Clusters of S1 nuclease-hypersensitive sites induced in vivo by DNA damage

Molecular and Cellular Biology

Volumn 17, Issue 9, 1997, Pages 5437-5452

  Legault, Jean ^a   Tremblay, Alain ^a   Ramotar, Dindial ^a,c   Mirault, Marc Edouard ^a,b  

^a UNIVERSITÉ LAVAL   (Canada)

^b LAVAL UNIVERSITY   (Canada)

^c MAISONNEUVE ROSEMONT HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; DNA POLYMERASE; ENDONUCLEASE; GYRASE INHIBITOR; MENADIONE; MESYLIC ACID METHYL ESTER; NUCLEASE S1; PLASMID DNA; RUFOCROMOMYCIN; TENIPOSIDE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; DNA STRAND BREAKAGE; DOSE RESPONSE; ESCHERICHIA COLI; GAMMA IRRADIATION; HUMAN; HUMAN CELL; MAMMAL CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; RADIATION EXPOSURE;

ANIMALIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MAMMALIA;

EID: 0030750555     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.9.5437     Document Type: Article

References (83)

1. Adachi, Y., E. Käs, and U. K. Laemmli. 1989. Preferential, cooperative binding of DNA topoisomerase II to scaffold-associated regions. EMBO J. 8:3997-4006.
2. Ames, B. N. 1989. Endogenous DNA damage as related to cancer and aging. Mutat. Res. 214:41-46.
3. Ames, B. N., M. K. Shigenaga, and T. M. Hagen. 1993. Oxidants, antioxidants, and the degenerative diseases of aging. Proc. Natl. Acad. Sci. USA 90:7915-7922.
4. Aruoma, O. I., B. Halliwell, and M. Dizdaroglu. 1989. Iron ion-dependent modification of bases in DNA by the superoxide radical-generating system hypoxanthine/xanthine oxidase. J. Biol. Chem. 264:13024-13028.
5. Birnboim, H. C., and J. J. Jevcak. 1981. Fluorometric method for rapid detection of DNA strand breaks in human white blood cells produced by low doses of radiation. Cancer Res. 41:1889-1892.
6. Bode, J., Y. Kohwi, L. Dickinson, T. Joh, D. Klehr, C. Mielke, and T. Kohwi-Shigematsu. 1992. Biological significance of unwinding capability of nuclear matrix-associating DNAs. Science 225:195-197.
7. Challberg, M. D., and P. T. Englund. 1980. Specific labeling of 3′ termini with T4 DNA polymerase. Methods Enzymol. 65:39-42.
8. Chen, G. L., Y. Yang, T. C. Rowe, B. D. Galligan, K. M. Tewey, and L. F. Liu. 1984. Nonintercalative antitumor drugs interfere with the breakage-reunion reaction of mammalian DNA topoisomerase II. J. Biol. Chem. 259:13560-13566.
9. Ciccarone, V., B. A. Spengler, M. B. Meyers, J. L. Biedler, and R. A. Ross. 1989. Phenotypic diversification in human neuroblastoma cells: expression of distinct neural crest lineages. Cancer Res. 49:219-225.
10. Cockerill, P. N., and W. T. Garrard. 1986. Chromosomal loop anchorage of the kappa immunoglobulin gene occurs next to the enhancer in a region containing topoisomerase II sites. Cell 44:273-282.
11. Cohen, M. S., Y. Chai, B. E. Britigan, W. McKenna, J. Adams, T. Svendsen, K. Bean, D. J. Hassett, and P. F. Sparling. 1987. Role of extracellular iron in the action of the quinone antibiotic streptonigrin: mechanisms of killing and resistance of Neisseria gonorrhoeae. Antimicrob. Agents Chemother. 31:1507-1513.
12. Coquerelle, T., A. Bopp, B. Kessler, and U. Hagen. 1973. Strand breaks and 5′ end-groups of irradiated thymocytes. Int. J. Radiat. Biol. 24:397-404.
13. Demple, B., and L. Harrison. 1994. Repair of oxidative damage to DNA: enzymology and biology. Annu. Rev. Biochem. 63:915-948.
14. Dikomey, E., M. Flentje, and J. Dahm Daphi. 1995. Comparison between the alkaline unwinding technique and neutral filter elution using CHO, V79 and EAT cells. Int. J. Radiat. Biol. 67:269-275.
15. Dizdaroglu, M. 1994. Chemical determination of oxidative DNA damage by gas chromatography-mass spectroscopy. Methods Enzymol. 234:3-16.
16. Dworniczak, B., and M.-E. Mirault. 1987. Structure and expression of a human gene coding for a 71 Kd heat shock "cognate" protein. Nucleic Acids Res. 15:5181-5197.
17. Earnshaw, W. C., B. Halligan, C. A. Cooke, M. M. S. Heck, and L. F. Liu. 1985. Topoisomerase II is a structural component of mitotic chromosome scaffolds. J. Cell Biol. 100:1706-1715.
18. Egan, M. P., and D. Herrick. 1982. The effect of ara-C incorporation on DNA synthesis. Biochem. Pharmacol. 31:2937-2940.
19. Fridovich, I. 1986. Biological effects of the superoxide radical. Arch. Biochem. Biophys. 247:1-11.
20. Friedberg, E. C. 1985. DNA repair. W. H. Freeman & Co., New York, N.Y.
21. Gao, S., R. Drouin, and G. P. Holmquist. 1994. DNA repair rates mapped along the human PGK1 gene at nucleotide resolution. Science 263:1438-1440.
22. Gavrieli, Y., Y. Sherman, and S. A. Ben Sasson. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:493-501.
23. Gorczyca, W., J. Gong, and Z. Darzynkiewicz. 1993. Detection of DNA strand breaks in individual apoptotic cells by the in situ terminal deoxynucleotidyl transferase and nick translation assays. Cancer Res. 53:1945-1951.
24. Gromova, I. I., O. F. Nielsen, and S. V. Razin. 1995. Long-range fragmentation of the eukaryotic genome by exogenous and endogenous nucleases proceeds in a specific fashion via preferential DNA cleavage at matrix attachment sites. J. Biol. Chem. 270:18685-18690.
25. Halliwell, B., and O. I. Aruoma. 1991. DNA damage by oxygen-derived species: its mechanism and measurement in mammalian systems. FEBS Lett. 281:9-19.
26. Hanawalt, P. C., B. A. Donahue, and K. S. Sweden. 1994. Repair and transcription. Collision or collusion? Curr. Biol. 4:518-521.
27. Haring, M., H. Rudiger, B. Demple, S. Boiteux, and B. Epe. 1994. Recognition of oxidized abasic sites by repair endonucleases. Nucleic Acids Res. 22:2010-2015.
28. Hassett, D., B. E. Britigan, T. Svendsen, G. M. Rosen, and M. S. Cohen. 1987. Bacteria form intracellular free radicals in response to paraquat and streptonigrin: demonstration of the potency of hydroxyl radical. J. Biol. Chem. 262:13404-13408.
29. Henner, W. D., S. M. Grunberg, and W. A. Haseltine. 1983. Enzyme action at 3′ termini of ionizing radiation-induced DNA strand breaks. J. Biol. Chem. 258:15198-15205.
30. Henner, W. D., L. O. Rodriguez, S. M. Hecht, and W. Haseltine. 1983. Gamma-ray induced deoxyribonucleic acid strand breaks. J. Biol. Chem. 258:711-713.
31. Holmquist, G. P. 1994. Chromatin self-organization by mutation bias. J. Mol. Evol. 39:436-438.
32. Ide, H., K. Akamatsu, Y. Kimura, K. Michiue, K. Makino, A. Asaeda, Y. Takamori, and K. Kubo. 1993. Synthesis and damage specificity of a novel probe for the detection of abasic sites in DNA. Biochemistry 32:8276-8283.
33. Imlay, J. A., and S. Linn. 1988. DNA damage and oxygen radical toxicity. Science 240:1302-1309.
34. Jayaraman, J., and C. Prives. 1995. Activation of p53 sequence-specific DNA binding by short single strands of DNA requires the p53 C-terminus. Cell 81:1021-1029.
35. Kay, V., and J. Bode. 1994. Binding specificity of a nuclear scaffold: supercoiled, single-stranded, and scaffold-attached-region DNA. Biochemistry 33: 367-374.
36. Koehler, D. R., and P. C. Hanawalt. 1996. Recruitment of damaged DNA to the nuclear matrix in hamster cells following ultraviolet irradiation. Nucleic Acids Res. 24:2877-2884.
37. Kohn, K. W., L. C. Erickson, R. A. G. Ewig, and C. A. Friedman. 1976. Fractionation of DNA from mammalian cells by alkaline elution. Biochemistry 15:4629-4637.
38. Kubo, K., H. Ide, S. S. Wallace, and Y. W. Kow. 1992. A novel, sensitive, and specific assay for abasic sites, the most commonly produced DNA lesion. Biochemistry 31:3703-3708.
39. Laemmli, U. K., E. Käs, L. Poljak, and Y. Adachi. 1992. Scaffold-associated regions: cis-acting determinants of chromatin structural loops and functional domains. Curr. Opin. Genet. Dev. 2:275-285.
40. Lane, D. P. 1992. p53, guardian of the genome. Nature 358:15-16.
41. Lee, S., B. Elenbaas, A. Levine, and J. Griffith. 1995. p53 and its 14 kDa C-terminal domain recognize primary DNA damage in the form of insertion/deletion mismatches. Cell 81:1013-1020.
42. Legault, J. 1995. M.Sc. thesis. Laval University, Quebec City, Canada.
43. Legault, J., A. Tremblay, and M.-E. Mirault. Preferential localization of DNA damage induced by depurination and bleomycin in a plasmid containing a scaffold-associated region. Biochem. Cell Biol., in press.
44. Lennartz, M., T. Coquerelle, A. Bopp, and U. Hagen. 1975. Oxygen - effect on strand breaks and specific end-groups in DNA of irradiated thymocytes. Int. J. Radial. Biol. 27:577-587.
45. Levin, J. D., and B. Demple. 1990. Analysis of class II (hydrolytic) and class I (β-lyase) apurinic/apyrimidinic endonucleases with a synthetic DNA substrate. Nucleic Acids Res. 18:5069-5075.
46. Levin, J. D., A. W. Johnson, and B. Demple. 1988. Homogeneous Escherichia coli endonuclease IV: characterization of an enzyme that recognizes oxidative damage in DNA. J. Biol. Chem. 263:8066-8071.
47. Lindahl, T. 1993. Instability and decay of the primary structure of DNA. Nature 362:709-715.
48. Liu, L. F. 1989. DNA topoisomerase poisons as antitumor drugs. Annu. Rev. Biochem. 58:351-375.
49. Ljungman, M., and P. C. Hanawalt. 1992. Efficient protection against oxidative DNA damage in chromatin. Mol. Carcinog. 5:264-269.
50. Luderus, M. E., J. L. den Blaauwen, O. J. de Smit, D. A. Compton, and R. van Driel. 1994. Binding of matrix attachment regions to lamin polymers involves single-stranded regions and the minor groove. Mol. Cell. Biol. 14:6297-6305.
51. Mecocci, P., U. MacGarvey, A. E. Kaufman, D. Koontz, J. M. Shoffner, D. C. Wallace, and M. F. Beal. 1993. Oxidative damage to mitochondrial DNA shows marked age-dependent increases in human brain. Ann. Neurol. 34: 609-616.
52. Michelotti, G. A., E. F. Michelotti, A. Pullner, R. C. Duncan, D. Eick, and D. Levens. 1996. Multiple single-stranded cis elements are associated with active chromatin of the human c-myc gene in vivo. Mol. Cell. Biol. 16:2656-2669.
53. Miller, S. A., D. D. Dykes, and H. F. Polesky. 1988. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 16:1215.
54. Mirault, M.-E., A. Tremblay, N. Beaudouin, and M. Tremblay. 1991. Over-expression of seleno-glutathione peroxidase by gene transfer enhances the resistance of T47D human breast cells to clastogenic oxidants. J. Biol. Chem. 266:20752-20760.
55. Mirault, M.-E., A. Tremblay, L. Lavoie, M. Tremblay, and N. Beaudoin. 1992. Transgenic expression of glutathione peroxidase in human breast cells: increased resistance to clastogenic oxidants, p. 303-306. In A. J. Jesaitis and E. A. E. Dratz (ed.), The molecular basis of oxidative damage by leukocytes. CRC Press, Boca Raton, Fla.
56. Mirkovitch, J., M.-E. Mirault, and U. K. Laemmli. 1984. Organization of the higher-order chromatin loop: specific DNA attachment sites on nuclear scaffold. Cell 39:223-232.
57. Muller, B. F., D. Paulsen, and W. Deppert. 1996 Specific binding of MAR/SAR DNA-elements by mutant p53. Oncogene 12:1941-1952.
58. Mummenbrauer, T., F. Janus, B. Muller, L. Wiesmuller, W. Deppert, and F. Grosse. 1996. p53 protein exhibits 3′-to-5′ exonuclease activity. Cell 85: 1089-1099.
59. Pfeifer, G. P., R. Drouin, A. D. Riggs, and G. P. Holmquist. 1992. Binding of transcription factors creates hot spots for UV photoproducts in vivo. Mol. Cell. Biol. 12:1798-1804.
60. Pfeifer, G. P., R. Drouin, A. D. Riggs, and G. P. Holmquist. 1991. In vivo mapping of a DNA adduct at nucleotide resolution: detection of pyrimidine (6-4) pyrimidone photoproducts by ligation-mediated polymerase chain reaction. Proc. Natl. Acad. Sci. USA 88:1374-1378.
61. Pfeifer, G. P., and A. D. Riggs. 1991. Chromalin differences between active and inactive X chromosomes revealed by genomic footprinting of permeabilized cells using DNase I and ligation-mediated PCR. Genes Dev. 5:1102-1113.
62. Ramotar, D., and B. Demple. 1993. Enzymes that repair oxidative damage to DNA, p. 165-191. In B. H. O. I. Aruoma (ed.), DNA and free radical. Ellis Horwood, West Sussex, United Kingdom.
63. Rodolfo, C., A. Lanza, S. Tornaletti, G. Fronza, and A. M. Pedrini. 1994. The ultimate carcinogen of 4-nitroquinoline 1-oxide does not react with Z-DNA and hyperreacts with B-Z junctions. Nucleic Acids Res. 22:314-320.
64. Rodriguez, H., R. Drouin, G. P. Holmquist, T. R. O'Connor, S. Boiteux, J. Laval, J. H. Doroshow, and S. A. Akman. 1995. Mapping of copper/hydrogen peroxide-induced DNA damage at nucleotide resolution in human genomic DNA by ligation-mediated polymerase chain reaction. J. Biol. Chem. 270: 17633-17640.
65. Roti Roti, J. L., W. D. Wright, and Y. C. Taylor. 1993. DNA loop structure and radiation response. Adv. Radiat. Biol. 17:227-259.
66. Roychoudhury, R., and R. Wu. 1980. Terminal transferase-catalyzed addition of nucleotides to the 3′ termini of DNA. Methods Enzymol. 65:43-51.
67. Rydberg, B. 1980. Detection of induced DNA strand breaks with improved sensitivity in human cells. Radiat. Res. 81:492-495.
68. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
69. Shapiro, R. 1981. Damage to DNA caused by hydrolysis. Plenum Publishing Corp., New York, N.Y.
70. Singleton, C. K., J. Klysik, S. M. Stirdivant, and R. D. Wells. 1982. Left-handed Z-DNA is induced by supercoiling in physiological ionic conditions. Nature 299:312-316.
71. Sperry, A. O., V. C. Blasquez, and W. T. Garrard. 1989. Dysfunction of chromosomal loop attachment sites: illegitimate recombination linked to matrix association regions and topoisomerase II. Proc. Natl. Acad. Sci. USA 86:5497-5501.
72. Spivak, G., and P. C. Hanawalt. 1996. Fine structure mapping of DNA repair within a 100 kb genomic region in Chinese hamster ovary cells. Mutat. Res. 350:207-216.
73. Stamato, T., and N. Denko. 1990. Asymmetric field inversion gel electrophoresis: a new method for detecting DNA double-strand breaks in mammalian cells. Radiat. Res. 121:196-205.
74. Targa, F. R., S. V. Razin, C. V. de Moura Gallo, and K. Scherrer. 1994. Excision close to matrix attachment regions of the entire chicken alpha-globin gene domain by nuclease S1 and characterization of the framing structures. Proc. Natl. Acad. Sci. USA 91:4422-4426.
75. Thor, H., M. T. Smith, P. Hartzell, G. Bellomo, S. A. Jewell, and S. Orrenius. 1982. The metabolism of menadione (2-methyl-1,4-naphthoquinone) by isolated hepatocytes: a study of the implications of oxidative stress in intact cells. J. Biol. Chem. 257:12419-12425.
76. Tilly, J. L., K. I. Kowalski, A. L. Johnson, and A. J. Hsueh. 1991. Involvement of apoptosis in ovarian follicular atresia and postovulatory regression. Endocrinology 129:2799-2801.
77. Van der Schans, G. P., A. A. W. M. Van Loon, R. H. Groenendijk, and R. A. Baan. 1989. Detection of DNA damage in cells exposed to ionizing radiation by use of anti-single-stranded DNA monoclonal antibody. Int. J. Radiat. Biol. 55:747-760.
78. von Sonntag, C. 1987. The chemical basis of radiation biology, p. 116-166, 221-294. Taylor and Francis, London, United Kingdom.
79. Wallace, S. S. 1988. AP endonucleases and DNA glycosylases that recognize oxidative DNA damage. Environ. Mol. Mutagen. 12:431-477.
80. Weinfeld, M., and G. W. Buchko. 1993. Postlabelling methods for the detection of apurinic sites and radiation-induced DNA damage. IARC Sci. Publ. 124:95-103.
81. 32P-postlabeling assay for apurinic sites in DNA. Biochemistry 29:1737-1743.
82. 32P-postlabeling detection of radiation-induced DNA damage: identification and estimation of thymine glycols and phosphoglycolate termini. Biochemistry 30:1091-1097.
83. Yamashita, Y., S. Kawada, N. Fujii, and H. Nakano. 1990. Induction of mammalian DNA topoisomerase II dependent DNA cleavage by antitumor antibiotic streptonigrin. Cancer Res. 50:5841-5844.