Abstract
The bacteriophage T4 denV gene encodes a well-characterized DNA repair enzyme involved in pyrimidine photodimer excision. We have discovered the first homologs of the denV gene in chlorella viruses, which are common in fresh water. This gene functions in vivo and also when cloned in Escherichia coli. Photodamaged virus DNA can also be photoreactivated by the host chlorella. Since the chlorella viruses are continually exposed to solar radiation in their native environments, two separate DNA repair systems, one that functions in the dark and one that functions in the light, significantly enhance their survival.
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- Bernstein H., Bernstein C. Bacteriophage T4 genetic homologies with bacteria and eucaryotes. J Bacteriol. 1989 May;171(5):2265–2270. doi: 10.1128/jb.171.5.2265-2270.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Demple B., Linn S. DNA N-glycosylases and UV repair. Nature. 1980 Sep 18;287(5779):203–208. doi: 10.1038/287203a0. [DOI] [PubMed] [Google Scholar]
- Dodson M. L., Schrock R. D., 3rd, Lloyd R. S. Evidence for an imino intermediate in the T4 endonuclease V reaction. Biochemistry. 1993 Aug 17;32(32):8284–8290. doi: 10.1021/bi00083a032. [DOI] [PubMed] [Google Scholar]
- Doi T., Recktenwald A., Karaki Y., Kikuchi M., Morikawa K., Ikehara M., Inaoka T., Hori N., Ohtsuka E. Role of the basic amino acid cluster and Glu-23 in pyrimidine dimer glycosylase activity of T4 endonuclease V. Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9420–9424. doi: 10.1073/pnas.89.20.9420. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grafstrom R. H., Park L., Grossman L. Enzymatic repair of pyrimidine dimer-containing DNA. A 5' dimer DNA glycosylase: 3'-apyrimidinic endonuclease mechanism from Micrococcus luteus. J Biol Chem. 1982 Nov 25;257(22):13465–13474. [PubMed] [Google Scholar]
- Hamilton K. K., Kim P. M., Doetsch P. W. A eukaryotic DNA glycosylase/lyase recognizing ultraviolet light-induced pyrimidine dimers. Nature. 1992 Apr 23;356(6371):725–728. doi: 10.1038/356725a0. [DOI] [PubMed] [Google Scholar]
- Hori N., Doi T., Karaki Y., Kikuchi M., Ikehara M., Ohtsuka E. Participation of glutamic acid 23 of T4 endonuclease V in the beta-elimination reaction of an abasic site in a synthetic duplex DNA. Nucleic Acids Res. 1992 Sep 25;20(18):4761–4764. doi: 10.1093/nar/20.18.4761. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Howard-Flanders P., Theriot L., Stedeford J. B. Some properties of excision-defective recombination-deficient mutants of Escherichia coli K-12. J Bacteriol. 1969 Mar;97(3):1134–1141. doi: 10.1128/jb.97.3.1134-1141.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kokjohn T. A., Miller R. V. IncN plasmids mediate UV resistance and error-prone repair in Pseudomonas aeruginosa PAO. Microbiology. 1994 Jan;140(Pt 1):43–48. doi: 10.1099/13500872-140-1-43. [DOI] [PubMed] [Google Scholar]
- Landstein D., Burbank D. E., Nietfeldt J. W., Van Etten J. L. Large deletions in antigenic variants of the chlorella virus PBCV-1. Virology. 1995 Dec 20;214(2):413–420. doi: 10.1006/viro.1995.0051. [DOI] [PubMed] [Google Scholar]
- Lloyd R. S., Hanawalt P. C. Expression of the denV gene of bacteriophage T4 cloned in Escherichia coli. Proc Natl Acad Sci U S A. 1981 May;78(5):2796–2800. doi: 10.1073/pnas.78.5.2796. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lu Z., Li Y., Zhang Y., Kutish G. F., Rock D. L., Van Etten J. L. Analysis of 45 kb of DNA located at the left end of the chlorella virus PBCV-1 genome. Virology. 1995 Jan 10;206(1):339–352. doi: 10.1016/s0042-6822(95)80049-2. [DOI] [PubMed] [Google Scholar]
- Manuel R. C., Czerwinski E. W., Lloyd R. S. Identification of the structural and functional domains of MutY, an Escherichia coli DNA mismatch repair enzyme. J Biol Chem. 1996 Jul 5;271(27):16218–16226. doi: 10.1074/jbc.271.27.16218. [DOI] [PubMed] [Google Scholar]
- Mitra A., Higgins D. W., Rohe N. J. A Chlorella virus gene promoter functions as a strong promoter both in plants and bacteria. Biochem Biophys Res Commun. 1994 Oct 14;204(1):187–194. doi: 10.1006/bbrc.1994.2443. [DOI] [PubMed] [Google Scholar]
- Morikawa K., Matsumoto O., Tsujimoto M., Katayanagi K., Ariyoshi M., Doi T., Ikehara M., Inaoka T., Ohtsuka E. X-ray structure of T4 endonuclease V: an excision repair enzyme specific for a pyrimidine dimer. Science. 1992 Apr 24;256(5056):523–526. doi: 10.1126/science.1575827. [DOI] [PubMed] [Google Scholar]
- Mullis K. B., Faloona F. A. Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction. Methods Enzymol. 1987;155:335–350. doi: 10.1016/0076-6879(87)55023-6. [DOI] [PubMed] [Google Scholar]
- Nakabeppu Y., Sekiguchi M. Physical association of pyrimidine dimer DNA glycosylase and apurinic/apyrimidinic DNA endonuclease essential for repair of ultraviolet-damaged DNA. Proc Natl Acad Sci U S A. 1981 May;78(5):2742–2746. doi: 10.1073/pnas.78.5.2742. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Piersen C. E., Prince M. A., Augustine M. L., Dodson M. L., Lloyd R. S. Purification and cloning of Micrococcus luteus ultraviolet endonuclease, an N-glycosylase/abasic lyase that proceeds via an imino enzyme-DNA intermediate. J Biol Chem. 1995 Oct 6;270(40):23475–23484. doi: 10.1074/jbc.270.40.23475. [DOI] [PubMed] [Google Scholar]
- Radany E. H., Friedberg E. C. A pyrimidine dimer-DNA glycosylase activity associated with the v gene product of bacterophage T4. Nature. 1980 Jul 10;286(5769):182–185. doi: 10.1038/286182a0. [DOI] [PubMed] [Google Scholar]
- Reisser W., Burbank D. E., Meints S. M., Meints R. H., Becker B., Van Etten J. L. A comparison of viruses infecting two different Chlorella-like green algae. Virology. 1988 Nov;167(1):143–149. doi: 10.1016/0042-6822(88)90063-3. [DOI] [PubMed] [Google Scholar]
- Rohozinski J., Girton L. E., Van Etten J. L. Chlorella viruses contain linear nonpermuted double-stranded DNA genomes with covalently closed hairpin ends. Virology. 1989 Feb;168(2):363–369. doi: 10.1016/0042-6822(89)90277-8. [DOI] [PubMed] [Google Scholar]
- Ross P. M., Woodley K., Baird M. Quantitative autoradiography of dot blots using a microwell densitometer. Biotechniques. 1989 Jul-Aug;7(7):680–688. [PubMed] [Google Scholar]
- Schrock R. D., 3rd, Lloyd R. S. Reductive methylation of the amino terminus of endonuclease V eradicates catalytic activities. Evidence for an essential role of the amino terminus in the chemical mechanisms of catalysis. J Biol Chem. 1991 Sep 15;266(26):17631–17639. [PubMed] [Google Scholar]
- Schuster A. M., Girton L., Burbank D. E., Van Etten J. L. Infection of a Chlorella-like alga with the virus PBCV-1: transcriptional studies. Virology. 1986 Jan 15;148(1):181–189. doi: 10.1016/0042-6822(86)90413-7. [DOI] [PubMed] [Google Scholar]
- Seawell P. C., Smith C. A., Ganesan A. K. den V gene of bacteriophage T4 determines a DNA glycosylase specific for pyrimidine dimers in DNA. J Virol. 1980 Sep;35(3):790–796. doi: 10.1128/jvi.35.3.790-796.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shiota S., Nakayama H. UV endonuclease of Micrococcus luteus, a cyclobutane pyrimidine dimer-DNA glycosylase/abasic lyase: cloning and characterization of the gene. Proc Natl Acad Sci U S A. 1997 Jan 21;94(2):593–598. doi: 10.1073/pnas.94.2.593. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Simonson C. S., Kokjohn T. A., Miller R. V. Inducible UV repair potential of Pseudomonas aeruginosa PAO. J Gen Microbiol. 1990 Jul;136(7):1241–1249. doi: 10.1099/00221287-136-7-1241. [DOI] [PubMed] [Google Scholar]
- Skrdla M. P., Burbank D. E., Xia Y., Meints R. H., Van Etten J. L. Structural proteins and lipids in a virus, PBCV-1, which replicates in a Chlorella-like alga. Virology. 1984 Jun;135(2):308–315. doi: 10.1016/0042-6822(84)90188-0. [DOI] [PubMed] [Google Scholar]
- Suttle C. A., Chan A. M. Dynamics and Distribution of Cyanophages and Their Effect on Marine Synechococcus spp. Appl Environ Microbiol. 1994 Sep;60(9):3167–3174. doi: 10.1128/aem.60.9.3167-3174.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Suttle C. A., Chen F. Mechanisms and rates of decay of marine viruses in seawater. Appl Environ Microbiol. 1992 Nov;58(11):3721–3729. doi: 10.1128/aem.58.11.3721-3729.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- VAN Etten J. L., Burbank D. E., Kuczmarski D., Meints R. H. Virus infection of culturable chlorella-like algae and dlevelopment of a plaque assay. Science. 1983 Feb 25;219(4587):994–996. doi: 10.1126/science.219.4587.994. [DOI] [PubMed] [Google Scholar]
- Valerie K., Henderson E. E., de Riel J. K. Expression of a cloned denV gene of bacteriophage T4 in Escherichia coli. Proc Natl Acad Sci U S A. 1985 Jul;82(14):4763–4767. doi: 10.1073/pnas.82.14.4763. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Van Etten J. L., Burbank D. E., Schuster A. M., Meints R. H. Lytic viruses infecting a Chlorella-like alga. Virology. 1985 Jan 15;140(1):135–143. doi: 10.1016/0042-6822(85)90452-0. [DOI] [PubMed] [Google Scholar]
- Van Etten J. L., Lane L. C., Meints R. H. Viruses and viruslike particles of eukaryotic algae. Microbiol Rev. 1991 Dec;55(4):586–620. doi: 10.1128/mr.55.4.586-620.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Van Etten J. L., Van Etten C. H., Johnson J. K., Burbank D. E. A survey for viruses from fresh water that infect a eucaryotic chlorella-like green alga. Appl Environ Microbiol. 1985 May;49(5):1326–1328. doi: 10.1128/aem.49.5.1326-1328.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vassylyev D. G., Kashiwagi T., Mikami Y., Ariyoshi M., Iwai S., Ohtsuka E., Morikawa K. Atomic model of a pyrimidine dimer excision repair enzyme complexed with a DNA substrate: structural basis for damaged DNA recognition. Cell. 1995 Dec 1;83(5):773–782. doi: 10.1016/0092-8674(95)90190-6. [DOI] [PubMed] [Google Scholar]
- Wang I. N., Li Y., Que Q., Bhattacharya M., Lane L. C., Chaney W. G., Van Etten J. L. Evidence for virus-encoded glycosylation specificity. Proc Natl Acad Sci U S A. 1993 May 1;90(9):3840–3844. doi: 10.1073/pnas.90.9.3840. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Warner H. R., Demple B. F., Deutsch W. A., Kane C. M., Linn S. Apurinic/apyrimidinic endonucleases in repair of pyrimidine dimers and other lesions in DNA. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4602–4606. doi: 10.1073/pnas.77.8.4602. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weigle J. J. Induction of Mutations in a Bacterial Virus. Proc Natl Acad Sci U S A. 1953 Jul;39(7):628–636. doi: 10.1073/pnas.39.7.628. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yamada T., Higashiyama T., Fukuda T. Screening of natural waters for viruses which infect chlorella cells. Appl Environ Microbiol. 1991 Dec;57(12):3433–3437. doi: 10.1128/aem.57.12.3433-3437.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yasuda S., Sekiguchi M. T4 endonuclease involved in repair of DNA. Proc Natl Acad Sci U S A. 1970 Dec;67(4):1839–1845. doi: 10.1073/pnas.67.4.1839. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhang Y. P., Burbank D. E., Van Etten J. L. Chlorella viruses isolated in China. Appl Environ Microbiol. 1988 Sep;54(9):2170–2173. doi: 10.1128/aem.54.9.2170-2173.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]