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Telomeres, aging and cancer: In search of a happy ending

Oncogene volume 21, pages 503–511 (2002)Cite this article

Abstract

Telomeres are distinctive structures, composed of a repetitive DNA sequence and associated proteins, that cap the ends of linear chromosomes. Telomeres are essential for maintaining the integrity and stability of eukaryotic genomes. In addition, under some circumstances, telomeres can influence cellular gene expression. In mammals, the length, structure, and function of telomeres have been proposed to contribute to cellular and organismal phenotypes associated with cancer and aging. Here, we discuss what is known about the basis for the links between telomeres, aging and cancer, and some of the known and proposed consequences of telomere dysfunction and maintenance for mammalian cells and organisms.

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References

  • Allsopp RC, Chang E, Kashefi-Aazam M, Rogaev EI, Piatyszek MA, Shay JW, Harley CB . 1995 Exp. Cell Res. 220: 194–200

  • Artandi SE, Chang S, Lee SL, Alson S, Gottlieb GJ, Chin L, DePinho RA . 2000 Nature 406: 641–645

  • Bailey S, Meyne J, Chen DJ, Kurimasa A, Li GC, Lehnert BE, Goodwin EH . 1999 Proc. Natl. Acad. Sci. USA 96: 14899–14904

  • Bailey SM, Cornforth MN, Kurimasa A, Chen DJ, Goodwin EH . 2001 Science 293: 2462–2465

  • Baumann P, Cech T . 2001 Science 292: 1171–1175

  • Blackburn EH . 2000 Nature 408: 53–56

  • Blasco MA, Lee HW, Hande MP, Samper E, Lansdorp PM, DePinho RA, Greider CW . 1997 Cell 91: 25–34

  • Bodnar AG, Ouellette M, Frolkis M, Holt SE, Chiu CP, Morin GB, Harley CB, Shay JW, Lichtsteiner S, Wright WE . 1998 Science 279: 349–352

  • Broccoli D, Smogorzewska A, Chong L, de Lange T . 1997 Nat. Genet. 17: 231–235

  • Bryan TM, Englezou A, Dalla-Pozza L, Dunham MA, Reddel R . 1997 Nature Med. 3: 1271–1274

  • Buchkovich KJ, Greider CW . 1996 Mol. Cell. Biol. 7: 1443–1454

  • Cahill DP, Kinzler KW, Vogelstein B, Lengauer C . 1999 Trends Cell Biol. 9: M57–M60

  • Campisi J, Dimri GP, Hara E . 1996 Handbook of the Biology of Aging E Schneider, J Rowe (eds) Academic Press: New York pp 121–149

    Google Scholar 

  • Campisi J . 1999 The Molecular Basis of Cell Cycle and Growth Control Stein G, Baserga R, Giordano A, Denhardt D (eds) Wiley-Liss Press: New York pp 348–373

    Google Scholar 

  • Campisi J . 2000 In Vivo 14: 183–188

  • Campisi J . 2001 Exp. Gerontol. 36: 607–618

  • Cha RS, Thilly WG, Zarbl H . 1994 Proc. Natl. Acad. Sci. USA 91: 3749–3753

  • Chang E, Harley CB . 1995 Proc. Natl. Acad. Sci. USA 92: 11190–11194

  • Chen Q, Bartholomew JC, Campisi J, Acosta M, Reagen JD, Ames B . 1998 Biochem. J. 332: 43–50

  • Chi NW, Lodish HF . 2000 J. Biol. Chem. 275: 38437–38444

  • Chin L, Artandi SE, Shen Q, Tam A, Lee SL, Gottlieb GJ, Greider CW, DePinho RA . 1999 Cell 97: 527–538

  • Chiu CP, Harley CB . 1997 Proc. Soc. Exp. Biol. Med. 214: 99–106

  • Chong L, van Steensel B, Broccoli D, Erdjument-Briomage H, Hanish J, Tempst P, de Lange T . 1995 Science 270: 1663–1667

  • Coviello-McLaughlin GM, Prowse KR . 1997 Nucl. Acids Res. 25: 3051–3058

  • d'Adda di Fagagna F, Hande MP, Tong WM, Lansdorp PM, Wang ZQ, Jackson SP . 1999 Nat. Genet. 23: 76–80

  • D'Amours D, Desnoyers S, D'Silva I, Poirier GG . 1999 Biochem. J. 342: 249–268

  • Deng G, Lu Y, Zlotnikov G, Thor AD, Smith HS . 1996 Science 274: 2057–2059

  • DePinho R . 2000 Nature 408: 248–254

  • Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, Medrano EE, Linskens M, Rubelj I, Pereira-Smith OM, Peacocke M, Campisi J . 1995 Proc. Natl. Acad. Sci. USA 92: 9363–9367

  • Dollé ME, Giese H, Hopkins CL, Martus HJ, Hausdorff JM, Vijg J . 1997 Nat. Genet. 17: 431–434

  • Dollé ME, Snyder WK, Gossen JA, Lohman PH, Vijg J . 2000 Proc. Natl. Acad. Sci. USA 97: 8403–8408

  • Dubrana K, Perrod S, Gasser SM . 2001 Curr. Opin. Cell Biol. 13: 281–289

  • Dunham MA, Neumann AA, Fasching CL, Reddel RR . 2000 Nat. Genet. 26: 447–450

  • Effros RB . 1998 Am. J. Hum. Genet. 62: 1003–1007

  • Funk WD, Wang CK, Shelton DN, Harley CB, Pagon GD, Hoeffler WK . 2000 Exp. Cell Res. 258: 270–278

  • Gasser SM . 2000 Science 288: 1377–1379

  • Gonzalez-Suarez E, Samper E, Flores JM, Blasco MA . 2000 Nat. Genet. 26: 114–117

  • Gonzalez-Suarez E, Samper E, Flores JM, Blasco MA . 2001 EMBO J. 20: 2619–2630

  • Gray JW, Collins C . 2000 Carcinog. 21: 443–452

  • Greenberg RA, Chin L, Femino A, Lee KH, Gottlieb GJ, Singer RH, Greider CW, DePinho RA . 1999 Cell 97: 515–525

  • Greider CW . 1996 Annu. Rev. Biochem. 65: 337–365

  • Griffith JD, Comeau L, Rosenfield S, Stansel RM, Bianchi A, Moss H, de Lange T . 1999 Cell 97: 503–514

  • Hahn WC, Stewart SA, Brooks MW, York SG, Eaton E, Kurachi A, Beijersbergen R, Knoll JHM, Meyerson M, Weinberg RA . 1999a Nature Med. 5: 1164–1170

  • Hahn WC, Counter CM, Lundberg AS, Beijersbergen RL, Brooks MW, Weinberg RA . 1999b Nature 400: 464–468

  • Harlebachor C, Boukamp P . 1996 Proc. Natl. Acad. Sci. USA 93: 6476–6481

  • Hemann MT, Greider CW . 2000 Nucl. Acid Res. 28: 4474–4478

  • Herrera E. Samper E, Martin-Caballero J, Flores JM, Lee HW, Blasco MA . 1999 EMBO J. 18: 2950–2960

  • Herrera E, Martinez AC, Blasco MA . 2000 EMBO J. 19: 472–481

  • Holt SE, Wright WE, Shay JW . 1997 Eur. J. Canc. 33: 761–766

  • Hsu HL, Gilley D, Blackburn EH, Chen DJ . 1999 Proc. Natl. Acad. Sci. USA 96: 12454–12458

  • Hsu HL, Gilley D, Galande SA, Hande MP, Allen B, Kim SH, Li GC, Campisi J, Kohwi-Shigematsu T, Chen DJ . 2000 Genes Dev. 14: 2807–2812

  • Jiang XR, Jimenez G, Chang E, Frolkis M, Jusler B, Sage M, Beeche M, Bodnar AG, Wahl GM, Tlsty TD, Chiu CP . 1999 Nat. Genet. 21: 111–114

  • Jonason AS, Kunala S, Price GT, Restifo RJ, Spinelli HM, Persing JA, Leffell DJ, Tarone RE, Brash DE . 1996 Proc. Natl. Acad. Sci. USA 93: 14025–14029

  • Kakuo S, Asaoka K, Ide T . 1999 Biochem. Biophys. Res. Comm. 263: 308–314

  • Kaminker P, Kim SH, Taylor RD, Zebarjadian Y, Funk WD, Morin GB, Yaswen P, Campisi J . 2001 J. Biol. Chem. 276: 35891–35899

  • Karlseder J, Broccoli D, Dai Y, Hardy S, de Lange T . 1999 Science 283: 1321–1325

  • Kim NW, Platyszek M, Prowse KR, Harley CB, West MD, Ho PL, Coviello GM, Wright WE, Weinrich SL, Shay JW . 1994 Science 266: 2011–2015

  • Kim SH, Kaminker P, Campisi J . 1999 Nat. Genet. 23: 405–412

  • Kirkwood TB, Austad SN . 2000 Nature 408: 233–238

  • Klapper W, Parwaresch R, Krupp G . 2001 Mech. Ageing Dev. 122: 695–712

  • Kohn KW . 1999 Mol. Biol. Cell 10: 2703–2734

  • Krtolica A, Parrinello S, Lockette S, Desprez P, Campisi J . 2001 Proc. Natl. Acad. Sci. USA 98: 12071–12077

  • Lee HW, Blasco MA, Gottlieb GJ, Horner JW, Greider CW, DePinho RA . 1998 Nature 392: 569–574

  • Levy MZ, Allsopp RC, Futcher AB, Greider CW, Harley CB . 1992 J. Mol. Biol. 225: 951–960

  • Li B, Oestreich S, de Lange T . 2000 Cell 101: 471–483

  • Lingner J, Cech TR . 1998 Curr. Opin. Genet. Dev. 8: 226–232

  • Lundberg AS, Hahn WC, Gupta P, Weinberg RA . 2000 Curr. Opin. Cell Biol. 12: 705–709

  • Makarov VL, Hirose Y, Langmore JP . 1997 Cell 88: 657–666

  • McEachern MJ, Krauskopf A, Blackburn EH . 2000 Annu. Rev. Genet. 34: 331–358

  • Miller RA . 1991 Cancer 68: 2496–2501

  • Mishima K, Handa JT, Aotaki-Keen A, Lutty GA, Morse LS, Hjelmeland LM . 1999 Invest. Ophthalmol. Vis. Sci. 40: 1590–1593

  • Mitchell JR, Wood E, Collins K . 1999 Nature 402: 551–555

  • Morales CP, Holt SE, Ouellette M, Kaur KJ, Yan Y, Wilson KS, White MA, Wright WE, Shay JW . 1999 Nat. Genet. 21: 115–118

  • Munoz-Jordan JL, Cross GA, de Lange T, Griffith JD . 2001 EMBO J. 20: 579–588

  • Ouellette MM, Liao M, Herbert BS, Johnson M, Holt SE, Liss HS, Shay JW, Wright WE . 2000 J. Biol. Chem. 275: 10072–10076

  • Paradis V, Youssef N, Dargere D, Ba N, Bonvoust F, Bedossa P . 2001 Hum. Pathol. 32: 327–332

  • Park CC, Bissell MJ, Barcellos-Hoff MH . 2000 Molec. Med. Today 6: 324–329

  • Pendergrass WR, Lane MA, Bodkin NL, Hansen BC, Ingram DK, Roth GS, Yi L, Bin H, Wolf NS . 1999 J. Cell. Physiol. 180: 123–130

  • Prowse KR, Greider CW . 1995 Proc. Natl. Acad. Sci. USA 92: 4818–4822

  • Rinehart CA, Torti VR . 1997 Molec. Carcinog. 18: 187–192

  • Rudolph KL, Chang S, Lee HW, Blasco M, Gottlieb GJ, Greider C, DePinho RA . 1999 Cell 96: 701–712

  • Samper E, Goytisolo FA, Slijepcevic P, van Buul PP, Blasco MA . 2000 EMBO Rep. 1: 244–252

  • Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW . 1997 Cell 88: 593–602

  • Shay JW, Pereira-Smith OM, Wright WE . 1991 Exp. Cell Res. 196: 33–39

  • Shay JW, Wright WE . 2001 Novartis Found. Symp. 235: 116–125

  • Sherr CJ, DePinho RA . 2000 Cell 102: 407–410

  • Shore D . 1997 Trends Biochem. Sci. 22: 233–235

  • Smith S, Giriat I, Schmitt A, de Lange T . 1998 Science 282: 1484–1487

  • Smith S, de Lange T . 1999 J. Cell Sci. 112: 3649–3656

  • Smith GC, Jackson SP . 1999 Genes Dev. 13: 916–934

  • Song K, Jung D, Jung Y, Lee SG, Lee I . 2000 FEBS Lett. 48: 81–85

  • Vaziri H, Benchimol S . 1998 Curr. Biol. 8: 279–282

  • Vaziri H, Squire JA, Pandita TK, Bradley G, Kuba RM, Zhang H, Gulyas S, Hill RP, Nolan GP, Benchimol S . 1999 Mol. Cell. Biol. 19: 2373–2379

  • van Steensel B, Smogorzewska A, de Lange T . 1998 Cell 92: 410–413

  • Wei S, Wei S, Sedivy JM . 1999 Cancer Res. 59: 1539–1543

  • Wellinger RJ, Sen D . 1997 Eur. J. Cancer 33: 735–749

  • Weng NP, Levine BL, June C, Hodes RJ . 1996 J. Exp. Med. 183: 2471–2479

  • Wright WE, Shay JW . 1996 Modern Cell Biology Series–Cellular Aging and Cell Death. Holbrook NJ, Martin GR, Lockshin RA, (eds) Wiley & Sons, NY pp 153–167

    Google Scholar 

  • Wright WE, Shay JW . 2000 Nature Med. 6: 849–851

  • Wu G, Lee WH, Chen PL . 2000 J. Biol. Chem. 275: 30618–30622

  • Yang J, Chang E, Cherry AM, Bangs CD, Oei Y, Bodnar A, Bronstein A, Chiu CP, Herron GS . 1999 J. Biol. Chem. 274: 26141–26148

  • Yang L, Suwa T, Wright WE, Shay JW, Hornsby PJ . 2001 Mech. Ageing Dev. 122: 1685–1694

  • Zhang X, Mar V, Zhou W, Harrrington L, Robinson MO . 1999 Genes Dev. 13: 2388–2399

  • Zhu L, Hathcock KS, Hande P, Lansdorp PM, Seldin MF, Hodes RJ . 1998 Proc. Natl. Acad. Sci. USA 95: 8648–8653

  • Zhu XD, Kuster B, Mann M, Petrini JH, de Lange T . 2000 Nat. Genet. 25: 347–352

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Acknowledgements

We thank present and past members of our laboratory for their hard work and stimulating discussions, our many colleagues and collaborators for generously sharing their reagents and ideas, and the National Institute on Aging, Ellison Medical Foundation, California Breast Cancer Research Program, and Department of Energy for research support.

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  1. Life Sciences Division, Lawrence Berkeley National Laboratory, 1 Cyclotron Road, Berkeley, 94720, California, CA, USA

    Sahn-ho Kim, Patrick Kaminker & Judith Campisi

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Correspondence to Judith Campisi.

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Kim, Sh., Kaminker, P. & Campisi, J. Telomeres, aging and cancer: In search of a happy ending. Oncogene 21, 503–511 (2002). https://doi.org/10.1038/sj.onc.1205077

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