Home LiteratureArticle Details
PMID: 8760868 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Recruitment of damaged DNA to the nuclear matrix in hamster cells following ultraviolet irradiation.

Nucleic acids research ·Vol. 24 ·No. 15 ·1996-08-01 ·Pages 2877-84

Koehler DR, Hanawalt PC

Abstract

We examined the relationship between the nuclear matrix and DNA in the dihydrofolate reductase domain following irradiation of Chinese hamster cells with UV light. The fraction of matrix-bound DNA increased in transcribed and non-transcribed regions during a 3 h period after irradiation. However, no increase was observed with excision repair-deficient cells mutant for the ERCC1 gene. The major UV-induced lesion, the cyclobutane pyrimidine dimer, increased in frequency in the matrix-bound DNA 1 h after irradiation, in both transcribed and non-transcribed regions, but decreased subsequently. This phenomenon was also lacking in excision repair-deficient cells. These data demonstrate that recruitment of lesion-containing DNA to the nuclear matrix occurs following UV irradiation and suggest that this recruitment is dependent upon nucleotide excision repair. This is consistent with the concept of a 'repair factory' residing on the nuclear matrix at which excision repair occurs.

MeSH Terms
Animals CHO Cells Cell Compartmentation Cricetinae DNA Damage DNA Repair Nuclear Matrix/metabolism Subcellular Fractions Tetrahydrofolate Dehydrogenase/metabolism Ultraviolet Rays/adverse effects
Chemicals
Tetrahydrofolate Dehydrogenase
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Koehler D R
Department of Biological Sciences, Stanford University, CA 94305-5020, USA.
Hanawalt P C
References (80)
80 references, click to expand
  1. Evidence for a repair enzyme complex involving ERCC1 and complementing activities of ERCC4, ERCC11 and xeroderma pigmentosum group F.
    EMBO J. 1993 Sep;12(9):3693-701 PMID: 8253091
  2. Deficient repair of the transcribed strand of active genes in Cockayne's syndrome cells.
    Nucleic Acids Res. 1993 Dec 25;21(25):5890-5 PMID: 8290349
  3. Dual role of TFIIH in DNA excision repair and in transcription by RNA polymerase II.
    Nature. 1994 Apr 21;368(6473):769-72 PMID: 8152490
  4. Specific association between the human DNA repair proteins XPA and ERCC1.
    Proc Natl Acad Sci U S A. 1994 May 24;91(11):5012-6 PMID: 8197174
  5. Formation of a ternary complex by human XPA, ERCC1, and ERCC4(XPF) excision repair proteins.
    Proc Natl Acad Sci U S A. 1994 May 24;91(11):5017-21 PMID: 8197175
  6. RNA polymerase: structural determinant of the chromatin loop and the chromosome.
    Bioessays. 1994 Jun;16(6):425-30 PMID: 7521639
  7. XPG endonuclease makes the 3' incision in human DNA nucleotide excision repair.
    Nature. 1994 Sep 29;371(6496):432-5 PMID: 8090225
  8. Specific cleavage of model recombination and repair intermediates by the yeast Rad1-Rad10 DNA endonuclease.
    Science. 1994 Sep 30;265(5181):2082-5 PMID: 8091230
  9. Sites in human nuclei where DNA damaged by ultraviolet light is repaired: visualization and localization relative to the nucleoskeleton.
    J Cell Sci. 1994 Jul;107 ( Pt 7):1745-52 PMID: 7983144
  10. Sites in human nuclei where damage induced by ultraviolet light is repaired: localization relative to transcription sites and concentrations of proliferating cell nuclear antigen and the tumour suppressor protein, p53.
    J Cell Sci. 1994 Jul;107 ( Pt 7):1753-60 PMID: 7983145
  11. Transcription-coupled repair and human disease.
    Science. 1994 Dec 23;266(5193):1957-8 PMID: 7801121
  12. Different forms of TFIIH for transcription and DNA repair: holo-TFIIH and a nucleotide excision repairosome.
    Cell. 1995 Jan 13;80(1):21-8 PMID: 7813015
  13. Transcription-coupled repair removes both cyclobutane pyrimidine dimers and 6-4 photoproducts with equal efficiency and in a sequential way from transcribed DNA in xeroderma pigmentosum group C fibroblasts.
    EMBO J. 1995 Jan 16;14(2):360-7 PMID: 7835346
  14. The general transcription-repair factor TFIIH is recruited to the excision repair complex by the XPA protein independent of the TFIIE transcription factor.
    J Biol Chem. 1995 Mar 3;270(9):4896-902 PMID: 7876263
  15. Mutations in XPA that prevent association with ERCC1 are defective in nucleotide excision repair.
    Mol Cell Biol. 1995 Apr;15(4):1993-8 PMID: 7891694
  16. Mammalian DNA nucleotide excision repair reconstituted with purified protein components.
    Cell. 1995 Mar 24;80(6):859-68 PMID: 7697716
  17. Replication forks are associated with the nuclear matrix.
    Nucleic Acids Res. 1990 Apr 25;18(8):1965-9 PMID: 2336385
  18. Selective repair of specific chromatin domains in UV-irradiated cells from xeroderma pigmentosum complementation group C.
    Mutat Res. 1990 May;235(3):171-80 PMID: 2342504
  19. Site-specific DNA repair at the nucleosome level in a yeast minichromosome.
    Cell. 1990 May 18;61(4):675-84 PMID: 2188732
  20. The genetic defect in Cockayne syndrome is associated with a defect in repair of UV-induced DNA damage in transcriptionally active DNA.
    Proc Natl Acad Sci U S A. 1990 Jun;87(12):4707-11 PMID: 2352945
  21. Active RNA polymerase I is fixed within the nucleus of HeLa cells.
    EMBO J. 1990 Jul;9(7):2207-14 PMID: 2357967
  22. Mapping of structural and transcription-related matrix attachment sites in the alpha-globin gene domain of avian erythroblasts and erythrocytes.
    Mol Cell Biol. 1990 Oct;10(10):5349-58 PMID: 2398893
  23. Complementation of DNA repair in xeroderma pigmentosum group A cell extracts by a protein with affinity for damaged DNA.
    EMBO J. 1991 Dec;10(12):3913-21 PMID: 1935910
  24. The channels model of nuclear matrix structure.
    Bioessays. 1995 May;17(5):443-50 PMID: 7786290
  25. Partial characterization of the DNA repair protein complex, containing the ERCC1, ERCC4, ERCC11 and XPF correcting activities.
    Mutat Res. 1995 Jul;337(1):25-39 PMID: 7596355
  26. Enhancement of damage-specific DNA binding of XPA by interaction with the ERCC1 DNA repair protein.
    Biochem Biophys Res Commun. 1995 Jun 26;211(3):960-6 PMID: 7598728
  27. Nuclear organization: uniting replication foci, chromatin domains and chromosome structure.
    Bioessays. 1995 Jul;17(7):587-91 PMID: 7646480
  28. Human DNA repair excision nuclease. Analysis of the roles of the subunits involved in dual incisions by using anti-XPG and anti-ERCC1 antibodies.
    J Biol Chem. 1995 Sep 1;270(35):20862-9 PMID: 7657672
  29. DNA repair deficiencies associated with mutations in genes encoding subunits of transcription initiation factor TFIIH in yeast.
    Nucleic Acids Res. 1996 Apr 15;24(8):1540-6 PMID: 8628689
  30. Kinetics of pyrimidine(6-4)pyrimidone photoproduct repair in Escherichia coli.
    J Bacteriol. 1996 Mar;178(5):1347-50 PMID: 8631712
  31. Low ionic strength extraction of nuclease-treated nuclei destroys the attachment of transcriptionally active DNA to the nuclear skeleton.
    Nucleic Acids Res. 1985 Oct 25;13(20):7427-44 PMID: 2414739
  32. Transcribed human ribosomal RNA genes are attached to the nuclear matrix.
    J Mol Biol. 1986 Jan 5;187(1):15-21 PMID: 3959082
  33. Distribution of u.v.-induced repair events in higher-order chromatin loops in human and hamster fibroblasts.
    Carcinogenesis. 1986 Jun;7(6):995-1002 PMID: 3708760
  34. Replication occurs at a nucleoskeleton.
    EMBO J. 1986 Jun;5(6):1403-10 PMID: 3732249
  35. Preferential DNA repair of an active gene in human cells.
    Proc Natl Acad Sci U S A. 1986 Dec;83(23):8878-82 PMID: 3466163
  36. Intranuclear localization of UV-induced DNA repair in human VA13 cells.
    Mutat Res. 1987 Mar;183(2):177-84 PMID: 3029583
  37. Pre-mRNA splicing and the nuclear matrix.
    Mol Cell Biol. 1987 Jan;7(1):111-20 PMID: 3031450
  38. Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene.
    Cell. 1987 Oct 23;51(2):241-9 PMID: 3664636
  39. Anchorage of the Chinese hamster dihydrofolate reductase gene to the nuclear scaffold occurs in an intragenic region.
    J Mol Biol. 1987 Dec 20;198(4):677-92 PMID: 3430625
  40. Identification of a nuclear protein matrix.
    Biochem Biophys Res Commun. 1974 Oct 23;60(4):1410-7 PMID: 4214419
  41. Nuclear protein matrix: association with newly synthesized DNA.
    Science. 1975 Jul 25;189(4199):291-3 PMID: 1145202
  42. Improved microfluorometric DNA determination in biological material using 33258 Hoechst.
    Anal Biochem. 1979 Nov 15;100(1):188-97 PMID: 94515
  43. The influence of the wavelength of ultraviolet radiation on survival, mutation induction and DNA repair in irradiated Chinese hamster cells.
    Mutat Res. 1980 Aug;72(3):491-509 PMID: 7453709
  44. Sensitive determination of pyrimidine dimers in DNA of UV-irradiated mammalian cells. Introduction of T4 endonuclease V into frozen and thawed cells.
    Mutat Res. 1981 Jun;82(1):173-89 PMID: 6267456
  45. The ovalbumin gene is associated with the nuclear matrix of chicken oviduct cells.
    Cell. 1982 Jan;28(1):99-106 PMID: 7066988
  46. Association of globin ribonucleic acid and its precursors with the chicken erythroblast nuclear matrix.
    Biochemistry. 1982 Feb 16;21(4):764-71 PMID: 6176264
  47. Ribonucleic acid precursors are associated with the chick oviduct nuclear matrix.
    Biochemistry. 1982 Sep 28;21(20):4945-53 PMID: 6182907
  48. The use of an immunological probe to measure the kinetics of DNA repair in normal and UV-sensitive mammalian cell lines.
    Mutat Res. 1983 Oct;112(5):287-99 PMID: 6633556
  49. Actively transcribed genes are associated with the nuclear matrix.
    Nature. 1983 Dec 8-14;306(5943):607-9 PMID: 6646237
  50. Organization of the higher-order chromatin loop: specific DNA attachment sites on nuclear scaffold.
    Cell. 1984 Nov;39(1):223-32 PMID: 6091913
  51. Association of transcriptionally active vitellogenin II gene with the nuclear matrix of chicken liver.
    EMBO J. 1984 Sep;3(9):2005-8 PMID: 6489318
  52. Preferential repair of nuclear matrix associated DNA in xeroderma pigmentosum complementation group C.
    Mutat Res. 1984 Oct;141(2):75-82 PMID: 6493270
  53. Lesions induced in DNA by ultraviolet light are repaired at the nuclear cage.
    J Cell Sci. 1984 Aug;70:189-96 PMID: 6501435
  54. 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. 1985 Feb;40(2):359-69 PMID: 3838150
  55. Initiated complexes of RNA polymerase II are concentrated in the nuclear skeleton associated DNA.
    Exp Cell Res. 1985 May;158(1):273-5 PMID: 3996482
  56. (6-4)Photoproducts are removed from the DNA of UV-irradiated mammalian cells more efficiently than cyclobutane pyrimidine dimers.
    Mutat Res. 1985 Jul;143(3):109-12 PMID: 4010689
  57. A general method for preparing chromatin containing intact DNA.
    EMBO J. 1985 Apr;4(4):913-8 PMID: 3894011
  58. Transcription occurs at a nucleoskeleton.
    EMBO J. 1985 Apr;4(4):919-25 PMID: 2990913
  59. Nuclear matrix associated DNA is preferentially repaired in normal human fibroblasts, exposed to a low dose of ultraviolet light but not in Cockayne's syndrome fibroblasts.
    Nucleic Acids Res. 1988 Nov 25;16(22):10607-22 PMID: 3205718
  60. Matrix attachment regions are positioned near replication initiation sites, genes, and an interamplicon junction in the amplified dihydrofolate reductase domain of Chinese hamster ovary cells.
    Mol Cell Biol. 1988 Dec;8(12):5398-409 PMID: 3244360
  61. Preferential DNA repair of (6-4) photoproducts in the dihydrofolate reductase gene of Chinese hamster ovary cells.
    J Biol Chem. 1989 Oct 25;264(30):18005-10 PMID: 2808361
  62. Induction of the Escherichia coli lactose operon selectively increases repair of its transcribed DNA strand.
    Nature. 1989 Nov 2;342(6245):95-8 PMID: 2554145
  63. The size of chromatin loops in HeLa cells.
    EMBO J. 1990 Feb;9(2):567-71 PMID: 2303042
  64. The residual repair capacity of xeroderma pigmentosum complementation group C fibroblasts is highly specific for transcriptionally active DNA.
    Nucleic Acids Res. 1990 Feb 11;18(3):443-8 PMID: 2308842
  65. The nuclear matrix: a heuristic model for investigating genomic organization and function in the cell nucleus.
    J Cell Biochem. 1991 Oct;47(2):109-23 PMID: 1757479
  66. Simultaneous establishment of monoclonal antibodies specific for either cyclobutane pyrimidine dimer or (6-4)photoproduct from the same mouse immunized with ultraviolet-irradiated DNA.
    Photochem Photobiol. 1991 Aug;54(2):225-32 PMID: 1780359
  67. Requirement for ERCC-1 and ERCC-3 gene products in DNA excision repair in vitro. Complementation using rodent and human cell extracts.
    J Biol Chem. 1992 Apr 5;267(10):6879-85 PMID: 1551896
  68. Inhibition of transcription and strand-specific DNA repair by alpha-amanitin in Chinese hamster ovary cells.
    Mutat Res. 1992 Aug;274(2):93-101 PMID: 1378211
  69. Strand-selective repair of DNA damage in the yeast GAL7 gene requires RNA polymerase II.
    J Biol Chem. 1992 Nov 15;267(32):23175-82 PMID: 1429664
  70. Preferential repair of cyclobutane pyrimidine dimers in the transcribed strand of a gene in yeast chromosomes and plasmids is dependent on transcription.
    Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):10696-700 PMID: 1438266
  71. Identification of cellular defect in UVS1, a UV-sensitive Chinese hamster ovary mutant cell line.
    Cancer Res. 1993 Feb 1;53(3):495-9 PMID: 8425182
  72. Attachment of vitellogenin genes to the nucleoskeleton accompanies their activation.
    Biochem Biophys Res Commun. 1993 Feb 26;191(1):308-13 PMID: 7680557
  73. Visualization of focal sites of transcription within human nuclei.
    EMBO J. 1993 Mar;12(3):1059-65 PMID: 8458323
  74. Visualization of replication factories attached to nucleoskeleton.
    Cell. 1993 Apr 23;73(2):361-73 PMID: 8097433
  75. 3-Amino-1,4-dimethyl-5H-pyrido[4,3-b]indole (Trp-P-1) inhibits the removal of both cyclobutane dimers and (6-4) photoproducts from the DNA of ultraviolet-irradiated E. coli.
    Carcinogenesis. 1993 Jul;14(7):1475-8 PMID: 8330368
  76. Nucleotide excision repair I: from E. coli to yeast.
    Trends Genet. 1993 May;9(5):173-7 PMID: 8337754
  77. Nucleotide excision repair. II: From yeast to mammals.
    Trends Genet. 1993 Jun;9(6):211-7 PMID: 8337762
  78. Visualization of replication sites in unfixed human cells.
    J Cell Sci. 1993 Jun;105 ( Pt 2):541-50 PMID: 8408283
  79. Preferential binding of the xeroderma pigmentosum group A complementing protein to damaged DNA.
    Biochemistry. 1993 Nov 16;32(45):12096-104 PMID: 8218288
  80. Co-correction of the ERCC1, ERCC4 and xeroderma pigmentosum group F DNA repair defects in vitro.
    EMBO J. 1993 Sep;12(9):3685-92 PMID: 8253090
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
0305-1048
Published
1996-08-01
Pages
2877-84
Language
English
Region
England
NLM ID
0411011
PMCID
PMC146037
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com