Role of p14^ARF in Replicative and Induced Senescence of Human Fibroblasts

REFERENCES

• Alcorta, D. A., Y. Xiong, D. Phelps, G. Hannon, D. Beach, and J. C. Barrett. 1996. Involvement of the cyclin-dependent kinase inhibitor p16(INK4a) in replicative senescence of normal human fibroblasts. Proc. Natl. Acad. Sci. USA 93:13742–13747.
   PubMed Web of Science ®Google Scholar
• Artandi, S. E., and R. A. DePinho. 2000. Mice without telomerase: what can they teach us about human cancer?. Nat. Med. 6:852–855.
   PubMedGoogle Scholar
• Atadja, P., H. Wong, I. Garkavtsev, C. Veillette, and K. Riabowol. 1995. Increased activity of p53 in senescing fibroblasts. Proc. Natl. Acad. Sci. USA 92:8348–8352.
   PubMed Web of Science ®Google Scholar
• Bates, S., A. C. Phillips, P. A. Clark, F. Stott, G. Peters, R. L. Ludwig, and K. H. Vousden. 1998. p14ARF links the tumour suppressors RB and p53. Nature 395:124–125.
   PubMed Web of Science ®Google Scholar
• Bayreuther, K., H. P. Rodemann, R. Hommel, K. Dittmann, M. Albiez, and P. I. Francz. 1988. Human skin fibroblasts in vitro differentiate along a terminal cell lineage. Proc. Natl. Acad. Sci. USA 85:5112–5116.
   PubMed Web of Science ®Google Scholar
• Bean, L. J. H., and G. R. Stark. 2001. Phosphorylation of serines 15 and 37 is necessary for efficient accumulation of p53 following irradiation with UV. Oncogene 20:1076–1084.
   PubMedGoogle Scholar
• Blasco, M. A., H. W. Lee, M. P. Hande, E. Samper, P. M. Lansdorp, R. A. Depinho, and C. W. Greider. 1997. Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91:25–34.
   PubMed Web of Science ®Google Scholar
• Bodnar, A. G., M. Quellette, M. Frolkis, S. E. Holt, C. P. Chiu, G. B. Morin, C. B. Harley, J. W. Shay, S. Lichtsteiner, and W. E. Wright. 1998. Extension of life-span by introduction of telomerase into normal human cells. Science 279:349–352.
   PubMed Web of Science ®Google Scholar
• Brenner, A. J., M. R. Stampfer, and C. M. Aldaz. 1998. Increased p16 expression with first senescence arrest in human mammary epithelial cells and extended growth capacity with p16 inactivation. Oncogene 17:199–205.
   PubMed Web of Science ®Google Scholar
• Brown, J. P., W. Wei, and J. M. Sedivy. 1997. Bypass of senescence after disruption of p21CIP1/WAF1 gene in normal diploid human fibroblasts. Science 277:831–834.
   PubMed Web of Science ®Google Scholar
• Bunz, F., A. Dutriaux, C. Lengauer, T. Waldman, S. Zhou, J. P. Brown, J. M. Sedivy, K. W. Kinzler, and B. Vogelstein. 1998. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282:1497–1501.
   PubMed Web of Science ®Google Scholar
• Cairns, P., T. J. Polasik, Y. Eby, K. Tokino, J. Califano, A. Merlo, L. Mao, J. Herath, R. Jenkins, W. Westra, J. L. Rutter, A. Buckler, E. Gabrielson, M. Tockman, K. R. Cho, L. Hedrick, G. S. Bova, W. Issacs, W. Koch, D. Schwab, and D. Sidransky. 1995. Frequency of homologous deletion at p16/CDKN2 in primary human tumours. Nat. Genet. 11:210–212.
   PubMed Web of Science ®Google Scholar
• Campisi, J.. 2000. Cancer, aging and cellular senescence. In Vivo 14:183–188.
   PubMed Web of Science ®Google Scholar
• Chen, Q. M., J. C. Bartholomew, J. Campisi, M. Acosta, J. D. Reagan, and B. N. Ames. 1998. Molecular analysis of H2O2-induced senescent-like growth arrest in normal human fibroblasts: p53 and Rb control G1 arrest but not cell replication. Biochem. J. 332:43–50.
   PubMed Web of Science ®Google Scholar
• Chien, M., C. Rinker-Schaeffer, and W. M. Stadler. 2000. A G2/M growth arrest response to low-dose intermittent H2O2 in normal uroepithelial cells. Int. J. Oncol. 17:425–432.
   PubMedGoogle Scholar
• Cristofalo, V. J., and R. J. Pignolo. 1996. Molecular markers of senescence in fibroblast-like cultures. Exp. Gerontol. 31:111–123.
   PubMed Web of Science ®Google Scholar
• de Stanchina, E., M. E. McCurrach, F. Zindy, S.-Y. Shieh, G. Ferbeyre, A. V. Samuelson, C. Prives, M. F. Roussel, C. J. Sherr, and S. W. Lowe. 1998. E1A signaling to p53 involves the p19ARF tumor suppressor. Genes Dev. 12:2434–2442.
   PubMed Web of Science ®Google Scholar
• Dickson, M. A., W. C. Hahn, Y. Ino, V. Ronfard, J. Y. Wu, R. A. Weinberg, D. N. Louis, F. P. Li, and J. G. Rheinwald. 2000. Human keratinocytes that express hTERT and also bypass a p16INK4a-enforced mechanism that limits life span become immortal yet retain normal growth and differentiation characteristics. Mol. Cell. Biol. 20:1436–1447.
   PubMed Web of Science ®Google Scholar
• Dimri, G. P., K. Itahana, M. Acosta, and J. Campisi. 2000. Regulation of a senescence checkpoint response by the E2F1 transcription factor and p14ARF tumor suppressor. Mol. Cell. Biol. 20:273–285.
   PubMed Web of Science ®Google Scholar
• Dimri, G. P., X. Lee, G. Basile, M. Acosta, G. Scott, C. Roskelley, E. E. Medrano, M. Linskens, I. Rubelj, O. Pereira-Smith, M. Peacocke, and J. Campisi. 1995. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. USA 92:9363–9367.
   PubMed Web of Science ®Google Scholar
• Farwell, D. G., K. A. Shera, J. I. Koop, G. A. Bonnet, C. P. Matthews, G. W. Reuther, M. D. Coltrera, J. K. McDougall, and A. J. Klingelhutz. 2000. Genetic and epigenetic changes in human epithelial cells immortalized by telomerase. Am. J. Pathol. 156:1537–1547.
   PubMedGoogle Scholar
• Ferbeyre, G., E. de Stanchina, E. Querido, N. Baptiste, C. Prives, and S. W. Lowe. 2000. PML is induced by oncogenic ras and promotes premature senescence. Genes Dev. 15:2015–2027.
   Google Scholar
• Gire, V., and D. Wynford-Thomas. 1998. Reinitiation of DNA synthesis and cell division in senescent human fibroblasts by microinjection of anti-p53 antibodies. Mol. Cell. Biol. 18:1611–1621.
   PubMedGoogle Scholar
• Goldstein, S.. 1990. Replicative senescence: the human fibroblast comes of age. Science 249:1129–1133.
   PubMed Web of Science ®Google Scholar
• Groth, A., J. D. Weber, B. M. Willumens, C. J. Sherr, and M. F. Roussel. 2000. Oncogenic Ras induces p19ARF and growth arrest in mouse embryo fibroblasts lacking p21Cip1 and p27Kip1 without activating cyclin D-dependent kinases. J. Biol. Chem. 275:27473–27480.
   PubMedGoogle Scholar
• Haber, D. A.. 1997. Splicing into senescence: the curious case of p16 and p19ARF. Cell 91:555–558.
   PubMed Web of Science ®Google Scholar
• Harley, C. B., A. B. Futcher, and C. W. Greider. 1990. Telomeres shorten during aging of human fibroblasts. Nature 345:458–460.
   PubMed Web of Science ®Google Scholar
• Huschtscha, L. I., and R. R. Reddel. 1999. p16INK4a and the control of cellular proliferative life span. Carcinogenesis 20:921–926.
   PubMedGoogle Scholar
• Jacks, T.. 1996. Lessons from the p53 mutant mouse. J. Cancer Res. Clin. Oncol. 122:319–327.
   PubMedGoogle Scholar
• Jiang, H., H. S. Chou, and L. Zhu. 1998. Requirement of cyclin E-Cdk2 inhibition in p16INK4a-mediated growth suppression. Mol. Cell. Biol. 18:5284–5290.
   PubMedGoogle Scholar
• Kamijo, T., F. Zindy, M. F. Roussel, D. E. Quelle, J. R. Downing, R. A. Ashmun, G. Grosveld, and C. J. Sherr. 1997. Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 91:649–659.
   PubMed Web of Science ®Google Scholar
• Kiyono, T., S. A. Foster, J. I. Koop, J. K. McDougall, D. A. Galloway, and A. J. Klingelhutz. 1998. Both Rb/p16INK4a inactivation and telomerase activity are required to immortalize human epithelial cells. Nature 396:84–88.
   PubMed Web of Science ®Google Scholar
• Konstantinidis, A. K., R. Radhakrishnan, F. Gu, R. N. Rao, and W. K. Yeh. 1998. Purification, characterization, and kinetic mechanism of cyclin D1·CDK4: a major target for cell cycle regulation. J. Biol. Chem. 273:26506–26515.
   PubMedGoogle Scholar
• Li, Y., C. W. Jenkins, M. A. Nichols, and Y. Xiong. 1994. Cell cycle expression and p53 regulation of the cyclin-dependent kinase inhibitor p21. Oncogene 9:2261–2268.
   PubMed Web of Science ®Google Scholar
• Lin, A. W., M. Barradas, J. C. Stone, L. V. Aelst, M. Serrano, and S. W. Lowe. 1998. Premature senescence involving p53 and p16 is activated in response to constitutive MEK/MAPK mitogenic signaling. Genes Dev. 12:3008–3019.
   PubMed Web of Science ®Google Scholar
• Lu, K. K., A. V. Bazarov, L. S. Yoon, and J. M. Sedivy. 1998. Isolation of temperature-sensitive mutations in the c-raf-1 catalytic domain and expression of conditionally active and dominant-negative forms of Raf-1 in cultured mammalian cells. Cell Growth Differ. 9:367–380.
   PubMedGoogle Scholar
• Ly, D. H., D. J. Lockhart, R. A. Lerner, and P. G. Schultz. 2000. Mitotic misregulation and human aging. Science 287:2486–2492.
   PubMed Web of Science ®Google Scholar
• Mateyak, M. K., A. J. Obaya, S. Adachi, and J. M. Sedivy. 1997. Phenotypes of c-Myc-deficient rat fibroblasts isolated by targeted homologous recombination. Cell Growth Differ. 8:1039–1048.
   PubMedGoogle Scholar
• Mazars, G. R., and P. S. Jat. 1997. Expression of p24, a novel p21Waf1/Cip1/Sdi1-related protein, correlates with measurement of the finite proliferative potential of rodent embryo fibroblasts. Proc. Natl. Acad. Sci. USA 94:151–156.
   PubMedGoogle Scholar
• McConnell, B. B., M. Starborg, S. Brookes, and G. Peters. 1998. Inhibitors of cyclin-dependent kinases induce features of replicative senescence in early passage human diploid fibroblasts. Curr. Biol. 8:351–356.
   PubMed Web of Science ®Google Scholar
• Meyerson, M., C. M. Counter, E. N. Eaton, L. W. Ellisen, P. Steiner, S. D. Caddle, L. Ziaugra, R. L. Beijersbergen, M. J. Davidoff, Q. Liu, S. Bacchetti, D. A. Haber, and R. A. Weinberg. 1997. hEST2, the putative human telomerase catalytic subunit gene, is up-regulated in tumor cells and during immortalization. Cell 90:785–795.
   PubMed Web of Science ®Google Scholar
• Migliaccio, M., M. Amacker, T. Just, P. Reichenbach, D. Valmori, J. C. Cerottini, P. Romero, and M. Nabholz. 2000. Ectopic human telomerase catalytic subunit expression maintains telomere length but is not sufficient for CD8(+) T lymphocyte immortalization. J. Immunol. 165:4978–4984.
   PubMed Web of Science ®Google Scholar
• Mitra, J., C. Y. Dai, K. Somasundaram, W. S. El-Deiry, K. Satymoorthy, M. Herlyn, and G. H. Enders. 1999. Induction of p21WAF1/CIP1 and inhibition of Cdk2 mediated by the tumor suppressor p16INK4a. Mol. Cell. Biol. 19:3916–3928.
   PubMed Web of Science ®Google Scholar
• Modestou, M., V. Puig-Antich, C. Korgaonkar, A. Eapen, and D. E. Quelle. 2001. The alternative reading frame tumor suppressor inhibits growth through p21-dependent and p21-independent pathways. Cancer Res. 61:3145–3150.
   PubMedGoogle Scholar
• Morales, C. P., S. E. Holt, M. Ouellette, K. J. Kaur, Y. Yan, K. S. Wilson, M. A. White, W. E. Wright, and J. W. Shay. 1999. Absence of cancer-associated changes in human fibroblasts immortalized with telomerase. Nat. Genet. 21:115–118.
   PubMed Web of Science ®Google Scholar
• Morgenstern, J. P., and H. Land. 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.
   PubMed Web of Science ®Google Scholar
• Nanayama, H., H. Yokoi, and J. Fujita. 1992. Quantification of mRNA by non-radioactive RT-PCR and CCD imaging system. Nucleic Acids Res. 18:4939
   Google Scholar
• Ogryzko, V. V., T. H. Hirai, V. R. Russanova, D. A. Barbie, and B. H. Howard. 1996. Human fibroblast commitment to a senescence-like state in response to histone deacetylase inhibitors is cell cycle dependent. Mol. Cell. Biol. 16:5210–5218.
   PubMed Web of Science ®Google Scholar
• Ohtani, N., Z. Zobedee, T. J. G. Huot, J. A. Stinson, M. Sugimoto, Y. Ohashi, A. D. Sharrocks, G. Peters, and E. Hara. 2001. Opposing effects of Ets and Id proteins on p16INK4a expression during cellular senescence. Nature 409:1067–1070.
   PubMed Web of Science ®Google Scholar
• Palmero, I., C. Pantoja, and M. Serrano. 1998. p19ARF links the tumour suppressor p53 to Ras. Nature 395:125–126.
   PubMed Web of Science ®Google Scholar
• Pantoja, C., and M. Serrano. 1999. Murine fibroblasts lacking p21 undergo senescence and are resistant to transformation by oncogenic Ras. Oncogene 18:4974–4982.
   PubMed Web of Science ®Google Scholar
• Pearson, M., R. Carbone, C. Sebastiani, M. Cioce, M. Fagioli, S. Saito, Y. Higashimoto, E. Appella, S. Minucci, P. P. Pandolfi, and P. G. Pelicci. 2000. PML regulates p53 acetylation and premature senescence by oncogenic Ras. Nature 406:207–210.
   PubMed Web of Science ®Google Scholar
• Pomerantz, J., N. Schreiber-Agus, N. J. Liegeois, A. Silverman, L. Alland, L. Chin, J. Potes, K. Chen, I. Orlow, H. W. Lee, C. Cordon-Cardo, and R. A. DePinho. 1998. The Ink4a tumor suppressor gene product, p19Arf, interacts with MDM2 and neutralizes MDM2's inhibition of p53. Cell 92:713–723.
   PubMed Web of Science ®Google Scholar
• Radfar, A., I. Unnikrishnan, H. W. Lee, R. A. Depinho, and N. Rosenberg. 1998. p19Arf induces p53-dependent apoptosis during Abelson virus-mediated pre-B cell transformation. Proc. Natl. Acad. Sci. USA 95:13194–13199.
   PubMed Web of Science ®Google Scholar
• Reddel, R. R.. 1998. A reassessment of the telomere hypothesis of senescence. Bioessays 20:977–984.
   PubMedGoogle Scholar
• Ries, S., C. Biederer, D. Woods, O. Shifman, S. Shirasawa, T. Sasazuki, M. McMahon, M. Oren, and F. McCormick. 2000. Opposite effects of Ras on p53: transcriptional activation of mdm2 and induction of p19ARF. Cell 103:321–330.
   PubMed Web of Science ®Google Scholar
• Robles, S. J., and G. R. Adami. 1998. Agents that cause DNA double strand breaks lead to p16INK4a enrichment and the premature senescence of normal fibroblasts. Oncogene 16:1113–1123.
   PubMed Web of Science ®Google Scholar
• Sage, J., G. J. Mulligan, L. D. Attardi, A. Miller, S. Q. Chen, B. Williams, E. Theodorou, and T. Jacks. 2000. Targeted disruption of the three Rb-related genes leads to loss of G1 control and immortalization. Genes Dev. 14:3037–3050.
   PubMed Web of Science ®Google Scholar
• Serrano, M., A. W. Lin, M. E. McCurrach, D. Beach, and S. W. Lowe. 1997. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88:593–602.
   PubMed Web of Science ®Google Scholar
• Sharpless, N. E., and R. A. DePinho. 1999. The INK4a/ARF locus and its two gene products. Curr. Opin. Genet. Dev. 9:22–30.
   PubMed Web of Science ®Google Scholar
• Shay, J. W., O. M. Pereira-Smith, and W. E. Wright. 1991. A role for both Rb and p53 in the regulation of human cellular senescence. Exp. Cell Res. 196:33–39.
   PubMed Web of Science ®Google Scholar
• Shelton, D. N., E. Chang, P. S. Whittier, D. Choi, and W. D. Funk. 1999. Microarray analysis of replicative senescence. Curr. Biol. 9:939–945.
   PubMed Web of Science ®Google Scholar
• Sherr, C. J., and R. A. DePinho. 2000. Cellular senescence: mitotic clock or culture clock?. Cell 102:407–410.
   PubMed Web of Science ®Google Scholar
• Stein, G. H., L. F. Drullinger, A. Soulard, and V. Dulic. 1999. Differential role for cyclin-dependent kinase inhibitors p21 and p16 in the mechanisms of senescence and differentiation in human fibroblasts. Mol. Cell. Biol. 19:2109–2117.
   PubMed Web of Science ®Google Scholar
• Stott, F. J., S. Bates, M. C. James, B. B. McConnell, M. Starborg, S. Brookes, I. Palmero, K. Ryan, E. Hara, K. H. Vousden, and G. Peters. 1998. The alternative product from the human CDKN2A locus, p14ARF, participates in a regulatory feedback loop with p53 and MDM2. EMBO J. 17:5001–5014.
   PubMed Web of Science ®Google Scholar
• Tahara, H., E. Sato, A. Noda, and T. Ide. 1995. Increase in the expression level of p21sdi1/cip1/waf1 with increasing division age in both normal and SV40-transformed human fibroblasts. Oncogene 10:835–840.
   PubMed Web of Science ®Google Scholar
• Vaziri, H., M. D. West, R. C. Allsopp, T. S. Davison, Y. Wu, C. H. Arrowsmith, G. G. Poirier, and S. Benchimol. 1997. ATM-dependent telomere loss in aging human diploid fibroblasts and DNA damage lead to the post-translational activation of p53 protein involving poly (ADP-ribose) polymerase. EMBO J. 16:6018–6033.
   PubMed Web of Science ®Google Scholar
• Webley, K., J. A. Bond, C. J. Jones, J. P. Blaydes, A. Craig, T. Hupp, and D. Wynford-Thomas. 2000. Posttranslational modifications of p53 in replicative senescence overlapping but distinct from those induced by DNA damage. Mol. Cell. Biol. 20:2803–2808.
   PubMed Web of Science ®Google Scholar
• Wei, S., W. Wei, and J. M. Sedivy. 1999. Expression of catalytically active telomerase does not prevent premature senescence caused by overexpression of oncogenic Ha-Ras in normal human fibroblasts. Cancer Res. 59:1539–1543.
   PubMed Web of Science ®Google Scholar
• Wei, W., and J. M. Sedivy. 1999. Differentiation between senescence (M1) and crisis (M2) in human fibroblast cultures. Exp. Cell Res. 253:519–522.
   PubMedGoogle Scholar
• Weller, E. M., M. Poot, and H. Hoehn. 1993. Induction of replicative senescence by 5-azacytidine: fundamental cell kinetic differences between human diploid fibroblasts and NIH-3T3 cells. Cell Prolif. 26:45–54.
   PubMedGoogle Scholar
• Wright, W. E., and J. W. Shay. 2000. Telomere dynamics in cancer progression and prevention: fundamental differences in human and mouse telomere biology. Nat. Med. 6:849–851.
   PubMed Web of Science ®Google Scholar
• Zglinicki, T. V., G. Saretzki, W. Docke, and C. Lotze. 1995. Mild hyperoxia shortens telomeres and inhibits proliferation of fibroblasts: a model for senescence?. Exp. Cell Res. 220:186–193.
   PubMedGoogle Scholar
• Zhang, Y., Y. Xiong, and W. G. Yarbrough. 1998. ARF promotes MDM2 degradation and stabilizes p53: ARF-INK4a locus deletion impairs both the Rb and p53 tumor suppression pathways. Cell 92:725–734.
   PubMed Web of Science ®Google Scholar
• Zhu, J., D. Woods, M. MacMahon, and J. M. Bishop. 1998. Senescence of human fibroblasts induced by oncogenic Raf. Genes Dev. 12:2997–3007.
   PubMed Web of Science ®Google Scholar
• Zindy, F., C. M. Eischen, D. H. Randle, T. Kamijo, J. L. Cleveland, C. J. Sherr, and M. F. Roussel. 1998. Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev. 12:2424–2433.
   PubMed Web of Science ®Google Scholar