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. 1996 Aug 1;24(15):2877–2884. doi: 10.1093/nar/24.15.2877

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

D R Koehler 1, P C Hanawalt 1
PMCID: PMC146037  PMID: 8760868

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.

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Selected References

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  1. Aboussekhra A., Biggerstaff M., Shivji M. K., Vilpo J. A., Moncollin V., Podust V. N., Protić M., Hübscher U., Egly J. M., Wood R. D. Mammalian DNA nucleotide excision repair reconstituted with purified protein components. Cell. 1995 Mar 24;80(6):859–868. doi: 10.1016/0092-8674(95)90289-9. [DOI] [PubMed] [Google Scholar]
  2. Bardwell A. J., Bardwell L., Tomkinson A. E., Friedberg E. C. Specific cleavage of model recombination and repair intermediates by the yeast Rad1-Rad10 DNA endonuclease. Science. 1994 Sep 30;265(5181):2082–2085. doi: 10.1126/science.8091230. [DOI] [PubMed] [Google Scholar]
  3. Berezney R., Coffey D. S. Identification of a nuclear protein matrix. Biochem Biophys Res Commun. 1974 Oct 23;60(4):1410–1417. doi: 10.1016/0006-291x(74)90355-6. [DOI] [PubMed] [Google Scholar]
  4. Berezney R., Coffey D. S. Nuclear protein matrix: association with newly synthesized DNA. Science. 1975 Jul 25;189(4199):291–293. doi: 10.1126/science.1145202. [DOI] [PubMed] [Google Scholar]
  5. Berezney R. The nuclear matrix: a heuristic model for investigating genomic organization and function in the cell nucleus. J Cell Biochem. 1991 Oct;47(2):109–123. doi: 10.1002/jcb.240470204. [DOI] [PubMed] [Google Scholar]
  6. Biggerstaff M., Szymkowski D. E., Wood R. D. Co-correction of the ERCC1, ERCC4 and xeroderma pigmentosum group F DNA repair defects in vitro. EMBO J. 1993 Sep;12(9):3685–3692. doi: 10.1002/j.1460-2075.1993.tb06043.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Biggerstaff M., Wood R. D. 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):6879–6885. [PubMed] [Google Scholar]
  8. Bohr V. A., Smith C. A., Okumoto D. S., 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. 1985 Feb;40(2):359–369. doi: 10.1016/0092-8674(85)90150-3. [DOI] [PubMed] [Google Scholar]
  9. Cesarone C. F., Bolognesi C., Santi L. Improved microfluorometric DNA determination in biological material using 33258 Hoechst. Anal Biochem. 1979 Nov 15;100(1):188–197. doi: 10.1016/0003-2697(79)90131-3. [DOI] [PubMed] [Google Scholar]
  10. Christians F. C., Hanawalt P. C. Inhibition of transcription and strand-specific DNA repair by alpha-amanitin in Chinese hamster ovary cells. Mutat Res. 1992 Aug;274(2):93–101. doi: 10.1016/0921-8777(92)90056-9. [DOI] [PubMed] [Google Scholar]
  11. Ciejek E. M., Nordstrom J. L., Tsai M. J., O'Malley B. W. Ribonucleic acid precursors are associated with the chick oviduct nuclear matrix. Biochemistry. 1982 Sep 28;21(20):4945–4953. doi: 10.1021/bi00263a018. [DOI] [PubMed] [Google Scholar]
  12. Ciejek E. M., Tsai M. J., O'Malley B. W. Actively transcribed genes are associated with the nuclear matrix. Nature. 1983 Dec 8;306(5943):607–609. doi: 10.1038/306607a0. [DOI] [PubMed] [Google Scholar]
  13. Clarkson J. M., Mitchell D. L., Adair G. M. 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):287–299. doi: 10.1016/0167-8817(83)90004-4. [DOI] [PubMed] [Google Scholar]
  14. Cook P. R. RNA polymerase: structural determinant of the chromatin loop and the chromosome. Bioessays. 1994 Jun;16(6):425–430. doi: 10.1002/bies.950160611. [DOI] [PubMed] [Google Scholar]
  15. Dickinson P., Cook P. R., Jackson D. A. Active RNA polymerase I is fixed within the nucleus of HeLa cells. EMBO J. 1990 Jul;9(7):2207–2214. doi: 10.1002/j.1460-2075.1990.tb07390.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dijkwel P. A., Hamlin J. L. 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):5398–5409. doi: 10.1128/mcb.8.12.5398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Drapkin R., Reardon J. T., Ansari A., Huang J. C., Zawel L., Ahn K., Sancar A., Reinberg D. Dual role of TFIIH in DNA excision repair and in transcription by RNA polymerase II. Nature. 1994 Apr 21;368(6473):769–772. doi: 10.1038/368769a0. [DOI] [PubMed] [Google Scholar]
  18. Farache G., Razin S. V., Rzeszowska-Wolny J., Moreau J., Targa F. R., Scherrer K. 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):5349–5358. doi: 10.1128/mcb.10.10.5349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hanawalt P. C. Transcription-coupled repair and human disease. Science. 1994 Dec 23;266(5193):1957–1958. doi: 10.1126/science.7801121. [DOI] [PubMed] [Google Scholar]
  20. Harless J., Hewitt R. R. Intranuclear localization of UV-induced DNA repair in human VA13 cells. Mutat Res. 1987 Mar;183(2):177–184. doi: 10.1016/0167-8817(87)90060-5. [DOI] [PubMed] [Google Scholar]
  21. Hassan A. B., Cook P. R. Visualization of replication sites in unfixed human cells. J Cell Sci. 1993 Jun;105(Pt 2):541–550. doi: 10.1242/jcs.105.2.541. [DOI] [PubMed] [Google Scholar]
  22. Hoeijmakers J. H. Nucleotide excision repair I: from E. coli to yeast. Trends Genet. 1993 May;9(5):173–177. doi: 10.1016/0168-9525(93)90164-d. [DOI] [PubMed] [Google Scholar]
  23. Hoeijmakers J. H. Nucleotide excision repair. II: From yeast to mammals. Trends Genet. 1993 Jun;9(6):211–217. doi: 10.1016/0168-9525(93)90121-w. [DOI] [PubMed] [Google Scholar]
  24. Hozák P., Hassan A. B., Jackson D. A., Cook P. R. Visualization of replication factories attached to nucleoskeleton. Cell. 1993 Apr 23;73(2):361–373. doi: 10.1016/0092-8674(93)90235-i. [DOI] [PubMed] [Google Scholar]
  25. Jackson D. A., Balajee A. S., Mullenders L., Cook P. R. 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):1745–1752. doi: 10.1242/jcs.107.7.1745. [DOI] [PubMed] [Google Scholar]
  26. Jackson D. A., Cook P. R. A general method for preparing chromatin containing intact DNA. EMBO J. 1985 Apr;4(4):913–918. doi: 10.1002/j.1460-2075.1985.tb03718.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Jackson D. A., Cook P. R. Replication occurs at a nucleoskeleton. EMBO J. 1986 Jun;5(6):1403–1410. doi: 10.1002/j.1460-2075.1986.tb04374.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Jackson D. A., Cook P. R. Transcription occurs at a nucleoskeleton. EMBO J. 1985 Apr;4(4):919–925. doi: 10.1002/j.1460-2075.1985.tb03719.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Jackson D. A., Dickinson P., Cook P. R. The size of chromatin loops in HeLa cells. EMBO J. 1990 Feb;9(2):567–571. doi: 10.1002/j.1460-2075.1990.tb08144.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Jackson D. A., Hassan A. B., Errington R. J., Cook P. R. 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):1753–1760. doi: 10.1242/jcs.107.7.1753. [DOI] [PubMed] [Google Scholar]
  31. Jackson D. A., Hassan A. B., Errington R. J., Cook P. R. Visualization of focal sites of transcription within human nuclei. EMBO J. 1993 Mar;12(3):1059–1065. doi: 10.1002/j.1460-2075.1993.tb05747.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Jackson D. A. Nuclear organization: uniting replication foci, chromatin domains and chromosome structure. Bioessays. 1995 Jul;17(7):587–591. doi: 10.1002/bies.950170704. [DOI] [PubMed] [Google Scholar]
  33. Jones C. J., Wood R. D. Preferential binding of the xeroderma pigmentosum group A complementing protein to damaged DNA. Biochemistry. 1993 Nov 16;32(45):12096–12104. doi: 10.1021/bi00096a021. [DOI] [PubMed] [Google Scholar]
  34. Jost J. P., Seldran M. Association of transcriptionally active vitellogenin II gene with the nuclear matrix of chicken liver. EMBO J. 1984 Sep;3(9):2005–2008. doi: 10.1002/j.1460-2075.1984.tb02082.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kantor G. J., Barsalou L. S., Hanawalt P. C. Selective repair of specific chromatin domains in UV-irradiated cells from xeroderma pigmentosum complementation group C. Mutat Res. 1990 May;235(3):171–180. doi: 10.1016/0921-8777(90)90071-c. [DOI] [PubMed] [Google Scholar]
  36. Keppel F. Transcribed human ribosomal RNA genes are attached to the nuclear matrix. J Mol Biol. 1986 Jan 5;187(1):15–21. doi: 10.1016/0022-2836(86)90402-x. [DOI] [PubMed] [Google Scholar]
  37. Koehler D. R., Courcelle J., Hanawalt P. C. Kinetics of pyrimidine(6-4)pyrimidone photoproduct repair in Escherichia coli. J Bacteriol. 1996 Mar;178(5):1347–1350. doi: 10.1128/jb.178.5.1347-1350.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Käs E., Chasin L. A. 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):677–692. doi: 10.1016/0022-2836(87)90209-9. [DOI] [PubMed] [Google Scholar]
  39. Leadon S. A., Lawrence D. A. Strand-selective repair of DNA damage in the yeast GAL7 gene requires RNA polymerase II. J Biol Chem. 1992 Nov 15;267(32):23175–23182. [PubMed] [Google Scholar]
  40. Li L., Elledge S. J., Peterson C. A., Bales E. S., Legerski R. J. Specific association between the human DNA repair proteins XPA and ERCC1. Proc Natl Acad Sci U S A. 1994 May 24;91(11):5012–5016. doi: 10.1073/pnas.91.11.5012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Li L., Peterson C. A., Lu X., Legerski R. J. Mutations in XPA that prevent association with ERCC1 are defective in nucleotide excision repair. Mol Cell Biol. 1995 Apr;15(4):1993–1998. doi: 10.1128/mcb.15.4.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Matsunaga T., Mu D., Park C. H., Reardon J. T., Sancar A. 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):20862–20869. doi: 10.1074/jbc.270.35.20862. [DOI] [PubMed] [Google Scholar]
  43. McCready S. J., Cook P. R. Lesions induced in DNA by ultraviolet light are repaired at the nuclear cage. J Cell Sci. 1984 Aug;70:189–196. doi: 10.1242/jcs.70.1.189. [DOI] [PubMed] [Google Scholar]
  44. Mellon I., Bohr V. A., Smith C. A., Hanawalt P. C. Preferential DNA repair of an active gene in human cells. Proc Natl Acad Sci U S A. 1986 Dec;83(23):8878–8882. doi: 10.1073/pnas.83.23.8878. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Mellon I., Hanawalt P. C. Induction of the Escherichia coli lactose operon selectively increases repair of its transcribed DNA strand. Nature. 1989 Nov 2;342(6245):95–98. doi: 10.1038/342095a0. [DOI] [PubMed] [Google Scholar]
  46. Mellon I., Spivak G., Hanawalt P. C. Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell. 1987 Oct 23;51(2):241–249. doi: 10.1016/0092-8674(87)90151-6. [DOI] [PubMed] [Google Scholar]
  47. Mirkovitch J., Mirault M. E., Laemmli U. K. Organization of the higher-order chromatin loop: specific DNA attachment sites on nuclear scaffold. Cell. 1984 Nov;39(1):223–232. doi: 10.1016/0092-8674(84)90208-3. [DOI] [PubMed] [Google Scholar]
  48. Mitchell D. L., Haipek C. A., Clarkson J. M. (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):109–112. doi: 10.1016/s0165-7992(85)80018-x. [DOI] [PubMed] [Google Scholar]
  49. Mori T., Nakane M., Hattori T., Matsunaga T., Ihara M., Nikaido O. 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):225–232. doi: 10.1111/j.1751-1097.1991.tb02010.x. [DOI] [PubMed] [Google Scholar]
  50. Mori T., Shimoi K., Sasaki Y. F., Wakabayashi K., Nagao M., Kinae N. 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):1475–1478. doi: 10.1093/carcin/14.7.1475. [DOI] [PubMed] [Google Scholar]
  51. Mullenders L. H., van Kesteren van Leeuwen A. C., van Zeeland A. A., Natarajan A. T. 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):10607–10622. doi: 10.1093/nar/16.22.10607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Mullenders L. H., van Kesteren A. C., Bussmann C. J., van Zeeland A. A., Natarajan A. T. Distribution of u.v.-induced repair events in higher-order chromatin loops in human and hamster fibroblasts. Carcinogenesis. 1986 Jun;7(6):995–1002. doi: 10.1093/carcin/7.6.995. [DOI] [PubMed] [Google Scholar]
  53. Mullenders L. H., van Kesteren A. C., Bussmann C. J., van Zeeland A. A., Natarajan A. T. Preferential repair of nuclear matrix associated DNA in xeroderma pigmentosum complementation group C. Mutat Res. 1984 Oct;141(2):75–82. doi: 10.1016/0165-7992(84)90014-9. [DOI] [PubMed] [Google Scholar]
  54. Nagai A., Saijo M., Kuraoka I., Matsuda T., Kodo N., Nakatsu Y., Mimaki T., Mino M., Biggerstaff M., Wood R. D. 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):960–966. doi: 10.1006/bbrc.1995.1905. [DOI] [PubMed] [Google Scholar]
  55. Numata M., Hata H., Shiomi T., Matsunaga T., Mori T., Nikaido O., Yasui A., Oikawa A. Identification of cellular defect in UVS1, a UV-sensitive Chinese hamster ovary mutant cell line. Cancer Res. 1993 Feb 1;53(3):495–499. [PubMed] [Google Scholar]
  56. O'Donovan A., Davies A. A., Moggs J. G., West S. C., Wood R. D. XPG endonuclease makes the 3' incision in human DNA nucleotide excision repair. Nature. 1994 Sep 29;371(6496):432–435. doi: 10.1038/371432a0. [DOI] [PubMed] [Google Scholar]
  57. Park C. H., Mu D., Reardon J. T., Sancar A. 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):4896–4902. doi: 10.1074/jbc.270.9.4896. [DOI] [PubMed] [Google Scholar]
  58. Park C. H., Sancar A. 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):5017–5021. doi: 10.1073/pnas.91.11.5017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Razin S. V., Gromova I. I. The channels model of nuclear matrix structure. Bioessays. 1995 May;17(5):443–450. doi: 10.1002/bies.950170512. [DOI] [PubMed] [Google Scholar]
  60. Razin S. V., Yarovaya O. V., Georgiev G. P. 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):7427–7444. doi: 10.1093/nar/13.20.7427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Razin S. V., Yarovaya O. V. Initiated complexes of RNA polymerase II are concentrated in the nuclear skeleton associated DNA. Exp Cell Res. 1985 May;158(1):273–275. doi: 10.1016/0014-4827(85)90451-3. [DOI] [PubMed] [Google Scholar]
  62. Robins P., Jones C. J., Biggerstaff M., Lindahl T., Wood R. D. 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):3913–3921. doi: 10.1002/j.1460-2075.1991.tb04961.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Robinson S. I., Nelkin B. D., Vogelstein B. The ovalbumin gene is associated with the nuclear matrix of chicken oviduct cells. Cell. 1982 Jan;28(1):99–106. doi: 10.1016/0092-8674(82)90379-8. [DOI] [PubMed] [Google Scholar]
  64. Ross D. A., Yen R. W., Chae C. B. Association of globin ribonucleic acid and its precursors with the chicken erythroblast nuclear matrix. Biochemistry. 1982 Feb 16;21(4):764–771. doi: 10.1021/bi00533a029. [DOI] [PubMed] [Google Scholar]
  65. Smerdon M. J., Thoma F. Site-specific DNA repair at the nucleosome level in a yeast minichromosome. Cell. 1990 May 18;61(4):675–684. doi: 10.1016/0092-8674(90)90479-x. [DOI] [PubMed] [Google Scholar]
  66. Svejstrup J. Q., Wang Z., Feaver W. J., Wu X., Bushnell D. A., Donahue T. F., Friedberg E. C., Kornberg R. D. Different forms of TFIIH for transcription and DNA repair: holo-TFIIH and a nucleotide excision repairosome. Cell. 1995 Jan 13;80(1):21–28. doi: 10.1016/0092-8674(95)90447-6. [DOI] [PubMed] [Google Scholar]
  67. Sweder K. S., Chun R., Mori T., Hanawalt P. C. 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):1540–1546. doi: 10.1093/nar/24.8.1540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Sweder K. S., Hanawalt P. C. 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):10696–10700. doi: 10.1073/pnas.89.22.10696. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Thomas D. C., Okumoto D. S., Sancar A., Bohr V. A. 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):18005–18010. [PubMed] [Google Scholar]
  70. Thorburn A., Knowland J. Attachment of vitellogenin genes to the nucleoskeleton accompanies their activation. Biochem Biophys Res Commun. 1993 Feb 26;191(1):308–313. doi: 10.1006/bbrc.1993.1218. [DOI] [PubMed] [Google Scholar]
  71. Vaughn J. P., Dijkwel P. A., Mullenders L. H., Hamlin J. L. Replication forks are associated with the nuclear matrix. Nucleic Acids Res. 1990 Apr 25;18(8):1965–1969. doi: 10.1093/nar/18.8.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Venema J., Mullenders L. H., Natarajan A. T., van Zeeland A. A., Mayne L. V. 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):4707–4711. doi: 10.1073/pnas.87.12.4707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Venema J., van Hoffen A., Natarajan A. T., van Zeeland A. A., Mullenders L. H. 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):443–448. doi: 10.1093/nar/18.3.443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Zeitlin S., Parent A., Silverstein S., Efstratiadis A. Pre-mRNA splicing and the nuclear matrix. Mol Cell Biol. 1987 Jan;7(1):111–120. doi: 10.1128/mcb.7.1.111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Zelle B., Reynolds R. J., Kottenhagen M. J., Schuite A., Lohman P. H. 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. doi: 10.1016/0027-5107(80)90121-9. [DOI] [PubMed] [Google Scholar]
  76. van Hoffen A., Natarajan A. T., Mayne L. V., van Zeeland A. A., Mullenders L. H., Venema J. Deficient repair of the transcribed strand of active genes in Cockayne's syndrome cells. Nucleic Acids Res. 1993 Dec 25;21(25):5890–5895. doi: 10.1093/nar/21.25.5890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. van Hoffen A., Venema J., Meschini R., van Zeeland A. A., Mullenders L. H. 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):360–367. doi: 10.1002/j.1460-2075.1995.tb07010.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. van Vuuren A. J., Appeldoorn E., Odijk H., Humbert S., Moncollin V., Eker A. P., Jaspers N. G., Egly J. M., Hoeijmakers J. H. 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. doi: 10.1016/0921-8777(95)00009-9. [DOI] [PubMed] [Google Scholar]
  79. van Vuuren A. J., Appeldoorn E., Odijk H., Yasui A., Jaspers N. G., Bootsma D., Hoeijmakers J. H. 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):3693–3701. doi: 10.1002/j.1460-2075.1993.tb06044.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. van Zeeland A. A., Smith C. A., Hanawalt P. C. 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):173–189. doi: 10.1016/0027-5107(81)90148-2. [DOI] [PubMed] [Google Scholar]

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