Telomere-based proliferative lifespan barriers in Werner-syndrome fibroblasts involve both p53-dependent and p53-independent mechanisms

Journal of Cell Science

Volumn 116, Issue 7, 2003, Pages 1349-1357

  Davis, Terence ^a   Sinhrao, Sim K ^a   Wyllie, Fiona S ^a   Haughton, Michele F ^a   Smith, Paul J ^a   Wiltshire, Marie ^a   Wynford Thomas, David ^a   Jones, Christopher J ^a   Faragher, Richard G A ^b   Kipling, David ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF BRIGHTON   (United Kingdom)

Author keywords

Ageing; Cellular senescence; Microinjection; Oncoprotein; Telomerase

Indexed keywords

CELL PROTEIN; DNA; NEUTRALIZING ANTIBODY; ONCOPROTEIN; PROTEIN P16; PROTEIN P21; PROTEIN P53; TELOMERASE;

AGING; CELL CYCLE; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DNA CONTENT; ENZYME SYNTHESIS; FIBROBLAST CULTURE; HUMAN; HUMAN CELL; MICROINJECTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; REVIEW; SENESCENCE; SIGNAL TRANSDUCTION; TELOMERE; WART VIRUS; WERNER SYNDROME;

AGING; ANTIBODIES; CELL AGING; CELL DIVISION; CELL LINE; CYCLIN-DEPENDENT KINASE INHIBITOR P16; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLINS; DNA; DNA-BINDING PROTEINS; FIBROBLASTS; GENES, CDC; HUMANS; LONGEVITY; MITOSIS; ONCOGENE PROTEINS, VIRAL; PLOIDIES; RETINOBLASTOMA PROTEIN; SIGNAL TRANSDUCTION; TELOMERASE; TELOMERE; TUMOR SUPPRESSOR PROTEIN P53; WERNER SYNDROME;

HUMAN PAPILLOMAVIRUS TYPES; MENTHA; PAPILLOMAVIRUS;

EID: 0037383795     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00331     Document Type: Review

References (50)

1. Allsopp, R. C. and Harley, C. B. (1995). Evidence for a critical telomere length in senescent human fibroblasts. Exp. Cell Res. 219, 130-136.
2. 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.
3. Bohr, V. A., Souza Pinto, N., Nyaga, S. G., Dianov, G., Kraemer, K., Seidman, M. M. and Brosh, R. M., Jr (2001). DNA repair and mutagenesis in Werner syndrome. Environ. Mol. Mutagen. 38, 227-234.
4. Bohr, V. A., Brosh, R. M., Jr, von Kobbe, C., Opresko, P. and Karmakar, P. (2002). Pathways defective in the human premature aging disease Werner syndrome. Biogerontology 3, 89-94.
5. Bond, J. A., Wyllie, F. S. and Wynford-Thomas. D. (1994). Escape from senescence in human diploid fibroblasts induced directly by mutant p53. Oncogene 9, 1885-1889.
6. Bond, J. A., Blaydes, J. P., Rowson, J., Haughton, M. F., Smith, J. R., Wynford-Thomas, D. and Wyllie, F. S. (1995). Mutant p53 rescues human diploid cells from senescence without inhibiting the induction of SDI1/WAF1. Cancer Res. 55, 2404-2409.
7. Bond, J., Haughton, M., Blaydes, J., Gire, V., Wynford-Thomas, D. and Wyllie, F. (1996). Evidence that transcriptional activation by p53 plays a direct role in the induction of cellular senescence. Oncogene 13, 2097-2104.
8. Bond, J. A., Haughton, M. F., Rowson, J. M., Gire, V., Wynford-Thomas, D. and Wyllie, F. S. (1999). Control of replicative life span in human cells: barriers to clonal expansion intermediate between M1 senescence and M2 crisis. Mol. Cell. Biol. 19, 3103-3114.
9. Böttger, V., Böttger, A., Howard, S. F., Picksley, S. M., Chène, P., Garcia-Echeverria, C., Hochkeppel, H.-K. and Lane, D. P. (1996). Identification of novel mdm2 binding peptides by phage display. Oncogene 13, 2141-2147.
10. Bringold, F. and Serrano, M. (2000). Tumor suppressors and oncogenes in cellular senescence. Exp. Gerontol. 35, 317-329.
11. Brown, W. T., Kieras, F. J., Houck, G. E., Jr, Dutkowski, R. and Jenkins, E. C. (1985). A comparison of adult and childhood progerias: Werner syndrome and Hutchinson-Guildford progeria syndrome. Adv. Exp. Med. Biol. 190, 229-244.
12. CIP1/Waf1 gene in normal diploid human fibroblasts. Science 277, 831-834.
13. Choi, D., Whittier, P. S., Oshima, J. and Funk, W. D. (2001). Telomerase expression prevents replicative senescence but does not fully reset mRNA expression patterns in Werner syndrome cell strains. FASEB. J. 15, 1014-1020.
14. Dimri, G. P., Lee, X., Basile, G., Acosta, M., Scott, G., Roskelley, C., Medrano, E. E., Linskens, M., Rubelj, I., Pereira-Smith, O. et al. (1995). A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad Sci. USA 92, 9363-9367.
15. Dulic, V., Beney, G.-E., Frebourg, G., Drullinger, L. F. and Stein, G. H. (2000). Uncoupling between phenotypic senescence and cell cycle arrest in ageing p21-deficient fibroblasts. Mol. Cell. Biol. 20, 6741-6754.
16. Epstein, C. J., Martin, G. M., Schultz, A. L. and Motulsky, A. G. (1996). Werner syndrome: a review of its symptomatology, natural history, pathologic features, genetics and relationship to the natural aging process. Medicine 45, 177-221.
17. Faragher, R. G. A., Kill, I. R., Hunter, J. A., Pope, F. M., Tannock, C. and Shall, S. (1993). The gene responsible for Werner syndrome may be a cell division 'counting' gene. Proc. Natl. Acad. Sci. USA 90, 12030-12034.
18. Filatov, L., Golubovskaya, V., Hurt, J. C., Byrd, L. L., Phillips, J. M. and Kaufmann, W. K. (1998). Chromosomal instability is correlated with telomere erosion and inactivation of G2 checkpoint function in human fibroblasts expressing human papillomavirus type 16 E6 oncoprotein. Oncogene 16, 1825-1838.
19. Fukuchi, K., Martin, G. M. and Monnat, R. J., Jr (1989). Mutator phenotype of Werner syndrome is characterised by extensive deletions. Proc. Natl. Acad. Sci. USA 86, 5893-5897.
20. Gire, V. and Wynford-Thomas, D. (1998). Re-initiation of DNA synthesis and cell division in senescent human fibroblasts by microinjection of anti-p53 antibodies. Mol. Cell. Biol. 18, 1611-1621.
21. Goto, M., Miller, R. W., Ishikawa, Y. and Sugano, H. (1996). Excess of rare cancers in Werner syndrome (adult progeria). Cancer Epidemiol. Biomarkers Prev. 5, 239-246.
22. Gray, M. D., Wang, L., Youssoufian, H., Martin, G. M. and Oshima, J. (1998). Werner helicase is localized to transcriptionally active nucleoli of cycling cells. Exp. Cell. Res. 242, 487-494.
23. Halbert, C. L., Demers, G. W. and Galloway, D. A. (1991). The E7 gene of human papillomavirus type 16 is sufficient for immortalization of human epithelial cells. J. Virol. 65, 473-478.
24. Hoehn, H., Bryant, E. M., Au, K., Norwood, T. H., Boman, H. and Martin, G. M. (1975). Cytogenetics of Werner's syndrome cultured skin fibroblasts. Cytogenet. Cell Genet. 15, 282-298.
25. Huang, S., Li, B., Gray, M. D., Oshima, J., Mian, I. S. and Campisi, J. (1998). The premature ageing syndrome protein, WRN, is a 3′→5′ exonuclease. Nat. Genet. 20, 114-116.
26. Itahana, K., Dimri, G. and Campisi, J. (2001). Regulation of cellular senescence by p53. Eur. J. Biochem. 268, 2784-2791.
27. Lin, J., Teresky, A. K. and Levine, A. J. (1995). Two critical hydrophobic amino acids in the N-terminal domain of the p53 protein are required for the gain of function phenotypes of human p53 mutants. Oncogene 10, 2387-2390.
28. Marciniak, R. A., Lombard, D. B., Johnson, F. B. and Guarente, L. (1998). Nucleolar localization of the Werner syndrome protein in human cells. Proc. Natl. Acad. Sci. USA 95, 6887-6892.
29. Martin, G. M., Sprague, C. C. and Epstein, C. J. (1970). Replicative life span of cultivated human cells. Lab. Invest. 23, 86-92.
30. Martin, G. M., Oshima, J., Gray, M. D. and Pool, M. (1999). What geriatricians should know about the Werner syndrome. J. Am. Geriatr. Soc. 47, 1136-1144.
31. McConnell, B. B., Starborg, M., Brookes, S. and Peters, G. (1998). Inhibitors of cyclin-dependent kinases induce features of replicative senescence in early passage human diploid fibroblasts. Curr. Biol. 12, 351-354.
32. Morgenstern, J. P. and Land, H. (1990). Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18, 3587-3596.
33. 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.
34. Ouellette, M. M., McDaniel, L. D., Wright, W. E., Shay, J. W. and Schultz, R. A. (2000). The establishment of telomerase-immortalised cell lines representing human chromosome instability syndromes. Hum. Mol. Genet. 9, 403-411.
35. Salk, D. (1982). Werner's syndrome: a review of recent research with an analysis of connective tissue metabolism, growth control of cultured cells, and chromosomal aberrations. Hum. Genet. 62, 1-5.
36. Salk, D., Au, K., Hoehn, H. and Martin, G. M. (1981). Cytogenetics of Werner's syndrome cultured skin fibroblasts: variegated translocation mosaicism. Cytogenet. Cell Genet. 30, 92-107.
37. Schulz, V. P., Zakian, V. A., Ogburn, C. E., McKay, J., Jarzebowicz, A. A., Edland, S. D. and Martin, G. M. (1996). Accelerated loss of telomere repeats may not explain accelerated replicative decline in Werner syndrome cells. Hum. Genet. 97, 750-754.
38. Shen, J.-C. and Loeb, L. A. (2001). Unwinding the molecular basis of the Werner syndrome. Mech. Ageing Dev. 122, 921-944.
39. Sherwood, S. W., Rush, D., Ellsworth, J. L. and Schimke, R. T. (1988). Defining cellular senescence in IMR-90 cells: a flow cytometric analysis. Proc. Natl. Acad. Sci. USA 85, 9086-9090.
40. Shiratori, M., Sakamoto, S., Suzuki, N., Tokutake, Y., Kawabe, Y., Enomoto, T., Sugimoto, M., Goto, M., Matsumoto, T. and Furuichi, Y. (1999). Detection by epitope-defined monoclonal antibodies of Werner DNA helicases in the nucleoplasm and their upregulation by cell transformation and immortalization. J. Cell Biol. 144, 1-9.
41. Smith, P. J., Wiltshire, M., Chin, S. F., Rabbitts, P. and Souès, S. (1999). Cell cycle checkpoint evasion and protracted cell cycle arrest in X-irradiated small cell lung carcinoma cells. Int. J. Radiat. Biol. 75, 1137-1147.
42. Stein, G. H., Beeson, M. and Gordon, L. (1990). Failure to phosphorylate the retinoblastoma gene product in senescent human fibroblasts. Science 249, 666-669.
43. Stephen, C. W., Helminen, P. and Lane, D. P. (1995). Characterisation of epitopes on human p53 using phage-displayed peptide libraries: insights into antibody-peptide interactions. J. Mol. Biol. 248, 58-78.
44. Vaziri, H. and Benchimol, S. (1998). Reconstitution of telomerase activity in normal human cells leads to elongation of telomeres and extended reproductive life span. Curr. Biol. 8, 279-282.
45. Cip1 in spontaneously immortalised human fibroblasts. Cell Growth Differ. 9, 139-146.
46. Webley, K., Bond, J. A., Jones, C. J., Blaydes, J. P., Craig, A., Hupp, T. and Wynford-Thomas, D. (2000). Posttranslational modifications of p53 in replicative senescence overlapping but distinct from those induced by DNA damage. Mol. Cell. Biol. 20, 2803-2808.
47. Wright, W. E. and Shay, J. W. (2002). Historical claims and current interpretations of replicative aging. Nat. Biotechnol. 20, 682-688.
48. Wyllie, F., Lemoine, N., Barton, C., Dawson, T., Bond, J. and Wynford-Thomas. D. (1993). Direct growth stimulation of normal human epithelial cells by mutant p53. Mol. Carcinogen. 7, 83-88.
49. Wyllie, F. S., Jones, C. J., Skinner, J. W., Haughton, M. F., Wallis, C., Wynford-Thomas, D., Faragher, R. G. A. and Kipling, D. (2000). Telomerase prevents the accelerated ageing of Werner syndrome fibroblasts. Nat. Genet. 24, 16-17.
50. Yu, C. E., Oshima, J., Fu, Y. H., Wijsman, E. M., Hisama, F., Alisch, R., Matthews, S., Nakura, J., Miki, T., Ouais, S. et al. (1996). Positional cloning of the Werner's syndrome gene. Science 272, 258-262.