Modulation of DNA damage and DNA repair in chromatin.

DNA is packaged in the highly compact and dynamic structure of chromatin in eukaryotic cells. It is generally accepted that DNA processing events in the nucleus, such as transcription, replication, recombination, and repair, are restricted by this packaging. For some processes (e.g., transcription), the chromatin fiber is "preset" in a more open structure to allow access of proteins to specific regions of DNA within this structural hierarchy. These regions contain modified nucleosomes that accommodate a less compact state of chromatin and allow access to specific regions of DNA. DNA repair proteins, however, must access DNA lesions in all structural domains of chromatin after sudden insult to the genome. Damaged DNA must be recognized, removed, and replaced by repair enzymes at all levels of chromatin packaging. Therefore, the modulation of DNA damage and its repair in chromatin is crucial to our understanding of the fate of potential mutagenic and carcinogenic lesions in DNA. In this review, we discuss the modulation of DNA damage and DNA repair by chromatin structure, and the modulation of chromatin structure by these events.

[1]  B. Suter,et al.  RNA polymerase II transcription inhibits DNA repair by photolyase in the transcribed strand of active yeast genes. , 1997, Nucleic acids research.

[2]  K. Powell,et al.  Interference of benzo[a]pyrene diol epoxide‐deoxyguanosine adducts in a GC box with binding of the transcription factor Sp1 , 1996, Molecular carcinogenesis.

[3]  P. Cerutti,et al.  Nucleosomal distribution of thymine photodimers following far- and near-ultraviolet irradiation. , 1982, Biochemical and biophysical research communications.

[4]  P. Hanawalt,et al.  DNA repair mechanisms and their biologic implications in mammalian cells. Report of a NATO advanced research workshop, Fontevraud, France, Oct. 2-7, 1988. , 1990, Journal of the American Academy of Dermatology.

[5]  B. Thrall,et al.  Nucleosome structure modulates benzo[a]pyrenediol epoxide adduct formation. , 1994, Biochemistry.

[6]  E. Wingender,et al.  Modulation of the nucleosome structure by histone acetylation. , 1980, European journal of biochemistry.

[7]  M. Smerdon,et al.  Distribution within chromatin of deoxyribonucleic acid repair synthesis occurring at different times after ultraviolet radiation. , 1980, Biochemistry.

[8]  J. M. Gale,et al.  UV INDUCED (6‐4) PHOTOPRODUCTS ARE DISTRIBUTED DIFFERENTLY THAN CYCLOBUTANE DIMERS IN NUCLEOSOMES , 1990, Photochemistry and photobiology.

[9]  S. Tornaletti,et al.  UV damage and repair mechanisms in mammalian cells , 1996, BioEssays : news and reviews in molecular, cellular and developmental biology.

[10]  Silke Meyer,et al.  Compilation of vertebrate-encoded transcription factors , 1992, Nucleic Acids Res..

[11]  A. Klug,et al.  The structure of an oligo(dA)·oligo(dT) tract and its biological implications , 1987, Nature.

[12]  M. Churchill,et al.  Mapping functional regions of transcription factor TFIIIA , 1988, Molecular and cellular biology.

[13]  A. Huletsky,et al.  The effect of poly(ADP-ribosyl)ation on native and H1-depleted chromatin. A role of poly(ADP-ribosyl)ation on core nucleosome structure. , 1989, The Journal of biological chemistry.

[14]  J. M. Gale,et al.  Photofootprint of nucleosome core DNA in intact chromatin having different structural states. , 1988, Journal of molecular biology.

[15]  J. Pehrson.  Probing the conformation of nucleosome linker DNA in situ with pyrimidine dimer formation. , 1995, The Journal of biological chemistry.

[16]  D. Patel,et al.  CONTRASTING STRUCTURAL IMPACTS INDUCED BY cis‐syn CYCLOBUTANE DIMER AND (6–4) ADDUCT IN DNA DUPLEX DECAMERS: IMPLICATION IN MUTAGENESIS AND REPAIR ACTIVITY , 1995, Photochemistry and photobiology.

[17]  R. Sternglanz,et al.  Nucleosome structural changes during derepression of silent mating-type loci in yeast. , 1993, The Journal of biological chemistry.

[18]  R. Losa,et al.  Psoralen-crosslinking of soluble and of H1-depleted soluble rat liver chromatin. , 1984, Journal of molecular biology.

[19]  M. Smerdon,et al.  Strand-specific modulation of UV photoproducts in 5S rDNA by TFIIIA binding and their effect on TFIIIA complex formation. , 1997, Biochemistry.

[20]  J. M. Gale,et al.  UV-induced pyrimidine dimers and trimethylpsoralen cross-links do not alter chromatin folding in vitro. , 1988, Biochemistry.

[21]  James C. Wang,et al.  Use of light for footprinting DNA in vivo , 1984, Nature.

[22]  I. Jackson,et al.  Domains of the positive transcription factor specific for the Xenopus 5S RNA gene , 1984, Cell.

[23]  R. Gupta,et al.  Transcription, nucleosome stability, and DNA repair in a yeast minichromosome. , 1992, The Journal of biological chemistry.

[24]  Z. Wang,et al.  Selective visualization of gene structure with ultraviolet light. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[25]  R. Lloyd,et al.  T4 Endonuclease V: Perspectives on Catalysis a , 1994, Annals of the New York Academy of Sciences.

[26]  E. Friedberg,et al.  INCREASED LEVELS OF UNSCHEDULED DNA SYNTHESIS IN UV‐IRRADIATED HUMAN FIBROBLASTS PRETREATED WITH SODIUM BUTYRATE , 1982, Photochemistry and photobiology.

[27]  M. Guéron,et al.  Evidence from base-pair kinetics for two types of adenine tract structures in solution: their relation to DNA curvature. , 1988, Biochemistry.

[28]  M. Smerdon,et al.  Stability of nucleosome placement in newly repaired regions of DNA. , 1986, The Journal of biological chemistry.

[29]  M. Broggini,et al.  O6-methylguanine inhibits the binding of transcription factors to DNA. , 1991, Nucleic acids research.

[30]  R. Waters,et al.  Excision repair at the level of the nucleotide in the Saccharomyces cerevisiae MFA2 gene: mapping of where enhanced repair in the transcribed strand begins or ends and identification of only a partial rad16 requisite for repairing upstream control sequences. , 1997, Journal of molecular biology.

[31]  M. Smerdon,et al.  Enhanced DNA repair synthesis in hyperacetylated nucleosomes. , 1989, The Journal of biological chemistry.

[32]  A. Wolffe,et al.  Histone acetylation: chromatin in action. , 1997, Trends in biochemical sciences.

[33]  F. Baudin,et al.  Mutations in 5S DNA and 5S RNA have different effects on the binding of Xenopus transcription factor IIIA. , 1991, Biochemistry.

[34]  P. Hanawalt.  Role of transcription-coupled DNA repair in susceptibility to environmental carcinogenesis. , 1996, Environmental health perspectives.

[35]  R. Reeves,et al.  Sodium butyrate stimulates DNA repair in UV-irradiated normal and xeroderma pigmentosum human fibroblasts. , 1982, The Journal of biological chemistry.

[36]  L. Hurley,et al.  Binding of Sp1 to the 21-bp repeat region of SV40 DNA: effect of intrinsic and drug-induced DNA bending between GC boxes. , 1994, Gene.

[37]  A. Dunker,et al.  Limited nucleosome migration can completely randomize DNA repair patches in intact human cells. , 1987, Journal of molecular biology.

[38]  R. Sternglanz,et al.  Nucleosome fractionation by mercury affinity chromatography. Contrasting distribution of transcriptionally active DNA sequences and acetylated histones in nucleosome fractions of wild-type yeast cells and cells expressing a histone H3 gene altered to encode a cysteine 110 residue. , 1991, The Journal of biological chemistry.

[39]  K. Yarema,et al.  Synthesis and biological activity of DNA damaging agents that form decoy binding sites for the estrogen receptor. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[40]  M. Smerdon,et al.  Rad23 is required for transcription-coupled repair and efficient overrall repair in Saccharomyces cerevisiae , 1996, Molecular and cellular biology.

[41]  M. Smerdon,et al.  UV damage to DNA strongly influences its rotational setting on the histone surface of reconstituted nucleosomes. , 1993, The Journal of biological chemistry.

[42]  H. Drew,et al.  Sequence periodicities in chicken nucleosome core DNA. , 1986, Journal of molecular biology.

[43]  F. Althaus,et al.  Uncoupling of DNA excision repair and nucleosomal unfolding in poly(ADP-ribose)-depleted mammalian cells. , 1990, Carcinogenesis.

[44]  D. Bazett-Jones,et al.  Histone hyperacetylation can induce unfolding of the nucleosome core particle. , 1990, Nucleic acids research.

[45]  D. Brash.  UV MUTAGENIC PHOTOPRODUCTS IN Escherichia coli AND HUMAN CELLS: A MOLECULAR GENETICS PERSPECTIVE ON HUMAN SKIN CANCER * , 1988, Photochemistry and photobiology.

[46]  M. Smerdon,et al.  Bleomycin-induced DNA damage and repair in human cells permeabilized with lysophosphatidylcholine. , 1990, Cancer research.

[47]  V. Bohr,et al.  Repair of ribosomal RNA genes in hamster cells after UV irradiation, or treatment with cisplatin or alkylating agents. , 1993, Carcinogenesis.

[48]  G. Felsenfeld,et al.  Chromatin structure and gene expression. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[49]  D. Mitchell,et al.  Nonrandom induction of pyrimidine-pyrimidone (6-4) photoproducts in ultraviolet-irradiated human chromatin. , 1990, The Journal of biological chemistry.

[50]  P. Gray.  Sulphur mustards inhibit binding of transcription factor AP2 in vitro. , 1995, Nucleic acids research.

[51]  C. Ryan,et al.  Ribosomal gene clusters are uniquely proportioned between open and closed chromatin structures in both tomato leaf cells and exponentially growing suspension cultures. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[52]  S. Dresler.  Stimulation of deoxyribonucleic acid excision repair in human fibroblasts pretreated with sodium butyrate. , 1985, Biochemistry.

[53]  D. Bazett-Jones,et al.  Visualization and analysis of unfolded nucleosomes associated with transcribing chromatin. , 1996, Nucleic acids research.

[54]  P. Sung,et al.  DNA repair genes and proteins of Saccharomyces cerevisiae. , 1993, Annual review of genetics.

[55]  M. Broggini,et al.  Differential inhibition of the DNA binding of transcription factors NF kappa B and OTF-1 by nitrogen mustard and quinacrine mustard: transcriptional implications. , 1993, Carcinogenesis.

[56]  M. Smerdon,et al.  Effect of histone H1 removal on the distribution of ultraviolet-induced deoxyribonucleic acid repair synthesis within chromatin. , 1982, Biochemistry.

[57]  T. Hsu,et al.  Bleomycin causes release of nucleosomes from chromatin and chromosomes , 1978, Nature.

[58]  B. Jernström,et al.  Inhibitory effects on the DNA binding of AP-1 transcription factor to an AP-1 binding site modified by benzo[a]pyrene 7,8-dihydrodiol 9,10-epoxide diastereomers. , 1996, Carcinogenesis.

[59]  M. Smerdon,et al.  Site-specific DNA repair at the nucleosome level in a yeast minichromosome , 1990, Cell.

[60]  A. Klug,et al.  Structure of the nucleosome core particle at 7 Å resolution , 1984, Nature.

[61]  E. Bradbury,et al.  Nucleosome linking number change controlled by acetylation of histones H3 and H4. , 1990, The Journal of biological chemistry.

[62]  U. Schieferstein,et al.  Modulation of cyclobutane pyrimidine dimer formation in a positioned nucleosome containing poly(dA.dT) tracts. , 1996, Biochemistry.

[63]  F. Thoma.  Protein-DNA interactions and nuclease-sensitive regions determine nucleosome positions on yeast plasmid chromatin. , 1986, Journal of molecular biology.

[64]  M. Smerdon,et al.  Unfolding of nucleosome cores dramatically changes the distribution of ultraviolet photoproducts in DNA. , 1993, Biochemistry.

[65]  H. Naegeli,et al.  Histone shuttle driven by the automodification cycle of poly(ADP‐ribose) polymerase , 1993, Environmental and molecular mutagenesis.

[66]  M. Smerdon,et al.  Nucleosome Unfolding during DNA Repair in Normal and Xeroderma Pigmentosum (Group C) Human Cells* , 1998, The Journal of Biological Chemistry.

[67]  D. Hunting,et al.  Aphidicolin-sensitive DNA repair synthesis in human fibroblasts damaged with bleomycin is distinct from UV-induced repair. , 1990, Carcinogenesis.

[68]  J. H. Vos,et al.  Differential introduction of DNA damage and repair in mammalian genes transcribed by RNA polymerases I and II , 1991, Molecular and cellular biology.

[69]  F. Thoma,et al.  Poly(dA).poly(dT) rich sequences are not sufficient to exclude nucleosome formation in a constitutive yeast promoter. , 1990, Nucleic acids research.

[70]  K. Powell,et al.  Binding of the transcription factor, Sp1, to non-target sites in DNA modified by benzo[a]pyrene diol epoxide. , 1995, Carcinogenesis.

[71]  R. Cole,et al.  Differential scanning calorimetry of nuclei as a test for the effects of anticancer drugs on human chromatin. , 1989, Cancer research.

[72]  M. Grunstein,et al.  Histones and the regulation of heterochromatin in yeast. , 1993, Cold Spring Harbor symposia on quantitative biology.

[73]  M. Smerdon,et al.  DNA damage can alter the stability of nucleosomes: effects are dependent on damage type. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[74]  E. Berkowitz,et al.  Methylation of chromosomal DNA by two alkylating agents differing in carcinogenic potential. , 1981, Cancer letters.

[75]  M. Smerdon,et al.  Nucleosome rearrangement in human cells following short patch repair of DNA damaged by bleomycin. , 1990, Biochemistry.

[76]  Claudio Nicolini,et al.  Chromatin Structure and Function , 1979, NATO Advanced Study Institutes Series.

[77]  E. Friedberg.  Relationships between DNA repair and transcription. , 1996, Annual review of biochemistry.

[78]  J M Gale,et al.  UV-induced formation of pyrimidine dimers in nucleosome core DNA is strongly modulated with a period of 10.3 bases. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[79]  R. Dammann,et al.  Chromatin structures and transcription of rDNA in yeast Saccharomyces cerevisiae. , 1993, Nucleic acids research.

[80]  T. Richmond,et al.  Crystal structure of the nucleosome core particle at 2.8 Å resolution , 1997, Nature.

[81]  A. Sancar.  DNA excision repair. , 1996, Annual review of biochemistry.

[82]  J. P. Mueller,et al.  Repair of plasmid and genomic DNA in a rad7Δ mutant of yeast , 1995 .

[83]  M. Smerdon,et al.  A nonuniform distribution of excision repair synthesis in nucleosome core DNA. , 1985, Biochemistry.

[84]  M. Smerdon,et al.  DNA repair within nucleosome cores of UV-irradiated human cells. , 1990, Biochemistry.

[85]  S. Elgin,et al.  Architectural variations of inducible eukaryotic promoters: Preset and remodeling chromatin structures , 1994, BioEssays : news and reviews in molecular, cellular and developmental biology.

[86]  B. Stillman,et al.  Chromatin Assembly Coupled to DNA Repair: A New Role for Chromatin Assembly Factor I , 1996, Cell.

[87]  A. Wolffe,et al.  Developmental regulation of two 5S ribosomal RNA genes. , 1988, Science.

[88]  S. Lippard,et al.  Specific binding of chromosomal protein HMG1 to DNA damaged by the anticancer drug cisplatin. , 1992, Science.

[89]  M. Smerdon,et al.  Nucleosome rearrangement in human chromatin during UV-induced DNA- reapir synthesis. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[90]  A. Riggs,et al.  Binding of transcription factors creates hot spots for UV photoproducts in vivo , 1992, Molecular and cellular biology.

[91]  J. Hayes,et al.  Structure of the TFIIIA-5 S DNA complex. , 1992, Journal of molecular biology.

[92]  D. K. Treiber,et al.  Cisplatin-DNA adducts are molecular decoys for the ribosomal RNA transcription factor hUBF (human upstream binding factor). , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[93]  S. Selleck,et al.  Photofootprinting in vivo detects transcription-dependent changes in yeast TATA boxes , 1987, Nature.

[94]  M. Smerdon,et al.  Strand Breaks Are Repaired Efficiently in Human Ribosomal Genes* , 1996, The Journal of Biological Chemistry.

[95]  M. Smerdon,et al.  Repair of UV damage in actively transcribed ribosomal genes. , 1995, Biochemistry.

[96]  M. Kastan,et al.  Distribution of repair-incorporated nucleotides and nucleosome rearrangement in the chromatin of normal and xeroderma pigmentosum human fibroblasts. , 1979, Biochemistry.

[97]  Joseph A. DiGiuseppe,et al.  Bleomycin-induced DNA repair synthesis in permeable human fibroblasts: mediation of long-patch and short-patch repair by distinct DNA polymerases. , 1989, Biochemistry.

[98]  P. Hanawalt,et al.  Lack of transcription-coupled repair in mammalian ribosomal RNA genes. , 1993, Biochemistry.

[99]  R. Parish,et al.  Psoralen-crosslinking of DNA as a probe for the structure of active nucleolar chromatin. , 1984, Journal of molecular biology.

[100]  D. Mitchell,et al.  Repair of UV-induced) Photoproducts in Nucleosome Core DNA (*) , 1995, The Journal of Biological Chemistry.

[101]  J. Davie,et al.  Histone acetylation alters the capacity of the H1 histones to condense transcriptionally active/competent chromatin. , 1990, The Journal of biological chemistry.

[102]  J. Taylor,et al.  Site-specific effect of thymine dimer formation on dAn.dTn tract bending and its biological implications. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[103]  D. S. Garrett,et al.  Solution-state structure of the Dewar pyrimidinone photoproduct of thymidylyl-(3'----5')-thymidine. , 1988, Biochemistry.

[104]  D. Mitchell,et al.  THE BIOLOGY OF THE (6–4) PHOTOPRODUCT , 1989, Photochemistry and photobiology.

[105]  T. Ohnishi,et al.  THE EFFECTS OF ULTRAVIOLET C ON in vitro NUCLEOSOME ASSEMBLY AND STABILITY , 1994, Photochemistry and photobiology.

[106]  M. Smerdon,et al.  Nucleosome rearrangement in vitro. 1. Two phases of salt-induced nucleosome migration in nuclei. , 1985, Biochemistry.

[107]  J. Sogo,et al.  Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle , 1989, Cell.

[108]  J. Pehrson.  Thymine dimer formation as a probe of the path of DNA in and between nucleosomes in intact chromatin. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[109]  A Klug,et al.  Repetitive zinc‐binding domains in the protein transcription factor IIIA from Xenopus oocytes. , 1985, The EMBO journal.

[110]  M. Macleod,et al.  Covalent binding of the carcinogen benzo[a]pyrene diol epoxide to Xenopus laevis 5 S DNA reconstituted into nucleosomes. , 1993, The Journal of biological chemistry.

[111]  G. Schroth,et al.  Transcription factor IIIA induced bending of the Xenopus somatic 5S gene promoter , 1989, Nature.

[112]  P. Wright,et al.  Relative contributions of the zinc fingers of transcription factor IIIA to the energetics of DNA binding. , 1994, Journal of molecular biology.

[113]  M. Smerdon.  Completion of excision repair in human cells. Relationship between ligation and nucleosome formation. , 1986, The Journal of biological chemistry.

[114]  D. Hunting,et al.  Multiple conformational states of repair patches in chromatin during DNA excision repair. , 1985, Biochemistry.

[115]  B. Suter,et al.  Chromatin structure modulates DNA repair by photolyase in vivo , 1997, The EMBO journal.

[116]  E. Wagner,et al.  Mice lacking ADPRT and poly(ADP-ribosyl)ation develop normally but are susceptible to skin disease. , 1995, Genes & development.

[117]  L. Ray,et al.  Catalytic activity of poly(ADP-ribose) polymerase is necessary for repair of N-methylpurines in nontranscribed, but not in transcribed, nuclear DNA sequences. , 1996, Mutation research.

[118]  A. Sancar.  Structure and function of DNA photolyase. , 1994, Biochemistry.

[119]  P. Smith.  n-Butyrate alters chromatin accessibility to DNA repair enzymes. , 1986, Carcinogenesis.

[120]  J. Pehrson,et al.  Effects of DNA looping on pyrimidine dimer formation. , 1992, Nucleic acids research.

[121]  M. Smerdon,et al.  Nucleosome rearrangement in vitro. 2. Formation of nucleosomes in newly repaired regions of DNA. , 1985, Biochemistry.

[122]  D. Mitchell,et al.  Evidence from mutation spectra that the UV hypermutability of xeroderma pigmentosum variant cells reflects abnormal, error-prone replication on a template containing photoproducts , 1993, Molecular and cellular biology.

[123]  G. Pfeifer,et al.  Inhibition of transcription factor binding by ultraviolet-induced pyrimidine dimers. , 1996, Biochemistry.