CoChat
Sign Up
Cited by 118Telomeres, Telomerase, and SenescenceDNA Repair MechanismsChromosomal and Genetic Variations

Chromosome Instability as a Result of Double-Strand Breaks near Telomeres in Mouse Embryonic Stem Cells

Open access
Lo, Anthony W. I., Sprung, Carl N., Fouladi, Bijan, Pedram, Mehrdad, Sabatier, Laure, Ricoul, Michelle, Reynolds, Gloria E., Murnane, John P.·2002·Molecular and Cellular Biology
DOI 10.1128/mcb.22.13.4836-4850.2002PMC PMC133890
Open this paper in CoChat — free account

Abstract

Telomeres are essential for protecting the ends of chromosomes and preventing chromosome fusion. Telomere loss has been proposed to play an important role in the chromosomal rearrangements associated with tumorigenesis. To determine the relationship between telomere loss and chromosome instability in mammalian cells, we investigated the events resulting from the introduction of a double-strand break near a telomere with I-SceI endonuclease in mouse embryonic stem cells. The inactivation of a selectable marker gene adjacent to a telomere as a result of the I-SceI-induced double-strand break involved either the addition of a telomere at the site of the break or the formation of inverted repeats and large tandem duplications on the end of the chromosome. Nucleotide sequence analysis demonstrated large deletions and little or no complementarity at the recombination sites involved in the formation of the inverted repeats. The formation of inverted repeats was followed by a period of chromosome instability, characterized by amplification of the subtelomeric region, translocation of chromosomal fragments onto the end of the chromosome, and the formation of dicentric chromosomes. Despite this heterogeneity, the rearranged chromosomes eventually acquired telomeres and were stable in most of the cells in the population at the time of analysis. Our observations are consistent with a model in which broken chromosomes that do not regain a telomere undergo sister chromatid fusion involving nonhomologous end joining. Sister chromatid fusion is followed by chromosome instability resulting from breakage-fusion-bridge cycles involving the sister chromatids and rearrangements with other chromosomes. This process results in highly rearranged chromosomes that eventually become stable through the addition of a telomere onto the broken end. We have observed similar events after spontaneous telomere loss in a human tumor cell line, suggesting that chromosome instability resulting from telomere loss plays a role in chromosomal rearrangements associated with tumor cell progression.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1128/mcb.22.13.4836-4850.2002

Cites

9 of 9 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The segmental aneuploidies identified by cytogenetics analysis most probably point to the occurrence of complex genomic rearrangements in OCT4-targeted samples, such as chromosomal translocations or end-to-end fusions.

    “The segmental aneuploidies identified by cytogenetics analysis (Figs. 1B and S3-S5) most probably point to the occurrence of complex genomic rearrangements in OCT4-targeted samples, such as chromosomal translocations or end-to-end fusions, as it seems unlikely that the rest of the chromosome would continue to be retained without a telomere (31)(32)(33).”

    From Frequent loss of heterozygosity in CRISPR-Cas9–edited early human embryos (2021) · cites this paper as [32]

    The Results and Discussion (page numbers not provided) show that telomere loss in mouse embryonic stem cells can lead to chromosome fusions, translocations, and complex rearrangements. The paper does not examine OCT4-targeted samples or establish that their segmental aneuploidies indicate those rearrangements; that application is the citing authors’ inference. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 74

  1. [1]Akgun, E., J. Zahn, S. Baumes, G. Brown, F. Liang, P. J. Romanienko, S. Lewis, and M. Jasin. 1997. Palindrome resolution and recombination in the mammalian germ line. Mol. Cell. Biol. 17:5559-5570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. [2]Aladjem, M. I., B. T. Spike, L. W. Rodewald, T. J. Hope, M. Klemm, R. Jaenisch, and G. M. Wahl. 1998. ES cells do not activate p53-dependent stress responses and undergo p53-independent apoptosis in response to DNA damage. Curr. Biol. 8:145-155. [DOI] [PubMed] [Google Scholar]
  3. [3]Artandi, S. E., S. Chang, S.-L. Lee, S. Alson, G. J. Gottlieb, L. Chin, and R. A. DePinho. 2000. Telomere dysfunction promotes non-reciprocal translocations and epithelial cancers in mice. Nature 406:641-645. [DOI] [PubMed] [Google Scholar]
  4. [4]Bailey, S. M., J. Meyne, D. J. Chen, A. Kurimasa, G. C. Li, B. E. Lehnert, and E. H. Goodwin. 1999. DNA double-strand break repair proteins are required to cap the ends of mammalian chromosomes. Proc. Natl. Acad. Sci. USA 96:14899-14904. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. [5]Barnett, M. A., J. Buckle, E. P. Evans, A. C. G. Porter, D. Rout, A. G. Smith, and W. R. A. Brown. 1993. Telomere-directed fragmentation of mammalian chromosomes. Nucleic Acids Res. 21:27-36. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. [6]Benner, S. E., G. M. Wahl, and D. D. Von Hoff. 1991. Double minute chromosomes and homogenously staining regions in tumors taken directly from patients verses in human tumor cell lines. Anticancer Drugs 2:11-25. [DOI] [PubMed] [Google Scholar]
  7. [7]Blackburn, E. H. 2001. Switching and signaling at the telomere. Cell 106:661-673. [DOI] [PubMed] [Google Scholar]
  8. [8]Bosco, G., and J. E. Haber. 1998. Chromosome break-induced replication leads to nonreciprocal translocations and telomere capture. Genetics 150:1037-1047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. [9]Brisebois, J. J., and M. S. DuBow. 1993. Selection for spontaneous null mutations in a chromosomally integrated HSV-1 thymidine kinase gene yields deletions and a mutation caused by intragenic illegitimate recombination. Mutat. Res. 287:191-205. [DOI] [PubMed] [Google Scholar]
  10. [10]Collins, J. 1981. Instability of palindromic DNA in Escherichia coli. Cold Spring Harbor Symp. Quant. Biol. 45:409-416. [DOI] [PubMed] [Google Scholar]
  11. [11]Cooper, M. J., J. J. Haluschak, D. Johnson, S. Schwartz, L. J. Morrison, M. Lippa, G. Hatzivassiliou, and J. Tan. 1994. p53 mutations in bladder carcinoma cell lines. Oncol. Res. 6:569-579. [PubMed] [Google Scholar]
  12. [12]Coquelle, A., E. Pipiras, F. Toledo, G. Buttin, and M. Debatisse. 1997. Expression of fragile sites triggers intrachromosomal mammalian gene amplification and sets bounderies to early amplification. Cell 89:215-225. [DOI] [PubMed] [Google Scholar]
  13. [13]de Lange, T. 1995. Telomere dynamics and genome instability in human cancer, p. 265-293. In E. H. Blackburn and C. W. Greider (ed.), Telomeres. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
  14. [16]Farr, C., J. Fantes, P. Goodfellow, and H. Cooke. 1991. Functional reintroduction of human telomeres into mammalian cells. Proc. Natl. Acad. Sci. USA 88:7006-7010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. [17]Flint, J., K. Thomas, G. Micklem, H. Raynham, K. Clark, N. A. Doggett, A. King, and D. R. Higgs. 1997. The relationship between chromosome structure and function at a human telomeric region. Nat. Genet. 15:252-257. [DOI] [PubMed] [Google Scholar]
  16. [18]Floridia, G., M. Piantanida, A. Minelli, C. Dellavecchia, C. Bonaglia, E. Rossi, G. Gimelli, G. Croci, F. Franchi, S. Gilgenkrantz, P. Grammatico, L. Dalpra, S. Wood, C. Danesino, and O. Zuffardi. 1996. The same molecular mechanism at the maternal meiosis I produces mono- and dicentric 8p duplications. Am. J. Hum. Genet. 58:785-796. [PMC free article] [PubMed] [Google Scholar]
  17. [20]Gebow, D., N. Miselis, and H. L. Liber. 2000. Homologous and nonhomologous recombination resulting in deletion: effects of p53 status, microhomology, and repetitive DNA length and orientation. Mol. Cell. Biol. 20:4028-4035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. [21]Gisselsson, D., T. Jonson, A. Petersen, B. Strombeck, P. Dal Cin, M. Hoglund, F. Mitelman, F. Mertens, and N. Mandahl. 2001. Telomere dysfunction triggers extensive DNA fragmentation and evolution of complex chromosome abnormalities in human malignant tumors. Proc. Natl. Acad. Sci. USA 98:12683-12688. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. [22]Gisselsson, D., L. Pettersson, M. Hoglund, M. Heidenblad, L. Gorunova, J. Wiegant, F. Mertens, P. Dal Cin, F. Mitelman, and N. Mandahl. 2000. Chromosomal breakage-fusion-bridge events cause genetic intratumor heterogeneity. Proc. Natl. Acad. Sci. USA 97:5357-5362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. [23]Godwin, A. R., R. J. Bollag, D.-M. Christie, and R. M. Liskay. 1994. Spontaneous and restriction enzyme-induced chromosomal recombination in mammalian cells. Proc. Natl. Acad. Sci. USA 91:12554-12558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. [24]Goytisolo, F. A., E. Samper, S. Edmonson, G. E. Taccioli, and M. A. Blasco. 2001. The absence of the DNA-dependent protein kinase catalytic subunit in mice results in anaphase bridges and increased telomeric fusions with normal telomere length and G-strand overhang. Mol. Cell. Biol. 21:3642-3651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. [25]Hackett, J. A., D. M. Feldser, and C. W. Greider. 2001. Telomere dysfunction increases mutation rates and genomic instability. Cell 106:275-286. [DOI] [PubMed] [Google Scholar]
  23. [26]Hahn, P. J. 1993. Molecular biology of double-minute chromosomes. Bioessays 15:477-484. [DOI] [PubMed] [Google Scholar]
  24. [28]Hanish, J. P., J. L. Yanowitz, and T. De Lange. 1994. Stringent sequence requirements for the formation of human telomeres. Proc. Natl. Acad. Sci. USA 91:8861-8865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. [29]Hellman, A., E. Ziotorynski, S. W. Scherer, J. Cheung, J. B. Vincent, D. I. Smith, L. Trakhtenbrot, and B. Kerem. 2002. A role for common fragile site induction in amplification of human oncogenes. Cancer Cell 1:89-97. [DOI] [PubMed] [Google Scholar]
  26. [30]Hoo, J. J., M. Chao, K. Szego, M. Rauer, S. C. Echiverri, and C. Harris. 1995. Four new cases of inverted terminal duplications. Am. J. Med. Genet. 58:299-304. [DOI] [PubMed] [Google Scholar]
  27. [31]Hsu, H.-L., D. Gilley, S. A. Galande, M. P. Hande, B. Allen, S.-H. Kim, G. C. Li, J. Campisi, T. Kohwi-Shigematsu, and D. J. Chen. 2000. Ku acts in a unique way at the mammalian telomere to prevent end joining. Genes Dev. 14:2807-2812. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. [32]Johnson, R. D., and M. Jasin. 2000. Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells. EMBO J. 19:3398-3407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. [33]Kramer, K. M., and J. E. Haber. 1993. New telomeres in yeast are initiated with a highly selected subset of TG1-3 repeats. Genes Dev. 7:2345-2356. [DOI] [PubMed] [Google Scholar]
  30. [34]Kruk, P. A., N. J. Rampino, and V. A. Bohr. 1995. DNA damage and repair in telomeres: relation to aging. Proc. Natl. Acad. Sci. USA 92:258-262. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. [35]Lejnine, S., V. L. Makarov, and J. P. Langmore. 1995. Conserved nucleoprotein structure at the ends of vertebrate and invertebrate chromosomes. Proc. Natl. Acad. Sci. USA 92:2393-2397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. [36]Lemieux, N., B. Dutrillaux, and E. Viegas-Pequignot. 1992. A simple method for simultaneous R- or G-banding and fluorescence in situ hybridization of small single-copy genes. Cytogenet. Cell Genet. 59:311-312. [DOI] [PubMed] [Google Scholar]
  33. [39]Lin, Y., T. Lukacsovich, and A. S. Waldman. 1999. Multiple pathways for repair of DNA double-strand breaks in mammalian cells. Mol. Cell. Biol. 19:8353-8360. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. [40]Lin, Y., and A. S. Waldman. 2001. Capture of DNA sequences at double-strand breaks in mammalian cells. Genetics 158:1665-1674. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. [41]Lo, A. W., G. C. Liao, M. Rocchi, and K. H. Choo. 1999. Extreme reduction of chromosome-specific alpha-sattellite array is unusually common in human chromosome 21. Genome Res. 9:895-908. [DOI] [PubMed] [Google Scholar]
  36. [42]Lobachev, K. S., D. A. Gordenin, and M. A. Resnick. 2002. The Mre11 complex is required for repair of hairpin-capped double-strand breaks and prevention of chromosome rearrangements. Cell 108:183-193. [DOI] [PubMed] [Google Scholar]
  37. [43]Ma, C., S. Martin, B. Trask, and J. L. Hamlin. 1993. Sister chromatid fusion initiates amplification of the dihydrofolate reductase gene in Chinese hamster cells. Genes Dev. 7:605-620. [DOI] [PubMed] [Google Scholar]
  38. [44]McClintock, B. 1941. The stability of broken ends of chromosomes in Zea mays. Genetics 41:234-282. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. [46]McIlwrath, A. J., P. A. Vasey, G. M. Ross, and R. Brown. 1994. Cell cycle arrests and radiosensitivity of human tumor cell lines: dependence on wild-type p53 for radiosensitivity. Cancer Res. 54:3718-3722. [PubMed] [Google Scholar]
  40. [47]Meltzer, P. S., X.-Y. Guan, and J. M. Trent. 1993. Telomere capture stabilizes chromosome breakage. Nat. Genet. 4:252-255. [DOI] [PubMed] [Google Scholar]
  41. [48]Meuth, M. 1989. Illegitimate recombination in mammalian cells, p. 833-860. In D. E. Berg and M. M. Howe (ed.), Mobile DNA. American Society for Microbiology, Washington, D.C.
  42. [49]Mizuuchi, K., M. Mizuuchi, and M. Gellert. 1982. Cruciform structures in palindromic DNA are favored by DNA supercoiling. J. Mol. Biol. 156:229-243. [DOI] [PubMed] [Google Scholar]
  43. [50]Murata, S., T. Matsuzaki, S. Takai, H. Yaoita, and M. Noda. 1995. A new retroviral vector for detecting mutations and chromosomal instability in mammalian cells. Mutat. Res. 334:375-383. [DOI] [PubMed] [Google Scholar]
  44. [51]Murnane, J. P., L. F. Fuller, and R. B. Painter. 1985. Establishment and characterization of a permanent pSVori−-transformed ataxia-telangiectasia cell line. Exp. Cell Res. 158:119-126. [DOI] [PubMed] [Google Scholar]
  45. [52]Myung, K., C. Chen, and R. D. Kolodner. 2001. Multiple pathways cooperate in the suppression of genome instability in Saccharomyces cerevisiae. Nature 411:1073-1076. [DOI] [PubMed] [Google Scholar]
  46. [53]Myung, K., A. Datta, and R. D. Kolodner. 2001. Suppression of spontaneous chromosomal rearrangements by S phase checkpoint functions in Saccharomyces cerevisiae. Cell 104:397-408. [DOI] [PubMed] [Google Scholar]
  47. [54]O'Toole, C. M., S. Povey, P. Hepburn, and L. M. Franks. 1983. Identity of some human bladder cancer cell lines. Nature 301:429-430. [DOI] [PubMed] [Google Scholar]
  48. [56]Phillips, J. W., and W. F. Morgan. 1994. Illegitimate recombination induced by DNA double-strand breaks in a mammalian chromosome. Mol. Cell. Biol. 14:5794-5803. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. [57]Pipiras, E., A. Coquelle, A. Bieth, and M. Debatisse. 1998. Interstitial deletions and intrachromosomal amplification initiated from a double-strand break targeted to a mammalian chromosome. EMBO J. 17:325-333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. [58]Riboni, R., A. Casati, T. Nardo, E. Zaccaro, L. Ferretti, F. Nuzzo, and C. Mondello. 1997. Telomeric fusions in cultured fibroblasts as a source of genomic instability. Cancer Genet. Cytogenet. 95:130-136. [DOI] [PubMed] [Google Scholar]
  51. [59]Richard, C. W., III, D. A. Withers, T. C. Meeker, S. Maurer, G. A. Evans, R. M. Myers, and D. R. Cox. 1991. A radiation hybrid map of the proximal long arm of human chromosome 11 containing the multiple endocrine neoplasia type 1 (MEN-1) and bcl-1 disease loci. Am. J. Hum. Genet. 49:1189-1196. [PMC free article] [PubMed] [Google Scholar]
  52. [60]Richardson, C., and M. Jasin. 2000. Frequent chromosomal translocations induced by DNA double-strand breaks. Nature 405:697-700. [DOI] [PubMed] [Google Scholar]
  53. [61]Richardson, C., M. E. Moynahan, and M. Jasin. 1998. Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations. Genes Dev. 12:3831-3842. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. [62]Robertson, E. J. 1987. Embryo-derived stem cells, p. 71-112. In E. J. Robertson (ed.), Teratocarcinomas and embryonic stem cells: a practical approach. Oxford University Press, Oxford, England.
  55. [63]Roth, D. B., X.-B. Chang, and J. H. Wilson. 1989. Comparison of filler DNA at immune, nonimmune, and oncogenic rearrangements suggests multiple mechanisms of formation. Mol. Cell. Biol. 9:3049-3057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. [64]Roth, D. B., and J. H. Wilson. 1986. Nonhomologous recombination in mammalian cells: role for short sequence homologies in the joining reaction. Mol. Cell. Biol. 6:4295-4304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. [65]Rouet, P., F. Smih, and M. Jasin. 1994. Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease. Mol. Cell. Biol. 14:8096-8106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. [67]Sargent, R. G., M. A. Brenneman, and J. H. Wilson. 1997. Repair of site-specific double-strand breaks in a mammalian chromosome by homologous and illegitimate recombination. Mol. Cell. Biol. 17:267-277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. [68]Schulz, V. P., and V. A. Zakian. 1994. The Saccharomyces PIF1 DNA helicase inhibits telomere elongation and de novo telomere formation. Cell 76:145-155. [DOI] [PubMed] [Google Scholar]
  60. [69]Shuster, M. I., L. Han, M. M. Le Beau, E. Davis, M. Sawicki, C. M. Lese, N. H. Park, J. Colicelli, and S. M. Gollin. 2000. A consistent pattern of RIN1 rearrangements in oral squamous cell carcinoma cell lines supports a breakage-fusion-bridge cycle model for 11q23 amplification. Genes Chromosomes Cancer 28:153-163. [PubMed] [Google Scholar]
  61. [70]Singer, M. J., L. D. Mesner, C. L. Friedman, B. J. Trask, and J. L. Hamlin. 2000. Amplification of the human dihydrofolate reductase gene via double minutes is initiated by chromosome breaks. Proc. Natl. Acad. Sci. USA 97:7921-7926. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. [71]Smith, K. A., M. B. Stark, P. A. Gorman, and G. R. Stark. 1992. Fusions near telomeres occur very early in the amplification of CAD genes in Syrian hamster cells. Proc. Natl. Acad. Sci. USA 89:5427-5431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. [72]Soriano, P., C. Montgomery, R. Geske, and A. Bradley. 1991. Targeted disruption of the c-src proto-oncogene leads to osteoporosis in mice. Cell 64:693-702. [DOI] [PubMed] [Google Scholar]
  64. [73]Sprung, C. N., G. Afshar, E. A. Chavez, P. Lansdorp, L. Sabatier, and J. P. Murnane. 1999. Telomere instability in a human cancer cell line. Mutat. Res. 429:209-223. [DOI] [PubMed] [Google Scholar]
  65. [74]Sprung, C. N., G. E. Reynolds, M. Jasin, and J. P. Murnane. 1999. Chromosome healing in mouse embryonic stem cells. Proc. Natl. Acad. Sci. USA 96:6781-6786. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. [75]Sprung, C. N., L. Sabatier, and J. P. Murnane. 1999. Telomere dynamics in human cancer cell line. Exp. Cell Res. 247:29-37. [DOI] [PubMed] [Google Scholar]
  67. [76]Thomas, K. R., and M. R. Capecchi. 1987. Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 51:503-512. [DOI] [PubMed] [Google Scholar]
  68. [77]Toledo, F., G. Buttin, and M. Debatisse. 1993. The origin of chromosome rearrangements at early stages of AMPD2 gene amplification in Chinese hamster cells. Curr. Biol. 3:255-264. [DOI] [PubMed] [Google Scholar]
  69. [78]Tommerup, H., A. Dousmanis, and T. de Lange. 1994. Unusual chromatin in human telomeres. Mol. Cell. Biol. 14:5777-5785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. [80]Varley, H., S. Di, S. W. Scherer, and N. J. Royle. 2000. Characterization of terminal deletions at 7q32 and 22q13.3 healed by de novo telomere addition. Am. J. Hum. Genet. 67:610-622. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. [81]Waldman, A. S., H. Tran, E. C. Goldsmith, and M. A. Resnick. 1999. Long inverted repeats are an at-risk motif for recombination in mammalian cells. Genetics 153:1873-1883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. [82]Wong, A. C., Y. Ning, J. Flint, K. Clark, J. P. Dumanski, D. H. Ledbetter, and H. E. McDermid. 1997. Molecular characterization of a 130-kb terminal microdeletion at 22q in a child with mild mental retardation. Am. J. Hum. Genet. 60:113-120. [PMC free article] [PubMed] [Google Scholar]
  73. [83]Yu, G., and E. H. Blackburn. 1991. Developmentally programmed healing of chromosomes by telomerase in Tetrahymena. Cell 67:823-832. [DOI] [PubMed] [Google Scholar]
  74. [84]Zijlmans, J. M., U. M. Martens, S. S. S. Poon, A. K. Raap, H. J. Tanke, R. K. Ward, and P. M. Lansdorp. 1997. Telomeres in the mouse have large inter-chromosomal variations in the number of T2AG3 repeats. Proc. Natl. Acad. Sci. USA 94:7423-7428. [DOI] [PMC free article] [PubMed] [Google Scholar]

Cited by

Sorted by citations

Authors
Lo, A. W. I., Sprung, C. N., Fouladi, B., Pedram, M., Sabatier, L., Ricoul, M., Reynolds, G. E., & Murnane, J. P.
Affiliations
  • University of California, San Francisco (US)
  • Commissariat à l'Énergie Atomique et aux Énergies Alternatives (FR)
Corresponding author
Murnane, John P.
ORCID
Venue
Molecular and Cellular Biology
Publisher
Informa UK Limited
Published
2002-07
Volume
22
Issue
13
Pages
4836-4850
ISSN
  • 0270-7306 (ISSN-L)
  • 1098-5549
DOI
10.1128/mcb.22.13.4836-4850.2002
PMC
PMC133890
OpenAlex
W2028452487
Cited by
118
References
9
Citations by year
2025: 1 · 2023: 2 · 2022: 10 · 2021: 2 · 2020: 5 · 2018: 2 · 2017: 3 · 2016: 5 · 2015: 4 · 2014: 3 · 2013: 3 · 2012: 4
FWCI
5.80
Type
journal article
Language
en
Open access
Licence
journals.asm.org/non-commercial-tdm-license (tdm)
Locations
  • Molecular and Cellular Biology (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Cancer Institute (R01CA069044, R01 CA69044)
  • National Institute of Environmental Health Sciences (R01ES008427)
Topics
  • Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
Keywords
chromosomal instability, telomere loss, DNA double-strand breaks, telomeres, mouse embryonic stem cells, I-SceI endonuclease, inverted repeats, tandem duplication, non-homologous end joining, breakage-fusion-bridge cycles, dicentric chromosomes, tumor progression, chromosomal rearrangements
MeSH terms
Animals, Cloning, Molecular, DNA, DNA Damage, Embryo, Mammalian, Female, Genetic Markers, Humans, Male, Mice, Inbred Strains, Molecular Sequence Data, Plasmids, Repetitive Sequences, Nucleic Acid, Stem Cells, Thymidine Kinase, Deoxyribonucleases, Type II Site-Specific, Gene Rearrangement, Telomere, Simplexvirus, Saccharomyces cerevisiae Proteins, Mice

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review