Abstract
We compared the removal of pyrimidine(6-4)pyrimidone photoproducts [(6-4) photoproducts] and cyclobutane pyrimidine dimers (CPDs) from the genome of repair-proficient Escherichia coli, using monoclonal antibodies specific for each type of lesion. We found that (6-4) photoproducts were removed at a higher rate than CPDs in the first 30 min following a moderate UV dose (40 J/m2). The difference in rates was less than that typically reported for cultured mammalian cells, in which the removal of (6-4) photoproducts is far more rapid than that of CPDs.
Full Text
The Full Text of this article is available as a PDF (235.6 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Brash D. E., Rudolph J. A., Simon J. A., Lin A., McKenna G. J., Baden H. P., Halperin A. J., Pontén J. A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma. Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10124–10128. doi: 10.1073/pnas.88.22.10124. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Broyles S. S., Pettijohn D. E. Interaction of the Escherichia coli HU protein with DNA. Evidence for formation of nucleosome-like structures with altered DNA helical pitch. J Mol Biol. 1986 Jan 5;187(1):47–60. doi: 10.1016/0022-2836(86)90405-5. [DOI] [PubMed] [Google Scholar]
- 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]
- Cooper P. K. Characterization of long patch excision repair of DNA in ultraviolet-irradiated Escherichia coli: an inducible function under rec-lex control. Mol Gen Genet. 1982;185(2):189–197. doi: 10.1007/BF00330785. [DOI] [PubMed] [Google Scholar]
- Doudney C. O., Haas F. L. MODIFICATION OF ULTRAVIOLET-INDUCED MUTATION FREQUENCY AND SURVIVAL IN BACTERIA BY POST-IRRADIATION TR000EATMENT. Proc Natl Acad Sci U S A. 1958 May;44(5):390–401. doi: 10.1073/pnas.44.5.390. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dumaz N., Drougard C., Sarasin A., Daya-Grosjean L. Specific UV-induced mutation spectrum in the p53 gene of skin tumors from DNA-repair-deficient xeroderma pigmentosum patients. Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10529–10533. doi: 10.1073/pnas.90.22.10529. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Franklin W. A., Haseltine W. A. Removal of UV light-induced pyrimidine-pyrimidone(6-4) products from Escherichia coli DNA requires the uvrA, uvrB, and urvC gene products. Proc Natl Acad Sci U S A. 1984 Jun;81(12):3821–3824. doi: 10.1073/pnas.81.12.3821. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gale J. M., Nissen K. A., Smerdon M. J. UV-induced formation of pyrimidine dimers in nucleosome core DNA is strongly modulated with a period of 10.3 bases. Proc Natl Acad Sci U S A. 1987 Oct;84(19):6644–6648. doi: 10.1073/pnas.84.19.6644. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gale J. M., Smerdon M. J. UV induced (6-4) photoproducts are distributed differently than cyclobutane dimers in nucleosomes. Photochem Photobiol. 1990 Apr;51(4):411–417. doi: 10.1111/j.1751-1097.1990.tb01732.x. [DOI] [PubMed] [Google Scholar]
- Ganesan A. K., Hanawalt P. C. Effect of a lexA41(Ts) mutation on DNA repair in recA(Def) derivatives of Escherichia coli K-12. Mol Gen Genet. 1985;201(3):387–392. doi: 10.1007/BF00331328. [DOI] [PubMed] [Google Scholar]
- Ganesan A. K., Smith K. C. Dark recovery processes in Escherichia coli irradiated with ultraviolet light. II. Effect of uvr genes on liquid holding recovery. J Bacteriol. 1969 Mar;97(3):1129–1133. doi: 10.1128/jb.97.3.1129-1133.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Green M. H., Bridges B. A., Eyfjörd J. E., Muriel W. J. Mutagenic DNA repair in escherichia coli. V. Mutation frequency decline and error-free post-replication repair in an excision-proficient strain. Mutat Res. 1977 Jan;42(1):33–44. doi: 10.1016/s0027-5107(77)80005-5. [DOI] [PubMed] [Google Scholar]
- Hanawalt P. C., Donahue B. A., Sweder K. S. Repair and transcription. Collision or collusion? Curr Biol. 1994 Jun 1;4(6):518–521. doi: 10.1016/s0960-9822(00)00112-3. [DOI] [PubMed] [Google Scholar]
- Kricker A., Armstrong B. K., English D. R. Sun exposure and non-melanocytic skin cancer. Cancer Causes Control. 1994 Jul;5(4):367–392. doi: 10.1007/BF01804988. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Mitchell D. L., Brash D. E., Nairn R. S. Rapid repair kinetics of pyrimidine(6-4)pyrimidone photoproducts in human cells are due to excision rather than conformational change. Nucleic Acids Res. 1990 Feb 25;18(4):963–971. doi: 10.1093/nar/18.4.963. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Mitchell D. L., Nairn R. S. The biology of the (6-4) photoproduct. Photochem Photobiol. 1989 Jun;49(6):805–819. doi: 10.1111/j.1751-1097.1989.tb05578.x. [DOI] [PubMed] [Google Scholar]
- Mitchell D. L., Nguyen T. D., Cleaver J. E. Nonrandom induction of pyrimidine-pyrimidone (6-4) photoproducts in ultraviolet-irradiated human chromatin. J Biol Chem. 1990 Apr 5;265(10):5353–5356. [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- SETLOW R. B., CARRIER W. L. THE DISAPPEARANCE OF THYMINE DIMERS FROM DNA: AN ERROR-CORRECTING MECHANISM. Proc Natl Acad Sci U S A. 1964 Feb;51:226–231. doi: 10.1073/pnas.51.2.226. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Svoboda D. L., Smith C. A., Taylor J. S., Sancar A. Effect of sequence, adduct type, and opposing lesions on the binding and repair of ultraviolet photodamage by DNA photolyase and (A)BC excinuclease. J Biol Chem. 1993 May 15;268(14):10694–10700. [PubMed] [Google Scholar]
- Szymkowski D. E., Lawrence C. W., Wood R. D. Repair by human cell extracts of single (6-4) and cyclobutane thymine-thymine photoproducts in DNA. Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):9823–9827. doi: 10.1073/pnas.90.21.9823. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vreeswijk M. P., van Hoffen A., Westland B. E., Vrieling H., van Zeeland A. A., Mullenders L. H. Analysis of repair of cyclobutane pyrimidine dimers and pyrimidine 6-4 pyrimidone photoproducts in transcriptionally active and inactive genes in Chinese hamster cells. J Biol Chem. 1994 Dec 16;269(50):31858–31863. [PubMed] [Google Scholar]
- 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]
- Ziegler A., Leffell D. J., Kunala S., Sharma H. W., Gailani M., Simon J. A., Halperin A. J., Baden H. P., Shapiro P. E., Bale A. E. Mutation hotspots due to sunlight in the p53 gene of nonmelanoma skin cancers. Proc Natl Acad Sci U S A. 1993 May 1;90(9):4216–4220. doi: 10.1073/pnas.90.9.4216. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
