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PMID: 8264606 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Preferential repair of UV damage in highly transcribed DNA diminishes UV-induced intrachromosomal recombination in mammalian cells.

Molecular and cellular biology ·Vol. 14 ·No. 1 ·1994-01-00 ·Pages 391-9

Deng WP, Nickoloff JA

Abstract

The relationships among transcription, recombination, DNA damage, and repair in mammalian cells were investigated. We monitored the effects of transcription on UV-induced intrachromosomal recombination between neomycin repeats including a promoterless allele and an inducible heteroallele regulated by the mouse mammary tumor virus promoter. Although transcription and UV light separately stimulated recombination, increasing transcription levels reduced UV-induced recombination. Preferential repair of UV damage in transcribed strands was shown in highly transcribed DNA, suggesting that recombination is stimulated by unrepaired UV damage and that increased DNA repair in highly transcribed alleles removes recombinogenic lesions. This study indicates that the genetic consequences of DNA damage depend on transcriptional states and provides a basis for understanding tissue- and gene-specific responses to DNA-damaging agents.

Related Genes
neo
MeSH Terms
Animals CHO Cells/metabolism,radiation effects Cricetinae DNA/genetics,metabolism,radiation effects DNA Damage DNA Repair/genetics Drug Resistance/genetics Mammary Tumor Virus, Mouse/drug effects,genetics Mutation Neomycin/pharmacology Phenotype Promoter Regions, Genetic Recombination, Genetic/radiation effects Transcription, Genetic Ultraviolet Rays
Chemicals
DNA Neomycin
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Deng W P
Department of Cancer Biology, Harvard University School of Public Health, Boston, Massachusetts 02115.
Nickoloff J A
References (69)
69 references, click to expand
  1. Carcinogens can induce homologous recombination between duplicated chromosomal sequences in mouse L cells.
    Mol Cell Biol. 1988 Jan;8(1):196-202 PMID: 3122022
  2. DNA repair in the metallothionein gene increases with transcriptional activation.
    Nucleic Acids Res. 1987 Dec 10;15(23):10021-30 PMID: 2827103
  3. Thymine dimers bend DNA.
    Proc Natl Acad Sci U S A. 1988 Apr;85(8):2558-62 PMID: 3357882
  4. Transcription generates positively and negatively supercoiled domains in the template.
    Cell. 1988 May 6;53(3):433-40 PMID: 2835168
  5. Repair of DNA-containing pyrimidine dimers.
    FASEB J. 1988 Aug;2(11):2696-701 PMID: 3294078
  6. Transcription-driven supercoiling of DNA: direct biochemical evidence from in vitro studies.
    Cell. 1989 Jan 13;56(1):111-8 PMID: 2535966
  7. Elevated recombination rates in transcriptionally active DNA.
    Cell. 1989 Feb 24;56(4):619-30 PMID: 2645056
  8. UV-induced DNA-binding proteins in human cells.
    Proc Natl Acad Sci U S A. 1989 Feb;86(4):1163-7 PMID: 2919165
  9. Life cycle of the budding yeast Saccharomyces cerevisiae.
    Microbiol Rev. 1988 Dec;52(4):536-53 PMID: 3070323
  10. Ability of structurally related polycyclic aromatic carcinogens to induce homologous recombination between duplicated chromosomal sequences in mouse L cells.
    Mutat Res. 1989 Apr;211(2):205-14 PMID: 2494440
  11. DNA double-chain breaks in recombination of phage lambda and of yeast.
    Annu Rev Genet. 1988;22:169-97 PMID: 2977087
  12. Differential repair of DNA damage in the human metallothionein gene family.
    Mol Cell Biol. 1988 Dec;8(12):5331-8 PMID: 3149714
  13. Identification and characterization of X-ray-induced proteins in human cells.
    Cancer Res. 1989 Jun 1;49(11):2871-8 PMID: 2720648
  14. A subthreshold level of DNA topoisomerases leads to the excision of yeast rDNA as extrachromosomal rings.
    Cell. 1989 Jun 16;57(6):975-85 PMID: 2544296
  15. Double-strand breaks stimulate alternative mechanisms of recombination repair.
    J Mol Biol. 1989 Jun 5;207(3):527-41 PMID: 2668534
  16. A DNA double chain break stimulates triparental recombination in Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1989 Aug;86(16):6225-9 PMID: 2668958
  17. Phasing of protein-induced DNA bends in a recombination complex.
    Nature. 1989 Sep 21;341(6239):255-7 PMID: 2528698
  18. Transcription by RNA polymerase I stimulates mitotic recombination in Saccharomyces cerevisiae.
    Mol Cell Biol. 1989 Aug;9(8):3464-72 PMID: 2677675
  19. 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
  20. A simple and efficient non-organic procedure for the isolation of genomic DNA from blood.
    Nucleic Acids Res. 1989 Oct 25;17(20):8390 PMID: 2813076
  21. Repair of double-stranded DNA breaks by homologous DNA fragments during transfer of DNA into mouse L cells.
    Mol Cell Biol. 1990 Jan;10(1):113-9 PMID: 2294397
  22. Homologous recombination in mammalian cells.
    Annu Rev Genet. 1989;23:199-225 PMID: 2694931
  23. Frequency of intrachromosomal homologous recombination induced by UV radiation in normally repairing and excision repair-deficient human cells.
    Proc Natl Acad Sci U S A. 1990 Feb;87(4):1566-70 PMID: 2154752
  24. A chromosome containing HOT1 preferentially receives information during mitotic interchromosomal gene conversion.
    Genetics. 1990 Mar;124(3):561-72 PMID: 2179054
  25. Preferential repair of damage in actively transcribed DNA sequences in vivo.
    Genome. 1989;31(2):605-11 PMID: 2698835
  26. Effect of nucleotide excision repair in human cells on intrachromosomal homologous recombination induced by UV and 1-nitrosopyrene.
    Mol Cell Biol. 1990 Aug;10(8):3945-51 PMID: 2164633
  27. DNA-damage-inducible genes in mammalian cells.
    Prog Clin Biol Res. 1990;340A:315-25 PMID: 1975098
  28. The strong ADH1 promoter stimulates mitotic and meiotic recombination at the ADE6 gene of Schizosaccharomyces pombe.
    Mol Cell Biol. 1991 Jan;11(1):289-98 PMID: 1986226
  29. 1H NMR assignment and melting temperature study of cis-syn and trans-syn thymine dimer containing duplexes of d(CGTATTATGC).d(GCATAATACG).
    Biochemistry. 1990 Sep 18;29(37):8858-66 PMID: 2271562
  30. Effect of caffeine on the expression of a major X-ray induced protein in human tumor cells.
    Radiat Res. 1991 Mar;125(3):313-7 PMID: 2000455
  31. Gene conversion tracts stimulated by HOT1-promoted transcription are long and continuous.
    Genetics. 1990 Dec;126(4):851-67 PMID: 2076817
  32. Heterogeneity of DNA repair at the gene level.
    Mutat Res. 1991 Apr;247(2):203-11 PMID: 2011138
  33. Preferential repair of DNA damage on the transcribed strand of the human metallothionein genes requires RNA polymerase II.
    Mutat Res. 1991 Jul;255(1):67-78 PMID: 1906131
  34. Oncogenic conversion of transcription factors by chromosomal translocations.
    Cell. 1991 Aug 23;66(4):619-22 PMID: 1878967
  35. Induction of tissue-type plasminogen activator by ionizing radiation in human malignant melanoma cells.
    Cancer Res. 1991 Oct 15;51(20):5587-95 PMID: 1913677
  36. Inhibition of chromatin assembly in Xenopus oocytes correlates with derepression of the mouse mammary tumor virus promoter.
    Mol Cell Biol. 1991 Oct;11(10):5259-65 PMID: 1656227
  37. Ultraviolet stimulation of intermolecular homologous recombination in Chinese hamster ovary cells.
    Mol Carcinog. 1991;4(6):519-26 PMID: 1793489
  38. Transcriptional regulatory elements stimulate recombination in extrachromosomal substrates carrying immunoglobulin switch-region sequences.
    Proc Natl Acad Sci U S A. 1992 May 1;89(9):4154-8 PMID: 1315054
  39. Site-directed mutagenesis of virtually any plasmid by eliminating a unique site.
    Anal Biochem. 1992 Jan;200(1):81-8 PMID: 1595905
  40. ATP-dependent branch migration of Holliday junctions promoted by the RuvA and RuvB proteins of E. coli.
    Cell. 1992 Jun 26;69(7):1171-80 PMID: 1617728
  41. Endonuclease from Micrococcus luteus which has activity toward ultraviolet-irradiated deoxyribonucleic acid: purification and properties.
    J Bacteriol. 1970 Apr;102(1):178-86 PMID: 4314477
  42. Exchanges between DNA strands in ultraviolet-irradiated Escherichia coli.
    J Mol Biol. 1971 Oct 14;61(1):25-44 PMID: 4947693
  43. Biochemical analysis of att-defective mutants of the phage lambda site-specific recombination system.
    J Mol Biol. 1982 Apr 15;156(3):505-22 PMID: 6214637
  44. Somatic generation of antibody diversity.
    Nature. 1983 Apr 14;302(5909):575-81 PMID: 6300689
  45. Transcription enhances intrachromosomal homologous recombination in mammalian cells.
    Mol Cell Biol. 1992 Dec;12(12):5311-8 PMID: 1333040
  46. Molecular mechanism of transcription-repair coupling.
    Science. 1993 Apr 2;260(5104):53-8 PMID: 8465200
  47. DNA repair helicase: a component of BTF2 (TFIIH) basic transcription factor.
    Science. 1993 Apr 2;260(5104):58-63 PMID: 8465201
  48. The repair of double-strand breaks in DNA; a model involving recombination.
    J Theor Biol. 1976 Jun;59(1):97-106 PMID: 940351
  49. Steroid induction of mouse mammary tumor virus: effect upon synthesis and degradation of viral RNA.
    J Virol. 1977 Jan;21(1):139-46 PMID: 189061
  50. Glucocorticoid-stimulated accumulation of mouse mammary tumor virus RNA: increased rate of synthesis of viral RNA.
    Proc Natl Acad Sci U S A. 1977 Jul;74(7):2879-83 PMID: 197523
  51. Gene and transcription unit mapping by radiation effects.
    Annu Rev Genet. 1978;12:329-63 PMID: 371526
  52. Selection for animal cells that express the Escherichia coli gene coding for xanthine-guanine phosphoribosyltransferase.
    Proc Natl Acad Sci U S A. 1981 Apr;78(4):2072-6 PMID: 7017722
  53. A position-effect control for gene transposition: state of expression of yeast mating-type genes affects their ability to switch.
    Cell. 1981 Aug;25(2):517-24 PMID: 6269749
  54. Yeast transformation: a model system for the study of recombination.
    Proc Natl Acad Sci U S A. 1981 Oct;78(10):6354-8 PMID: 6273866
  55. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity.
    Anal Biochem. 1983 Jul 1;132(1):6-13 PMID: 6312838
  56. Genomic sequencing.
    Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991-5 PMID: 6326095
  57. Homologous recombination between plasmids in mammalian cells can be enhanced by treatment of input DNA.
    Proc Natl Acad Sci U S A. 1984 May;81(10):3153-7 PMID: 6328502
  58. Model for homologous recombination during transfer of DNA into mouse L cells: role for DNA ends in the recombination process.
    Mol Cell Biol. 1984 Jun;4(6):1020-34 PMID: 6330525
  59. Cis-acting, recombination-stimulating activity in a fragment of the ribosomal DNA of S. cerevisiae.
    Cell. 1984 Dec;39(2 Pt 1):377-86 PMID: 6094015
  60. 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
  61. Homologous recombination between defective neo genes in mouse 3T6 cells.
    Cold Spring Harb Symp Quant Biol. 1984;49:171-81 PMID: 6597755
  62. Specific Saccharomyces cerevisiae genes are expressed in response to DNA-damaging agents.
    Mol Cell Biol. 1985 Jan;5(1):75-84 PMID: 3920512
  63. Recombination events after transient infection and stable integration of DNA into mouse cells.
    Mol Cell Biol. 1985 Apr;5(4):659-66 PMID: 3990687
  64. Regulation of genome rearrangement events during lymphocyte differentiation.
    Immunol Rev. 1986 Feb;89:5-30 PMID: 3081433
  65. Effect of double-strand breaks on homologous recombination in mammalian cells and extracts.
    Mol Cell Biol. 1985 Dec;5(12):3331-6 PMID: 3870133
  66. A 24-base-pair DNA sequence from the MAT locus stimulates intergenic recombination in yeast.
    Proc Natl Acad Sci U S A. 1986 Oct;83(20):7831-5 PMID: 3020559
  67. Recombination between immunoglobulin variable region gene segments is enhanced by transcription.
    Nature. 1986 Dec 11-17;324(6097):585-9 PMID: 3491327
  68. 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
  69. Supercoiling of the DNA template during transcription.
    Proc Natl Acad Sci U S A. 1987 Oct;84(20):7024-7 PMID: 2823250
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
DOI
10.1128/mcb.14.1.391-399.1994
Published
1994-01-00
Pages
391-9
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC358388
Subset
IM
Grants
NCI NIH HHS · CA 54079 · United States
External Links
PubMed source DOI: 10.1128/mcb.14.1.391-399.1994 PMC Full Text View journal details
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