Chromatin dynamics during cell cycle mediate conversion of DNA damage into chromatid breaks and affect formation of chromosomal aberrations: Biological and clinical significance

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 711, Issue 1-2, 2011, Pages 174-186

  Terzoudi, Georgia I ^a   Hatzi, Vasiliki I ^a   Donta Bakoyianni, Catherine ^b   Pantelias, Gabriel E ^a  

^a INSTITUTE OF NANOSCIENCE AND NANOTECHNOLOGY   (Greece)

^b UNIVERSITY OF ATHENS   (Greece)

Author keywords

Bystander effects; Chromatid breaks; Chromatin dynamics; Chromosome aberration; DNA damage; PCC

Indexed keywords

CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CHROMOSOME ABERRATION; CHROMOSOME BREAKAGE; CONFORMATIONAL TRANSITION; CYTOGENETICS; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; HISTONE MODIFICATION; HUMAN; LINEAR ENERGY TRANSFER; MITOSIS INHIBITION; NONHUMAN; PREMATURE CHROMOSOME CONDENSATION; PRIORITY JOURNAL; RADIATION EXPOSURE; RADIOSENSITIVITY; REVIEW;

ANIMALS; CELL CYCLE; CHROMATIDS; CHROMATIN; CHROMOSOME ABERRATIONS; DNA DAMAGE; G2 PHASE; HUMANS; MODELS, GENETIC;

EID: 79956221990     PISSN: 00275107     EISSN: 09218262     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2010.12.011     Document Type: Review

References (95)

1. Natarajan A.T. Chromosome aberrations: past, present and future. Mutat. Res. 2002, 504:3-16.
2. Natarajan A.T., Obe G., van Zeeland A.A., Palitti F., Meijers M., Verdegaal-Immerzeel E.A. Molecular mechanisms involved in the production of chromosomal aberrations. II. Utilization of Neurospora endonuclease for the study of aberration production by X-rays in G1 and G2 stages of the cell cycle. Mutat. Res. 1980, 69:293-305.
3. Natarajan A.T., Palitti F. DNA repair and chromosomal alterations. Mutat. Res. 2008, 657:3-7.
4. Natarajan A.T., Berni A., Marimuthu K.M., Palitti F. The type and yield of ionising radiation induced chromosomal aberrations depend on the efficiency of different DSB repair pathways in mammalian cells. Mutat. Res. 2008, 642:80-85.
5. Palitti F. Mechanisms of formation of chromosomal aberrations: insights from studies with DNA repair-deficient cells. Cytogenet. Genome Res. 2004, 104:95-99.
6. Iliakis G. The role of DNA double strand breaks in ionizing radiation-induced killing of eukaryotic cells. Bioessays 1991, 13:641-648.
7. Bryant P.E. Enzymatic restriction of mammalian cell DNA using Pvu II and Bam H1: evidence for the double-strand break origin of chromosomal aberrations. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 1984, 46:57-65.
8. Iliakis G., Wang H., Perrault A.R., Boecker W., Rosidi B., Windhofer F., Wu W., Guan J., Terzoudi G., Pantelias G. Mechanisms of DNA double strand break repair and chromosome aberration formation. Cytogenet. Genome Res. 2004, 104:14-20.
9. Obe G., Johannes C., Ritter S. The number and not the molecular structure of DNA double-strand breaks is more important for the formation of chromosomal aberrations: a hypothesis. Mutat. Res. 2010, 701:3-11.
10. Obe G., Durante M. DNA double strand breaks and chromosomal aberrations. Cytogenet. Genome Res. 2010, 128:8-16.
11. Natarajan A.T., Obe G. Molecular mechanisms involved in the production of chromosomal aberrations. III. Restriction endonucleases. Chromosoma 1984, 90:120-127.
12. Hair J.M., Terzoudi G.I., Hatzi V.I., Lehockey K.A., Srivastava D., Wang W., Pantelias G.E., Georgakilas A.G. BRCA1 role in the mitigation of radiotoxicity and chromosomal instability through repair of clustered DNA lesions. Chem. Biol. Interact. 2010, 188:350-358.
13. Hada M., Georgakilas A.G. Formation of clustered DNA damage after high-LET irradiation: a review. J. Radiat. Res. (Tokyo) 2008, 49:203-210.
14. Ward J.F. The complexity of DNA damage: relevance to biological consequences. Int. J. Radiat. Biol. 1994, 66:427-432.
15. Goodhead D.T. Initial events in the cellular effects of ionizing radiations: clustered damage in DNA. Int. J. Radiat. Biol. 1994, 65:7-17.
16. Sutherland B.M., Bennett P.V., Sidorkina O., Laval J. Clustered damages and total lesions induced in DNA by ionizing radiation: oxidized bases and strand breaks. Biochemistry 2000, 39:8026-8031.
17. Gollapalle E., Wang R., Adetolu R., Tsao D., Francisco D., Sigounas G., Georgakilas A.G. Detection of oxidative clustered DNA lesions in X-irradiated mouse skin tissues and human MCF-7 breast cancer cells. Radiat. Res. 2007, 167:207-216.
18. Ballarini F. From DNA radiation damage to cell death: theoretical approaches. J. Nucleic Acids 2010, 2010:350608.
19. Georgakilas A.G. Processing of DNA damage clusters in human cells: current status of knowledge. Mol. Biosyst. 2008, 4:30-35.
20. Blaisdell J.O., Wallace S.S. Abortive base-excision repair of radiation-induced clustered DNA lesions in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:7426-7430.
21. Nowsheen S., Wukovich R.L., Aziz K., Kalogerinis P.T., Richardson C.C., Panayiotidis M.I., Bonner W.M., Sedelnikova O.A., Georgakilas A.G. Accumulation of oxidatively induced clustered DNA lesions in human tumor tissues. Mutat. Res. 2009, 674:131-136.
22. Redon C.E., Dickey J.S., Nakamura A.J., Kareva I.G., Naf D., Nowsheen S., Kryston T.B., Bonner W.M., Georgakilas A.G., Sedelnikova O.A. Tumors induce complex DNA damage in distant proliferative tissues in vivo. Proc. Natl. Acad. Sci. U.S.A. 2010.
23. Rothkamm K., Kruger I., Thompson L.H., Lobrich M. Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol. Cell Biol. 2003, 23:5706-5715.
24. Kanaar R., Hoeijmakers J.H., van Gent D.C. Molecular mechanisms of DNA double strand break repair. Trends Cell Biol. 1998, 8:483-489.
25. Iliakis G. Backup pathways of NHEJ in cells of higher eukaryotes: cell cycle dependence. Radiother. Oncol. 2009, 92:310-315.
26. Obe G., Johannes C., Schulte-Frohlinde D. DNA double-strand breaks induced by sparsely ionizing radiation and endonucleases as critical lesions for cell death, chromosomal aberrations, mutations and oncogenic transformation. Mutagenesis 1992, 7:3-12.
27. Streffer C. Strong association between cancer and genomic instability. Radiat. Environ. Biophys. 2010, 49:125-131.
28. Taylor A.M. Unrepaired DNA strand breaks in irradiated ataxia telangiectasia lymphocytes suggested from cytogenetic observations. Mutat. Res. 1978, 50:407-418.
29. Natarajan A.T., Meyers M. Chromosomal radiosensitivity of ataxia telangiectasia cells at different cell cycle stages. Hum. Genet. 1979, 52:127-132.
30. Sasaki M.S. Advances in the biophysical and molecular bases of radiation cytogenetics. Int. J. Radiat. Biol. 2009, 85:26-47.
31. Sinha M., Peterson C.L. Chromatin dynamics during repair of chromosomal DNA double-strand breaks. Epigenomics 2009, 1:371-385.
32. Huertas D., Sendra R., Munoz P. Chromatin dynamics coupled to DNA repair. Epigenetics 2009, 4:31-42.
33. Falk M., Lukasova E., Gabrielova B., Ondrej V., Kozubek S. Chromatin dynamics during DSB repair. Biochim. Biophys. Acta 2007, 1773:1534-1545.
34. Jakob B., Splinter J., Durante M., Taucher-Scholz G. Live cell microscopy analysis of radiation-induced DNA double-strand break motion. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:3172-3177.
35. Durante M., Pignalosa D., Jansen J.A., Walboomers X.F., Ritter S. Influence of nuclear geometry on the formation of genetic rearrangements in human cells. Radiat. Res. 2010, 174:20-26.
36. Mosesso P., Palitti F., Pepe G., Pinero J., Bellacima R., Ahnstrom G., Natarajan A.T. Relationship between chromatin structure, DNA damage and repair following X-irradiation of human lymphocytes. Mutat. Res. 2010, 701:86-91.
37. Pandita T.K., Richardson C. Chromatin remodeling finds its place in the DNA double-strand break response. Nucleic Acids Res. 2009, 37:1363-1377.
38. Gotoh E. Visualizing the dynamics of chromosome structure formation coupled with DNA replication. Chromosoma 2007, 116:453-462.
39. Magnander K., Hultborn R., Claesson K., Elmroth K. Clustered DNA damage in irradiated human diploid fibroblasts: influence of chromatin organization. Radiat. Res. 2010, 173:272-282.
40. Pantelias G.E., Terzoudi G.I. Functional cell-cycle chromatin conformation changes in the presence of DNA damage result into chromatid breaks: a new insight in the formation of radiation-induced chromosomal aberrations based on the direct observation of interphase chromatin. Mutat. Res. 2010, 701:27-37.
41. Pantelias G.E. Radiation-induced cytogenetic damage in relation to changes in interphase chromosome conformation. Radiat. Res. 1986, 105:341-350.
42. Terzoudi G.I., Manola K.N., Pantelias G.E., Iliakis G. Checkpoint abrogation in G2 compromises repair of chromosomal breaks in ataxia telangiectasia cells. Cancer Res. 2005, 65(24).
43. Terzoudi G.I., Jung T., Hain J., Vrouvas J., Margaritis K., Donta-Bakoyianni C., Makropoulos V., Angelakis P., Pantelias G.E. Increased G2 chromosomal radiosensitivity in cancer patients: the role of cdk1/cyclin-B activity level in the mechanisms involved. Int. J. Radiat. Biol. 2000, 76:607-615.
44. Terzoudi G.I., Pantelias G.E. Conversion of DNA damage into chromosome damage in response to cell cycle regulation of chromatin condensation after irradiation. Mutagenesis 1997, 12:271-276.
45. Terzoudi G.I., Manola K.N., Pantelias G.E., Iliakis G. Checkpoint abrogation in G2 compromises repair of chromosomal breaks in ataxia telangiectasia cells. Cancer Res. 2005, 65:11292-11296.
46. Terzoudi G.I., Hatzi V.I., Barszczewska K., Manola K.N., Stavropoulou C., Angelakis P., Pantelias G.E. G2-checkpoint abrogation in irradiated lymphocytes: a new cytogenetic approach to assess individual radiosensitivity and predisposition to cancer. Int. J. Oncol. 2009, 35:1223-1230.
47. Terzoudi G.I., Donta-Bakoyianni C., Iliakis G., Pantelias G.E. Investigation of bystander effects in hybrid cells by means of cell fusion and premature chromosome condensation induction. Radiat. Res. 2010, 173:789-801.
48. Vral A., Thierens H., Baeyens A., DeRidder L. Induction and disappearance of G2 chromatid breaks in lymphocytes after low doses of low-LET gamma-rays and high-LET fast neutrons. Int. J. Radiat. Biol. 2002, 78:249-257.
49. Vral A., Thierens H., Baeyens A., De Ridder L. The micronucleus and G2-phase assays for human blood lymphocytes as biomarkers of individual sensitivity to ionizing radiation: limitations imposed by intraindividual variability. Radiat. Res. 2002, 157:472-477.
50. Scott D., Barber J.B., Spreadborough A.R., Burrill W., Roberts S.A. Increased chromosomal radiosensitivity in breast cancer patients: a comparison of two assays. Int. J. Radiat. Biol. 1999, 75:1-10.
51. Barquinero J.F., Barrios L., Ribas M., Egozcue J., Caballin M.R. Cytogenetic sensitivity of three Fanconi anemia heterozygotes to bleomycin and ionizing radiation. Cancer Genet. Cytogenet. 2001, 124:80-83.
52. Sax K. Chromosome aberrations induced by X-rays. Genetics 1938, 23:494-516.
53. Revell S.H. The accurate estimation of chromatid breakage, and its relevance to a new interpretation of chromatid aberrations induced by ionizing radiations. Proc. R. Soc. Lond. B Biol. Sci. 1959, 150:563-589.
54. Bryant P.E. The signal model: a possible explanation for the conversion of DNA double-strand breaks into chromatid breaks. Int. J. Radiat. Biol. 1998, 73:243-251.
55. Bryant P.E., Riches A.C., Terry S.Y. Mechanisms of the formation of radiation-induced chromosomal aberrations. Mutat. Res. 2010, 701:23-26.
56. Sanford K.K., Parshad R., Gantt R., Tarone R.E., Jones G.M., Price F.M. Factors affecting and significance of G2 chromatin radiosensitivity in predisposition to cancer. Int. J. Radiat. Biol. 1989, 55:963-981.
57. Parshad R., Price F.M., Bohr V.A., Cowans K.H., Zujewski J.A., Sanford K.K. Deficient DNA repair capacity, a predisposing factor in breast cancer. Br. J. Cancer 1996, 74:1-5.
58. Harvey A.N., Savage J.R. Investigating the nature of chromatid breaks produced by restriction endonucleases. Int. J. Radiat. Biol. 1997, 71:21-28.
59. Bryant P.E., Slijepcevic P. G2 chromatid aberrations: kinetics and possible mechanisms. Environ. Mol. Mutagen. 1993, 22:250-256.
60. Bryant P.E., Gray L.J., Peresse N. Progress towards understanding the nature of chromatid breakage. Cytogenet. Genome Res. 2004, 104:65-71.
61. MacLeod R.A., Bryant P.E. Similar kinetics of chromatid aberrations in X-irradiated xrs 5 and wild-type Chinese hamster ovary cells. Mutagenesis 1990, 5:407-410.
62. Bender M.A., Griggs H.G., Bedford J.S. Mechanisms of chromosomal aberration production. 3. Chemicals and ionizing radiation. Mutat. Res. 1974, 23:197-212.
63. Foray N., Arlett C.F., Malaise E.P. Dose-rate effect on induction and repair rate of radiation-induced DNA double-strand breaks in a normal and an ataxia telangiectasia human fibroblast cell line. Biochimie 1995, 77:900-905.
64. Mozdarani H., Bryant P.E. Induction and rejoining of chromatid breaks in X-irradiated A-T and normal human G2 fibroblasts. Int. J. Radiat. Biol. 1989, 56:645-650.
65. Bryant P.E. Repair and chromosomal damage. Radiother. Oncol. 2004, 72:251-256.
66. Pantelias G. Factors determining the yields of radiation-induced chromosome aberrations as visualized by means of premeture chromosome condensation in interphase cells. Chromosome Alterations: Origin and Significance 1993, 140-149. Springer-Verlag, Berlin. G. Obe, A.T. Natarajan (Eds.).
67. Folle G.A. Nuclear architecture, chromosome domains and genetic damage. Mutat. Res. 2008, 658:172-183.
68. Pantelias G.E., Maillie H.D. A simple method for premature chromosome condensation induction in primary human and rodent cells using polyethylene glycol. Somat. Cell Genet. 1983, 9:533-547.
69. Pantelias G.E., Maillie H.D. Direct analysis of radiation-induced chromosome fragments and rings in unstimulated human peripheral blood lymphocytes by means of the premature chromosome condensation technique. Mutat. Res. 1985, 149:67-72.
70. Cornforth M.N., Bedford J.S. X-ray-induced breakage and rejoining of human interphase chromosomes. Science 1983, 222:1141-1143.
71. Cornforth M.N., Bedford J.S. A quantitative comparison of potentially lethal damage repair and the rejoining of interphase chromosome breaks in low passage normal human fibroblasts. Radiat. Res. 1987, 111:385-405.
72. Terzoudi G.I., Singh S.K., Pantelias G.E., Iliakis G. Premature chromosome condensation reveals DNA-PK independent pathways of chromosome break repair. Int. J. Oncol. 2008, 33:871-879.
73. Gotoh E., Durante M. Chromosome condensation outside of mitosis: mechanisms and new tools. J. Cell. Physiol. 2006, 209:297-304.
74. Hatzi V.I., Terzoudi G.I., Paraskevopoulou C., Makropoulos V., Matthopoulos D.P., Pantelias G.E. The use of premature chromosome condensation to study in interphase cells the influence of environmental factors on human genetic material. ScientificWorldJournal 2006, 6:1174-1190.
75. Sankaranarayanan K., Natarajan A.T., Mullenders L.H., van Rijn J.L. Effects of pre-treatment with sodium butyrate on the frequencies of X-ray-induced chromosomal aberrations in human peripheral blood lymphocytes. Mutat. Res. 1985, 151:269-274.
76. Nagasawa H., Brogan J.R., Peng Y., Little J.B., Bedford J.S. Some unsolved problems and unresolved issues in radiation cytogenetics: a review and new data on roles of homologous recombination and non-homologous end joining. Mutat. Res. 2010, 701:12-22.
77. Schwartz J.L., Cowan J., Grdina D.J., Weichselbaum R.R. Attenuation of G2-phase cell cycle checkpoint control is associated with increased frequencies of unrejoined chromosome breaks in human tumor cells. Radiat. Res. 1996, 146:139-143.
78. Rodriguez P., Barquinero J.F., Duran A., Caballin M.R., Ribas M., Barrios L. Cells bearing chromosome aberrations lacking one telomere are selectively blocked at the G2/M checkpoint. Mutat. Res. 2009, 670:53-58.
79. Scott D., Spreadborough A.R., Roberts S.A. Less G(2) arrest in irradiated cells of breast cancer patients than in female controls: a contribution to their enhanced chromosomal radiosensitivity?. Int. J. Radiat. Biol. 2003, 79:405-411.
80. Pretazzoli V., Salone B., Bosi A., Olivieri G. Variability of G(2) checkpoint sensitivity to low doses of X-rays (2 cGy): correlation with G(2) chromatid aberrations but not with an adaptive response. Mutagenesis 2000, 15:531-535.
81. Scott D., Spreadborough A., Levine E., Roberts S.A. Genetic predisposition in breast cancer. Lancet 1994, 344:1444.
82. Riches A.C., Bryant P.E., Steel C.M., Gleig A., Robertson A.J., Preece P.E., Thompson A.M. Chromosomal radiosensitivity in G2-phase lymphocytes identifies breast cancer patients with distinctive tumour characteristics. Br. J. Cancer 2001, 85:1157-1161.
83. Baria K., Warren C., Roberts S.A., West C.M., Scott D. Chromosomal radiosensitivity as a marker of predisposition to common cancers?. Br. J. Cancer 2001, 84:892-896.
84. Smart V., Curwen G.B., Whitehouse C.A., Edwards A., Tawn E.J. Chromosomal radiosensitivity: a study of the chromosomal G(2) assay in human blood lymphocytes indicating significant inter-individual variability. Mutat. Res. 2003, 528:105-110.
85. Roberts S.A., Spreadborough A.R., Bulman B., Barber J.B., Evans D.G., Scott D. Heritability of cellular radiosensitivity: a marker of low-penetrance predisposition genes in breast cancer?. Am. J. Hum. Genet. 1999, 65:784-794.
86. Kihlman B.A., Sturelid S., Hartley-Asp B., Nilsson K. The enhancement by caffeine of the frequencies of chromosomal aberrations induced in plant and animal cells by chemical and physical agents. Mutat. Res. 1974, 26:105-122.
87. Natarajan A.T., Obe G., Dulout F.N. The effect of caffeine posttreatment on X-ray-induced chromosomal aberrations in human blood lymphocytes in vitro. Hum. Genet. 1980, 54:183-189.
88. Natarajan A.T., Meijers M., van Zeeland A.A., Simons J.W. Attempts to detect ataxia telangiectasia (AT) heterozygotes by cytogenetical techniques. Cytogenet. Cell Genet. 1982, 33:145-151.
89. Obe G., Pfeiffer P., Savage J.R., Johannes C., Goedecke W., Jeppesen P., Natarajan A.T., Martinez-Lopez W., Folle G.A., Drets M.E. Chromosomal aberrations: formation, identification and distribution. Mutat. Res. 2002, 504:17-36.
90. Cornforth M.N. Perspectives on the formation of radiation-induced exchange aberrations. DNA Repair (Amst) 2006, 5:1182-1191.
91. Bailey S.M., Bedford J.S. Studies on chromosome aberration induction: what can they tell us about DNA repair?. DNA Repair (Amst) 2006, 5:1171-1181.
92. Bryant P.E. Origin of chromosome aberrations: mechanisms. Chromosomal Alterations: Methods, Results and Importance in Human Health 2007, 177-200. Springer-Verlag, Berlin. G. Obe, Vijayalaxmi (Eds.).
93. Natarajan A.T., Obe G. Molecular mechanisms involved in the production of chromosomal aberrations. I. Utilization of Neurospora endonuclease for the study of aberration production in G2 stage of the cell cycle. Mutat. Res. 1978, 52:137-149.
94. Cheng X., Pantelias G.E., Okayasu R., Cheong N., Iliakis G. Mitosis-promoting factor activity of inducer mitotic cells may affect radiation yield of interphase chromosome breaks in the premature chromosome condensation assay. Cancer Res. 1993, 53:5592-5596.
95. Terzoudi G.I., Pantelias G.E. Cytogenetic methods for biodosimetry and risk individualisation after exposure to ionising radiation. Radiat. Prot. Dosimetry 2006, 122:513-520.