Efficient repair of bleomycin-induced double-strand breaks in barley ribosomal genes

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 601, Issue 1-2, 2006, Pages 179-190

  Manova, Vasilissa ^a   Gecheff, Kostadin ^a   Stoilov, Lubomir ^a  

^a INSTITUTE OF PHYSIOLOGY   (Bulgaria)

Author keywords

Barley; Bleomycin; DSB repair; Ribosomal genes

Indexed keywords

BLEOMYCIN; SPACER DNA;

ANALYTIC METHOD; ARTICLE; BARLEY; COMPARATIVE STUDY; CONTROLLED STUDY; DNA REPAIR; DNA STRAND BREAKAGE; GENE; GENOMICS; NONHUMAN; PRIORITY JOURNAL; RIBOSOME; SENSITIVITY ANALYSIS;

BLEOMYCIN; BLOTTING, SOUTHERN; DNA BREAKS, DOUBLE-STRANDED; DNA BREAKS, SINGLE-STRANDED; DNA DAMAGE; DNA REPAIR; DNA, PLANT; DNA, RIBOSOMAL; DNA, RIBOSOMAL SPACER; GENE EXPRESSION REGULATION, PLANT; HORDEUM; PLANT ROOTS; TIME FACTORS;

HORDEUM VULGARE SUBSP. VULGARE;

EID: 33749534669     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2006.07.004     Document Type: Article

References (84)

1. Pfeiffer P., Goedecke W., and Obe G. Mechanisms of DNA double-strand break repair and their potential to induce chromosomal aberrations. Mutagenesis 15 (2000) 289-302
2. van Gent D.C., Hoeijmakers J.H., and Kanaar R. Chromosomal stability and the DNA double-stranded break connection. Nat. Rev. Genet. 2 (2001) 196-206
3. Boulikas T. Evolutionary consequences of nonrandom damage and repair of chromatin domains. J. Mol. Evol. 35 (1992) 156-180
4. Natarajan A.T., Balajee A.S., Boei J.J.W.A., Chatterjee S., Darroudi F., Grigorova M., Noditi M., Oh H.J., Slijepcevic P., and Vermeulen S. Recent developments in the assessment of chromosomal damage. Int. J. Radiat. Biol. 66 (1994) 615-623
5. Folle G.A., and Obe G. Localization of chromosome breakpoints induced by AluI and BamHI in Chinese hamster ovary (CHO) cells treated in the G1 phase of the cell cycle. Int. J. Radiat. Biol. 68 (1995) 437-445
6. Costa N.D., and Thacker J. Mutations induced by DNA double-strand breaks: the influence of genomic site. Somat. Cell Mol. Genet. 22 (1996) 249-259
7. Ahnström G., Nygren J., and Eriksson S. The effect of sulphoxide on the induction and repair of double-strand breaks in human cells after irradiation with γ-rays and accelerated ions: rapid or slow repair may depend on accessibility of breaks in chromatin of different compactness. Int. J. Radiat. Biol. 76 (2000) 533-538
8. van Zeeland A.A., Mullenders L.H.F., and Vrieling H. Gene and sequence specificity of DNA damage induction and repair: consequences for mutagenesis. Mutat. Res. 485 (2001) 15-21
9. Horvathova E., Dusinska M., Shaposhnikov S., and Collins A.R. DNA damage and repair measured in different genomic regions using the comet assay with fluorescent in situ hybridization. Mutagenesis 19 (2004) 269-276
10. Bohr V.A., Smith C.L., Okumoto D.S., and Hanawalt P.C. DNA repair in an active gene: removal of pyrimidine dimers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell 40 (1985) 359-369
11. Mellon I., Spivak G., and Hanawalt P.C. Selective removal of transcription-blocking DNA damage from the mammalian DHFR gene. Cell 51 (1987) 241-249
12. Bohr V.A., Okumoto D.S., Ho L., and Hanawalt P.C. Characterization of a DNA repair domain containing the dihydrofolate reductase gene in Chinese hamster ovary cells. J. Biol. Chem. 261 (1986) 16666-16672
13. Hu W., Feng Z., Chasin L.A., and Tang M.-S. Transcription-coupled and transcription-independent repair of cyclobutane pyrimidine dimers in the dihydrofolate reductase gene. J. Biol. Chem. 277 (2002) 38305-38310
14. Friedberg E.C. Relationship between DNA repair and transcription. Annu. Rev. Biochem. 65 (1996) 15-42
15. Vrieling H., van Zeeland A.A., and Mullenders L.H.F. Transcription-coupled repair and its impact on mutagenesis. Mutat. Res. 400 (1998) 135-142
16. Svejstrup J.Q. Mechanisms of transcription-coupled DNA repair. Nat. Rev. Mol. Cell. Biol. 3 (2002) 21-29
17. Surralles J., Ramirez M.J., Marcos R., Natarajan A.T., and Mullenders L.H.F. Clusters of transcription-coupled repair in the human genome. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 10571-10574
18. Feng Z., Hu W., Chasin L.A., and Tang M. Effects of genomic context and chromatin structure on transcription-coupled and global genomic repair in mammalian cells. Nucleic Acids Res. 31 (2003) 5897-5906
19. Vos J.-M.H., and Wauthier E.L. Differential introduction of DNA damage and repair in mammalian genes transcribed by RNA polymerases I and II. Mol. Cell. Biol. 11 (1991) 2245-2252
20. Christians F.C., and Hanawalt P.C. Lack of transcription-coupled repair in mammalian ribosomal RNA genes. Biochemistry 32 (1993) 10512-10518
21. Christians F.C., and Hanawalt P.C. Repair in ribosomal RNA genes is deficient in xeroderma pigmentosum group C and in Cockayne's syndrome cells. Mutat. Res. 323 (1994) 179-187
22. Fritz L.K., and Smerdon M.J. Repair of UV damage in actively transcribed ribosomal genes. Biochemistry 34 (1995) 13117-13124
23. Conconi A., Bespalov V.A., and Smerdon M.J. Transcription-coupled repair in RNA polymerase I-transcribed genes of yeast. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 649-654
24. Meier A., Livingstone-Zatchej M., and Thoma F. Repair of active and silenced rDNA in yeast: the contributions of photolyase and transcription-coupled nucleotide excision repair. J. Biol. Chem. 277 (2002) 11845-11852
25. Löbrich M., Ikpeme S., and Kiefer J. DNA double-strand break measurement in mammalian cells by pulsed-field gel electrophoresis: an approach using restriction enzymes and gene probing. Int. J. Radiat. Biol. 65 (1994) 623-630
26. Bunch R.T., Gewirtz D.A., and Povirk L.F. Ionizing radiation-induced DNA strand breakage and rejoining in specific genomic regions as determined by an alkaline unwinding/Southern blotting method. Int. J. Radiat. Biol. 68 (1995) 553-562
27. Löbrich M., Cooper P.K., and Rydberg B. Non-random distribution of DNA double-strand breaks induced by particle irradiation. Int. J. Radiat. Biol. 70 (1996) 493-503
28. Newman H.G., Prise K.M., Folkard M., and Michael B.D. DNA double-strand break distributions in X-ray and α-particle irradiated V79 cells: evidence for non-random breakage. Int. J. Radiat. Biol. 71 (1997) 347-363
29. Rothkamm K., and Löbrich M. Misrejoining of DNA double-strand breaks in primary and transformed human and rodent cells: a comparison between the HPRT region and other genomic locations. Mutat. Res. 433 (1999) 193-205
30. Sak A., and Stuschke M. Repair of ionizing radiation-induced DNA double-strand breaks (dsb) at the c-myc locus in comparison to the overall genome. Int. J. Radiat. Biol. 73 (1998) 35-43
31. May A., and Bohr V.A. Gene-specific repair of γ-ray-induced DNA strand breaks in colon cancer cells: no coupling to transcription and no removal from the mitochondrial genome. Biochem. Biophys. Res. Commun. 269 (2000) 433-437
32. Ljungman M. Repair of radiation-induced DNA strand breaks does not occur preferentially in transcriptionally active DNA. Radiat. Res. 152 (1999) 444-449
33. Fritz L.K., Suquet C., and Smerdon M.J. Strand breaks are repaired efficiently in human ribosomal genes. J. Biol. Chem. 271 (1996) 12972-12976
34. Balajee A.S., May A., and Bohr V.A. DNA repair of pyrimidine dimers and 6-4 photoproducts in the ribosomal DNA. Nucleic Acids Res. 27 (1999) 2511-2520
35. Gecheff K.I., Mirkova V., Dimitrova A., Georgiev S., and Stoilov L. Intrachromosomal mapping of chromatid aberrations induced by restriction endonucleases in barley. Theor. Appl. Genet. 94 (1997) 919-924
36. Stoilov L.M., Mirkova V., and Gecheff K.I. HaeIII induces position-dependent chromosomal breakage in barley (Hordeum vulgare L.). Mutagenesis 15 (2000) 277-279
37. Manova V.I., and Stoilov L.M. Induction and recovery of double-strand breaks in barley ribosomal DNA. DNA Repair 2 (2003) 983-990
38. Gecheff K. Cytogenetic study on a barley translocation line and some conclusions concerning chromosome karyogram designation. Genet. Pl. Breed. 11 (1978) 17-22
39. Gecheff K.I., Chvarleva T., Georgiev S., Wilkes T., and Karp A. Cytological and molecular evidence of deletion of ribosomal RNA genes in chromosome 6 of barley (Hordeum vulgare L.). Genome 37 (1994) 419-425
40. Charles H.C., Buys M., and Osinga J. Selective staining of the same set of nucleolar phosphoproteins by silver and Giemsa. A combined biochemical and cytochemical study on staining NORs. Chromosoma 89 (1984) 387-396
41. Gecheff K.I. Multiple reconstruction of barley karyotype resulting in complete cytological marking of the chromosome complement. Theor. Appl. Genet. 78 (1989) 683-688
42. Rogers S.O., and Bendich A.J. Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues. Plant Mol. Biol. 5 (1985) 69-76
43. 6-methylguanine in recombination hot spots of plant chromosomes. Env. Mol. Mutagen. 29 (1997) 394-399
44. Sutherland B.M., Bennett P.V., and Sutherland J.C. DNA damage quantitation by alkaline gel electrophoresis. In: Henderson D.S. (Ed). Methods Mol. Biol., vol. 113: DNA Repair Protocols: Eukaryotic Systems (1999), Humana Press Inc., Totowa 183-202
45. Sutherland B.M., Bennett P.V., Georgakilas A.G., and Sutherland J.C. Evaluation of number average length analysis in quantifying double strand breaks in genomic DNAs. Biochemistry 42 (2003) 3375-3384
46. Ananiev E. Nuclear genome structure and organization. In: Shewry P.R. (Ed). Barley Genetics, Biochemistry, Molecular Biology and Biotechnology (1992), CAB International 133-150
47. Subrahmanyam N.C., Bryngelsson T., Hagberg P., and Hagberg A. Differential amplification of rDNA repeats in barley translocation and duplication lines. Role of specific segments. Hereditas 121 (1994) 157-170
48. Ananiev E.V., Bochkanov S.S., Ryzhyc M.V., Sonina N.V., Chernyshev A.I., Shchypkova N.I., and Yakovleva E.U. Characterization of the cloned repeated DNA sequences from the barley genome. Genetika (Rus.) 22 (1986) 920-928
49. Vershinin A.V., and Heslop-Harrison J.S. Comparative analysis of the nucleosomal structure of rye, wheat and their relatives. Plant Mol. Biol. 36 (1998) 149-161
50. Philipps G., and Gigot C. DNA associated with nucleosomes in plants. Nucleic Acids Res. 4 (1977) 3617-3626
51. Chen J., and Stubbe J.A. Bleomycins: towards better therapeutics. Nat. Rev. Cancer 5 (2005) 102-112
52. Povirk L.F., and Finley Austin M.J. Genotoxicity of bleomycin. Mutat. Res. 257 (1991) 127-143
53. Povirk L.F. DNA damage and mutagenesis by radiomimetic DNA-cleaving agents: bleomycin, neocarzinostatin and other enediynes. Mutat. Res. 355 (1996) 71-89
54. Cheong N., and Iliakis G. In vitro rejoining of double strand breaks induced in cellular DNA by bleomycin and restriction endonucleases. Int. J. Radiat. Biol. 71 (1997) 365-375
55. Pastwa E., Neumann R.D., Mezhevaya K., and Winters T.A. Repair of radiation-induced DNA double-strand breaks is dependent upon radiation quality and the structural complexity of double-strand breaks. Radiat. Res. 159 (2003) 251-261
56. Kuo M.T. Preferential damage of active chromatin by bleomycin. Cancer Res. 41 (1981) 2439-2443
57. Bianchi N.O., Bianchi M.S., Lopez-Larraza D., Alitalo K., and de la Chapelle A. Damage and repair induced by bleomycin in the domain of human amplified MYC oncogenes. Cancer Res. 50 (1990) 2379-2384
58. Bennett R.A., Swerdlow P.S., and Povirk L.F. Spontaneous cleavage of bleomycin-induced abasic sites in chromatin and their mutagenisity in mammalian shuttle vectors. Biochemistry 32 (1993) 3188-3195
59. Kuo M.T., and Hsu T.C. Biochemical and cytological studies of bleomycin actions on chromatin and chromosomes. Chromosoma 68 (1978) 229-2240
60. Moore C.W., Jones C.S., and Wall L.A. Growth phase dependency of chromatin cleavage and degradation by bleomycin. Antimicrob. Agents Chemother. 33 (1989) 1592-1599
61. Lopez-Larraza D.M., and Bianchi N.O. DNA response to bleomycin in mammalian cells with variable degrees of chromatin condensation. Env. Mol. Mutagen. 21 (1993) 258-264
62. Heindorff K., Rieger R., Michaelis A., and Takehisa S. Clastogenic adaptation triggered by S-phase-independent clastogens in Vicia faba. Mutat. Res. 190 (1987) 131-136
63. Angelis K.J., Veleminsky J., Rieger R., and Schubert I. Repair of bleomycin-induced DNA double-strand breaks in Vicia faba. Mutat. Res. 212 (1989) 155-157
64. Menke M., Chen I.-P., Angelis K.J., and Schubert I. DNA damage and repair in Arabidopsis thaliana as measured by the comet assay after treatment with different classes of genotoxins. Mutat. Res. 493 (2001) 87-93
65. Smith B.L., Bauer G.B., and Povirk L.F. DNA damage induced by bleomycin, neocarzinostatin, and melphalan in a precisely positioned nucleosome. J. Biol. Chem. 269 (1994) 30587-30594
66. Beckmann R.P., Agostino M.G., McHugh M.M., Sigmund R.D., and Beerman T.A. Assessment of preferential cleavage of an actively transcribed retroviral hybrid gene in murine cells by deoxyribonuclease I, bleomycin, neocarzinostatin, or ionizing radiation. Biochemistry 26 (1987) 5409-5415
67. Tounekti O., Pron G., Belehradek Jr. J., and Mir L.M. Bleomycin, an apoptosis-mimetic drug that induces two types of cell death depending on the number of molecules internalized. Cancer Res. 53 (1993) 5462-5469
68. Tounekti O., Belehradek Jr. J., and Mir L.M. Bleomycin is an antineoplastic agent capable of mimicking apoptosis. Bull. Cancer 81 (1994) 1043-1049
69. Iqbal Z.M., Kohn K.W., Ewig R.A., and Fornace Jr. A.J. Single-strand scission and repair of DNA in mammalian cells by bleomycin. Cancer Res. 36 (1976) 3834-3838
70. Conconi A., Sogo J.M., and Ryan C.A. Ribosomal gene clusters are uniquely proportioned between open and closed chromatin structures in both tomato leaf cells and exponentially growing suspension cultures. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 5256-5260
71. Iwano M., Che F.S., Takayama S., Fukui K., and Isogai A. Three-dimensional architecture of ribosomal DNA within barley nucleoli revealed with electron microscopy. Scanning 25 (2003) 257-263
72. Conconi A., Widmer R.M., Koller T., and Sogo J.M. Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle. Cell 57 (1989) 753-761
73. Chubb J.R., Boyle S., Perry P., and Bickmore W.A. Chromatin motion is constrained by association with nuclear compartments in human cells. Curr. Biol. 12 (2002) 439-445
74. Rief N., and Löbrich M. Efficient rejoining of radiation-induced DNA double-strand breaks in centromeric DNA of human cells. J. Biol. Chem. 277 (2002) 20572-20582
75. Verhage R.A., van de Putte P., and Brouwer J. Repair of rDNA in Saccharomyces cerevisiae: RAD4-independendent strand-specific nucleotide excision repair of RNA polymerase I transcribed genes. Nucleic Acids Res. 24 (1996) 1020-1025
76. Tamura K., Adachi K., Oguchi K., and Takahashi H. Identification of Ku70 and Ku80 homologues in Arabidopsis thaliana: evidence for a role in the repair of DNA double-strand breaks. Plant J. 29 (2002) 771-781
77. West C.E., Waterworth W.M., Story G.W., Sunderland P.A., Jiang Q., and Bray C.M. Disruption of the Arabidopsis AtKu80 gene demonstrates an essential role for AtKu80 protein in efficient repair of DNA double-strand breaks in vivo. Plant J. 31 (2002) 517-528
78. Ozenberger B.A., and Roeder S.G. A unique pathway of double-strand break repair operates in tandemly repeated genes. Mol. Cell. Biol. 11 (1991) 1222-1231
79. Schuermann D., Molinier J., Fritsch O., and Hohn B. The dual nature of homologous recombination in plants. Trends Genet. 21 (2005) 172-181
80. Papazova N., Chvarleva T., Atanassov A., and Gecheff K. The role of cytosine methylation for rRNA gene expression in reconstructed karyotypes of barley. Biotech. Biotechnol. Eq. 15 (2001) 35-44
81. Allard R.W., Saghai Maroof M.A., Zhang Q., and Jorgensen R.A. Genetic and molecular organization of ribosomal DNA (rDNA) variants in wild and cultivated barley. Genetics 126 (1990) 743-751
82. Vinsentz M., and Flavell R.B. Mapping of ribosomal RNA transcripts in wheat. Plant Cell 1 (1989) 579-589
83. Thompson W.F., and Flavell R.B. DNase I sensitivity of ribosomal RNA genes in chromatin and nucleolar dominance in wheat. J. Mol. Biol. 204 (1988) 535-548
84. Abdulova G., and Ananiev E.D. DNase I hypersensitivity sites within the intergenic spacer of rRNA genes of Cucurbita pepo L. (Zucchini). Compt. Rend. Bulg. Acad. Sci. 56 (2003) 65-70