Telomerase-dependent and -independent chromosome healing in mouse embryonic stem cells

DNA Repair

Volumn 7, Issue 8, 2008, Pages 1233-1249

  Gao, Qing ^a   Reynolds, Gloria E ^a   Wilcox, Andrew ^a   Miller, Douglas ^a   Cheung, Peggie ^b   Artandi, Steven E ^b   Murnane, John P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Chromosome fusion; Chromosome healing; Chromosome instability; Telomerase; Telomere

Indexed keywords

TELOMERASE;

ANIMAL CELL; ARTICLE; CHROMOSOMAL INSTABILITY; CHROMOSOME ABERRATION; CHROMOSOME FUSION; CONTROLLED STUDY; DNA STRAND BREAKAGE; EMBRYONIC STEM CELL; GENE REARRANGEMENT; KNOCKOUT MOUSE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TELOMERE; TRANSGENIC MOUSE;

ANIMALS; BASE SEQUENCE; CHROMOSOMES; DNA PRIMERS; EMBRYONIC STEM CELLS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; SEQUENCE HOMOLOGY, NUCLEIC ACID; TELOMERASE;

MAMMALIA;

EID: 46649105250     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2008.04.004     Document Type: Article

References (63)

1. McEachern M.J., Krauskopf A., and Blackburn E.H. Telomeres and their control. Annu. Rev. Genet. 34 (2000) 331-358
2. Blackburn E.H. Switching and signaling at the telomere. Cell 106 (2001) 661-673
3. In: Blackburn E.H., and Greider C.W. (Eds). Telomeres (1995), Cold Spring Harbor Laboratory Press, Plainview, NY
4. de Lange T. Telomere dynamics and genome instability in human cancer. In: Blackburn E.H., and Greider C.W. (Eds). Telomeres (1995), Cold Spring Harbor Press, Plainview, NY 265-293
5. Karlseder J., Smogorzewska A., and de Lange T. Senescence induced by altered telomere state, not telomere loss. Science 295 (2002) 2446-2449
6. d'Adda di Fagagna F.d.A.d., Reaper P.M., Clay-Farrace L., Fiegler H., Carr P., von Zglinicki T., Saretzki G., Carter N.P., and Jackson S.P. A DNA damage checkpoint response in telomere-initiated senescence. Nature 426 (2003) 194-198
7. Herbig U., Jobling W.A., Chen B.P., Chen D.J., and Sedivy J.M. Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21(CIP1), but not p16(INK4a). Mol. Cell 14 (2004) 501-513
8. Counter C.M., Avilion A.A., LeFeuvre C.E., Stewart N.G., Greider C.W., Harley C.B., and Bacchetti S. Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J. 11 (1992) 1921-1929
9. Harley C.B. Telomeres and aging. In: Blackburn E.H., and Greider C.W. (Eds). Telomeres (1995), Cold Spring Harbor Laboratory Press, Cold Spring Harbor 247-263
10. Shay J.W., and Wrigh W.E. Senescence and immortalization: role of telomeres and telomerase. Carcinogenesis 26 (2005) 867-874
11. Reddel R.R. Alternative lengthening of telomeres, telomerase, and cancer. Cancer Lett. 194 (2003) 155-162
12. Hackett J.A., and Greider C.W. End resection initiates genomic instability in the absence of telomerase. Mol. Cell Biol. 23 (2003) 8450-8461
13. Lo A.W.I., Sprung C.N., Fouladi B., Pedram M., Sabatier L., Ricoul M., Reynolds G.E., and Murnane J.P. Chromosome instability as a result of double-strand breaks near telomeres in mouse embryonic stem cells. Mol. Cell Biol. 22 (2002) 4836-4850
14. Fouladi B., Miller D., Sabatier L., and Murnane J.P. The relationship between spontaneous telomere loss and chromosome instability in a human tumor cell line. Neoplasia 2 (2000) 540-554
15. Lo A.W.I., Sabatier L., Fouladi B., Pottier G., Ricoul M., and Murnane J.P. DNA amplification by breakage/fusion/bridge cycles initiated by spontaneous telomere loss in a human cancer cell line. Neoplasia 6 (2002) 531-538
16. Murnane J.P. Telomeres and chromosome instability. DNA Repair (Amst.) 5 (2006) 1082-1092
17. Ingvarsson S. Molecular genetics of breast cancer progression. Sem. Cancer Biol. 9 (1999) 277-288
18. Schwab M. Oncogene amplification in solid tumors. Sem. Cancer Biol. 9 (1999) 319-325
19. Diede S.J., and Gottschling D.E. Telomerase-mediated telomere addition in vivo requires DNA primase and DNA polymerase α and δ. Cell 99 (1999) 723-733
20. Yu G., and Blackburn E.H. Developmentally programmed healing of chromosomes by telomerase in Tetrahymena. Cell 67 (1991) 823-832
21. Zhou J.-Q., Monson E.K., Teng S.-C., Schultz V.P., and Zakian V.A. Pif1p helicase, a catalytic inhibitor of telomerase in yeast. Science 289 (2000) 771-774
22. Varley H., Di S., Scherer S.W., and Royle N.J. Characterization of terminal deletions at 7q32 and 22q13.3 healed by de novo telomere addition. Am. J. Hum. Genet. 67 (2000) 610-622
23. Wong A.C., Ning Y., Flint J., Clark K., Dumanski J.P., Ledbetter D.H., and McDermid H.E. Molecular characterization of a 130-kb terminal microdeletion at 22q in a child with mild mental retardation. Am. J. Hum. Genet. 60 (1997) 113-120
24. Flint J., Thomas K., Micklem G., Raynham H., Clark K., Doggett N.A., King A., and Higgs D.R. The relationship between chromosome structure and function at a human telomeric region. Nat. Genet. 15 (1997) 252-257
25. Morin G.B. Recognition of a chromosome truncation site associated with α-thalassaimia by human telomerase. Nature 353 (1991) 454-456
26. Honma M., Sakuraba M., Koizumi T., Takashima Y., Sakamoto H., and Hayashi M. Non-homologous end-joining for repairing I-SceI-induced DNA double strand breaks in human cells. DNA Repair (Amst.) 6 (2007) 781-788
27. Lin Y., and Waldman A.S. Capture of DNA sequences at double-strand breaks in mammalian cells. Genetics 158 (2001) 1665-1674
28. Rebuzzini P., Khoriauli L., Azzalin C.M., Magnani E., Mondello C., and Giulotto E. New mammalian cellular systems to study mutations introduced at the break site by non-homologous end-joining. DNA Repair (Amst.) 4 (2005) 546-555
29. Sargent R.G., Brenneman M.A., and Wilson J.H. Repair of site-specific double-strand breaks in a mammalian chromosome by homologous and illegitimate recombination. Mol. Cell Biol. 17 (1997) 267-277
30. Latre L., Genesca A., Martin M., Ribas M., Egozcue J., Blasco M.A., and Tusell L. Repair of DNA broken ends is similar in embryonic fibroblasts with and without telomerase. Radiat. Res. 162 (2004) 136-142
31. Sprung C.N., Reynolds G.E., Jasin M., and Murnane J.P. Chromosome healing in mouse embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 6781-6786
32. Murnane J.P., and Yu L.-C. Acquisition of telomere repeat sequences by transfected DNA integrated at the site of a chromosome break. Mol. Cell Biol. 13 (1993) 977-983
33. Murnane J.P., Sabatier L., Marder B.A., and Morgan W.F. Telomere dynamics in an immortal human cell line. EMBO J. 13 (1994) 4953-4962
34. Ricchetti M., Dujon B., and Fairhead C. Distance from the chromosome end determines the efficiency of double-strand break repair in subtelomeres of haploid yeast. J. Mol. Biol. 328 (2003) 847-862
35. Michelson R.J., Rosenstein S., and Weinert T. A telomeric repeat sequence adjacent to a DNA double-stranded break produces an anticheckpoint. Genes Dev. 19 (2005) 2546-2559
36. Karlseder J., Hoke K., Mirzoeva O.K., Bakkenist C., Kastan M.B., Petrini J.H., and de Lange T. The telomeric protein TRF2 binds the ATM kinase and can inhibit the ATM-dependent DNA damage response. PLoS Biol. 2 (2004) E240
37. Gao Q., Reynolds G.E., Innes L., Pedram M., Jones E., Junabi M., Gao D.-W., Ricoule M., Sabatier L., Van Brocklin H., Franc B.L., and Murnane J.P. Telomeric transgenes are silenced in adult mouse tissues and embryo fibroblasts, but are expressed in embryonic stem cells. Stem Cells 25 (2007) 3085-3092
38. Pedram M., Sprung C.N., Gao Q., Lo A.W.I., Reynolds G., and Murnane J.P. Telomere position effect and silencing of transgenes near telomeres in the mouse. Mol. Cell Biol. 26 (2006) 1865-1878
39. Nagy A., Gertsenstein M., Vinersten K., and Behringer R. Manipulating the Mouse Embryo: A Laboratory Manual (2003), Cold Spring Harbor Laboratory Press
40. Richardson C., Moynahan M.E., and Jasin M. Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations. Genes Dev. 12 (1998) 3831-3842
41. Brisebois J.J., and DuBow M.S. 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 (1993) 191-205
42. Murata S., Matsuzaki T., Takai S., Yaoita H., and Noda M. A new retroviral vector for detecting mutations and chromosomal instability in mammalian cells. Mutat. Res. 334 (1995) 375-383
43. Bai Y., and Murnane J.P. Telomere instability in a human tumor cell line expressing the NBS1 gene with mutations at sites phosphorylated by the ATM protein. Mol. Cancer Res. 1 (2003) 1058-1069
44. Poon S.S., and Lansdorp P.M. Measurements of telomere length on individual chromosomes by image cytometry. Methods Cell Biol. 64 (2001) 69-96
45. Johnson R.D., and Jasin M. Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells. EMBO J. 19 (2000) 3398-3407
46. 3 repeats. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 7423-7428
47. Niida H., Shinkai Y., Hande M.P., Matsumoto T., Takehara S., Tachibana M., Oshimura M., Lansdorp P.M., and Furuichi Y. Telomere maintenance in telomerase-deficient mouse embryonic stem cells: characterization of an amplified telomeric DNA. Mol. Cell Biol. 20 (2000) 4115-4127
48. Prowse K.R., and Greider C.W. Development and tissue-specific regulation of mouse telomerase and telomere length. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 4818-4822
49. Capper R., Britt-Compton B., Tankimanova M., Rowson J., Letsolo B., Man S., Haughton M., and Baird D.M. The nature of telomere fusion and a definition of the critical telomere length in human cells. Genes Dev. 21 (2007) 2495-2508
50. Hande P., Samper E., Lansdorp P., and Blasco M.A. Telomere length dynamics and chromosomal instability in cells derived from telomerase null mice. J. Cell Biol. 144 (1999) 589-601
51. Lieber M.R., Ma Y., Pannicke U., and Schwarz K. Mechanism and regulation of human non-homologous DNA end-joining. Nat. Rev. Mol. Cell Biol. 4 (2003) 712-720
52. Feldmann E., Schmiemann V., Goedecke W., Reichenberger S., and Pfeiffer P. DNA double-strand break repair in cell-free extracts from Ku80-deficient cells: implications for Ku serving as an alignment factor in non-homologous DNA end joining. Nucleic Acids Res. 28 (2000) 2585-2596
53. Prowse K.R., Avilion A.A., and Greider C.W. Identification of a nonprocessive telomerase activity from mouse cells. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 1493-1497
54. Liu Y., Kha H., Ungrin M., Robinson M.O., and Harrington L. Preferential maintenance of critically short telomeres in mammalian cells heterozygous for mTert. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 3597-3602
55. Erdmann N., Liu Y., and Harrington L. Distinct dosage requirements for the maintenance of long and short telomeres in mTert heterozygous mice. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 6080-6085
56. Harrington L. Making the most of a little: dosage effects in eukaryotic telomere length maintenance. Chromosome Res. 13 (2005) 493-504
57. Slijepcevic P., and Bryant P.E. Chromosome healing, telomere capture and mechanisms of radiation-induced chromosome breakage. Int. J. Radiat. Biol. 73 (1998) 1-13
58. Blasco M.A. Telomeres and human disease: ageing, cancer and beyond. Nat. Rev. Genet. 6 (2005) 611-622
59. Artandi S.E., Chang S., Lee S.-L., Alson S., Gottlieb G.J., Chin L., and DePinho R.A. Telomere dysfunction promotes non-reciprocal translocations and epithelial cancers in mice. Nature 406 (2000) 641-645
60. Chang S., Khoo C., and DePinho R.A. Modeling chromosomal instability and epithelial carcinogenesis in the telomerase-deficient mouse. Cancer Biol. 11 (2001) 227-238
61. Rudolph K.L., Millard M., Bosenberg M.W., and DePinho R.A. Telomere dysfunction and evolution of intestinal carcinoma in mice and humans. Nat. Genet. 28 (2001) 155-159
62. Gisselsson D., Jonson T., Petersen A., Strombeck B., Dal Cin P., Hoglund M., Mitelman F., Mertens F., and Mandahl N. Telomere dysfunction triggers extensive DNA fragmentation and evolution of complex chromosome abnormalities in human malignant tumors. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 12683-12688
63. Chin K., de Solorzano C.O., Knowles D., Jones A., Chou W., Rodriguez E.G., Kuo W.-L., Ljung B.-M., Chew K., Myambo K., Miranda M., Krig S., Garbe J., Stampfer M., Yaswen P., Gray J.W., and Lockett S. In situ analysis of genome instability in breast cancer. Nat. Genet. 16 (2004) 984-988