Regulation of base excision repair: Ntg1 nuclear and mitochondrial dynamic localization in response to genotoxic stress

Nucleic Acids Research

Volumn 38, Issue 12, 2010, Pages 3963-3974

  Swartzlander, Dan B ^a   Griffiths, Lyra M ^a   Lee, Joan ^a   Degtyareva, Natalya P ^a   Doetsch, Paul W ^a   Corbett, Anita H ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONTRAST MEDIUM; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; NTG1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SIGNAL PEPTIDE;

ARTICLE; CELL STRESS; GENOTOXICITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; ACTIVE TRANSPORT; AMINO ACID SUBSTITUTION; CELL NUCLEUS; CHEMISTRY; DNA DAMAGE; DNA REPAIR; ENZYMOLOGY; METABOLISM; MITOCHONDRION; NUCLEAR LOCALIZATION SIGNAL; OXIDATIVE STRESS;

SACCHAROMYCES CEREVISIAE;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SUBSTITUTION; CELL NUCLEUS; DNA DAMAGE; DNA REPAIR; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; MITOCHONDRIA; NUCLEAR LOCALIZATION SIGNALS; OXIDATIVE STRESS; PROTEIN SORTING SIGNALS; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 77955073759     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq108     Document Type: Article

References (68)

1. Polyak, K., Li, Y., Zhu, H., Lengauer, C., Willson, J.K., Markowitz, S.D., Trush, M.A., Kinzler, K.W. and Vogelstein, B. (1998) Somatic mutations of the mitochondrial genome in human colorectal tumours. Nat. Genet., 20, 291-293.
2. Kujoth, G.C., Hiona, A., Pugh, T.D., Someya, S., Panzer, K., Wohlgemuth, S.E., Hofer, T., Seo, A.Y., Sullivan, R., Jobling, W.A. et al. (2005) Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science, 309, 481-484.
3. Altieri, F., Grillo, C., Maceroni, M. and Chichiarelli, S. (2008) DNA damage and repair: from molecular mechanisms to health implications. Antioxid. Redox Signal, 10, 891-937.
4. Slupphaug, G., Kavli, B. and Krokan, H.E. (2003) The interacting pathways for prevention and repair of oxidative DNA damage. Mutat. Res., 531, 231-251.
5. Richter, C., Park, J.W. and Ames, B.N. (1988) Normal oxidative damage to mitochondrial and nuclear DNA is extensive. Proc. Natl Acad. Sci. USA, 85, 6465-6467.
6. Augeri, L., Hamilton, K.K., Martin, A.M., Yohannes, P. and Doetsch, P.W. (1994) Methods in Enzymology, Vol. 234. Academic Press, San Diego, CA, USA, pp. 102-115.
7. Senturker, S., Auffret van der Kemp, P., You, H.J., Doetsch, P.W., Dizdaroglu, M. and Boiteux, S. (1998) Substrate specificities of the Ntg1 and Ntg2 proteins of Saccharomyces cerevisiae for oxidized DNA bases are not identical. Nucleic Acids Res., 26, 5270-5276.
8. You, H.J., Swanson, R.L. and Doetsch, P.W. (1998) Saccharomyces cerevisiae possesses two functional homologues of Escherichia coli endonuclease III. Biochemistry, 37, 6033-6040.
9. Hanna, M., Chow, B.L., Morey, N.J., Jinks-Robertson, S., Doetsch, P.W. and Xiao, W. (2004) Involvement of two endonuclease III homologs in the base excision repair pathway for the processing of DNA alkylation damage in Saccharomyces cerevisiae. DNA Repair, 3, 51-59.
10. Aspinwall, R., Rothwell, D.G., Roldan-Arjona, T., Anselmino, C., Ward, C.J., Cheadle, J.P., Sampson, J.R., Lindahl, T., Harris, P.C. and Hickson, I.D. (1997) Cloning and characterization of a functional human homolog of Escherichia coli endonuclease III. Proc. Natl Acad. Sci. USA, 94, 109-114.
11. You, H.J., Swanson, R.L., Harrington, C., Corbett, A.H., Jinks-Robertson, S., Senturker, S., Wallace, S.S., Boiteux, S., Dizdaroglu, M. and Doetsch, P.W. (1999) Saccharomyces cerevisiae Ntg1p and Ntg2p: broad specificity N-glycosylases for the repair of oxidative DNA damage in the nucleus and mitochondria. Biochemistry, 38, 11298-11306.
12. Gossett, J., Lee, K., Cunningham, R.P. and Doetsch, P.W. (1988) Yeast redoxyendonuclease, a DNA repair enzyme similar to Escherichia coli endonuclease III. Biochemistry, 27, 2629-2634.
13. Hilbert, T.P., Chaung, W., Boorstein, R.J., Cunningham, R.P. and Teebor, G.W. (1997) Cloning and expression of the cDNA encoding the human homologue of the DNA repair enzyme, Escherichia coli endonuclease III. J. Biol. Chem., 272, 6733-6740.
14. Alseth, I., Eide, L., Pirovano, M., Rognes, T., Seeberg, E. and Bjoras, M. (1999) The Saccharomyces cerevisiae homologues of endonuclease III from Escherichia coli, Ntg1 and Ntg2, are both required for efficient repair of spontaneous and induced oxidative DNA damage in yeast. Mol. Cell. Biol., 19, 3779-3787.
15. Griffiths, L.M., Swartzlander, D., Meadows, K.L., Wilkinson, K.D., Corbett, A.H. and Doetsch, P.W. (2009) Dynamic compartmentalization of base excision repair proteins in response to nuclear and mitochondrial oxidative stress. Mol. Cell. Biol., 29, 794-807.
16. Ikeda, S., Kohmoto, T., Tabata, R. and Seki, Y. (2002) Differential intracellular localization of the human and mouse endonuclease III homologs and analysis of the sorting signals. DNA Repair (Amst), 1, 847-854.
17. Evert, B.A., Salmon, T.B., Song, B., Jingjing, L., Siede, W. and Doetsch, P.W. (2004) Spontaneous DNA damage in Saccharomyces cerevisiae elicits phenotypic properties similar to cancer cells. J. Biol. Chem., 279, 22585-22594.
18. Doudican, N.A., Song, B., Shadel, G.S. and Doetsch, P.W. (2005) Oxidative DNA damage causes mitochondrial genomic instability in Saccharomyces cerevisiae. Mol. Cell. Biol., 25, 5196-5204.
19. Ide, H. and Kotera, M. (2004) Human DNA glycosylases involved in the repair of oxidatively damaged DNA. Biol. Pharm. Bull., 27, 480-485.
20. 2 induces translocation of APE/Ref-1 to mitochondria in the Raji B-cell line. J. Cell. Physiol., 193, 180-186.
21. Yoon, J.H., Qiu, J., Cai, S., Chen, Y., Cheetham, M.E., Shen, B. and Pfeifer, G.P. (2006) The retinitis pigmentosa-mutated RP2 protein exhibits exonuclease activity and translocates to the nucleus in response to DNA damage. Exp. Cell. Res., 312, 1323-1334.
22. Liu, W., Nichols, A.F., Graham, J.A., Dualan, R., Abbas, A. and Linn, S. (2000) Nuclear transport of human DDB protein induced by ultraviolet light. J. Biol. Chem., 275, 21429-21434.
23. Augeri, L., Lee, Y.M., Barton, A.B. and Doetsch, P.W. (1997) Purification, Characterization, Gene Cloning, and Expression of Saccharomyces cerevisiae Redoxyendonuclease, a Homolog of Escherichia coli Endonuclease III. Biochemistry, 36, 721-729.
24. Lange, A., Mills, R.E., Lange, C.J., Stewart, M., Devine, S.E. and Corbett, A.H. (2007) Classical nuclear localization signals: definition, function, and interaction with importin alpha. J. Biol. Chem., 282, 5101-5105.
25. Görlich, D., Kostka, S., Kraft, R., Dingwall, C., Laskey, R.A., Hartmann, E. and Prehn, S. (1995) Two different subunits of importin cooperate to recognize nuclear localization signals and bind them to the nuclear envelope. Curr. Biol., 5, 383-392.
26. Neupert, W. and Herrmann, J.M. (2007) Translocation of Proteins into Mitochondria. Annu. Rev. Biochem., 76, 723-749.
27. Bruch, M.D. and Hoyt, D.W. (1992) Conformational analysis of a mitochondrial presequence derived from the F1-ATPase [beta]-subunit by CD and NMR spectroscopy. Biochim. Biophys. Acta - Protein Struct. Mol. Enzymol., 1159, 81-93.
28. Wang, Y. and Weiner, H. (1994) Evaluation of electrostatic and hydrophobic effects on the interaction of mitochondrial signal sequences with phospholipid bilayers. Biochemistry, 33, 12860-12867.
29. Dekker, P.J., Martin, F., Maarse, A.C., Bomer, U., Muller, H., Guiard, B., Meijer, M., Rassow, J. and Pfanner, N. (1997) The Tim core complex defines the number of mitochondrial translocation contact sites and can hold arrested preproteins in the absence of matrix Hsp70-Tim44. EMBO J., 16, 5408-5419.
30. Dietmeier, K., Honlinger, A., Bomer, U., Dekker, P.J., Eckerskorn, C., Lottspeich, F., Kubrich, M. and Pfanner, N. (1997) Tom5 functionally links mitochondrial preprotein receptors to the general import pore. Nature, 388, 195-200.
31. Ito, H., Fukuda, Y., Murata, K. and Kimura, A. (1983) Transformation of intact yeast cells treated with alkali cations. J. Bacteriol., 153, 163-168.
32. Kahana, J.A., Schnapp, B.J. and Silver, P.A. (1995) Kinetics of spindle pole body separation in budding yeast. Proc. Natl Acad. Sci., 92, 9707-9711.
33. Winston, F., Dollard, C. and Ricupero-Hovasse, S.L. (1995) Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast, 11, 53-55.
34. Hodel, A.E., Harreman, M.T., Pulliam, K.F., Harben, M.E., Holmes, J.S., Hodel, M.R., Berland, K.M. and Corbett, A.H. (2006) Nuclear localization signal receptor affinity correlates with in vivo localization in Saccharomyces cerevisiae. J. Biol. Chem., 281, 23545-23556.
35. Storici, F. and Resnick, M.A. (2006) The delitto perfetto approach to in vivo site-directed mutagenesis and chromosome rearrangements with synthetic oligonucleotides in yeast. Methods Enzymol., 409, 329-345.
36. Seedorf, M., Damelin, M., Kahana, J., Taura, T. and Silver, P.A. (1999) Interactions between a nuclear transporter and a subset of nuclear pore complex proteins depend on Ran GTPase. Mol. Cell. Biol., 19, 1547-1557.
37. Meadows, K.L., Song, B. and Doetsch, P.W. (2003) Characterization of AP lyase activities of Saccharomyces cerevisiae Ntg1p and Ntg2p: implications for biological function. Nucleic Acids Res., 31, 5560-5567.
38. Leung, S.W., Harreman, M.T., Hodel, M.R., Hodel, A.E. and Corbett, A.H. (2003) Dissection of the karyopherin {alpha} nuclear localization signal (NLS)-binding groove: Functional requirements for NLS binding. J. Biol. Chem., 278, 41947-41953.
39. Gruss, O.J., Carazo-Salas, R.E., Schatz, C.A., Guarguaglini, G., Kast, J., Wilm, M., Le Bot, N., Vernos, I., Karsenti, E. and Mattaj, I.W. (2001) Ran induces spindle assembly by reversing the inhibitory effect of importin [alpha] on TPX2 activity. Cell, 104, 83-93.
40. Fasken, M.B., Stewart, M. and Corbett, A.H. (2008) Functional significance of the interaction between the mRNA-binding protein, Nab2, and the nuclear pore-associated protein, Mlp1, in mRNA export. J. Biol. Chem., 283, 27130-27143.
41. Kelly, S.M., Pabit, S.A., Kitchen, C.M., Guo, P., Marfatia, K.A., Murphy, T.J., Corbett, A.H. and Berland, K.M. (2007) Recognition of polyadenosine RNA by zinc finger proteins. Proc. Natl Acad. Sci. USA, 104, 12306-12311.
42. Venkhataraman, R., Donald, C.D., Roy, R., You, H.J., Doetsch, P.W. and Kow, Y.W. (2001) Enzymatic processing of DNA containing tandem dihydrouracil by endonucleases III and VIII. Nucleic Acids Res., 29, 407-414.
43. 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. Mol. Cell. Biol., 19, 2929-2935.
44. Drake, J.W. (1992) Mutation rates. Bioessays, 14, 137-140.
45. Wierdl, M., Greene, C.N., Datta, A., Jinks-Robertson, S. and Petes, T.D. (1996) Destabilization of simple repetitive DNA sequences by transcription in yeast. Genetics, 143, 713-721.
46. Chi, N.W. and Kolodner, R.D. (1994) Purification and characterization of MSH1, a yeast mitochondrial protein that binds to DNA mismatches. J. Biol. Chem., 269, 29984-29992.
47. Nakai, K. and Horton, P. (1999) PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem. Sci., 24, 34-35.
48. Claros, M.G. and Vincens, P. (1996) Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem., 241, 779-786.
49. Paine, P.L., Moore, L.C. and Horowitz, S.B. (1975) Nuclear envelope permeability. Nature, 254, 109-114.
50. Koepp, D.M., Wong, D.H., Corbett, A.H. and Silver, P.A. (1996) Dynamic localization of the nuclear import receptor and its interactions with transport factors. J. Cell Biol., 133, 1163-1176.
51. Yano, R., Oakes, M., Yamaghishi, M., Dodd, J.A. and Nomura, M. (1992) Cloning and characterization of SRP1, a suppressor of temperature-sensitive RNA polymerase I mutations, in Saccharomyces cerevisiae. Mol. Cell. Biol., 12, 5640-5651.
52. Aitchison, J.D., Blobel, G. and Rout, M.P. (1996) Kap104p: a karyopherin involved in the nuclear transport of messenger RNA binding proteins. Science, 274, 624-627.
53. Rosenblum, J.S., Pemberton, L.F. and Blobel, G. (1997) A nuclear import pathway for a protein involved in tRNA maturation. J. Cell Biol., 139, 1655-1661.
54. Fanara, P., Hodel, M.R., Corbett, A.H. and Hodel, A.E. (2000) Quantitative analysis of nuclear localization signal (NLS)-importin alpha interaction through fluorescence depolarization. Evidence for auto-inhibitory regulation of NLS binding. J. Biol. Chem., 275, 21218-21223.
55. Kobe, B. (1999) Autoinhibition by an internal nuclear localization signal revealed by the crystal structure of mammalian importin alpha. Nat. Struct. Biol., 6, 388-397.
56. Salmon, T.B., Evert, B.A., Song, B. and Doetsch, P.W. (2004) Biological consequences of oxidative stress-induced DNA damage in Saccharomyces cerevisiae. Nucleic Acids Res., 32, 3712-3723.
57. Rowe, L.A., Degtyareva, N. and Doetsch, P.W. (2008) DNA damage-induced reactive oxygen species (ROS) stress response in Saccharomyces cerevisiae. Free Radic. Biol. Med., 45, 1167-1177.
58. Morey, N.J., Doetsch, P.W. and Jinks-Robertson, S. (2003) Delineating the requirements for spontaneous DNA damage resistance pathways in genome maintenance and viability in Saccharomyces cerevisiae. Genetics, 164, 443-455.
59. Netter, P., Petrochilo, E., Slonimski, P.P., Bolotin-Fukuhara, M., Coen, D., Deutsch, J. and Dujon, B. (1974) Mitochondrial genetics VII. Allelism and mapping studies of ribosomal mutants resistant to chloramphenicol, erythromycin and spiramycin in S. cerevisiae. Genetics, 78, 1063-1100.
60. Larsen, N.B., Rasmussen, M. and Rasmussen, L.J. (2005) Nuclear and mitochondrial DNA repair: similar pathways? Mitochondrion, 5, 89-108.
61. Tell, G., Zecca, A., Pellizzari, L., Spessotto, P., Colombatti, A., Kelley, M.R., Damante, G. and Pucillo, C. (2000) An 'environment to nucleus' signaling system operates in B lymphocytes: redox status modulates BSAP/Pax-5 activation through Ref-1 nuclear translocation. Nucleic Acids Res., 28, 1099-1105.
62. Chatterjee, A. and Singh, K.K. (2001) Uracil-DNA glycosylase-deficient yeast exhibit a mitochondrial mutator phenotype. Nucleic Acids Res., 29, 4935-4940.
63. Takao, M., Aburatani, H., Kobayashi, K. and Yasui, A. (1998) Mitochondrial targeting of human DNA glycosylases for repair of oxidative DNA damage. Nucleic Acids Res., 26, 2917-2922.
64. Kuge, S., Jones, N. and Nomoto, A. (1997) Regulation of yAP-1 nuclear localization in response to oxidative stress. EMBO J., 16, 1710-1720.
65. Degtyareva, N.P., Chen, L., Mieczkowski, P., Petes, T.D. and Doetsch, P.W. (2008) Chronic oxidative DNA damage due to DNA repair defects causes chromosomal instability in Saccharomyces cerevisiae. Mol. Cell. Biol., 28, 5432-5445.
66. Goto, M., Shinmura, K., Igarashi, H., Kobayashi, M., Konno, H., Yamada, H., Iwaizumi, M., Kageyama, S., Tsuneyoshi, T., Tsugane, S. et al. (2009) Altered expression of the human base excision repair gene NTH1 in gastric cancer. Carcinogenesis, 30, 1345-1352.
67. Koketsu, S., Watanabe, T. and Nagawa, H. (2004) Expression of DNA repair protein: MYH, NTH1, and MTH1 in colorectal cancer. Hepatogastroenterology, 51, 638-642.
68. Green, D.M., Marfatia, K.A., Crafton, E.B., Zhang, X., Cheng, X. and Corbett, A.H. (2002) Nab2p is required for poly(A) RNA export in Saccharomyces cerevisiae and is regulated by arginine methylation via Hmt1p. J. Biol. Chem., 277, 7752-7760.