The mutagenic potential of a single DNA double-strand break in a mammalian chromosome is not influenced by transcription

DNA Repair

Volumn 2, Issue 10, 2003, Pages 1147-1156

  Allen, Chris ^a   Miller, Cheryl A ^a   Nickoloff, Jac A ^a  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

Author keywords

Genome stability; Homologous recombination; Non homologous end joining

Indexed keywords

DEXAMETHASONE; DOUBLE STRANDED DNA; I SCEI NUCLEASE; NUCLEASE; REPETITIVE DNA; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; DNA; MEMBRANE PROTEIN; MTVR2 PROTEIN, MOUSE; VIRUS RECEPTOR;

ARTICLE; CHROMOSOME; CONTROLLED STUDY; DNA REPAIR; DNA STRAND BREAKAGE; GENE DELETION; GENE EXPRESSION; GENE FREQUENCY; GENE INSERTION; GENE ISOLATION; GENETIC TRANSCRIPTION; HOMOLOGOUS RECOMBINATION; KARYOTYPE; MAMMAL; MOUSE MAMMARY TUMOR ONCOVIRUS; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; SEQUENCE HOMOLOGY; TRANSCRIPTION REGULATION; ANIMAL; CELL DIVISION; CHO CELL; DNA DAMAGE; DRUG EFFECT; GENETIC RECOMBINATION; GENETICS; HAMSTER; MOUSE; MUTATION; PLASMID;

EUKARYOTA; MAMMALIA; MOUSE MAMMARY TUMOR VIRUS;

ANIMALS; CELL DIVISION; CHO CELLS; CHROMOSOMES, MAMMALIAN; CRICETINAE; DEXAMETHASONE; DNA; DNA DAMAGE; DNA REPAIR; MEMBRANE PROTEINS; MICE; MUTATION; PLASMIDS; RECEPTORS, VIRUS; RECOMBINATION, GENETIC; TRANSCRIPTION, GENETIC;

EID: 2542456982     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1568-7864(03)00139-3     Document Type: Article

References (65)

1. F. Paques, J.E. Haber, Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae, Microbiol. Mol. Biol. Rev. 63 (1999) 349-404.
2. M. Takata, M.S. Sasaki, E. Sonoda, T. Fukushima, C. Morrison, J.S. Abala, S.M.A. Swagemakers, R. Kanaar, L.H. Thompson, S. Takeda, The Rad51 paralog Rad51B promotes homologous recombinational repair, Mol. Cell. Biol. 20 (2000) 6476-6482.
3. M. Takata, M.S. Sasaki, S. Tachiiri, T. Fukushima, E. Sonoda, D. Schild, L.H. Thompson, S. Takeda, Chromosome instability and defective recombinational repair in knockout mutants of the five Rad51 paralogs, Mol. Cell. Biol. 21 (2001) 2858-2866.
4. R.D. Johnson, N. Liu, M. Jasin, Mammalian XRCC2 promotes the repair of DNA double-strand breaks by homologous recombination, Nature 401 (1999) 397-399.
5. A.J. Pierce, R.D. Johnson, L.H. Thompson, M. Jasin, XRCC3 promotes homology-directed repair of DNA damage in mammalian cells, Genes Dev. 13 (1999) 2633-2638.
6. M.A. Brenneman, A.E. Weiss, J.A. Nickoloff, D.J. Chen, XRCC3 is required for efficient repair of chromosome breaks by homologous recombination, Mutat. Res. 459 (2000) 89-97.
7. Y. Yamaguchi-Iwai, E. Sonoda, J.M. Buerstedde, O. Bezzubova, C. Morrison, M. Takata, A. Shinohara, S. Takeda, Homologous recombination, but not DNA repair, is reduced in vertebrate cells deficient in RAD52, Mol. Cell. Biol. 18 (1998) 6430-6435.
8. M.L.G. Dronkert, H.B. Beverloo, R.D. Johnson, J.H.J. Hoeijmakers, M. Jasin, R. Kanaar, Mouse RAD54 affects DNA double-strand break repair and sister chromatid exchange, Mol. Cell. Biol. 20 (2000) 3147-3156.
9. P. Bertrand, D. Rouillard, A. Boulet, C. Levalois, T. Soussi, B.S. Lopez, Increase of spontaneous intrachromosomal homologous recombination in mammalian cells expressing a mutant p53 protein, Oncogene 14 (1997) 1117-1122.
10. K.L. Mekeel, W. Tang, L.A. Kachnic, C.M. Luo, J.S. Defrank, S.N. Powell, Inactivation of p53 results in high-rates of homologous recombination, Oncogene 14 (1997) 1847-1857.
11. M.S. Meyn, High spontaneous intrachromosomal recombination rates in ataxia-telangiectasia, Science 260 (1993) 1327-1330.
12. C. Iftode, Y. Daniely, J.A. Borowiec, Replication protein A (RPA): the eukaryotic SSB, Crit. Rev. Biochem. Mol. Biol. 34 (1999) 141-180.
13. M.E. Moynahan, A.J. Pierce, M. Jasin, BRCA2 is required for homology-directed repair of chromosomal breaks, Mol. Cells 7 (2001) 263-272.
14. M.E. Moynahan, J.W. Chiu, B.H. Koller, M. Jasin, Brcal controls homology-directed DNA repair, Mol. Cells 4 (1999) 511-518.
15. J.H.J. Petrini, R.S. Maser, D.A. Bressan, The MRE11-RAD50 complex: diverse functions in the cellular DNA damage response, in: J.A. Nickoloff, M.F. Hoekstra (Eds.), DNA Damage and Repair: Advances from Phage to Humans, vol. III, Humana Press, Totowa, NJ, 2001.
16. M.A. Brenneman, BRCA1 and BRCA2 in DNA repair and genome stability, in: J.A. Nickoloff, M.F. Hoekstra (Eds.), DNA Damage and Repair: Advances from Phage to Humans, vol. 3, Humana Press, Totowa, NJ, 2001, pp. 237-267.
17. M.A. Brenneman, B.M. Wagener, C.A. Miller, C. Allen, J.A. Nickoloff, XRCC3 controls the fidelity of homologous recombination: roles for XRCC3 in late stages of recombination, Mol. Cells 10 (2002) 387-395.
18. C. Chen, R.D. Kolodner, Gross chromosomal rearrangements in Saccharomyces cerevisiae replication and recombination defective mutants, Nat. Genet. 23 (1999) 81-85.
19. S.P. Jackson, Sensing and repairing DNA double-strand breaks, Carcinogenesis 23 (2002) 687-696.
20. P.A. Jeggo, P. O'Neill, The Greek goddess, Artemis, reveals the secrets of her cleavage, DNA Rep. 1 (2002) 771-777.
21. A.J. Pierce, P. Hu, M.G. Han, N. Ellis, M. Jasin, Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells, Genes Dev. 15 (2001) 3237-3242.
22. C. Allen, A. Kurimasa, M.A. Brennemann, D.J. Chen, J.A. Nickoloff, DNA-dependent protein kinase suppresses double-strand break-induced and spontaneous homologous recombination, Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 3758-3763.
23. S.A. Leadon, P.K. Cooper, Preferential repair of ionizing radiation-induced damage in the transcribed strand of an active human gene is defective in Cockayne syndrome, Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 10499-10503.
24. S.A. Leadon, D.A. Lawrence, Preferential repair of DNA damage on the transcribed strand of the human metallothionein genes requires RNA polymerase II, Mutat. Res. 255 (1991) 67-78.
25. I. Mellon, P.C. Hanawalt, Induction of the Escherichia coli lactose operon selectively increases repair of its transcribed DNA strand, Nature 342 (1989) 95-98.
26. I. Mellon, G. Spivak, P.C. Hanawalt, Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene, Cell 51 (1987) 241-249.
27. P.C. Hanawalt, Heterogeneity of DNA repair at the gene level, Mutat. Res. 247 (1991) 203-211.
28. P.C. Hanawalt, DNA repair comes of age, Mutat. Res. 336 (1995) 101-113.
29. J.Q. Svejstrup, Mechanisms of transcription-coupled DNA repair, Nat. Rev. Mol. Cell Biol. 3 (2002) 21-29.
30. R.L. Keil, G.S. Roeder, cis-Acting, recombination-stimulating activity in fragment of the ribosomal DNA of S. cerevisiae, Cell 39 (1984) 377-386.
31. S.E. Stewart, G.S. Roeder, Transcription by RNA polymerase I stimulates mitotic recombination in Saccharomyces cerevisiae, Mol. Cell. Biol. 9 (1989) 3464-3472.
32. K. Voelkel-Meiman, G.S. Roeder, Gene conversion tracts stimulated by HOT1-promoted transcription are long and continuous, Genetics 126 (1990) 851-867.
33. K. Voelkel-Meiman, G.S. Roeder, A chromosome containing HOT1 preferentially receives information during mitotic interchromosomal gene conversion, Genetics 124 (1990) 561-572.
34. B.J. Thomas, R. Rothstein, Elevated recombination rates in transcriptionally active DNA, Cell 56 (1989) 619-630.
35. C. Grimm, P. Schaer, P. Munz, J. Kohli, The strong ADH1 promoter stimulates mitotic and meiotic recombination at the ADE6 gene of Schizosaccharomyces pombe, Mol. Cell. Biol. 11 (1991) 289-298.
36. J.A. Nickoloff, Transcription enhances intrachromosomal homologous recombination in mammalian cells, Mol. Cell. Biol. 12 (1992) 5311-5318.
37. J.A. Nickoloff, R.J. Reynolds, Transcription stimulates homologous recombination in mammalian cells, Mol. Cell. Biol. 10 (1990) 4837-4845.
38. A. Aguilera, The connection between transcription and genomic instability, EMBO J. 21 (2002) 195-201.
39. Y.-S. Weng, D. Xing, J.A. Clikeman, J.A. Nickoloff, Transcriptional effects on double-strand break-induced gene conversion tracts, Mutat. Res. 461 (2000) 119-132.
40. D.G. Taghian, J.A. Nickoloff, Chromosomal double-strand breaks induce gene conversion at high frequency in mammalian cells, Mol. Cell. Biol. 17 (1997) 6386-6393.
41. T.C. He, S.B. Zhou, L.T. Dacosta, J. Yu, K.W. Kinzler, B. Vogelstein, A simplified system for generating recombinant adenoviruses, Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 2509-2514.
42. P.M. Kim, C. Allen, B.M. Wagener, Z. Shen, J.A. Nickoloff, Overexpression of human RAD51 and RAD52 reduces double-strand break-induced homologous recombination in mammalian cells, Nucleic Acids Res. 29 (2001) 4352-4360.
43. D.G. Taghian, J.A. Nickoloff, Subcloning strategies and protocols, in: A. Harwood (Ed.), Basic DNA and RNA Protocols, Humana Press, Totowa, NJ, 1996, pp. 221-235.
44. J. Sambrook, E.F. Fritsch, T. Maniatis, Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
45. F. Liang, M.G. Han, P.J. Romanienko, M. Jasin, Homology-directed repair is a major double-strand break repair pathway in mammalian cells, Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 5172-5177.
46. Y. Lin, T. Lukacsovich, A.S. Waldman, Multiple pathways for repair of double-strand breaks in mammalian chromosomes, Mol. Cell. Biol. 19 (1999) 8353-8360.
47. T. Fukushima, M. Takata, C. Morrison, R. Araki, A. Fujimori, M. Abe, K. Tatsumi, M. Jasin, P.K. Dhar, E. Sonoda, T. Chiba, S. Takeda, Genetic analysis of the DNA-dependent protein kinase reveals an inhibitory role of Ku in late S-G(2) phase DNA double-strand break repair, J. Biol. Chem. 276 (2001) 44413-44418.
48. S.E. Lee, R.A. Mitchell, A. Cheng, E.A. Hendrickson, Evidence for DNA-PK-dependent and DNA-PK-independent DNA double-strand break repair pathways in mammalian cells as a function of the cell cycle, Mol. Cell. Biol. 17 (1997) 1425-1433.
49. T.T. Paull, M. Gellert, A mechanistic basis for Mre11-directed DNA joining at microhomologies, Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 6409-6414.
50. E. Feldmann, V. Schmiemann, W. Goedecke, S. Reichenberger, P. Pfeiffer, 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.
51. J.W. Phillips, W.F. Morgan, Illegitimate recombination induced by DNA double-strand breaks in a mammalian chromosome, Mol. Cell. Biol. 14 (1994) 5794-5803.
52. D.B. Roth, J.H. Wilson, Nonhomologous recombination in mammalian cells: role for short sequence homologies in the joining reaction, Mol. Cell. Biol. 6 (1986) 4295-4304.
53. Y.-S. Weng, J. Whelden, L. Gunn, J.A. Nickoloff, Double-strand break-induced gene conversion: examination of tract polarity and products of multiple recombinational repair events, Curr. Genet. 29 (1996) 335-343.
54. J.A. Nickoloff, D.B. Sweetser, J.A. Clikeman, G.J. Khalsa, S.L. Wheeler, Multiple heterologies increase mitotic double-strand break-induced allelic gene conversion tract lengths in yeast, Genetics 153 (1999) 665-679.
55. J.A. Clikeman, G.J. Khalsa, S.L. Barton, J.A. Nickoloff, Homologous recombinational repair of double-strand breaks in yeast is enhanced by MAT heterozygosity through yKu-dependent and -independent mechanisms, Genetics 157 (2001) 579-589.
56. W.P. Deng, J.A. Nickoloff, Preferential repair of UV damage in highly transcribed DNA diminishes UV-induced intrachromosomal recombination in mammalian cells, Mol. Cell. Biol. 14 (1994) 391-399.
57. R. Kanaar, J.H.J. Hoeijmakers, D.C. Vangent, Molecular mechanisms of DNA double-strand break repair, Trends Cell Biol. 8 (1998) 483-489.
58. P. Stankiewicz, J.R. Lupski, Genome architecture, rearrangements and genomic disorders, Trends Genet. 18 (2002) 74-82.
59. P. Pfeiffer, W. Goedecke, G. Obe, Mechanisms of DNA double-strand break repair and their potential to induce chromosomal aberrations, Mutagenesis 15 (2000) 289-302.
60. R.E. Moses, DNA damage processing defects and disease, Annu. Rev. Genom. Hum. Genet. 2 (2001) 41-68.
61. M.J. Difilippantonio, S. Petersen, H.T. Chen, R.E. Johnson, M. Jasin, R. Kanaar, T. Reid, A. Nussenzweig, Evidence for replicative repair of DNA double-strand breaks leading to oncogenic translocation and gene amplification, J. Exp. Med. 196 (2002) 469-480.
62. L. Colleaux, L. d'Auriol, F. Galibert, B. Dujon, Recognition and cleavage site of the intron-encoded omega transposase, Proc. Natl. Acad. Sci. U.S.A. 85 (1988) 6022-6026.
63. H. Nakayama, RecQ family helicases: roles as tumor suppressor proteins, Oncogene 21 (2002) 9008-9021.
64. H. Tauchi, S. Matsuura, J. Kobayashi, S. Sakamoto, K. Komatsu, Nijmegen breakage syndrome gene, NBS1, and molecular links to factors for genome stability, Oncogene 58 (2002) 8967-8980.
65. J.H.J. Petrini, The Mre11 complex and ATM: collaborating to navigate S phase, Curr. Opin. Cell. Biol. 12 (2000) 293-296.