., Saretzki G., Docke W., and Lotze C. Mild hyperoxia shortens telomeres and inhibits proliferation of fibroblasts: a model for senescence?. Exp Cell Res 220 (1995) 186-193
5. Makarov V.L., Hirose Y., and Langmore J.P. Long G tails at both ends of human chromosomes suggest a C strand degradation mechanism for telomere shortening. Cell 88 (1997) 657-666
6. Allsopp R.C., Chang E., Kashefi-Aazam M., Rogaev E.I., Piatyszek M.A., Shay J.W., et al. Telomere shortening is associated with cell division in vitro and in vivo. Exp Cell Res 220 (1995) 194-200
7. Munro J., Steeghs K., Morrison V., Ireland H., and Parkinson E.K. Human fibroblast replicative senescence can occur in the absence of extensive cell division and short telomeres. Oncogene 20 (2001) 3541-3552
8. Bodnar A.G., Ouellette M., Frolkis M., Holt S.E., Chiu C.P., Morin G.B., et al. Extension of life-span by introduction of telomerase into normal human cells. Science 279 (1998) 349-352
9. Chiang Y.J., Hemann M.T., Hathcock K.S., Tessarollo L., Feigenbaum L., Hahn W.C., et al. Expression of telomerase RNA template, but not telomerase reverse transcriptase, is limiting for telomere length maintenance in vivo. Mol Cell Biol 24 (2004) 7024-7031
10. Rudolph K.L., Chang S., Lee H.W., Blasco M., Gottlieb G.J., Greider C., et al. Longevity, stress response, and cancer in aging telomerase-deficient mice. Cell 96 (1999) 701-712
11. Vulliamy T., Marrone A., Dokal I., and Mason P.J. Association between aplastic anaemia and mutations in telomerase RNA. Lancet 359 (2002) 2168-2170
12. Vulliamy T., Marrone A., Goldman F., Dearlove A., Bessler M., Mason P.J., et al. The RNA component of telomerase is mutated in autosomal dominant dyskeratosis congenita. Nature 413 (2001) 432-435
13. Yamaguchi H., Calado R.T., Ly H., Kajigaya S., Baerlocher G.M., Chanock S.J., et al. Mutations in TERT, the gene for telomerase reverse transcriptase, in aplastic anemia. N Engl J Med 352 (2005) 1413-1424
14. Blackburn E.H. Telomere states and cell fates. Nature 408 (2000) 53-56
15. d'Adda di Fagagna F., Reaper P.M., Clay-Farrace L., Fiegler H., Carr P., Von Zglinicki T., et al. A DNA damage checkpoint response in telomere-initiated senescence. Nature 426 (2003) 194-198
16. Smogorzewska A., and de Lange T. Different telomere damage signaling pathways in human and mouse cells. Embo J 21 (2002) 4338-4348
17. Karlseder J., Broccoli D., Dai Y., Hardy S., and de Lange T. p53- and ATM-dependent apoptosis induced by telomeres lacking TRF2. Science 283 (1999) 1321-1325
18. Bartkova J., Horejsi Z., Koed K., Kramer A., Tort F., Zieger K., et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434 (2005) 864-870
19. Gorgoulis V.G., Vassiliou L.V., Karakaidos P., Zacharatos P., Kotsinas A., Liloglou T., et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434 (2005) 907-913
20. Jacobs J.J., and de Lange T. Significant role for p16INK4a in p53-independent telomere-directed senescence. Curr Biol 14 (2004) 2302-2308
21. Gisselsson D., Pettersson L., Hoglund M., Heidenblad M., Gorunova L., Wiegant J., et al. Chromosomal breakage-fusion-bridge events cause genetic intratumor heterogeneity. Proc Natl Acad Sci USA 97 (2000) 5357-5362
22. Gordon K.E., Ireland H., Roberts M., Steeghs K., McCaul J.A., MacDonald D.G., et al. High levels of telomere dysfunction bestow a selective disadvantage during the progression of human oral squamous cell carcinoma. Cancer Res 63 (2003) 458-467
23. Counter C.M., Hahn W.C., Wei W., Caddle S.D., Beijersbergen R.L., Lansdorp P.M., et al. Dissociation among in vitro telomerase activity, telomere maintenance, and cellular immortalization. Proc Natl Acad Sci USA 95 (1998) 14723-14728
24. Bryan T.M., Englezou A., Dalla-Pozza L., Dunham M.A., and Reddel R.R. Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nat Med 3 (1997) 1271-1274
25. Goytisolo F.A., Samper E., Martin-Caballero J., Finnon P., Herrera E., Flores J.M., et al. Short telomeres result in organismal hypersensitivity to ionizing radiation in mammals. J Exp Med 192 (2000) 1625-1636
26. Wong K.K., Chang S., Weiler S.R., Ganesan S., Chaudhuri J., Zhu C., et al. Telomere dysfunction impairs DNA repair and enhances sensitivity to ionizing radiation. Nat Genet 26 (2000) 85-88
27. Latre L., Tusell L., Martin M., Miro R., Egozcue J., Blasco M.A., et al. Shortened telomeres join to DNA breaks interfering with their correct repair. Exp Cell Res 287 (2003) 282-288
28. Rubio M.A., Davalos A.R., and Campisi J. Telomere length mediates the effects of telomerase on the cellular response to genotoxic stress. Exp Cell Res 298 (2004) 17-27
29. Nakamura M., Masutomi K., Kyo S., Hashimoto M., Maida Y., Kanaya T., et al. Efficient inhibition of human telomerase reverse transcriptase expression by RNA interference sensitizes cancer cells to ionizing radiation and chemotherapy. Hum Gene Ther (2005)
30. Gisselsson D., Jonson T., Petersen A., Strombeck B., Dal Cin P., Hoglund M., et al. Telomere dysfunction triggers extensive DNA fragmentation and evolution of complex chromosome abnormalities in human malignant tumors. Proc Natl Acad Sci USA 98 (2001) 12683-12688
31. Edington K.G., Loughran O.P., Berry I.J., and Parkinson E.K. Cellular immortality: a late event in the progression of human squamous cell carcinoma of the head and neck associated with p53 alteration and a high frequency of allele loss. Mol Carcinog 13 (1995) 254-265
32. Loughran O., Clark L.J., Bond J., Baker A., Berry I.J., Edington K.G., et al. Evidence for the inactivation of multiple replicative lifespan genes in immortal human squamous cell carcinoma keratinocytes. Oncogene 14 (1997) 1955-1964
33. Parkinson E.K., Hume W.J., and Potten C.S. The radiosensitivity of cultured human and mouse keratinocytes. Int J Radiat Biol Relat Stud Phys Chem Med 50 (1986) 717-726
34. Rudolph K.L., Millard M., Bosenberg M.W., and DePinho R.A. Telomere dysfunction and evolution of intestinal carcinoma in mice and humans. Nat Genet 28 (2001) 155-159
35. Jung M., Notario V., and Dritschilo A. Mutations in the p53 gene in radiation-sensitive and -resistant human squamous carcinoma cells. Cancer Res 52 (1992) 6390-6393
36. Brachman D.G., Beckett M., Graves D., Haraf D., Vokes E., and Weichselbaum R.R. p53 mutation does not correlate with radiosensitivity in 24 head and neck cancer cell lines. Cancer Res 53 (1993) 3667-3669
37. Goytisolo F.A., and Blasco M.A. Many ways to telomere dysfunction: in vivo studies using mouse models. Oncogene 21 (2002) 584-591
38. Louis S.F., Vermolen B.J., Garini Y., Young I.T., Guffei A., Lichtensztejn Z., et al. c-Myc induces chromosomal rearrangements through telomere and chromosome remodeling in the interphase nucleus. Proc Natl Acad Sci USA 102 (2005) 9613-9618
39. Hingorani S.R., Wang L., Multani A.S., Combs C., Deramaudt T.B., Hruban R.H., et al. Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell 7 (2005) 469-483
40. Gisselsson D., Jonson T., Yu C., Martins C., Mandahl N., Wiegant J., et al. Centrosomal abnormalities, multipolar mitoses, and chromosomal instability in head and neck tumours with dysfunctional telomeres. Br J Cancer 87 (2002) 202-207
41. Agochiya M., Brunton V.G., Owens D.W., Parkinson E.K., Paraskeva C., Keith W.N., et al. Increased dosage and amplification of the focal adhesion kinase gene in human cancer cells. Oncogene 18 (1999) 5646-5653
42. Malliri A., Yeudall W.A., Nikolic M., Crouch D.H., Parkinson E.K., and Ozanne B. Sensitivity to transforming growth factor beta 1-induced growth arrest is common in human squamous cell carcinoma cell lines: c-MYC down-regulation and p21waf1 induction are important early events. Cell Growth Differ 7 (1996) 1291-1304
43. McIlrath J., Bouffler S.D., Samper E., Cuthbert A., Wojcik A., Szumiel I., et al. Telomere length abnormalities in mammalian radiosensitive cells. Cancer Res 61 (2001) 912-915
44. Kampinga H.H., Van Waarde-Verhagen M.A., Van Assen-Bolt A.J., Nieuwenhuis B., Rodemann H.P., Prowse K.R., et al. Reconstitution of active telomerase in primary human foreskin fibroblasts: effects on proliferative characteristics and response to ionizing radiation. Int J Radiat Biol 80 (2004) 377-388
45. Pirzio L.M., Freulet-Marriere M.A., Bai Y., Fouladi B., Murnane J.P., Sabatier L., et al. Human fibroblasts expressing hTERT show remarkable karyotype stability even after exposure to ionizing radiation. Cytogenet Genome Res 104 (2004) 87-94
46. Rubio M.A., Kim S.H., and Campisi J. Reversible manipulation of telomerase expression and telomere length. Implications for the ionizing radiation response and replicative senescence of human cells. J Biol Chem 277 (2002) 28609-28617
47. Masutomi K., Possemato R., Wong J.M., Currier J.L., Tothova Z., Manola J.B., et al. The telomerase reverse transcriptase regulates chromatin state and DNA damage responses. Proc Natl Acad Sci USA 102 (2005) 8222-8227
48. Lue N.F., Bosoy D., Moriarty T.J., Autexier C., Altman B., and Leng S. Telomerase can act as a template- and RNA-independent terminal transferase. Proc Natl Acad Sci USA 102 (2005) 9778-9783
49. Masutomi K., and Hahn W.C. Telomerase expression - only half the story. Cancer Biol Ther 2 (2003) 685-686
50. Petersen S., Saretzki G., and von Zglinicki T. Preferential accumulation of single-stranded regions in telomeres of human fibroblasts. Exp Cell Res 239 (1998) 152-160
51. von Zglinicki T. Oxidative stress shortens telomeres. Trends Biochem Sci 27 (2002) 339-344
52. von Zglinicki T., and Martin-Ruiz C.M. Telomeres as biomarkers for ageing and age-related diseases. Curr Mol Med 5 (2005) 197-203
53. Bergamaschi D., Gasco M., Hiller L., Sullivan A., Syed N., Trigiante G., et al. p53 polymorphism influences response in cancer chemotherapy via modulation of p73-dependent apoptosis. Cancer Cell 3 (2003) 387-402
54. Erber R., Conradt C., Homann N., Enders C., Finckh M., Dietz A., et al. TP53 DNA contact mutations are selectively associated with allelic loss and have a strong clinical impact in head and neck cancer. Oncogene 16 (1998) 1671-1679
55. Sullivan A., Syed N., Gasco M., Bergamaschi D., Trigiante G., Attard M., et al. Polymorphism in wild-type p53 modulates response to chemotherapy in vitro and in vivo. Oncogene 23 (2004) 3328-3337
56. Yamazaki Y., Chiba I., Hirai A., Notani K., Kashiwazaki H., Tei K., et al. Radioresistance in oral squamous cell carcinoma with p53 DNA contact mutation. Am J Clin Oncol 26 (2003) e124-e129
57. Yamazaki Y., Chiba I., Hirai A., Sugiura C., Notani K., Kashiwazaki H., et al. Specific p53 mutations predict poor prognosis in oral squamous cell carcinoma. Oral Oncol 39 (2003) 163-169
58. Burns J.E., Baird M.C., Clark L.J., Burns P.A., Edington K., Chapman C., et al. Gene mutations and increased levels of p53 protein in human squamous cell carcinomas and their cell lines. Br J Cancer 67 (1993) 1274-1284