Manipulating mouse telomeres: Models of tumorigenesis and aging

Cytogenetic and Genome Research

Volumn 105, Issue 2-4, 2004, Pages 471-478

  Xin, Z ^a   Broccoli, D ^a  

^a FOX CHASE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TELOMERASE;

AGING; ARTICLE; CARCINOGENESIS; CELL CYCLE; CHROMOSOME REPLICATION; DISEASE MODEL; DNA REPLICATION; DNA TRANSCRIPTION; ENZYME DEFICIENCY; GENE TARGETING; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; STRUCTURE ANALYSIS; TELOMERE;

AGING; ANIMALS; ANTIGENS, NUCLEAR; CELL TRANSFORMATION, NEOPLASTIC; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DISEASE MODELS, ANIMAL; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; MICE; MODELS, ANIMAL; PROTEIN-SERINE-THREONINE KINASES; RNA; TELOMERASE; TELOMERE; TUMOR SUPPRESSOR PROTEIN P14ARF; TUMOR SUPPRESSOR PROTEIN P53;

EUKARYOTA;

EID: 3242753419     PISSN: 14248581     EISSN: None     Source Type: Journal    
DOI: 10.1159/000078221     Document Type: Article

References (87)

1. Artandi SE, Chang S, Lee SL, Alson S, Gottlieb GJ, Chin L, DePinho RA: Telomere dysfunction promotes non-reciprocal translocations and epithelial cancers in mice. Nature 406:641-645 (2000).
2. Artandi SE, Alson S, Tietze MK, Sharpless NE, Ye S, Greenberg RA, Castrillon DH, Horner JW, Weiler SR, Carrasco RD, DePinho RA: Constitutive telomerase expression promotes mammary carcinomas in aging mice. Proc Natl Acad Sci USA 99:8191-8196 (2002).
3. Bailey SM, Meyne J, Chen DJ, Kurimasa A, Li GC, Lehnert BE, Goodwin EH: DNA double-strand break repair proteins are required to cap the ends of mammalian chromosomes. Proc Natl Acad Sci USA 96:14899-14904 (1999).
4. Barlow C, Hirotsune S, Paylor R, Liyanage M, Eckhaus M, Collins F, Shiloh Y, Crawley JN, Ried T, Tagle D, Wynshaw-Boris A: Atm-deficient mice: A paradigm of ataxia telangiectasia. Cell 86:159-171 (1996).
5. Baumann P, Cech TR: Pot1, the putative telomere endbinding protein in fission yeast and humans. Science 292:1171-1175 (2001).
6. Baumann P, Podell E, Cech TR: Human Pot1 (protection of telomeres) protein: Cytolocalization, gene structure, and alternative splicing. Mol Cell Biol 22:8079-8087 (2002).
7. Bianchi A, de Lange T: Ku binds telomeric DNA in vitro. J Biol Chem 274:21223-21227 (1999).
8. Bilaud T, Koering CE, Binet-Brasselet E, Ancelin K, Pollice A, Gasser SM, Gilson E: The telobox, a Myb-related telomeric DNA binding motif found in proteins from yeast, plants and human. Nucleic Acids Res 24:1294-1303 (1996).
9. Bilaud T, Brun C, Ancelin K, Koering CE, Laroche T, Gilson E: Telomeric localization of TRF2, a novel human telobox protein. Nat Genet 17:236-239 (1997).
10. Blasco MA, Rizen M, Greider CW, Hanahan D: Differential regulation of telomerase activity and telomerase RNA during multi-stage tumorigenesis. Nat Genet 12:200-204 (1996).
11. Blasco MA, Lee HW, Hande MP, Samper E, Lansdorp PM, DePinho RA, Greider CW: Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91:25-34 (1997).
12. Borghesani PR, Alt FW, Bottaro A, Davidson L, Aksoy S, Rathbun GA, Roberts TM, Swat W, Segal RA, Gu Y: Abnormal development of Purkinje cells and lymphocytes in Atm mutant mice. Proc Natl Acad Sci USA 97:3336-3341 (2000).
13. Broccoli D, Godley LA, Donehower LA, Varmus HE, de Lange T: Telomerase activation in mouse mammary tumors: Lack of detectable telomere shortening and evidence for regulation of telomerase RNA with cell proliferation. Mol Cell Biol 16:3765-3772 (1996).
14. Broccoli D, Smogorzewska A, Chong L, de Lange T: Human telomeres contain two distinct Myb-related proteins, TRF1 and TRF2. Nat Genet 17:231-235 (1997).
15. Bryan TM, Englezou A, Gupta J, Bacchetti S, Reddel RR: Telomere elongation in immortal human cells without detectable telomerase activity. EMBO J 14:4240-4248 (1995).
16. Bryan TM, Englezou A, Dalla-Pozza L, Dunham MA, Reddel RR: Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nat Med 3:1271-1274 (1997).
17. Campisi J: Cancer, aging and cellular senescence. In Vivo 14:183-188 (2000).
18. Chadeneau C, Siegel P, Harley CB, Muller WJ, Bacchetti S: Telomerase activity in normal and malignant murine tissues. Oncogene 11:893-898 (1995).
19. Chang S, Khoo CM, Naylor ML, Maser RS, DePinho RA: Telomere-based crisis: Functional differences between telomerase activation and ALT in tumor progression. Genes Dev 17:88-100 (2003a).
20. Chang W, Dynek JN, Smith S: TRF1 is degraded by ubiquitin-mediated proteolysis after release from telomeres. Genes Dev 17:1328-1333 (2003b).
21. Chin L, Artandi SE, Shen Q, Tam A, Lee SL, Gottlieb GJ, Greider CW, DePinho RA: p53 deficiency rescues the adverse effects of telomere loss and cooperates with telomere dysfunction to accelerate carcinogenesis. Cell 97:527-538 (1999).
22. Chong L, van Steensel B, Broccoli D, Erdjument-Bromage H, Hanish J, Tempst P, de Lange T: A human telomeric protein. Science 270:1663-1667 (1995).
23. Collins K: Mammalian telomeres and telomerase. Curr Opin Cell Biol 12:378-383 (2000).
24. Cook BD, Dynek JN, Chang W, Shostak G, Smith S: Role for the related poly(ADP-Ribose) polymerases tankyrase 1 and 2 at human telomeres. Mol Cell Biol 22:332-342 (2002).
25. Cooke HJ, Smith BA: Variability at the telomeres of the human X/Y pseudoautosomal region. Cold Spring Harb Symp Quant Biol 51:213-219 (1986).
26. de Lange T, Shiue L, Myers RM, Cox DR, Naylor SL, Killery AM, Varmus HE: Structure and variability of human chromosome ends. Mol Cell Biol 10:518-527 (1990).
27. Difilippantonio MJ, Zhu J, Chen HT, Meffre E, Nussenzweig MC, Max EE, Ried T, Nussenzweig A: DNA repair protein Ku80 suppresses chromosomal aberrations and malignant transformation. Nature 404:510-514 (2000).
28. Elson A, Wang Y, Daugherty CJ, Morton CC, Zhou F, Campos-Torres J, Leder P: Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc Natl Acad Sci USA 93:13084-13089 (1996).
29. Espejel S, Blasco MA: Identification of telomere-dependent "senescence-like" arrest in mouse embryonic fibroblasts. Exp Cell Res 276:242-248 (2002).
30. Espejel S, Franco S, Rodriguez-Perales S, Bouffler SD, Cigudosa JC, Blasco MA: Mammalian Ku86 mediates chromosomal fusions and apoptosis caused by critically short telomeres. EMBO J 21:2207-2219 (2002).
31. Gonzalez-Suarez E, Samper E, Flores JM, Blasco MA: Telomerase-deficient mice with short telomeres are resistant to skin tumorigenesis. Nat Genet 26:114-117 (2000).
32. Gonzalez-Suarez E, Samper E, Ramirez A, Flores JM, Martin-Caballero J, Jorcano JL, Blasco MA: Increased epidermal tumors and increased skin wound healing in transgenic mice overexpressing the catalytic subunit of telomerase, mTERT, in basal keratinocytes. EMBO J 20:2619-2630 (2001).
33. Goytisolo FA, Blasco MA: Many ways to telomere dysfunction: In vivo studies using mouse models. Oncogene 21:584-591 (2002).
34. Greenberg RA, Chin L, Femino A, Lee KH, Gottlieb GJ, Singer RH, Greider CW, DePinho RA: Short dysfunctional telomeres impair tumorigenesis in the INK4a(delta2/3) cancer-prone mouse. Cell 97:515-525 (1999).
35. Griffith JD, Comeau L, Rosenfield S, Stansel RM, Bianchi A, Moss H, de Lange T: Mammalian telomeres end in a large duplex loop. Cell 97:503-514 (1999).
36. Hahn W, Stewart SA, Brooks M, York S, Eaton E, Kurachi A, Beijersbergen R, Knoll J, Meyerson M, Weinberg R: Inhibition of telomerase limits the growth of human cancer cells. Nature Med 5:1164-1170 (1999).
37. Harley CB, Futcher AB, Greider CW: Telomeres shorten during ageing of human fibroblasts. Nature 345:458-460 (1990).
38. Harley CB, Vaziri H, Counter CM, Allsopp RC: The telomere hypothesis of cellular aging. Exp Gerontol 27:375-382 (1992).
39. Hemann MT, Greider CW: Wild-derived inbred mouse strains have short telomeres. Nucleic Acids Res 28:4474-4478 (2000).
40. Hemann MT, Strong MA, Hao LY, Greider CW: The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell 107:67-77 (2001).
41. Herrera E, Samper E, Martin-Caballero J, Flores JM, Lee HW, Blasco MA: Disease states associated with telomerase deficiency appear earlier in mice with short telomeres. EMBO J 18:2950-2960 (1999).
42. Herrera E, Martinez AC, Blasco MA: Impaired germinal center reaction in mice with short telomeres. EMBO J 19:472-481 (2000).
43. Hiyama E, Hiyama K: Clinical utility of telomerase in cancer. Oncogene 21:643-649 (2002).
44. Holt SE, Wright WE, Shay JW: Multiple pathways for the regulation of telomerase activity. Eur J Cancer 33:761-766 (1997).
45. Hsu HL, Gilley D, Blackburn EH, Chen DJ: Ku is associated with the telomere in mammals. Proc Natl Acad Sci USA 96:12454-12458 (1999).
46. Hsu HL, Gilley D, Galande SA, Hande MP, Allen B, Kim SH, Li GC, Campisi J, Kohwi-Shigematsu T, Chen DJ: Ku acts in a unique way at the mammalian telomere to prevent end joining. Genes Dev 14:2807-2812 (2000).
47. Kaminker PG, Kim SH, Taylor RD, Zebarjadian Y, Funk WD, Morin GB, Yaswen P, Campisi J: TANK2, a new TRF1-associated poly(ADP-ribose) polymerase, causes rapid induction of cell death upon overexpression. J Biol Chem 276:35891-35899 (2001).
48. Karlseder J, Broccoli D, Dai Y, Hardy S, de Lange T: p53- and ATM-dependent apoptosis induced by telomeres lacking TRF2. Science 283:1321-1325 (1999).
49. Karlseder J, Kachatrian L, Takai H, Mercer K, Hingorani S, Jacks T, de Lange T: Targeted deletion reveals an essential function for the telomere length regulator Trf1. Mol Cell Biol 23:6533-6541 (2003).
50. Kastan MB, Lim DS: The many substrates and functions of ATM. Nat Rev Mol Cell Biol 1:179-186 (2000).
51. Kim SH, Kaminker P, Campisi J: TIN2, a new regulator of telomere length in human cells. Nat Genet 23:405-412 (1999).
52. Kipling D, Cooke HJ: Hypervariable ultra-long telomeres in mice. Nature 347:400-402 (1990).
53. Lee HW, Blasco MA, Gottlieb GJ, Horner JW, 2nd, Greider CW, DePinho RA: Essential role of mouse telomerase in highly proliferative organs. Nature 392:569-574 (1998).
54. Li B, Oestreich S, de Lange T: Identification of human Rap1: implications for telomere evolution. Cell 101:471-483 (2000).
55. Lim DS, Vogel H, Willerford DM, Sands AT, Platt KA, Hasty P: Analysis of ku80-mutant mice and cells with deficient levels of p53. Mol Cell Biol 20:3772-3780 (2000).
56. Liu Y, Snow BE, Hande MP, Yeung D, Erdmann NJ, Wakeham A, Itie A, Siderovski DP, Lansdorp PM, Robinson MO, Harrington L: The telomerase reverse transcriptase is limiting and necessary for telomerase function in vivo. Curr Biol 10:1459-1462 (2000).
57. Loayza D, de Lange T: POT1 as a terminal transducer of TRF1 telomere length control. Nature 424:1013-1018 (2003).
58. Luderus ME, van Steensel B, Chong L, Sibon OC, Cremers FF, de Lange T: Structure, subnuclear distribution, and nuclear matrix association of the mammalian telomeric complex. J Cell Biol 135:867-881 (1996).
59. McIlrath J, Bouffler SD, Samper E, Cuthbert A, Wojcik A, Szumiel I, Bryant PE, Riches AC, Thompson A, Blasco MA, Newbold RF, Slijepcevic P: Telomere length abnormalities in mammalian radiosensitive cells. Cancer Res 61:912-915 (2001).
60. Metcalfe JA, Parkhill J, Campbell L, Stacey M, Biggs P, Byrd PJ, Taylor AM: Accelerated telomere shortening in ataxia telangiectasia. Nat Genet 13:350-353 (1996).
61. Mitton-Fry RM, Anderson EM, Hughes TR, Lundblad V, Wuttke DS: Conserved structure for single-stranded telomeric DNA recognition. Science 296:145-147 (2002).
62. Niida H, Matsumoto T, Satoh H, Shiwa M, Tokutake Y, Furuichi Y, Shinkai Y: Severe growth defect in mouse cells lacking the telomerase RNA component. Nat Genet 19:203-206 (1998).
63. Nussenzweig A, Chen C, da Costa Soares V, Sanchez M, Sokol K, Nussenzweig MC, Li GC: Requirement for Ku80 in growth and immunoglobulin V(D)J recombination. Nature 382:551-555 (1996).
64. Olovnikov AM: 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 (1973).
65. Pandita TK: ATM function and telomere stability. Oncogene 21:611-618 (2002).
66. Prowse KR, Greider CW: Developmental and tissue-specific regulation of mouse telomerase and telomere length. Proc Natl Acad Sci USA 92:4818-4822 (1995).
67. Rudolph KL, Chang S, Lee HW, Blasco M, Gottlieb GJ, Greider C, DePinho RA: Longevity, stress response, and cancer in aging telomerase-deficient mice. Cell 96:701-712 (1999).
68. Samper E, Goytisolo FA, Slijepcevic P, van Buul PP, Blasco MA: Mammalian Ku86 protein prevents telomeric fusions independently of the length of TTAGGG repeats and the G-strand overhang. EMBO Rep 1:244-252 (2000).
69. Shay JW, Bacchetti S: A survey of telomerase activity in human cancer. Eur J Cancer 33:787-791 (1997).
70. Sherr CJ, DePinho RA: Cellular senescence: Mitotic clock or culture shock? Cell 102:407-410 (2000).
71. Shiloh Y, Kastan MB: ATM: genome stability, neuronal development, and cancer cross paths. Adv Cancer Res 83:209-254 (2001).
72. Smith GC, Jackson SP: The DNA-dependent protein kinase. Genes Dev 13:916-934 (1999).
73. Smith S, de Lange T: Tankyrase promotes telomere elongation in human cells. Curr Biol 10:1299-1302 (2000).
74. Smith S, Giriat I, Schmitt A, de Lange T: Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. Science 282:1484-1487 (1998).
75. Smogorzewska A, de Lange T: Different telomere damage signaling pathways in human and mouse cells. EMBO J 21:4338-4348 (2002).
76. Song K, Jung D, Jung Y, Lee SG, Lee I: Interaction of human Ku70 with TRF2. FEBS Lett 481:81-85 (2000).
77. Starling JA, Maule J, Hastie ND, Allshire RC: Extensive telomere repeat arrays in mouse are hypervariable. Nucleic Acids Res 18:6881-6888 (1990).
78. Tyner SD, Venkatachalam S, Choi J, Jones S, Ghebranious N, Igelmann H, Lu X, Soron G, Cooper B, Brayton C, Hee Park S, Thompson T, Karsenty G, Bradley A, Donehower LA: p53 mutant mice that display early ageing-associated phenotypes. Nature 415:45-53 (2002).
79. van Steensel B, Smogorzewska A, de Lange T: TRF2 protects human telomeres from end-to-end fusions. Cell 92:401-413 (1998).
80. Vogel H, Lim DS, Karsenty G, Finegold M, Hasty P: Deletion of Ku86 causes early onset of senescence in mice. Proc Natl Acad Sci USA 96:10770-10775 (1999).
81. Wong KK, Maser RS, Bachoo RM, Menon J, Carrasco DR, Gu Y, Alt FW, DePinho RA: Telomere dysfunction and Atm deficiency compromises organ homeostasis and accelerates ageing. Nature 421:643-648 (2003).
82. Wright WE, Shay JW: Telomere dynamics in cancer progression and prevention: Fundamental differences in human and mouse telomere biology. Nat Med 6:849-851 (2000).
83. Xu Y, Ashley T, Brainerd EE, Bronson RT, Meyn MS, Baltimore D: Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev 10:2411-2422 (1996).
84. Yuan X, Ishibashi S, Hatakeyama S, Saito M, Nakayama J, Nikaido R, Haruyama T, Watanabe Y, Iwata H, Iida M, Sugimura H, Yamada N, Ishikawa F: Presence of telomeric G-strand tails in the telomerase catalytic subunit TERT knockout mice. Genes Cells 4:563-572 (1999).
85. Zhang X, Mar V, Zhou W, Harrington L, Robinson M: Telomere shortening and apoptosis in telomerase-inhibited human tumor cells. Genes Dev 13:2388-2399 (1999).
86. Zhu XD, Kuster B, Mann M, Petrini JH, de Lange T: Cell-cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nat Genet 25:347-352 (2000).
87. Zijlmans JM, Martens UM, Poon SS, Raap AK, Tanke HJ, Ward RK, Lansdorp PM: Telomeres in the mouse have large inter-chromosomal variations in the number of T2AG3 repeats. Proc Natl Acad Sci USA 94:7423-7428 (1997).