The loss of a single telomere can result in instability of multiple chromosomes in a human tumor cell line

Molecular Cancer Research

Volumn 3, Issue 3, 2005, Pages 139-150

  Sabatier, Laure ^a   Ricoul, Michelle ^a   Pottier, Géraldine ^a   Murnane, John P ^b  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELIC IMBALANCE; ARTICLE; CANCER; CHROMOSOMAL INSTABILITY; CHROMOSOME ARM; CHROMOSOME DUPLICATION; CHROMOSOME LOSS; CHROMOSOME TRANSLOCATION; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; ISOCHROMOSOME; KARYOTYPE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TELOMERE; TUMOR CELL LINE;

ALLELES; CELL LINE, TUMOR; CHROMOSOME MAPPING; CHROMOSOMES; DNA; DNA SEQUENCE, UNSTABLE; GENE DUPLICATION; GENOME; HUMANS; KARYOTYPING; MODELS, BIOLOGICAL; MODELS, GENETIC; PLASMIDS; TELOMERE; TRANSLOCATION, GENETIC;

EID: 17144410403     PISSN: 15417786     EISSN: None     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-04-0194     Document Type: Article

References (59)

1. Blackburn EH. Switching and signaling at the telomere. Cell 2001;106:661-73.
2. de Lange T. Telomere dynamics and genome instability in human cancer. In: Blackbum EH, Greider CW, editors. Telomeres. Plainview (NY): Cold Spring Harbor Press; 1995. p. 265-93.
3. Itahana K, Campisi J, Dimri GP. Mechanisms of cellular senescence in human and mouse cells. Biogerontology 2004;5:1-10.
4. Herbig U, Jobling WA, Chen BP, Chen DJ, Sedivy JM. Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21(CIP1), but not p16(INK4a). Mol Cell 2004;14:501-13.
5. Counter CM, Avilion AA, LeFeuvre CE, et al. Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J 1992;11:1921-9.
6. Romanov SR, Kozakiewicz BK, Hoist CR, Stampfer MR, Haupt LM, Tlsty TD. Normal human mammary epithelial cells spontaneously escape senescence and acquire genomic changes. Nature 2001;409:633-7.
7. Ducray C, Pommier J-P, Martins L, Boussin F, Sabatier L. Telomere dynamics, end-to-end fusions and telomerase activation during the human fibroblast immortalization process. Oncogene 1999;18:4211-23.
8. Murnane JP, Sabatier L, Marder BA, Morgan WF. Telomere dynamics in an immortal human cell line. EMBO J 1994;13:4953-62.
9. Dunham MA, Neumann AA, Fasching CL, Reddel RR. Telomere maintenance by recombination in human cells. Nat Genet 2000;26:447-50.
10. Tlsty TD. Genomic instability and its role in neoplasia. Curr Top Microbiol Immunol 1997;221:37-46.
11. McClintock B. The stability of broken ends of chromosomes in Zea mays. Genetics 1941;41:234-82.
12. Fouladi B, Miller D, Sabatier L, Murnane JP. The relationship between spontaneous telomere loss and chromosome instability in a human tumor cell line. Neoplasia 2000;2:540-54.
13. Lo AWI, Sprung CN, Fouladi B, et al. Chromosome instability as a result of double-strand breaks near telomeres in mouse embryonic stem cells. Mol Cell Biol 2002;22:4836-50.
14. Artandi SE, Chang S, Lee S-L, et al. Telomere dysfunction promotes nonreciprocal translocations and epithelial cancers in mice. Nature 2000;406:641-5.
15. Chin K, de Solorzano CO, Knowles D, et al. In situ analysis of genome instability in breast cancer. Nat Genet 2004;16:984-8.
16. Gisselsson D, Jonson T, Petersen A, et al. Telomere dysfunction triggers extensive DNA fragmentation and evolution of complex chromosome abnormalities in human malignant tumors. Proc Natl Acad Sci U S A 2001;98:12683-8.
17. Lo AWI, Sabatier L, Fouladi B, Pottier G, Ricoul M, Murnane JP. DNA amplification by breakage/fusion/bridge cycles initiated by spontaneous telomere loss in a human cancer cell line. Neoplasia 2002;6:531-8.
18. Sawyer JR, Roloson GJ, Bell JM, Thomas JR, Teo C, Chadduck WM. Telomeric associations in the progression of chromosome aberrations in pediatric solid tumors. Cancer Genet Cytogenet 1996;90:1-13.
19. DePinho RA, Polyak K. Cancer chromosomes in crisis. Nat Genet 2004;36:932-4.
20. Murnane JP, Sabatier L. Chromosomal rearrangements resulting from telomere dysfunction and their role in cancer. BioEssays 2004;26:1164-74.
21. Schwartz JL, Jordan R, Liber H, Murnane JP, Evans HH. TP53-dependent chromosome instability is associated with transient reductions in telomere length in immortal telomerase-positive cell lines. Genes Chromosomes Cancer 2001;30:236-44.
22. Bryan TM, Englezou A, Dunham MA, Reddel RR. Telomere length dynamics in telomerase-positive immortal human cell populations. Exp Cell Res 1998;239:370-8.
23. Meeker AK, Hicks JL, Iacoluzio-Donahue CA, et al. Telomere length abnormalities occur early in the initiation of epithelial carcinogenesis. Clin Can Res 2004;10:3317-26.
24. Meeker AK, Hicks JL, Gabrielson E, Strauss WM, De Marzo AM, Argani P. Telomere shortening occurs in subsets of normal breast epithelium as well as in situ and invasive carcinoma. Am J Pathol 2004;164:925-35.
25. Sprung CN, Sabatier L, Murnane JP. Telomere dynamics in a human cancer cell line. Exp Cell Res 1999;247:29-37.
26. Smogorzewska A, van Steensel B, Bianchi A, et al. Control of human telomere length by TRF1 and TRF2. Mol Cell Biol 2000;20:1659-68.
27. Ohki R, Ishikawa F. Telomere-bound TRF1 and TRF2 stall the replication fork at telomeric repeats. Nucleic Acids Res 2004;32:1627-37.
28. Ivessa AS, Zhou J-Q, Schulz VP, Monson EK, Zakian VA. Saccharomyces Rrm3p, a 5′ to 3′ DNA helicase that promotes replication fork progression through telomeric and subtelomeric DNA. Genes Dev 2002;16:1383-96.
29. Crabbe L, Verdun RE, Haggblom CI, Karlseder J. Defective telomere lagging strand synthesis in cells lacking WRN helicase activity. Science 2004;306:1951-3.
30. Bai Y, Murnane JP. Telomere instability in a human tumor cell line expressing a dominant-negative WRN protein. Hum Genet 2003;113:337-47.
31. Ricchetti M, Dujon B, Fairhead C. Distance from the chromosome end determines the efficiency of double-strand break repair in subtelomeres of haploid yeast. J Mol Biol 2003;328:847-62.
32. Petersen S, Saretzki G, von Zglinicki T. Preferential accumulation of single-stranded regions in telomeres of human fibroblasts. Exp Cell Res 1998;239:152-60.
33. Kruk PA, Rampino NJ, Bohr VA. DNA damage and repair in telomeres: relation to aging. Proc Natl Acad Sci U S A 1995;92:258-62.
34. Ferguson DO, Alt FW. DNA double strand break repair and chromosomal translocation: lessons from animal models. Oncogene 2001;20:5572-9.
35. Pennaneach V, Kolodner RD. Recombination and the Tel1 and Mec1 checkpoints differentially effect genome rearrangements driven by telomere dysfunction in yeast. Nat Genet 2004;36:612-7.
36. Rudolph KL, Chang S, Lee H-W, et al. Longevity, stress response, and cancer in aging telomerase-deficient mice. Cell 1999;96:701-12.
37. Harley CB, Futcher AB, Greider CW. Telomeres shorten during ageing of human fibroblasts. Nature 1990;345:458-60.
38. Rudolph KL, Millard M, Bosenberg MW, DePinho RA. Telomere dysfunction and evolution of intestinal carcinoma in mice and humans. Nat Genet 2001;28:155-9.
39. Zhu C, Mills KD, Fergusion DO, et al. Unrepaired DNA breaks in p53-deficient cells lead to oncogenic gene amplification subsequent to translocations. Cell 2002;109:811-21.
40. Ingvarsson S. Molecular genetics of breast cancer progression. Semin Cancer Biol 1999;9:277-88.
41. Gollin SM. Chromosomal alterations in squamous cell carcinomas of the head and neck: window to the biology of disease. Head Neck 2001;23:238-53.
42. Difilippantonio MJ, Petersen S, Chen HT, et al. Evidence for replicative repair of DNA double-strand breaks leading to oncogenic translocation and gene amplification. J Exp Med 2002;196:469-80.
43. Lemyre E, Kaloustian VMD, Duncan AMV. Stable non-Robertsonian dicentric chromosomes: four new cases and a review. J Med Genet 2001;38:76-9.
44. Codina-Pascual M, Oliver-Bonet M, Navarro J, et al. FISH characterization of a dicentric Yq (p11.32) isochromosome in an axoospermic male. Am J Med Genet 2004;127A:302-6.
45. Aurias A, Dutrillaux B. A possible new type of chromosome rearrangement: telomere-centromere translocation (ct) followed by double duplication. Hum Genet 1986;72:25-6.
46. Pandita TK, Pathak S, Geard C. Chromosome end associations, telomeres and telomerase activity in ataxia telangiectasia cells. Cytogenet Cell Genet 1995;71:86-93.
47. Savage JRK. Classification and relationships of induced chromosomal structural changes. J Med Genet 1975;12:103-22.
48. Bosco G, Haber JE. Chromosome break-induced replication leads to nonreciprocal translocations and telomere capture. Genetics 1998;150:1037-47.
49. Hackett JA, Feldser DM, Greider CW. Telomere dysfunction increases mutation rates and genomic instability. Cell 2001;106:275-86.
50. Sprung CN, Reynolds GE, Jasin M, Mumane JP. Chromosome healing in mouse embryonic stem cells. Proc Natl Acad Sci U S A 1999;96:6781-6.
51. Diede SJ, Gottschling DE. Telomerase-mediated telomere addition in vivo requires DNA primase and DNA polymerase α and δ. Cell 1999;99:723-33.
52. Zhou J-Q, Monson EK, Teng S-C, Schultz VP, Zakian VA. Pif1p helicase, a catalytic inhibitor of telomerase in yeast. Science 2000;289:771-4.
53. Schwab M. Oncogene amplification in solid tumors. Semin Cancer Biol 1999;9:319-25.
54. Dutrillaux B, Couturier J. La pratique de l'analysee chromosomique. Paris: Masson; 1981.
55. Lemieux N, Dutrillaux B, Viegas-Pequignot E. A simple method for simultaneous R- or G-banding and fluorescence in situ hybridization of small single-copy genes. Cytogenet Cell Genet 1992;59:311-2.
56. Lansdorp PM, Verwoerd NP, van de Rijke FM, et al. Heterogeneity in telomere length of human chromosomes. Hum Mol Genet 1996;5:685-91.
57. Doggert NA, Goodwin LA, Tesmer JG, et al. An integrated physical map of human chromosome 16. Nature 1995;377:335-65.
58. Longmire JL, Brown NC, Meincke LJ, et al. Construction and characterization of partial digest DNA. Genet Anal Tech Appl 1993;10:69-76.
59. Knight SJL, Lese CM, Precht KS, et al. An optimized set of human telomere clones for studying telomere integrity and architecture. Am J Hum Genet 2000;67:320-32.