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Global Genome Nucleotide Excision Repair Proteins Rhp7p and Rhp41p Are Involved in Abasic Site Repair of Schizosaccharomyces pombe

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DOI: 10.4236/abb.2015.64026    3,246 Downloads   3,703 Views   Citations

ABSTRACT

The roles of nucleotide excision repair (NER) proteins in removing UV-induced lesions are well defined. There are two distinct NER pathways: global genome NER (GG-NER) and transcription-coupled NER. In human GG-NER, two heteromeric protein complexes, DDB1-DDB2 and XPC-RAD23, are responsible for initial lesion recognition. Here, we examined the genetic interactions between GG-NER and base excision repair (BER) genes during abasic (AP) site repair of Schizosaccharomyces pombe. Mutants of rhp7 (rhp7-rhp16 are functional homologs of DDB1-DDB2) and rhp41 (XPC homolog) were moderately sensitive to methyl methanesulfonate and slightly to sodium bisulfite. Nth1p most actively cleaves the AP site in S. pombe. Deletion of rhp7 or rhp41 from nth1Δ cells greatly increased their sensitivity to alkylation and deamination, indicating that Rhp7p and Rhp41p are involved in repair of the AP sites generated by the action of DNA glycosylase. Induction of rhp7 and rhp16 genes by different types of DNA damage supports the ability of GG-NER to remove non-bulky lesions. Therefore, GG-NER activity not only targets bulky DNA helix-distorting lesions, but can also efficiently remove AP sites synergistically with BER.

Conflicts of Interest

The authors declare no conflicts of interest.

Cite this paper

Sakurai, E. , Susuki, M. , Kanamitsu, K. , Kawano, S. and Ikeda, S. (2015) Global Genome Nucleotide Excision Repair Proteins Rhp7p and Rhp41p Are Involved in Abasic Site Repair of Schizosaccharomyces pombe. Advances in Bioscience and Biotechnology, 6, 265-274. doi: 10.4236/abb.2015.64026.

References

[1] Friedberg, E.C., Walker, G.C., Siede, W., Wood, R.D., Schultz, R.A. and Ellenberger, T. (2006) DNA Repair and Mutagenesis. 2nd Edition, ASM Press, Washington DC.
[2] Hubscher, U., Maga, G. and Spadari, S. (2002) Eukaryotic DNA Polymerases. Annual Review of Biochemistry, 71, 133-163.
http://dx.doi.org/10.1146/annurev.biochem.71.090501.150041
[3] Goodman, M.F. (2002) Error-Prone Repair DNA Polymerases in Prokaryotes and Eukaryotes. Annual Review of Biochemistry, 71, 17-50.
http://dx.doi.org/10.1146/annurev.biochem.71.083101.124707
[4] Tornaletti, S., Maeda, L.S. and Hanawalt, P.C. (2006) Transcription Arrest at an Abasic Site in the Transcribed Strand of Template DNA. Chemical Research in Toxicology, 19, 1215-1220.
http://dx.doi.org/10.1021/tx060103g
[5] Hegde, M.L., Hazra, T.K. and Mitra, S. (2008) Early Steps in the DNA Base Excision/Single-Strand Interruption Repair Pathway in Mammalian Cells. Cell Research, 18, 27-47.
http://dx.doi.org/10.1038/cr.2008.8
[6] Robertson, A.B., Klungland, A., Rognes, T. and Leiros, I. (2009) Base Excision Repair: The Long and Short of It. Cellular and Molecular Life Sciences, 66, 981-993.
[7] Alseth, I., Korvald, H., Osman, F., Seeberg, E. and Bjørås, M. (2004) A General Role of the DNA Glycosylase Nth1 in the Abasic Sites Cleavage Step of Base Excision Repair in Schizosaccharomyces pombe. Nucleic Acids Research, 32, 5119-5125.
http://dx.doi.org/10.1093/nar/gkh851
[8] Sugimoto, T., Igawa, E., Tanihigashi, H., Matsubara, M., Ide, H. and Ikeda, S. (2005) Roles of Base Excision Repair Enzymes Nth1p and Apn2p from Schizosaccharomyces pombe in Processing Alkylation and Oxidative DNA Damage. DNA Repair, 4, 1270-1280.
http://dx.doi.org/10.1016/j.dnarep.2005.06.009
[9] Kanamitsu, K. and Ikeda, S. (2010) Early Steps in the DNA Base Excision Repair Pathway of a Fission Yeast Schizosaccharomyces pombe. Journal of Nucleic Acids, 2010, Article ID: 450926, 9 pages.
[10] Naegeli, H. and Sugasawa, K. (2011) The Xeroderma Pigmentosum Pathway: Decision Tree Analysis of DNA Quality. DNA Repair, 10, 673-683.
http://dx.doi.org/10.1016/j.dnarep.2011.04.019
[11] Melis, J.P., van Steeg, H. and Luijten, M. (2013) Oxidative DNA Damage and Nucleotide Excision Repair. Antioxidants & Redox Signaling, 18, 2409-2419.
http://dx.doi.org/10.1089/ars.2012.5036
[12] Lombaerts, M., Peltola, P.H., Visse, R., den Dulk, H., Brandsma, J.A. and Brouwer, J. (1999) Characterization of the rhp7+ and rhp16+ Genes in Schizosaccharomyces pombe. Nucleic Acids Research, 27, 3410-3416.
http://dx.doi.org/10.1093/nar/27.17.3410
[13] Latypov, V.F., Tubbs, J.L., Watson, A.J., Marriott, A.S., McGown, G., Thorncroft, M., Wilkinson, O.J., Senthong, P., Butt, A., Arvai, A.S., Millington, C.L., Povey, A.C., Williams, D.M., Santibanez-Koref, M.F., Tainer, J.A. and Margison, G.P. (2012) Atl1 Regulates Choice between Global Genome and Transcription-Coupled Repair of O6-Alkylguanines. Molecular Cell, 47, 50-60.
http://dx.doi.org/10.1016/j.molcel.2012.04.028
[14] Verhage, R., Zeeman, A.M., de Groot, N., Gleig, F., Bang, D.D., van de Putte, P. and Brouwer, J. (1994) 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. Molecular and Cellular Biology, 14, 6135-6142. http://dx.doi.org/10.1128/MCB.14.9.6135
[15] Reed, S.H., Akiyama, M., Stillman, B. and Friedberg, E.C. (1999) Yeast Autonomously Replicating Sequence Binding Factor Is Involved in Nucleotide Excision Repair. Genes & Development, 13, 3052-3058.
http://dx.doi.org/10.1101/gad.13.23.3052
[16] Teng, Y., Liu, H., Gill, H.W., Yu, Y., Waters, R. and Reed, S.H. (2008) Saccharomyces cerevisiae Rad16 Mediates Ultraviolet-Dependent Histone H3 Acetylation Required for Efficient Global Genome Nucleotide-Excision Repair. EMBO Reports, 9, 97-102.
http://dx.doi.org/10.1038/sj.embor.7401112
[17] Waters, R., Evans, K., Bennett, M., Yu, S. and Reed, S. (2012) Nucleotide Excision Repair in Cellular Chromatin: Studies with Yeast from Nucleotide to Gene to Genome. International Journal of Molecular Sciences, 13, 11141-11164.
http://dx.doi.org/10.3390/ijms130911141
[18] Fukumoto, Y., Hiyama, H., Yokoi, M., Nakaseko, Y., Yanagida, M. and Hanaoka, F. (2002) Two Budding Yeast RAD4 Homologs in Fission Yeast Play Different Roles in the Repair of UV-Induced DNA Damage. DNA Repair, 1, 833-845.
http://dx.doi.org/10.1016/S1568-7864(02)00108-8
[19] Marti, T.M., Kunz, C. and Fleck, O. (2003) Repair of Damaged and Mismatched DNA by the XPC Homologues Rhp41 and Rhp42 of Fission Yeast. Genetics, 164, 457-467.
[20] Yasuhira, S., Morimyo, M. and Yasui, A. (1999) Transcription Dependence and the Roles of Two Excision Repair Pathways for UV Damage in Fission Yeast Schizosaccharomyces pombe. The Journal of Biological Chemistry, 274, 26822-26827.
http://dx.doi.org/10.1074/jbc.274.38.26822
[21] Wang, L., Limbo, O., Fei, J., Chen, L., Kim, B., Luo, J., Chong, J., Conaway, R.C., Conaway, J.W., Ranish, J.A., Kadonaga, J.T., Russell, P. and Wang, D. (2014) Regulation of the Rhp26ERCC6/CSB Chromatin Remodeler by a Novel Conserved Leucine Latch Motif. Proceedings of the National Academy of Sciences of the United States of America, 111, 18566-18571.
http://dx.doi.org/10.1073/pnas.1420227112
[22] Xiao, W. and Chow, B.L. (1998) Synergism between Yeast Nucleotide and Base Excision Repair Pathways in the Protection against DNA Methylation Damage. Current Genetics, 33, 92-99.
http://dx.doi.org/10.1007/s002940050313
[23] Swanson, R.L., Morey, N.J., Doetsch, P.W. and Jinks-Robertson, S. (1999) Overlapping Specificities of Base Excision Repair, Nucleotide Excision Repair, Recombination, and Translesion Synthesis Pathways for DNA Base Damage in Saccharomyces cerevisiae. Molecular and Cellular Biology, 19, 2929-2935.
[24] Torres-Ramos, C.A., Johnson, R.E., Prakash, L. and Prakash, S. (2000) Evidence for the Involvement of Nucleotide Excision Repair in the Removal of Abasic Sites in Yeast. Molecular and Cellular Biology, 20, 3522-3528.
http://dx.doi.org/10.1128/MCB.20.10.3522-3528.2000
[25] Kim, N. and Jinks-Robertson, S. (2010) Abasic Sites in the Transcribed Strand of Yeast DNA Are Removed by Transcription-Coupled Nucleotide Excision Repair. Molecular and Cellular Biology, 30, 3206-3215.
http://dx.doi.org/10.1128/MCB.00308-10
[26] Memisoglu, A. and Samson, L. (2000) Contribution of Base Excision Repair, Nucleotide Excision Repair, and DNA Recombination to Alkylation Resistance of the Fission Yeast Schizosaccharomyces pombe. Journal of Bacteriology, 182, 2104-2112.
http://dx.doi.org/10.1128/JB.182.8.2104-2112.2000
[27] Alseth, I., Osman, F., Korvald, H., Tsaneva, I., Whitby, M.C., Seeberg, E. and Bjørås, M. (2005) Biochemical Characterization and DNA Repair Pathway Interactions of Mag1-Mediated Base Excision Repair in Schizosaccharomyces pombe. Nucleic Acids Research, 33, 1123-1131.
http://dx.doi.org/10.1093/nar/gki259
[28] Kanamitsu, K., Tanihigashi, H., Tanita, Y., Inatani, S. and Ikeda, S. (2007) Involvement of 3-Methyladenine DNA Glycosylases Mag1p and Mag2p in Base Excision Repair of Methyl Methanesulfonate-Damaged DNA in the Fission Yeast Schizosaccharomyces pombe. Genes & Genetic Systems, 82, 489-494.
http://dx.doi.org/10.1266/ggs.82.489
[29] Kunz, C. and Fleck, O. (2001) Role of the DNA Repair Nucleases Rad13, Rad2 and Uve1 of Schizosaccharomyces pombe in Mismatch Correction. Journal of Molecular Biology, 313, 241-253.
http://dx.doi.org/10.1006/jmbi.2001.5054
[30] Osman, F., Bjørås, M., Alseth, I., Morland, I., McCready, S., Seeberg, E. and Tsaneva, I. (2003) A New Schizosaccharomyces pombe Base Excision Repair Mutant, nth1, Reveals Overlapping Pathways for Repair of DNA Base Damage. Molecular Microbiology, 48, 465-480.
http://dx.doi.org/10.1046/j.1365-2958.2003.03440.x
[31] Kanamitsu, K. and Ikeda, S. (2011) Fission Yeast Homologs of Human XPC and CSB, rhp41 and rhp26, Are Involved in Transcription-Coupled Repair of Methyl Methanesulfonate-Induced DNA Damage. Genes & Genetic Systems, 86, 83-91.
http://dx.doi.org/10.1266/ggs.86.83
[32] Bähler, J., Wu, J.Q., Longtine, M.S., Shah, N.G., McKenzie 3rd, A., Steever, A.B., Wach, A., Philippsen, P. and Pringle, J.R. (1998) Heterologous Modules for Efficient and Versatile PCR-Based Gene Targeting in Schizosaccharomyces pombe. Yeast, 14, 943-951.
http://dx.doi.org/10.1002/(SICI)1097-0061(199807)14:10<943::AID-YEA292>3.0.CO;2-Y
[33] Lafuente, M.J., Petit, T. and Gancedo, C. (1997) A Series of Vectors to Construct lacZ Fusions for the Study of Gene Expression in Schizosaccharomyces pombe. FEBS Letters, 420, 39-42.
http://dx.doi.org/10.1016/S0014-5793(97)01486-5
[34] McCready, S.J., Osman, F. and Yasui, A. (2000) Repair of UV Damage in the Fission Yeast Schizosaccharomyces pombe. Mutation Research, 451, 197-210.
http://dx.doi.org/10.1016/S0027-5107(00)00050-6
[35] Tanihigashi, H., Yamada, A., Igawa, E. and Ikeda, S. (2006) The Role of Schizosaccharomyces pombe DNA Repair Enzymes Apn1p and Uve1p in the Base Excision Repair of Apurinic/Apyrimidinic Sites. Biochemistry and Biophysics Research Communications, 347, 889-894.
http://dx.doi.org/10.1016/j.bbrc.2006.06.191
[36] Hayatsu, H. (1976) Bisulfite Modification of Nucleic Acids and Their Constituents. Progress in Nucleic Acid Research and Molecular Biology, 16, 75-124.
http://dx.doi.org/10.1016/S0079-6603(08)60756-4
[37] Elder, R.T., Zhu, X., Priet, S., Chen, M., Yu, M., Navarro, J.M., Sire, J. and Zhao, Y. (2003) A Fission Yeast Homologue of the Human Uracil-DNA-Glycosylase and Their Roles in Causing DNA Damage after Overexpression. Biochemistry and Biophysics Research Communications, 306, 693-700.
http://dx.doi.org/10.1016/S0006-291X(03)01036-2
[38] Ikeda, M., Ikeda, R. and Ikeda, S. (2009) Spontaneous Mutation in Uracil DNA Gkycosylase-Deficient Cells of a Fission Yeast Schizosaccharomyces pombe. Current Topics in Biochemical Research, 11, 55-60.
[39] Pascucci, B., D’Errico, M., Parlanti, E., Giovannini, S. and Dogliotti, E. (2011) Role of Nucleotide Excision Repair Proteins in Oxidative DNA Damage Repair: An Updating. Biochemistry (Moscow), 76, 4-15.
http://dx.doi.org/10.1134/S0006297911010032
[40] Shimizu, Y., Iwai, S., Hanaoka, F. and Sugasawa, K. (2003) Xeroderma Pigmentosum Group C Protein Interacts Physically and Functionally with Thymine DNA Glycosylase. The EMBO Journal, 22, 164-173.
http://dx.doi.org/10.1093/emboj/cdg016
[41] Miao, F., Bouziane, M., Dammann, R., Masutani, C., Hanaoka, F., Pfeifer, G. and O’Connor, T.R. (2000) 3-Methyladenine-DNA Glycosylase (MPG Protein) Interacts with Human RAD23 Proteins. The Journal of Biological Chemistry, 275, 28433-28438.
http://dx.doi.org/10.1074/jbc.M001064200
[42] Shimizu, Y., Uchimura, Y., Dohmae, N., Saitoh, H., Hanaoka, F. and Sugasawa, K. (2010) Stimulation of DNA Glycosylase Activities by XPC Protein Complex: Roles of Protein-Protein Interactions. Journal of Nucleic Acids, 2010, Article ID: 805698.
[43] Huang, J.C., Hsu, D.S., Kazantsev, A. and Sancar, A. (1994) Substrate Spectrum of Human Excinuclease: Repair of Abasic Sites, Methylated Bases, Mismatches, and Bulky Adducts. Proceedings of the National Academy of Sciences of the United States of America, 91, 12213-12217. http://dx.doi.org/10.1073/pnas.91.25.12213
[44] Tubbs, J.L., Latypov, V., Kanugula, S., Butt, A., Melikishvili, M., Kraehenbuehl, R., Fleck, O., Marriott, A., Watson, A.J., Verbeek, B., McGown, G., Thorncroft, M., Santibanez-Koref, M.F., Millington, C., Arvai, A.S., Kroeger, M.D., Peterson, L.A., Williams, D.M., Fried, M.G., Margison, G.P., Pegg, A.E. and Tainer, J.A. (2009) Flipping of Alkylated DNA Damage Bridges Base and Nucleotide Excision Repair. Nature, 459, 808-813.
http://dx.doi.org/10.1038/nature08076
[45] Wittschieben, B.Ø., Iwai, S. and Wood, R.D. (2005) DDB1-DDB2 (Xeroderma Pigmentosum Group E) Protein Complex Recognizes a Cyclobutane Pyrimidine Dimer, Mismatches, Apurinic/Apyrimidinic Sites, and Compound Lesions in DNA. The Journal of Biological Chemistry, 280, 39982-39989.
http://dx.doi.org/10.1074/jbc.M507854200

  
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