A role for saccharomyces cerevisiae Tpa1 protein in direct alkylation repair

Journal of Biological Chemistry

Volumn 289, Issue 52, 2014, Pages 35939-35952

  Shivange, Gururaj ^a   Kodipelli, Naveena ^a   Monisha, Mohan ^a   Anindya, Roy ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY HYDERABAD   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLATION; AMINO ACIDS; CYTOTOXICITY; DNA; METHANE; METHYLATION; PROTEINS; TOXICITY; YEAST;

2-OXOGLUTARATE-DEPENDENT DIOXYGENASE; ALKYLATING AGENTS; AMINO ACID RESIDUES; BASE EXCISION REPAIRS; COFACTOR BINDING; DIRECT ALKYLATION; DNA REPAIR PROTEINS; HIGH-THROUGHPUT ANALYSIS;

REPAIR;

DNA DIRECTED DNA POLYMERASE; DNA DIRECTED DNA POLYMERASE ZETA; DNA GLYCOSYLASE MAG1; DNA GLYCOSYLTRANSFERASE; FUNGAL PROTEIN; PROTEIN TPA1; UNCLASSIFIED DRUG; CARRIER PROTEIN; FUNGAL DNA; MAG1 PROTEIN, S CEREVISIAE; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEIN; TPA1 PROTEIN, S CEREVISIAE;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; DEMETHYLATION; DNA ALKYLATION; DNA METHYLATION; DNA REPAIR; DNA SYNTHESIS; ESCHERICHIA COLI; EXCISION REPAIR; FUNGAL STRAIN; HYDROXYLATION; NONHUMAN; PHENOTYPE; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN QUATERNARY STRUCTURE; SACCHAROMYCES CEREVISIAE; ALKYLATION; DNA DAMAGE; GENETICS; METABOLISM; PHYSIOLOGY;

SACCHAROMYCES CEREVISIAE;

ALKYLATION; CARRIER PROTEINS; DNA DAMAGE; DNA GLYCOSYLASES; DNA METHYLATION; DNA REPAIR; DNA, FUNGAL; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84919798239     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.590216     Document Type: Article

References (70)

1. Rajski, S. R., and Williams, R. M. (1998) DNA cross-linking agents as antitumor drugs. Chem. Rev. 98, 2723-2796
2. Beranek, D. T. (1990) Distribution of methyl and ethyl adducts following alkylation with monofunctional alkylating agents. Mutat. Res. 231, 11-30
3. Singer, B., and Grunberger, D. (1983) molecular biology of mutagens and carcinogens, Plenum Publishing Corp., New York
4. Sedgwick, B. (2004) Repairing DNA-methylation damage. Nat. Rev. Mol. Cell Biol. 5, 148-157
5. Johnson, R. E., Yu, S. L., Prakash, S., and Prakash, L. (2007) A role for yeast and human translesion synthesis DNA polymerases in promoting replication through 3-methyl adenine. Mol. Cell Biol. 27, 7198-7205
6. Kunz, B. A., Straffon, A. F., and Vonarx, E. J. (2000)DNAdamage-induced mutation: tolerance via translesion synthesis. Mutat. Res. 451, 169-185
7. Washington, M. T., Johnson, R. E., Prakash, S., and Prakash, L. (2000) Accuracy of thymine-thymine dimer bypass by Saccharomyces cerevisiae DNA polymerase η. Proc. Natl. Acad. Sci. U.S.A. 97, 3094-3099
8. Acharya, N., Johnson, R. E., Prakash, S., and Prakash, L. (2006) Complex formation with Rev1 enhances the proficiency of Saccharomyces cerevisiae DNA polymerase ζ for mismatch extension and for extension opposite from DNA lesions. Mol. Cell Biol. 26, 9555-9563
9. Falnes, P. Ø., Bjørås, M., Aas, P. A., Sundheim, O., and Seeberg, E. (2004) Substrate specificities of bacterial and human AlkB proteins. Nucleic Acids Res. 32, 3456-3461
10. Falnes, P. Ø. (2004) Repair of 3-methylthymine and 1-methylguanine lesions by bacterial and human AlkB proteins. Nucleic Acids Res. 32, 6260-6267
11. Delaney, J. C., and Essigmann, J. M. (2004) Mutagenesis, genotoxicity, and repair of 1-methyladenine, 3-alkylcytosines, 1-methylguanine, and 3-methylthymine in alkB Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 101, 14051-14056
12. Falnes, P. Ø., Klungland, A., and Alseth, I. (2007) Repair of methyl lesions in DNA and RNA by oxidative demethylation. Neuroscience 145, 1222-1232
13. Trewick, S. C., Henshaw, T. F., Hausinger, R. P., Lindahl, T., and Sedgwick, B. (2002) Oxidative demethylation by Escherichia coli AlkB directly reverts DNA base damage. Nature 419, 174-178
14. Aas, P. A., Otterlei, M., Falnes, P. O., Vågbø, C. B., Skorpen, F., Akbari, M., Sundheim, O., Bjørås, M., Slupphaug, G., Seeberg, E., and Krokan, H. E. (2003) Human and bacterial oxidative demethylases repair alkylation damage in both RNA and DNA. Nature 421, 859-863
15. Ougland, R., Zhang, C. M., Liiv, A., Johansen, R. F., Seeberg, E., Hou, Y. M., Remme, J., and Falnes, P. Ø. (2004) AlkB restores the biological function of mRNA and tRNA inactivated by chemical methylation. Mol. Cell 16, 107-116
16. Kurowski, M. A., Bhagwat, A. S., Papaj, G., and Bujnicki, J. M. (2003) Phylogenomic identification of five new human homologs of the DNA repair enzyme AlkB. BMC Genomics 4, 48
17. Gerken, T., Girard, C. A., Tung, Y. C., Webby, C. J., Saudek, V., Hewitson, K. S., Yeo, G. S., McDonough, M. A., Cunliffe, S., McNeill, L. A., Galvanovskis, J., Rorsman, P., Robins, P., Prieur, X., Coll, A. P., Ma, M., Jovanovic, Z., Farooqi, I. S., Sedgwick, B., Barroso, I., Lindahl, T., Ponting, C. P., Ashcroft, F. M., O'Rahilly, S., and Schofield, C. J. (2007) The obesityassociated FTO gene encodes a 2-oxoglutarate-dependent nucleic acid demethylase. Science 318, 1469-1472
18. Sedgwick, B., Bates, P. A., Paik, J., Jacobs, S. C., and Lindahl, T. (2007) Repair of alkylated DNA: recent advances. DNA Repair 6, 429-442
19. Wei, Y. F., Chen, B. J., and Samson, L. (1995) Suppression of Escherichia coli alkB mutants by Saccharomyces cerevisiae genes. J. Bacteriol. 177, 5009-5015
20. Choudhary, V., and Schneiter, R. (2012) Pathogen-related yeast (PRY) proteins and members of the CAP superfamily are secreted sterol-binding proteins. Proc. Natl. Acad. Sci. U.S.A. 109, 16882-16887
21. Verna, J., Lodder, A., Lee, K., Vagts, A., and Ballester, R. (1997) A family of genes required for maintenance of cell wall integrity and for the stress response in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 94, 13804-13809
22. Aravind, L., and Koonin, E. V (2001) The DNA-repair protein AlkB, EGL-9, and leprecan define new families of 2-oxoglutarate- and iron-dependent dioxygenases. Genome Biol. 2, RESEARCH0007
23. Keeling, K. M., Salas-Marco, J., Osherovich, L. Z., and Bedwell, D. M. (2006) Tpa1p is part of an mRNP complex that influences translation termination, mRNA deadenylation, and mRNA turnover in Saccharomyces cerevisiae. Mol. Cell Biol. 26, 5237-5248
24. Henri, J., Rispal, D., Bayart, E., van Tilbeurgh, H., Séraphin, B., and Graille, M. (2010) Structural and functional insights into Saccharomyces cerevisiae Tpa1, a putative prolylhydroxylase influencing translation termination and transcription. J. Biol. Chem. 285, 30767-30778
25. Kim, H. S., Kim, H. L., Kim, K. H., Kim do, J., Lee, S. J., Yoon, J. Y., Yoon, H. J., Lee, H. Y., Park, S. B., Kim, S. J., Lee, J. Y., and Suh, S. W. (2010) Crystal structure of Tpa1 from Saccharomyces cerevisiae, a component of the messenger ribonucleoprotein complex. Nucleic Acids Res. 38, 2099-2110
26. Loenarz, C., Sekirnik, R., Thalhammer, A., Ge, W., Spivakovsky, E., Mackeen, M. M., McDonough, M. A., Cockman, M. E., Kessler, B. M., Ratcliffe, P. J., Wolf, A., and Schofield, C. J. (2014) Hydroxylation of the eukaryotic ribosomal decoding center affects translational accuracy. Proc. Natl. Acad. Sci. U.S.A. 111, 4019-4024
27. Hanway, D., Chin, J. K., Xia, G., Oshiro, G., Winzeler, E. A., and Romesberg, F. E. (2002) Previously uncharacterized genes in the UV- and MMSinduced DNA damage response in yeast. Proc. Natl. Acad. Sci. U.S.A. 99, 10605-10610
28. Choi, Y., Sims, G. E., Murphy, S., Miller, J. R., and Chan, A. P. (2012) Predicting the functional effect of amino acid substitutions and indels. PLoS ONE 7, e46688
29. Schymkowitz, J., Borg, J., Stricher, F., Nys, R., Rousseau, F., and Serrano, L. (2005) The FoldX web server: an online force field. Nucleic Acids Res. 33, W382-8
30. Westbye, M. P., Feyzi, E., Aas, P. A., Vågbø, C. B., Talstad, V. A., Kavli, B., Hagen, L., Sundheim, O., Akbari, M., Liabakk, N. B., Slupphaug, G., Otterlei, M., and Krokan, H. E. (2008) Human AlkB homolog 1 is a mitochondrial protein that demethylates 3-methylcytosine in DNA and RNA. J. Biol. Chem. 283, 25046-25056
31. Korvald, H., Falnes, P. Ø., Laerdahl, J. K., Bjørås, M., and Alseth, I. (2012) The Schizosaccharomyces pombe AlkB homolog Abh1 exhibits AP lyase activity but no demethylase activity. DNA Repair 11, 453-462
32. Anindya, R., Mari, P. O., Kristensen, U., Kool, H., Giglia-Mari, G., Mullenders, L. H., Fousteri, M., Vermeulen, W., Egly, J. M., and Svejstrup, J. Q. (2010) A ubiquitin-binding domain in Cockayne syndrome B required for transcription-coupled nucleotide excision repair. Mol. Cell 38, 637-648
33. Henshaw, T. F., Feig, M., and Hausinger, R. P. (2004) Aberrant activity of the DNA repair enzyme AlkB. J. Inorg. Biochem. 98, 856-861
34. Anindya, R., Aygün, O., and Svejstrup, J. Q. (2007) Damage-induced ubiquitylation of human RNA polymerase II by the ubiquitin ligase Nedd4, but not Cockayne syndrome proteins or BRCA1. Mol. Cell 28, 386-397
35. Shivange, G., Kodipelli, N., and Anindya, R. (2014) A nonradioactive restriction enzyme-mediated assay to detect DNA repair by Fe(II)/2-oxo-glutarate-dependent dioxygenase. Anal. Biochem. 465C, 35-37
36. Li, Q., Sritharathikhun, P., and Motomizu, S. (2007) Development of novel reagent for Hantzsch reaction for the determination of formaldehyde by spectrophotometry and fluorometry. Anal. Sci. 23, 413-417
37. Thomas, B. J., and Rothstein, R. (1989) Elevated recombination rates in transcriptionally active DNA. Cell 56, 619-630
38. Taschner, M., Harreman, M., Teng, Y., Gill, H., Anindya, R., Maslen, S. L., Skehel, J. M., Waters, R., and Svejstrup, J. Q. (2010) A role for checkpoint kinase-dependent Rad26 phosphorylation in transcription-coupled DNA repair in Saccharomyces cerevisiae. Mol. Cell Biol. 30, 436-446
39. Sikorski, R. S., and Hieter, P. (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27
40. Petrov, A. N., Meskauskas, A., Roshwalb, S. C., and Dinman, J. D. (2008) Yeast ribosomal protein L10 helps coordinate tRNA movement through the large subunit. Nucleic Acids Res. 36, 6187-6198
41. Kataoka, H., Yamamoto, Y., and Sekiguchi, M. (1983)Anew gene (alkB) of Escherichia coli that controls sensitivity to methyl methane sulfonate. J. Bacteriol. 153, 1301-1307
42. Dinglay, S., Trewick, S. C., Lindahl, T., and Sedgwick, B. (2000) Defective processing of methylated single-stranded DNA by E. coli AlkB mutants. Genes Dev. 14, 2097-2105
43. Spence, E. L., Kawamukai, M., Sanvoisin, J., Braven, H., and Bugg, T. D. (1996) Catechol dioxygenases from Escherichia coli (MhpB) and Alcaligenes eutrophus (MpcI): sequence analysis and biochemical properties of a third family of extradiol dioxygenases. J. Bacteriol. 178, 5249-5256
44. Eichhorn, E., van der Ploeg, J. R., Kertesz, M. A., and Leisinger, T. (1997) Characterization of α-ketoglutarate-dependent taurine dioxygenase from Escherichia coli. J. Biol. Chem. 272, 23031-23036
45. Simmons, J. M., Koslowsky, D. J., and Hausinger, R. P. (2012) Characterization of a Trypanosoma brucei Alkb homolog capable of repairing alkylated DNA. Exp. Parasitol. 131, 92-100
46. Bjørnstad, L. G., Zoppellaro, G., Tomter, A. B., Falnes, P. Ø., and Andersson, K. K. (2011) Spectroscopic and magnetic studies of wild-type and mutant forms of the Fe(II)- and 2-oxoglutarate-dependent decarboxylase ALKBH4. Biochem. J. 434, 391-398
47. Falnes, P. Ø., Johansen, R. F., and Seeberg, E. (2002) AlkB-mediated oxidative demethylation reverses DNA damage in Escherichia coli. Nature 419, 178-182
48. Chen, H., and Costa, M. (2009) Iron- and 2-oxoglutarate-dependent dioxygenases: an emerging group of molecular targets for nickel toxicity and carcinogenicity. Biometals 22, 191-196
49. Xiao, M., Yang, H., Xu, W., Ma, S., Lin, H., Zhu, H., Liu, L., Liu, Y., Yang, C., Xu, Y., Zhao, S., Ye, D., Xiong, Y., and Guan, K. L. (2012) Inhibition of α-KG-dependent histone and DNA demethylases by fumarate and succinate that are accumulated in mutations of FH and SDH tumor suppressors. Genes Dev. 26, 1326-1338
50. Couture, J. F., Collazo, E., Ortiz-Tello, P. A., Brunzelle, J. S., and Trievel, R. C. (2007) Specificity and mechanism of JMJD2A, a trimethyllysinespecific histone demethylase. Nat. Struct. Mol. Biol. 14, 689-695
51. Ma, W., Resnick, M. A., and Gordenin, D. A. (2008) Apn1 and Apn2 endonucleases prevent accumulation of repair-associated DNA breaks in budding yeast as revealed by direct chromosomal analysis. Nucleic Acids Res. 36, 1836-1846
52. Svilar, D., Dyavaiah, M., Brown, A. R., Tang, J. B., Li, J., McDonald, P. R., Shun, T. Y., Braganza, A., Wang, X. H., Maniar, S., St Croix, C. M., Lazo, J. S., Pollack, I. F., Begley, T. J., and Sobol, R. W. (2012) Alkylation sensitivity screens reveal a conserved cross-species functionome. Mol. Cancer Res. 10, 1580-1596
53. Moazed, D., and Noller, H. F. (1987) Interaction of antibiotics with functional sites in 16 S ribosomal RNA. Nature 327, 389-394
54. Röther, S., and Strässer, K. (2007) The RNA polymerase II CTD kinase Ctk1 functions in translation elongation. Genes Dev. 21, 1409-1421
55. Duncan, T., Trewick, S. C., Koivisto, P., Bates, P. A., Lindahl, T., and Sedgwick, B. (2002) Reversal of DNA alkylation damage by two human dioxygenases. Proc. Natl. Acad. Sci. U.S.A. 99, 16660-16665
56. Lee, D. H., Jin, S. G., Cai, S., Chen, Y., Pfeifer, G. P., and O'Connor, T. R. (2005) Repair of methylation damage in DNA and RNA by mammalian AlkB homologues. J. Biol. Chem. 280, 39448-39459
57. John, S., Howe, L., Tafrov, S. T., Grant, P. A., Sternglanz, R., and Workman, J. L. (2000) The something about silencing protein, Sas3, is the catalytic subunit of NuA3, a yTAF(II)30-containing HAT complex that interacts with the Spt16 subunit of the yeast CP (Cdc68/Pob3)-FACT complex. Genes Dev. 14, 1196-1208
58. Rout, M. P., and Aitchison, J. D. (2001) The nuclear pore complex as a transport machine. J. Biol. Chem. 276, 16593-16596
59. Volkert, M. R., and Hajec, L. I. (1991) Molecular analysis of the aidD6::Mu d1 (bla lac) fusion mutation of Escherichia coli K12. Mol. Gen. Genet. 229, 319-323
60. Xiao, W., Chow, B. L., and Rathgeber, L. (1996) The repair of DNA methylation damage in Saccharomyces cerevisiae. Curr. Genet. 30, 461-468
61. Hendricks, C. A., Razlog, M., Matsuguchi, T., Goyal, A., Brock, A. L., and Engelward, B. P. (2002) The S. cerevisiae Mag1 3-methyladenine DNA glycosylase modulates susceptibility to homologous recombination. DNA Repair 1, 645-659
62. Chang, M., Bellaoui, M., Boone, C., and Brown, G. W. (2002) A genomewide screen for methyl methanesulfonate-sensitive mutants reveals genes required for S phase progression in the presence of DNA damage. Proc. Natl. Acad. Sci. U.S.A. 99, 16934-16939
63. Calvo, J. A., Meira, L. B., Lee, C. Y., Moroski-Erkul, C. A., Abolhassani, N., Taghizadeh, K., Eichinger, L. W., Muthupalani, S., Nordstrand, L. M., Klungland, A., and Samson, L. D. (2012) DNA repair is indispensable for survival after acute inflammation. J. Clin. Invest. 122, 2680-2689
64. Van Sloun, P. P., Varlet, I., Sonneveld, E., Boei, J. J., Romeijn, R. J., Eeken, J. C., and De Wind, N. (2002) Involvement of mouse Rev3 in tolerance of endogenous and exogenous DNA damage. Mol. Cell Biol. 22, 2159-2169
65. Maxwell, P. H., Wiesener, M. S., Chang, G. W., Clifford, S. C., Vaux, E. C., Cockman, M. E., Wykoff, C. C., Pugh, C. W., Maher, E. R., and Ratcliffe, P. J. (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399, 271-275
66. Ivan, M., Kondo, K., Yang, H., Kim, W., Valiando, J., Ohh, M., Salic, A., Asara, J. M., Lane, W. S., and Kaelin, W. G., Jr. (2001) HIF- targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292, 464-468
67. Isaacs, J. S., Jung, Y. J., Mole, D. R., Lee, S., Torres-Cabala, C., Chung, Y. L., Merino, M., Trepel, J., Zbar, B., Toro, J., Ratcliffe, P. J., Linehan, W. M., and Neckers, L. (2005) HIF overexpression correlates with biallelic loss of fumarate hydratase in renal cancer: novel role of fumarate in regulation of HIF stability. Cancer Cell 8, 143-153
68. Selak, M. A., Armour, S. M., MacKenzie, E. D., Boulahbel, H., Watson, D. G., Mansfield, K. D., Pan, Y., Simon, M. C., Thompson, C. B., and Gottlieb, E. (2005) Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF- prolyl hydroxylase. Cancer Cell 7, 77-85
69. Lopes, M., Cotta-Ramusino, C., Pellicioli, A., Liberi, G., Plevani, P., Muzi-Falconi, M., Newlon, C. S., and Foiani, M. (2001) The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412, 557-561
70. Tercero, J. A., and Diffley, J. F. (2001) Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 412, 553-557