UV-induced Endonuclease III-sensitive Sites at the Mating Type Loci in Saccharomyces Cerevisiae Are Repaired by Nucleotide Excision Repair: RAD7 and RAD16 Are Not Required for Their Removal from HML Alpha

Overview

Journal Mol Gen Genet

Specialties Genetics
Molecular Biology

Date 1996 Mar 7

PMID 8602168

Citations 10

Authors

S H Reed

S Boiteux

R Waters

Affiliations

Soon will be listed here.

Abstract

Ultraviolet irradiation of DNA induces cyclobutane pyrimidine dimers (CPDs) 6-4'-(pyrimidine 2'-one) pyrimidines and pyrimidine hydrates. The dimer is the major photoproduct, and is specifically recognized by endonuclease V of phage T4. Pyrimidine hydrates represent a small fraction of the total photoproducts, and are substrates for endonuclease III of Escherichia coli. We used these enzymes to follow the fate of their substrates in the mating type loci of Saccharomyces cerevisiae. In a RAD strain, CPSs in the transcriptionally active MAT alpha locus are preferentially repaired relative to the inactive HML alpha locus, whilst repair of endonuclease III-sensitive sites is not preferential. The rad1, 2, 3 and 4 mutants, which lack factors that are essential for the incision step of nucleotide excision repair (NER), repair neither CPDs nor endonuclease III-sensitive sites, clearly showing that these lesions are repaired by by NER pathway. Previously it had been shown that the products of the RAD7 and RAD16 genes are required for the NER of CPDs from the HML alpha locus. We show that, in the same locus, these gene products are not needed for removal of endonuclease III-sensitive sites by the same mechanism. This indicates that the components required for NER differ depending on either the type of lesion encountered or on the specific location of the lesion within the genome.

Citing Articles

How chromatin is remodelled during DNA repair of UV-induced DNA damage in Saccharomyces cerevisiae.

Yu S, Teng Y, Waters R, Reed S PLoS Genet. 2011; 7(6):e1002124.

PMID: 21698136 PMC: 3116912. DOI: 10.1371/journal.pgen.1002124.

ABF1-binding sites promote efficient global genome nucleotide excision repair.

Yu S, Smirnova J, Friedberg E, Stillman B, Akiyama M, Owen-Hughes T J Biol Chem. 2008; 284(2):966-73.

PMID: 18996839 PMC: 3443742. DOI: 10.1074/jbc.M806830200.

Roles for Gcn5p and Ada2p in transcription and nucleotide excision repair at the Saccharomyces cerevisiae MET16 gene.

Ferreiro J, Powell N, Karabetsou N, Mellor J, Waters R Nucleic Acids Res. 2006; 34(3):976-85.

PMID: 16473851 PMC: 1363778. DOI: 10.1093/nar/gkj501.

Cbf1p modulates chromatin structure, transcription and repair at the Saccharomyces cerevisiae MET16 locus.

Ferreiro J, Powell N, Karabetsou N, Kent N, Mellor J, Waters R Nucleic Acids Res. 2004; 32(5):1617-26.

PMID: 15007107 PMC: 390324. DOI: 10.1093/nar/gkh324.

Photoreactivation of UV-induced cyclobutane pyrimidine dimers in the MFA2 gene of Saccharomyces cerevisiae.

Morse N, Meniel V, Waters R Nucleic Acids Res. 2002; 30(8):1799-807.

PMID: 11937634 PMC: 113223. DOI: 10.1093/nar/30.8.1799.

References

Mccready S . Repair of 6-4 photoproducts and cyclobutane pyrimidine dimers in rad mutants of Saccharomyces cerevisiae. Mutat Res. 1994; 315(3):261-73. DOI: 10.1016/0921-8777(94)90037-x. View

Van Houten B, Snowden A . Mechanism of action of the Escherichia coli UvrABC nuclease: clues to the damage recognition problem. Bioessays. 1993; 15(1):51-9. DOI: 10.1002/bies.950150108. View

Waters R, MOUSTACCHI E . The fate of ultraviolet-induced pyrimidine dimers in the mitochondrial DNA of Saccharomyces cerevisiae following various post-irradiation cell treatments. Biochim Biophys Acta. 1974; 366(3):241-50. DOI: 10.1016/0005-2787(74)90282-2. View

Sage E . Distribution and repair of photolesions in DNA: genetic consequences and the role of sequence context. Photochem Photobiol. 1993; 57(1):163-74. DOI: 10.1111/j.1751-1097.1993.tb02273.x. View

ODonnell R, Boorstein R, Cunningham R, Teebor G . Effect of pH and temperature on the stability of UV-induced repairable pyrimidine hydrates in DNA. Biochemistry. 1994; 33(33):9875-80. DOI: 10.1021/bi00199a008. View

Feaver W, Svejstrup J, Bardwell L, Bardwell A, Buratowski S, Gulyas K . Dual roles of a multiprotein complex from S. cerevisiae in transcription and DNA repair. Cell. 1993; 75(7):1379-87. DOI: 10.1016/0092-8674(93)90624-y. View

Leadon S, Cooper P . Preferential repair of ionizing radiation-induced damage in the transcribed strand of an active human gene is defective in Cockayne syndrome. Proc Natl Acad Sci U S A. 1993; 90(22):10499-503. PMC: 47804. DOI: 10.1073/pnas.90.22.10499. View

Schild D, Glassner B, MORTIMER R, Carlson M, Laurent B . Identification of RAD16, a yeast excision repair gene homologous to the recombinational repair gene RAD54 and to the SNF2 gene involved in transcriptional activation. Yeast. 1992; 8(5):385-95. DOI: 10.1002/yea.320080506. View

Reed S, Mccready S, Boiteux S, Waters R . The levels of repair of endonuclease III-sensitive sites, 6-4 photoproducts and cyclobutane pyrimidine dimers differ in a point mutant for RAD14, the Saccharomyces cerevisiae homologue of the human gene defective in XPA patients. Mol Gen Genet. 1996; 250(4):515-22. DOI: 10.1007/BF02174040. View

10.

Gossett J, Lee K, Cunningham R, Doetsch P . Yeast redoxyendonuclease, a DNA repair enzyme similar to Escherichia coli endonuclease III. Biochemistry. 1988; 27(7):2629-34. DOI: 10.1021/bi00407a054. View

11.

Sancar A, Tang M . Nucleotide excision repair. Photochem Photobiol. 1993; 57(5):905-21. DOI: 10.1111/j.1751-1097.1993.tb09233.x. View

12.

Lin J, Sancar A . A new mechanism for repairing oxidative damage to DNA: (A)BC excinuclease removes AP sites and thymine glycols from DNA. Biochemistry. 1989; 28(20):7979-84. DOI: 10.1021/bi00446a002. View

13.

Mellon I, HANAWALT P . Induction of the Escherichia coli lactose operon selectively increases repair of its transcribed DNA strand. Nature. 1989; 342(6245):95-8. DOI: 10.1038/342095a0. View

14.

Nakabeppu Y, Yamashita K, Sekiguchi M . Purification and characterization of normal and mutant forms of T4 endonuclease V. J Biol Chem. 1982; 257(5):2556-62. View

15.

Kow Y, Wallace S, Van Houten B . UvrABC nuclease complex repairs thymine glycol, an oxidative DNA base damage. Mutat Res. 1990; 235(2):147-56. DOI: 10.1016/0921-8777(90)90068-g. View

16.

Bohr V, Smith C, Okumoto D, HANAWALT P . 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; 40(2):359-69. DOI: 10.1016/0092-8674(85)90150-3. View

17.

Ganguly T, Duker N . Stability of DNA thymine hydrates. Nucleic Acids Res. 1991; 19(12):3319-23. PMC: 328329. DOI: 10.1093/nar/19.12.3319. View

18.

Verhage R, Zeeman A, De Groot N, Gleig F, Bang D, Van de Putte P . The RAD7 and RAD16 genes, which are essential for pyrimidine dimer removal from the silent mating type loci, are also required for repair of the nontranscribed strand of an active gene in Saccharomyces cerevisiae. Mol Cell Biol. 1994; 14(9):6135-42. PMC: 359140. DOI: 10.1128/mcb.14.9.6135-6142.1994. View

19.

Thompson J, Landy A . Empirical estimation of protein-induced DNA bending angles: applications to lambda site-specific recombination complexes. Nucleic Acids Res. 1988; 16(20):9687-705. PMC: 338773. DOI: 10.1093/nar/16.20.9687. View

20.

Wilcox D, Prakash L . Incision and postincision steps of pyrimidine dimer removal in excision-defective mutants of Saccharomyces cerevisiae. J Bacteriol. 1981; 148(2):618-23. PMC: 216247. DOI: 10.1128/jb.148.2.618-623.1981. View