Skip to main content
SpringerLink
Log in

Telomeres and Telomerase

  • Chapter
  • First Online:
The Comparative Biology of Aging

Abstract

Telomere-based replicative senescence is thought to function as a potent mechanism of tumor protection in humans. Whether this mechanism is conserved in other species is still unclear. In this review we present an inter-species critical overview of some of the available literature on the fundamental biology of telomeres and telomerase during development, regeneration, cancer and aging of living organisms during their evolutionary journey through time.

N.M.V. Gomes has been co-supported by the European Union Programs POCI 2010 & FSE and by national funds from the Portuguese Ministry for Science, Technology and Superior Education (SFRH/BD/8826/2002). Also supported by the Keck Foundation.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. McClintock B (1941). The stability of broken ends of chromo somes in Zea mays. Genetics 26: 234–282.

    PubMed  Google Scholar 

  2. Muller HJ (1938). The remaking of chromosomes. The Collecting Net 13: 181–198.

    Google Scholar 

  3. DeLange T (2005). Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev 19: 2100–2110.

    Google Scholar 

  4. Blackburn EH and Gall JG (1978). A tandemly repeated sequence at the termini of the extrachromosomal ribosomal RNA genes in Tetrahymena. J Mol Biol 120: 33–53.

    PubMed  Google Scholar 

  5. Moyzis RK, Buckingham JM, Cram LS, Dani M, Deaven LL, Jones MD, Meyne J, Ratliff RL, and Wu JR (1988). A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proc Natl Acad Sci U S A 85: 6622–6626.

    PubMed  Google Scholar 

  6. Watson JD (1972). Origin of concatameric T4 DNA. Nature 239: 197–201.

    Google Scholar 

  7. Olovnikov AM (1973). 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: 181–190.

    PubMed  Google Scholar 

  8. Shay JW and Wright WE (2000). Hayflick, his limit, and cellular ageing. Nature Rev Mol Cell Biol 1: 72–76.

    Google Scholar 

  9. Shay JW and Wright WE (2004). Senescence and immortalization: role of telomeres and telomerase. Carcinogenesis 26: 867–874.

    PubMed  Google Scholar 

  10. Hayflick L and Moorhead PS (1961). The serial cultivation of human diploid cell strains. Exp Cell Res 25: 585–621.

    Google Scholar 

  11. Shay JW and Wright WE (2001). Forward: aging and cancer: are telomeres and telomerase the connection? In Telomerase, Aging and Disease. (MP Mattson, ed.). Baltimore, MD: Elsevier, p. 231.

    Google Scholar 

  12. Krtolica A, Parrinello S, Lockett S, Desprez P-Y, and Campisi J (2001). Senescent fibroblasts promote epitelial cell growth and tumorigenesis: a link between cancer and aging. Proc Natl Acad Sci U S A 98: 12072–12077.

    PubMed  Google Scholar 

  13. Greider CW and Blackburn EH (1985). Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43: 405–413.

    PubMed  Google Scholar 

  14. Morin GB (1989). The human telomere terminal transferase enzyme is a ribonucleoprotein that synthesizes TTAGGG repeats. Cell 59: 521–529.

    PubMed  Google Scholar 

  15. Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PL, Coviello GM, Wright WE, Weinrich SL, and Shay JW (1994). Specific association of human telomerase activity with immortal cells and cancer. Science 266: 2011–2015.

    PubMed  Google Scholar 

  16. Forsyth NR, Wright WE, and Shay JW (2002). Telomerase and differentiation in multicellular organisms: turn it off, turn it on, and turn it off again. Differentiation 69: 188–197.

    PubMed  Google Scholar 

  17. Bodnar AG, Ouellete M, Frolkis M, Kolt SE, Chiu C-P, Morin GB, Harley CB, Shay JW, Lichtsteiner S, and Wright WE (1998). Extension of lifespan by introduction of telomerase into normal human cells. Science 279: 349–352.

    PubMed  Google Scholar 

  18. Griffith JD, Comeau L, Rosenfield S, Stansel RM, Bianchi A, Moss H, and de Lange T (1999). Mammalian telomeres end in a large duplex loop. Cell 97: 503–514.

    PubMed  Google Scholar 

  19. Wright WE and Shay JW (2000). Telomere dynamics in cancer progression and prevention: fundamental differences in human and mouse telomere biology. Nat Med 6: 849–851.

    PubMed  Google Scholar 

  20. Shay JW and Roninson IB (2004). Hallmarks of senescence in carcinogenesis and cancer therapy. Oncogene 23: 2919–2933.

    PubMed  Google Scholar 

  21. Bryan TM, Englezou A, Dalla-Pozza L, Dunham MA, and Reddel RR (1997). Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nat Med 3: 1271–1274.

    PubMed  Google Scholar 

  22. Teixeira MT, Arneric M, Sperisen P, and Lingner J (2004). Telomere length homeostasis is achieved via a switch between telomerase- extendible and -nonextendible states. Cell 117: 323–335.

    PubMed  Google Scholar 

  23. Baur JA, Zou Y, Shay JW, and Wright WE (2001). Telomere position effect in human cells. Science 292: 2075–2077.

    PubMed  Google Scholar 

  24. Crabbe L, Jauch A, Naeger CM, Holt-Grez H, and Karlseder J (2007). Telomere dysfunction as a cause of genomic instability in Werner syndrome. Proc Natl Acad Sci U S A 104: 2205–2210.

    PubMed  Google Scholar 

  25. Armanios MY, Chen JJ, Cogan JD, Alder JK, Ingersoll RG, Markin C, Lawson WE, Xie M, Vulto I, Phillips JA, 3rd, Lansdorp PM, Greider CW, and Loyd JE (2007). Telomerase mutations in families with idiopathic pulmonary fibrosis. N Eng J Med 356: 1370–1372.

    Google Scholar 

  26. Blasco MA (2007). Telomere length, stem cells and aging. Nat Chem Biol 3: 640–649.

    PubMed  Google Scholar 

  27. DeLange T (2004). T-loops and the origin of telomeres. Nat Rev Mol Cell Biol 5: 323–329.

    Google Scholar 

  28. Lundblad V and Blackburn EH (1993). An alternative pathway for yeast telomere maintenance rescues est1 – senescence. Cell 73: 347–360.

    PubMed  Google Scholar 

  29. Pluta AF, Kaine BP, and Spear BB (1982). The terminal organization of macromolecular DNA in Oxytricha fallax. Nucleic Acids Res 10: 8145–8154.

    PubMed  Google Scholar 

  30. Walter MF, Bozorgnia L, Mahesshwari A, and Biessmann H (2001). The rate of terminal nucleotide loss from a telomere of the mosquito Anopheles gambiae. Insect Mol Biol 10: 105–110.

    PubMed  Google Scholar 

  31. Coleman MJ, McHale MT, Arnau J, Watson A, and Oliver RP (1993). Cloning and characterization of telomeric DNA from Cladosporium fulvum. Gene 132: 67–73.

    PubMed  Google Scholar 

  32. Shampay J, Szostak JW, and Backburn EH (1984). DNA sequences of telomeres maintained in yeast. Nature 310: 154–157.

    PubMed  Google Scholar 

  33. McEachern MJ and Hicks JB (1993). Unusually large telomeric repeats in the yeast Candida albicans. Mol Cell Biol 13: 551–560.

    PubMed  Google Scholar 

  34. Wood JG and Sinclair DA (2002). TPE or not TPE? It’s no longer a question. Trends Pharmacol Sci 23: 1–4.

    PubMed  Google Scholar 

  35. Forstemann K, Zaug AJ, Cech TR, and Lingner J (2003). Yeast telomerase is specialized for C/A-rich RNA templates. Nucleic Acids Res 31: 1646–1655.

    PubMed  Google Scholar 

  36. Tomaska L, McEachern MJ, and Nosek J (2004). Alternatives to telomerase: keeping linear chromosomes via telomeric circles. FEBS Lett 567: 142–146.

    PubMed  Google Scholar 

  37. Nosek J, Rycovska A, Makhov AM, Griffith JD, and Tomaska L (2005). Amplification of telomeric arrays via rolling-circle mechanism. J Biol Chem 280: 10840–10845.

    PubMed  Google Scholar 

  38. Fajkus J, Sykorova E, and Leitch AR (2005). Telomeres in evolution and evolution of telomeres. Chromosome Res 13: 469–479.

    PubMed  Google Scholar 

  39. Galy V, Olivo-Marin J-C, Scherthan H, Doye V, Rascalou N, and Nehrbass U (2000). Nuclear pore complexes in the organization of silent telomeric chromatin. Nature 403: 108–112.

    PubMed  Google Scholar 

  40. Figueiredo L and Scherf A (2005). Plasmodium telomeres and telomerase: the usual actor in an unusual scenario. Chromosome Res 13: 517–524.

    PubMed  Google Scholar 

  41. Horn D and Barry D (2005). The central roles of telomeres and subtelomeres in antigenic variation in African trypanosomes. Chromosome Res 13: 525–533.

    PubMed  Google Scholar 

  42. Munoz-Jordan JL, Cross GA, de Lange T, and Griffith JD (2001). T-loops at trypanosome telomeres. EMBO J 20: 579–588.

    PubMed  Google Scholar 

  43. Murphy WJ, Eizirik E, O’Brien SJ, Madsen O, Scally M, Douady CJ, Teeling E, Ryder OA, Stanhope MJ, de Jong WW, and Springer MS (2001). Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294: 2348–2351.

    PubMed  Google Scholar 

  44. Cox AV, Bennett ST, Parokonny AS, Kenton A, Callimassia MA, and Bennett MD (1993). Comparison of plant telomere locations using a PCR-generated synthetic probe. Ann Bot 72: 239–247.

    Google Scholar 

  45. Fuchs J, Brandes A, and Schubert I (1995). Telomere sequence localization and karyotype evolution in higher plants. Plant Syst Evol 196: 227–241.

    Google Scholar 

  46. Flanary BE and Kletetschka G (2005). Analysis of telomere length and telomerase activity in tree species of various life-spans, and with age in the bristlecone pine Pinus longaeva. Biogerontology 6: 101–111.

    PubMed  Google Scholar 

  47. Flanary BE and Kletetschka G (2006). Analysis of telomere length and telomerase activity in tree species of various lifespans, and with age in the bristlecone pine Pinus longaeva. Rejuvenation Res 9: 61–63.

    PubMed  Google Scholar 

  48. Schulman E (1958). Bristlecone pine, oldest known living thing. Natl Geogr 113: 354–372.

    Google Scholar 

  49. McKnight TD, Riha K, and Shippen DE (2002). Telomeres, telomerase, and stability of the plant genome. Plant Mol Biol 48: 331–337.

    PubMed  Google Scholar 

  50. Muller F, Wicky C, Spicher A, and Tobler H (1991). New telomere formation after developmentally regulated chromosomal breakage during the process of chromatin diminution in Ascaris lumbricoides. Cell 67: 815–822.

    PubMed  Google Scholar 

  51. Richards EJ and Ausubel FM (1888). Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell 53: 127–136.

    Google Scholar 

  52. Fajkus J, Kovarik A, Kralovics R, and Bezdek M (1995). Organization of telomeric and subtelomeric chromatin in the higher plant Nicotiana tabacum. Mol Gen Genet 247: 633–638.

    PubMed  Google Scholar 

  53. Riha K, McKnight TD, Griffing LR, and Shippen DE (2001). Living with genome instability: plant responses to telomerase dysfunction. Science 291: 1797–1800.

    PubMed  Google Scholar 

  54. Fitzgerald PH and Morris CM (1984). Telomeric association of chromosomes in B-cell lymphoid leukemia. Hum Genet 67: 385–390.

    PubMed  Google Scholar 

  55. Walbot V (1996). Sources and consequences of phenotypic and genotypic plasticity in flowering plants. Trends Plant Sci 1: 27–32.

    Google Scholar 

  56. Fouche N, Cesare AJ, Willcox S, Ozgur S, Compton SA, and Griffith JD (2006). The basic domain of TRF2 directs binding to DNA junctions irrespective of the presence of TTAGGG repeats. J Biol Chem 281: 37486–37495.

    PubMed  Google Scholar 

  57. Ogilvie M, Yu X, Nicolas-Metral V, Pulido SM, Liu C, Ruegg UT, and Noguchi CT (2000). Erythropoietin stimulates proliferation and interferes with differentiation of myoblasts. J Biol Chem 275: 39754–39761.

    PubMed  Google Scholar 

  58. Traut W, Szczepanowski M, Vitkova M, Opitz C, Marec F, and Zrzavy J (2007). The telomere repeat motif of basal Metazoa. Chromosome Res 15: 371–382.

    PubMed  Google Scholar 

  59. Podlevsky JD, Bley CJ, Omana RV, Qi X, and Chen J, (2007). The telomerase database, Nucleic Acids Res. D339–D343 http://telomerase.asu.edu

  60. Finch CE (1990). Longevity, Senescence, and the Genome. Chicago, IL: University of Chicago Press, p. 922.

    Google Scholar 

  61. Koziol C, Borojevic R, Steffen R, and Muller WEG (1998). Sponges (Porifera) model systems to study the shift from immortal to senescent somatic cells: the telomerase activity in somatic cells. Mech Ageing Dev 100: 107–120.

    PubMed  Google Scholar 

  62. Muller WEG and Muller IM (2003). The hypothetical ancestral animal. The Urmetazoa: telomerase activity in sponges (Porifera). J Serb Chem Soc 68: 257–268.

    Google Scholar 

  63. Rinkevich B and Loya Y (1986). Senescence and dying signals in a reef-building coral. Experientia 42: 320–322.

    Google Scholar 

  64. Laird DJ and Weissman L (2004). Telomerase maintained in self-renewing tissues during serial regeneration of the urochordate Bothryllus schosserii. Dev Biol 273: 185–194.

    PubMed  Google Scholar 

  65. Castro LFC and Holand P (2002). Fluorescent in situ hybridisation to amphioxus chromosomes. Zool Sci 19: 1349–1353.

    PubMed  Google Scholar 

  66. Plohl M, Prats E, Martinez-Lage A, Gonzalez-Tizon A, Mendez J, and Cornudella L (2002). Telomeric localization of the vertebrate type hexamer repeat (TTAGGG)n in the wedgeshell clam Donax trunculus and other marine invertebrate genomes. J Biol Chem 277: 19839–19846.

    PubMed  Google Scholar 

  67. Joffe BI, Solovei I, and Macgregor HC (1998). Ends of chromosomes in Polycelis tenuis (Platyhelminthes) have telomeric epeat TTAGGG. Chromosome Res 4: 323–324.

    Google Scholar 

  68. Jha AN, Dominguez I, Balajee AS, Hutchinson TH, Dixon DR, and Natarajan AT (1995). Localization of a vertebrate telomeric sequence in the chromosomes of two marine worms (phylum Annelida: class polychaeta). Chromosome Res 3: 507–508.

    PubMed  Google Scholar 

  69. Vitturi R, Colomba MS, Gianguzza P, and Pirrone AM (2000). Chromosomal location of ribosomal DNA (rDNA), (GATA)n and (TTAGGG)n telomeric repeats in the neogastropod Fasciolaria lignaria (Mollusca: Prosobranchia). Genetica 108: 253–257.

    PubMed  Google Scholar 

  70. Wang YP and Guo XM (2001). Chromosomal mapping of the vertebrate telomeric sequence (TTAGGG)n in four bivalve molluscs by fluorescence in situ hybridization. J Shellfish Res 20: 1187–1190.

    Google Scholar 

  71. Vitkova M, Kral J, Traut W, Zrzavy J, and Marec F (2005). The evolutionary origin of insect telomeric repeats, (TTAGG)n. Chromosome Res 13: 145–156.

    PubMed  Google Scholar 

  72. Lejnine S, Makarov VL, and Langmore JP (1995). Conserved nucleoprotein structurear the ends of vertebrate and invertebrate chromosomes. Proc Natl Acad Sci U S A 94: 2393–2397.

    Google Scholar 

  73. Lanza RP, Cibelli JB, Blackwell C, Cristofalo VJ, Francis MK, Baerlocher GM, Mak J, Schertzer M, Chavez EA, Sawyer N, Lansdorp PM, and West MD (2000). Extension of cell life-span and telomere length in animals cloned from senescent somatic cells. Science 288: 665–669.

    PubMed  Google Scholar 

  74. Izbicka E, Nishioka D, Marcell V, Raymond E, Davidson KK, Lawrence RA, Lawrence RA, Wheelhouse RT, Hurley L, Wu RS, and Von Hoff D (1999). Telomere-interactive agents affect proliferation rates and induce chromosomal destabilization in sea urchin embryos. Anticancer Drug Des 4: 355–365.

    Google Scholar 

  75. http://www.pathology-registry.org

  76. Guo X and Allen SJ (1997). Fluorescence in situ hybridization of vertebrate telomere sequence to chromosome ends of the pacific oyster, Crassostrea gigas thunberg. J Shellfish Res 16: 87–89.

    Google Scholar 

  77. Estabrooks SL (1999). The telomeres of the bay scallop, Argopecten irradians (Lamark). J Shellfish Res 18: 401–404.

    Google Scholar 

  78. Niedermaier J and Moritz KB (2000). Organization and dynamics of satellite and telomere DNAs in Ascaris: implications for formation and programmed breakdown of compound chromosomes. Chromosoma 109: 439–452.

    PubMed  Google Scholar 

  79. Wicky C, Villeneuve AM, Lauper N, Codoureyy L, Tobler H, and Muller F (1996). Telomeric repeats (TTAGGC)n are sufficient for chromosome capping function in Caenorhabditis elegans. Proc Natl Acad Sci U S A 93: 8983–8988.

    PubMed  Google Scholar 

  80. Hirai H and LoVerde PT (1996). Identification of the telomeres on Schistosoma mansoni chromosomes by FISH. J Parasitol 82: 511–512.

    PubMed  Google Scholar 

  81. Klapper W, Heidorn K, Kuhne K, Parwaresch R, and Krupp G (1998). Telomerase activity in ‘immortal’ fish. FEBS Lett 434: 409–412.

    PubMed  Google Scholar 

  82. Okazaki S, Tsuchida K, Mackawa H, and Fugiwara H (1993). Identification of a pentanucleotide telomere sequence (TTAGG)n in the silkworm Bombyx mori and in other insects. Mol Cell Biol 13: 1424–1432.

    PubMed  Google Scholar 

  83. Meyne JH and Imai HT (1995). FISH analysis of the telomere sequences of bulldog ants (Myrmecia: Formicidae). Chromosoma 104: 14–18.

    PubMed  Google Scholar 

  84. Seluanov A, Chen Z, Hine C, Sasahara TH, Ribeiro AA, Catania KC, Presgraves DC, and Gorbunova V (2007). Telomerase activity coevolves with body mass not lifespan. Aging Cell 6: 45–52.

    PubMed  Google Scholar 

  85. Frydrychova R, Grossmann P, Trubac P, Vitkova M, and Marec F (2004). Phylogenetic distribution of TTAGG telomeric repeats in insects. Genome 47: 163–178.

    PubMed  Google Scholar 

  86. Sasaki T and Fujiwara H (2000). Detection and distribution patterns of telomerase activity in insects. Eur J Biochem 267: 3025–3031.

    PubMed  Google Scholar 

  87. Osanai M, Kojima KK, Futahashi R, Yaguchi S, and Fujiwara H (2006). Identification and characterization of the telomerase reverse transcriptase of Bombyx mori (silkworm) and Tribolium castaneum (flour beetle). Gene 376: 281–289.

    PubMed  Google Scholar 

  88. Frydrychova R and Marec F (2002). Repeated losses of TTAGG telomere repeats in evolution of beetles (Coleoptera). Genetica 115: 179–187.

    PubMed  Google Scholar 

  89. Nagaraju K, Casciola-Rosen L, Rosen A, Thompson C, Loeffler L, Parker T, Danning C, Rochon PJ, Gillespie J, and Plotz P (2000). The inhibition of apoptosis in myositis and in normal muscle cells. J Immunol 164: 5459–5465.

    PubMed  Google Scholar 

  90. Biessmann H and Mason JM (1997). Telomere maintenance without telomerase. Chromosoma 106: 63–69.

    PubMed  Google Scholar 

  91. Mason JM and Biessmann H (1995). The unusual telomeres of Drosophila. Trends Genet 11: 58–62.

    PubMed  Google Scholar 

  92. Mikhailovsky S, Belenkaya T, and Georgiev P (1999). Broken chromosomal ends can be elongated by conversion in Drosophila melanogaster. Chromosoma 108: 114–120.

    PubMed  Google Scholar 

  93. Kahn T, Savitsky M, and Georgiev P (2000). Attachment of HeTA sequences to chromosomal termini in Drosophila may occur by different mechanisms. Mol Cell Biol 20: 7634–7642.

    PubMed  Google Scholar 

  94. Meyne J, Ratliff RL, and Moyzis RK (1989). Conservation of the Human Telomere Sequence (TTAGGG)n among Vertebrates. Proc Natl Acad Sci U S A 86: 7049–7053.

    PubMed  Google Scholar 

  95. Chen J-L, Blasco MA, and Greider CW (2000). Secondary structure of vertebrate telomerase RNA. Cell 100: 503–514.

    PubMed  Google Scholar 

  96. Patbaik B, Mahapatro N, and Jena B (1994). Ageing in fishes. Gerontology 40: 113–132.

    Google Scholar 

  97. Mommsen TP (2001). Paradigms of growth in fish. Comp Biochem Physiol B Biochem Mol Biol 129: 207–219.

    PubMed  Google Scholar 

  98. Lau BW-M, Wong AO-L, Tsao GS-W, So K-F, and Yip HK-F (2008). Molecular cloning and characterization of the zebrafish (Danio rerio) telomerase catalytic subunit (telomerase reverse transcriptase, TERT). J Mol Neurosci 34: 63–75.

    PubMed  Google Scholar 

  99. Tsepkin YA and Sokolov LI (1971). The maximum size and age of some sturgeons. J Ichthyol 11: 444–446.

    Google Scholar 

  100. Rocco L, Costagliola D, and Stingo V (2001). (TTAGG)n telomeric sequence in selachian chromosomes. Heredity 87: 583–588.

    PubMed  Google Scholar 

  101. McChesney PA, Aisner DL, Frank BC, Wright WE, and Shay JW (2000). Telomere dynamics in cells with introduced telomerase: a rapid assay for telomerase activity on telomeres. Mol Cell Biol Res Commun 3: 312–318.

    PubMed  Google Scholar 

  102. Rocco L, Morescalchi MA, Costagliola D, and Stingo V (2002). Karyotype and genome characterization in four cartilaginous fishes. Gene 295: 289–298.

    PubMed  Google Scholar 

  103. Kishi S, Uchiyama J, Baughman AM, Tadateru G, Lin MC, and Stephanie BT (2003). The zebrafish as a vertebrate model of funcional aging and very gradual senescence. Exp Gerontol 38: 777–786.

    PubMed  Google Scholar 

  104. Pierce AJ, Johnson RD, Thompson LH, and Jasin M (1999). XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev 13: 2633–2638.

    PubMed  Google Scholar 

  105. Bradford GB, Williams B, Rossi R, and Bertoncello I (1997). Quiescence, cycling, and turnover in the primitive hematopoietic stem cell compartment. Exp Hematol 25: 445–453.

    PubMed  Google Scholar 

  106. Xie M, Mosig A, Qi X, Li Y, Stadler PF, and Chen J (2008). Structure and function of the smallest vertebrate telomerase RNA from teleost fish. J Biol Chem 283: 2049–2059.

    PubMed  Google Scholar 

  107. Jeyapalan JN, Varley H, Foxon JL, Pollock RE, Jeffreys AJ, Henson JD, Reddel RR, and Royle NJ (2005). Activation of the ALT pathway for telomere maintenance can affect other sequences in the human genome. Hum Mol Genet 14: 1785–1794.

    PubMed  Google Scholar 

  108. Bassham S, Beam A, and Shampay J (1998). Telomere variation in Xenopus laevis. Mol Cell Biol 18: 269–275.

    PubMed  Google Scholar 

  109. Kuramoto M, Ohsumi K, Kishimoto T, and Ishikawa F (2001). Identification and analyses of the Xenopus TERT gene that encodes the catalytic subunit of telomerase. Gene 277: 101–110.

    PubMed  Google Scholar 

  110. Mantell LL and Greider CW (1994). Telomerase activity in germline and embryonic cells of Xenopus. EMBO J 13: 3211–3217.

    PubMed  Google Scholar 

  111. Bousman S, Schneider G, and Shampay J (2003). Telomerase activity is widespread in adult somatic tissues of xenopus. J Exp Zool (Mol Dev Evol) 295B: 82–86.

    Google Scholar 

  112. Christiansen JL, Henderson ER, Budke B, Lynch M, Lu Q, and Johnson J (2001). A final report of studies of the Hayflick limit in reptiles, a test of potential immortality. In Proceedings of the Iowa Space Grant Consortium.

    Google Scholar 

  113. Christiansen J, Johnson J, Henderson ER, Budke B, and Lynch M (2001). The relationship between telomeres, telomerase, reptilian lifespan, and reptilian tissue regeneration. In Proceedings of the Iowa Space Grant Consortium.

    Google Scholar 

  114. Simpson SB and Rauch DM (1989). Cells from the lizard anolis do not exhibit senescence. Gerontologist, Special Issue, 29: 284A (Abstract).

    Google Scholar 

  115. Girondot M and Garcia J, Senescence and longevity in turtles: what telomeres tell us, in Proceedings of the 9th Ordinary General Meeting of the Societas Europaea Herpetologica In Current Studies in Herpetology:, C.M.a. R. Guyetant, Editor. 1999: Le Bourget du Lac, France, p. 133–137.

    Google Scholar 

  116. Carr A and Goodman D (1970). Ecologic implications of size and growth in Chelonia. Copeia 4: 783–786.

    Google Scholar 

  117. Goldstein S (1974). Growth of cultured cells from the galapagos tortoise. Exp Cell Res 83: 279–302.

    Google Scholar 

  118. Ogburn CE, Carlberg K, Ottinger MA, Holmes DJ, Martin GM, and Austad SN (2001). Exceptional cellular resistance to oxidative damage in long-lived birds requires active gene expression. J Gerontol A Biol Sci Med Sci 56: B468–B474.

    CAS  PubMed  Google Scholar 

  119. Scharff C, Kirn JR, Grossman M, Macklis J, and Nottebohm F (2000). Targeted neuronal death affects neuronal replacement and vocal behavior in adult songbirds. Neuron 25: 481–492.

    PubMed  Google Scholar 

  120. Delany ME and Daniels LM (2004). The chicken telomerase reverse transcriptase (chTERT): molecular and cytogenetic characterization with a comparative analysis. Gene 339: 61–69.

    PubMed  Google Scholar 

  121. Delany ME, Krupkin AB, and Miller MM (2000). Organization of telomere sequences in birds: evidence for arrays of extreme length and for in vivo shortening. Cytogenet Cell Genet 90: 139–145.

    PubMed  Google Scholar 

  122. Delany ME, Daniels LM, Swanberg SE, and Taylor HA (2003). Telomeres in the chicken: genome stability and chromosome ends. Poult Sci 82: 917–926.

    PubMed  Google Scholar 

  123. Nanda I, Schrama D, Feichtinger W, Haaf T, Schartl M, and Schmid M (2002). Distribution of telomeric (TTAGGG)n sequences in avian chromosomes. Chromosoma 111: 215–227.

    PubMed  Google Scholar 

  124. Taylor G, Lehrer MS, Jensen PJ, Sun TT, and Lavker RM (2000). Involvement of follicular stem cells in forming not only the follicle but also the epidermis. Cell 102: 451–461.

    PubMed  Google Scholar 

  125. Hiyama E, Kiyama K, Tatsumoto N, Kodama T, Shay J, and Yokoyama T (1996). Telomerase activity in human intestine. Int J Oncol 9: 453–458.

    Google Scholar 

  126. Venkatesan RN and Price C (1998). Telomerase expression in chickens: constitutive activity in somatic tissues and down-regulation in culture. Proc Natl Acad Sci U S A 95: 14763–14768.

    PubMed  Google Scholar 

  127. Haussmann MF, Winkler DW, O’Reilly KM, Huntington CE, Nisbet ICT, and Vleck CM (2003). Telomeres shorten more slowly in long-lived birds and mammals than in short-lived ones. Proc R Soc Lond B 270: 1387–1392.

    Google Scholar 

  128. Siegfried M (1983). Neoplasms identified in free-living birds. Avian Dis 27: 86–99.

    PubMed  Google Scholar 

  129. Haussmann MF, Winkler DW, Huntington CE, Nisbet ICT, and Vleck CM (2007). Telomerase activity is maintained throughout the lifespan of long-lived birds. Exp Gerontol 42: 610–618.

    PubMed  Google Scholar 

  130. Galkina S, Lukina N, Zakharova K, and Rodionov AV (2005). Interstitial (TTAGGG)n sequences are not hot spots of recombination in the chicken lampbrush macrochromosomes 1-3. Chromosome Res 13: 551–557.

    PubMed  Google Scholar 

  131. Sherr CJ and DePinho RA (2000). Cellular senescence: mitotic clock or culture shock? Cell 102: 407–410.

    PubMed  Google Scholar 

  132. Prowse KR and Greider CW (1995). Developmental and tissue-specific regulation of mouse telomerase and telomere length. Proc Natl Acad Sci U S A 92: 4818–4822.

    PubMed  Google Scholar 

  133. von Zglinicki T, Serra V, Lorenz M, Saretzki G, Lenzen-Grossimlighaus R, Gessner R, Risch A, and Steinhagen-Thiessen E (2000). Short telomeres in patients with vascular dementia: an indicator of low antioxidative capacity and a possible risk factor? Lab Invest 80: 1739–1747.

    Google Scholar 

  134. Oh H, Taffet GE, Youker KA, Entman ML, Overbeek PA, Michael LH, and Schneider MD (2001). Telomerase reverse transcriptase promotes cardiac muscle cell proliferation, hypertrophy and survival. Proc Natl Acad Sci U S A 98: 10308–10313.

    PubMed  Google Scholar 

  135. Coviello-McLaughlin GM and Prowse KR (1997). Telomere length regulation during postnatal development and ageing in Mus spretus. Nucleic Acids Res 25: 3051–3058.

    PubMed  Google Scholar 

  136. Martin-Rivera L, Herrera E, Albar JP, and Blasco MA (1998). Expression of mouse telomerase catalytic subunit in embryos and adult tissues. Proc Natl Acad Sci U S A 95: 10471–10476.

    PubMed  Google Scholar 

  137. Carman TA, Afshari CA, and Barrett JC (1998). Cellular senescence in telomerase-expressing syrian hamsterembryo cells. Exp Cell Res 24: 33–42.

    Google Scholar 

  138. Rohme D (1981). Evidence for a relationship between longevity of mammalian species and lifespans of normal fibroblasts in vitro and erytrocytes in vivo. Proc Natl Acad Sci U S A 78: 5009–5013.

    PubMed  Google Scholar 

  139. Lorenzini A, Tresini M, Austad SN, and Cristofalo VJ (2005). Cellular replicative capacity correlates primarily with species body mass not longevity. Mech Ageing Dev 126: 1130–1133.

    PubMed  Google Scholar 

  140. Blasco MA, Lee HW, Hande MP, Samper E, Lansdorp PM, DePinho RA, and Greider CW (1997). Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91: 25–34.

    PubMed  Google Scholar 

  141. Ramirez RD, Morales CP, Herbert BS, Rohde JM, Passons C, Shay JW, and Wright WE (2001). Putative telomere-independent mechanisms of replicative aging reflect inadequate growth conditions. Genes Dev 15: 398–403.

    PubMed  Google Scholar 

  142. Mathon NF, Malcolm DS, Harrisingh MC, Cheng L, and Lloyd AC (2001). Lack of replicative senescence in normal rodent glia. Science 291: 872–875.

    PubMed  Google Scholar 

  143. Loo DT, Fuquay JI, Rawson CL, and Barnes DW (1987). Extended culture of mouse embryo cells without senescence: inhibition by serum. Science 236: 200–202.

    PubMed  Google Scholar 

  144. Nussenzweig A, Chen C, da Costa Soares V, Sanchez M, Sokol K, Nussenzweig MC, and Li GC (1996). Requirement for Ku80 in growth and immunoglobulin V(D)J recombination. Nature 382: 551–555.

    PubMed  Google Scholar 

  145. Barlow C, Hirotsune S, Paylor R, Liyanage M, Eckhaus M, Collins F, Shiloh Y, Crawley JN, Ried T, Tagle D, and Wynshaw-Boris A (1996). Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 86: 159–171.

    PubMed  Google Scholar 

  146. Connor F, Bertwistle D, Mee PJ, Ross GM, Swift S, Grigorieva E, Tybulewicz VL, and Ashworth A (1997). Tumorigenesis and a DNA repair defect in mice with a truncating Brca2 mutation. Nat Genet 17: 423–430.

    PubMed  Google Scholar 

  147. Parrinello S, Samper E, Krtolica A, Goldstein J, Melov S, and Campisi J (2003). Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat Cell Biol 5: 741–747.

    PubMed  Google Scholar 

  148. Zalvide J and DeCaprio JA (1995). Role of pRb-related proteins in simian virus 40 large-T-antigen- mediated transformation. Mol Cell Biol 15: 5800–5810.

    PubMed  Google Scholar 

  149. Davisa T, Skinnera JW, Faragherb RGA, Jonesa CJ, and Kipling D (2005). Replicative senescence in sheep fibroblasts is a p53 dependent process. Exp Gerontol 40: 17–26.

    Google Scholar 

  150. Pathak S, Multani AS, McConkey DJ, Imam AS, and Amoss MS (2000). Spontaneous regression of cutaneous melanoma in sinclair swine is associated with defective telomerase activity and extensive telomere erosion. Int J Oncol 17: 1219–1224.

    PubMed  Google Scholar 

  151. McKevitt TP, Nasir L, Wallis CV, and Argyle DJ (2003). A cohort study of telomere and telomerase biology in cats. Am J Vet Res 64: 1496–1499.

    PubMed  Google Scholar 

  152. Brummendorf TH, Mak J, Sabo KM, Baerlocher GM, Dietz K, Abkowitz JL, and Lansdorp PM (2002). Longitudinal studies of telomere length in feline blood cells. Exp Hematol 30: 1147–1152.

    PubMed  Google Scholar 

  153. Nasir L, Devliny P, Mckevitt T, Ruttemanz G, and Argyle DJ (2001). Telomere lengths and telomerase activity in dog tissues: a potential model system to study human telomere and telomerase biology. Neoplasia 3: 351–359.

    PubMed  Google Scholar 

  154. Argyle DJ, Ellsmore V, Gault EA, Munro AF, and Nasir L (2003). Equine telomeres and telomerase in cellular immortalization and ageing. Mech Ageing Dev 124: 759–764.

    PubMed  Google Scholar 

  155. Steinert S, White DM, Zou Y, Shay JW, and Wright WE (2002). Telomere biology and cellular aging in nonhuman primate cells. Exp Cell Res 272: 146–152.

    PubMed  Google Scholar 

  156. Wurster DH and Benirschke K (1970). Indian muntjac, Muntiacus munjak: a deer with a low diploid chromosome number. Science 168: 1364–1366.

    PubMed  Google Scholar 

  157. Zou Y, Yi X, Wright WE, and Shay JW (2002). Human telomerase can immortalize Indian muntjac cells. Exp Cell Res 281: 63–76.

    PubMed  Google Scholar 

  158. Baxter SM, Greizerstein MB, Kushlan DM, and Ashley GW (1993). Conformational properties of DNA hairpins with TTT and TTTT loops. Biochemistry 32: 8702–8711.

    PubMed  Google Scholar 

  159. Day JP, Limoli CL, and Morgan WF (1998). Recombination involving interstitial telomere repeat-like sequences promotes chromosomal instability in Chinese hamster cells. Carcinogenesis 19: 259–265.

    PubMed  Google Scholar 

  160. Zou Y, Yi X, Wright W, and Shay J (2002). Human telomerase can immortalize Indian muntjac cells. Exp Cell Res 281: 63–76.

    PubMed  Google Scholar 

  161. Meyne J, Baker RJ, Hobart HH, Hsu TC, Ryder OA, Ward OG, Wiley JE, Wurster-Hill DH, Yates TL, and Moyzis RK (1990). Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequence in vertebrate chromosomes. Chromosoma 99: 3–10.

    PubMed  Google Scholar 

  162. Rocco L, Costagliola D, and Stingo V (2001). (TTAGGG)n telomeric sequence in selachian chromosomes. Heredity 87: 583–588.

    PubMed  Google Scholar 

  163. George JC, et al. (1999). Age and growth estimates of bowhead whales (Balaena mysticetus) via aspartic acid racemization. Can. J. Zool. 77:571–580.

    PubMed  Google Scholar 

  164. Rozell N (2001). Bowhead whales may be the world’s oldest mammals. In Alaska Science Forum.

    Google Scholar 

  165. Forsyth NR, Elder FF, Shay JW, and Wright WE (2005). Lagomorphs (rabbits, pikas and hares) do not use telomere-directed replicative aging in vitro. Mech Ageing Dev 126: 685–691.

    PubMed  Google Scholar 

  166. Austad SN (1997). Why We Age: What Science Is Discovering About the Body’s Journey Through Life. New York: John Wiley & Sons Inc., p. 244.

    Google Scholar 

  167. Guyton AC and Hall JE (1966). Transport of oxygen and carbon dioxide in the blood and bodily fluids. In Textbook of Medical Physiology. Philadelphia, PA: Saunders, pp. 513–523.

    Google Scholar 

  168. Wright WE and Shay JW (2006). Inexpensive low-oxygen incubators. Nat Protoc 1: 2088–2090.

    PubMed  Google Scholar 

  169. Oikawa S and Kawanishi S (1999). Site-specific DNA damage at GGG sequence by oxidative stress may accelerate telomere shortening. FEBS Lett 453: 365–368.

    PubMed  Google Scholar 

  170. von Zglinicki T (2002). Oxidative stress shortens telomeres. Trends Biochem Sci 27: 339–344.

    Google Scholar 

  171. Lorenz M, Saretzki G, Sitte N, Metzkow S, and von Zglinicki T (2001). BJ fibroblasts display high antioxidant capacity and slow telomere shortening independent of hTERT transfection. Free Radic Biol Med 31: 824–831.

    PubMed  Google Scholar 

  172. Masutomi K, Yu EY, Khurts S, Ben-Porath I, Currier JL, Metz GB, Brooks MW, Kaneko S, Murakami S, DeCaprio JA, Weinberg RA, Stewart SA, and Hahn WC (2003). Telomerase maintains telomere structure in normal human cells. Cell 114: 241–253.

    PubMed  Google Scholar 

  173. Harper JM, Salmon AB, Leiser SF, Galecki AT, and Miller RA (2007). Skin-derived fibroblasts from long-lived species are resistant to some, but not all, lethal stresses and to the mitochondrial inhibitor rotenone. Aging Cell 6: 1–13.

    PubMed  Google Scholar 

  174. Kapahi P, Boulton ME, and Kirkwood TB (1999). Positive correlation between mammalian life span and cellular resistance to stress. Free Radic Biol Med 26: 495–500.

    PubMed  Google Scholar 

  175. Shiels PG, Kind AJ, Campbell KHS, Wilmut I, Waddington D, Colman A, and Schnieke AE (1999). Analysis of telomere length in dolly, a sheep derived by nuclear transfer. Cloning 1: 119–125.

    PubMed  Google Scholar 

  176. Kubota C, Yamakuchi H, Todoroki J, Mizoshita K, Tabara N, Barber M, and Yang X (2000). Six cloned calves produced from adult fiboblast cells after long term culture. Proc Natl Acad Sci U S A 97: 990–995.

    PubMed  Google Scholar 

  177. Betts D, Bordignon V, Hill J, Winger Q, Westhusin M, Smith L, and King W (2001). Reprograming of telomerase activity and rebuilding of telomere length in cloned cattle. Proc Natl Acad Sci U S A 98: 1077–1082.

    PubMed  Google Scholar 

  178. Dikmen ZG, Gellert GC, Jackson S, Gryaznov S, Tressle R, Dogan P, Wright WE, and Shay JW (2005). In vivo inhibition of lung cancer by GRN163L: a novel human telomerase inhibitor. Cancer Res 65: 7866–7873.

    PubMed  Google Scholar 

  179. http://www.tasciences.com/index.html

Download references

Acknowledgments

We thank Agnel Sfeir for Fig. 1.

Author information

Authors and Affiliations

  1. Department of Cell Biology, The University of Texas Southwestern Medical Center at Dallas, Dallas, TX, 75390-9039, USA

    N.M.V. Gomes, J.W. Shay & W. E. Wright

Authors
  1. N.M.V. Gomes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J.W. Shay
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. W. E. Wright
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to W. E. Wright .

Editor information

Editors and Affiliations

  1. 98195-7470 98195-7470, Seattle, 98195-7470, U.S.A.

    Norman S. Wolf

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Gomes, N., Shay, J., Wright, W.E. (2010). Telomeres and Telomerase. In: Wolf, N. (eds) The Comparative Biology of Aging. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-3465-6_11

Download citation

Publish with us

Policies and ethics

Search

Navigation