Intrinsic 5′-deoxyribose-5-phosphate lyase activity in Saccharomyces cerevisiae Trf4 protein with a possible role in base excision DNA repair

DNA Repair

Volumn 7, Issue 2, 2008, Pages 187-198

  Gellon, Lionel ^a   Carson, Dena R ^b   Carson, Jonathan P ^b   Demple, Bruce ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Base excision repair; DNA repair; dRP lyase activity; Trf4

Indexed keywords

2 DEOXYRIBONOLACTONE; 5' DEOXYRIBOSE 5 PHOSPHATE LYASE; DEOXYRIBOSE; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; DNA DIRECTED DNA POLYMERASE BETA; DNA POLYMERASE; FUNGAL PROTEIN; LYASE; MESYLIC ACID METHYL ESTER; NUCLEIC ACID BINDING PROTEIN; NUCLEOTIDE; PHOSPHATE; PROTEIN RAD1; PROTEIN RAD27; PROTEIN TRF4; PROTEIN TRF5; RNA; SCHIFF BASE; UNCLASSIFIED DRUG; 5' DEOXYRIBOSE 5 PHOSPHATE; 5'-DEOXYRIBOSE-5-PHOSPHATE; DNA DIRECTED DNA POLYMERASE; DNA DIRECTED RNA POLYMERASE; FLAP ENDONUCLEASE; OLIGONUCLEOTIDE; RAD27 PROTEIN, S CEREVISIAE; RIBOSE PHOSPHATE; SACCHAROMYCES CEREVISIAE PROTEIN; TRF4 PROTEIN, S CEREVISIAE; TRF5 PROTEIN, S CEREVISIAE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CHROMATIN; CONTROLLED STUDY; DNA REPAIR; ENZYME ACTIVITY; ENZYME SUBSTRATE; EXCISION REPAIR; FUNGAL GENE; FUNGAL STRAIN; GENE INTERACTION; IN VITRO STUDY; NONHUMAN; NTG1 GENE; NTG2 GENE; OGG1 GENE; PHENOTYPE; POL4 GENE; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN FUNCTION; SACCHAROMYCES CEREVISIAE; STATISTICAL ANALYSIS; ULTRAVIOLET RADIATION; YEAST; COMPARATIVE STUDY; ENZYMOLOGY; GENETICS; IMMUNOBLOTTING; METABOLISM; MUTATION; PHYSIOLOGY; SITE DIRECTED MUTAGENESIS;

MAMMALIA; SACCHAROMYCES CEREVISIAE;

DNA REPAIR; DNA-DIRECTED DNA POLYMERASE; DNA-DIRECTED RNA POLYMERASES; FLAP ENDONUCLEASES; IMMUNOBLOTTING; MUTAGENESIS, SITE-DIRECTED; MUTATION; OLIGONUCLEOTIDES; RIBOSEMONOPHOSPHATES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 37549024225     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2007.09.009     Document Type: Article

References (73)

1. Friedberg E., Walker G., Siede W., Wood R.D., Schultz R.A., and Ellenberger T. DNA Repair and Mutagenesis. second ed. (2005), ASM Press
2. Hoeijmakers J.H. Genome maintenance mechanisms for preventing cancer. Nature 411 (2001) 366-374
3. Lindahl T. Instability and decay of the primary structure of DNA. Nature 362 (1993) 709-715
4. Sobol R.W., Prasad R., Evenski A., Baker A., Yang X.P., Horton J.K., and Wilson S.H. The lyase activity of the DNA repair protein beta-polymerase protects from DNA-damage-induced cytotoxicity. Nature 405 (2000) 807-810
5. Braithwaite E.K., Kedar P.S., Lan L., Polosina Y.Y., Asagoshi K., Poltoratsky V.P., Horton J.K., Miller H., Teebor G.W., Yasui A., and Wilson S.H. DNA polymerase lambda protects mouse fibroblasts against oxidative DNA damage and is recruited to sites of DNA damage/repair. J. Biol. Chem. 280 (2005) 31641-31647
6. Braithwaite E.K., Prasad R., Shock D.D., Hou E.W., Beard W.A., and Wilson S.H. DNA polymerase lambda mediates a back-up base excision repair activity in extracts of mouse embryonic fibroblasts. J. Biol. Chem. 280 (2005) 18469-18475
7. Grin I.R., Khodyreva S.N., Nevinsky G.A., and Zharkov D.O. Deoxyribophosphate lyase activity of mammalian endonuclease VIII-like proteins. FEBS Lett. 580 (2006) 4916-4922
8. Sung J.S., DeMott M.S., and Demple B. Long-patch base excision DNA repair of 2-deoxyribonolactone prevents the formation of DNA-protein cross-links with DNA polymerase beta. J. Biol. Chem. 280 (2005) 39095-39103
9. Dianov G.L., Prasad R., Wilson S.H., and Bohr V.A. Role of DNA polymerase beta in the excision step of long patch mammalian base excision repair. J. Biol. Chem. 274 (1999) 13741-13743
10. Matsumoto Y., Kim K., Hurwitz J., Gary R., Levin D.S., Tomkinson A.E., and Park M.S. Reconstitution of proliferating cell nuclear antigen-dependent repair of apurinic/apyrimidinic sites with purified human proteins. J. Biol. Chem. 274 (1999) 33703-33708
11. Pascucci B., Stucki M., Jonsson Z.O., Dogliotti E., and Hubscher U. Long patch base excision repair with purified human proteins. DNA ligase I as patch size mediator for DNA polymerases delta and epsilon. J. Biol. Chem. 274 (1999) 33696-33702
12. Prasad R., Dianov G.L., Bohr V.A., and Wilson S.H. FEN1 stimulation of DNA polymerase beta mediates an excision step in mammalian long patch base excision repair. J. Biol. Chem. 275 (2000) 4460-4466
13. Blank A., Kim B., and Loeb L.A. DNA polymerase delta is required for base excision repair of DNA methylation damage in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 9047-9051
14. Wang Z., Wu X., and Friedberg E.C. DNA repair synthesis during base excision repair in vitro is catalyzed by DNA polymerase epsilon and is influenced by DNA polymerases alpha and delta in Saccharomyces cerevisiae. Mol. Cell. Biol. 13 (1993) 1051-1058
15. Alseth I., Korvald H., Osman F., Seeberg E., and Bjoras M. A general role of the DNA glycosylase Nth1 in the abasic sites cleavage step of base excision repair in Schizosaccharomyces pombe. Nucleic Acids Res. 32 (2004) 5119-5125
16. Aravind L., and Koonin E.V. DNA polymerase beta-like nucleotidyltransferase superfamily: identification of three new families, classification and evolutionary history. Nucleic Acids Res. 27 (1999) 1609-1618
17. Hubscher U., Maga G., and Spadari S. Eukaryotic DNA polymerases. Annu. Rev. Biochem. 71 (2002) 133-163
18. Aoufouchi S., Flatter E., Dahan A., Faili A., Bertocci B., Storck S., Delbos F., Cocea L., Gupta N., Weill J.C., and Reynaud C.A. Two novel human and mouse DNA polymerases of the polX family. Nucleic Acids Res. 28 (2000) 3684-3693
19. Burgers P.M., Koonin E.V., Bruford E., Blanco L., Burtis K.C., Christman M.F., Copeland W.C., Friedberg E.C., Hanaoka F., Hinkle D.C., Lawrence C.W., Nakanishi M., Ohmori H., Prakash L., Prakash S., Reynaud C.A., Sugino A., Todo T., Wang Z., Weill J.C., and Woodgate R. Eukaryotic DNA polymerases: proposal for a revised nomenclature. J. Biol. Chem. 276 (2001) 43487-43490
20. Garcia-Diaz M., Dominguez O., Lopez-Fernandez L.A., de Lera L.T., Saniger M.L., Ruiz J.F., Parraga M., Garcia-Ortiz M.J., Kirchhoff T., del Mazo J., Bernad A., and Blanco L. DNA polymerase lambda (Pol lambda), a novel eukaryotic DNA polymerase with a potential role in meiosis. J. Mol. Biol. 301 (2000) 851-867
21. Nagasawa K., Kitamura K., Yasui A., Nimura Y., Ikeda K., Hirai M., Matsukage A., and Nakanishi M. Identification and characterization of human DNA polymerase beta 2, a DNA polymerase beta-related enzyme. J. Biol. Chem. 275 (2000) 31233-31238
22. Bebenek K., Garcia-Diaz M., Patishall S.R., and Kunkel T.A. Biochemical properties of Saccharomyces cerevisiae DNA polymerase IV. J. Biol. Chem. 280 (2005) 20051-20058
23. McInnis M., O'Neill G., Fossum K., and Reagan M.S. Epistatic analysis of the roles of the RAD27 and POL4 gene products in DNA base excision repair in S. cerevisiae. DNA Repair 1 (2002) 311-315
24. Prasad R., Widen S.G., Singhal R.K., Watkins J., Prakash L., and Wilson S.H. Yeast open reading frame YCR14C encodes a DNA beta-polymerase-like enzyme. Nucleic Acids Res. 21 (1993) 5301-5307
25. Sadoff B.U., Heath-Pagliuso S., Castano I.B., Zhu Y., Kieff F.S., and Christman M.F. Isolation of mutants of Saccharomyces cerevisiae requiring DNA topoisomerase I. Genetics 141 (1995) 465-479
26. Castano I.B., Heath-Pagliuso S., Sadoff B.U., Fitzhugh D.J., and Christman M.F. A novel family of TRF (DNA topoisomerase I-related function) genes required for proper nuclear segregation. Nucleic Acids Res. 24 (1996) 2404-2410
27. Edwards S., Li C.M., Levy D.L., Brown J., Snow P.M., and Campbell J.L. Saccharomyces cerevisiae DNA polymerase epsilon and polymerase sigma interact physically and functionally, suggesting a role for polymerase epsilon in sister chromatid cohesion. Mol. Cell. Biol. 23 (2003) 2733-2748
28. Walowsky C., Fitzhugh D.J., Castano I.B., Ju J.Y., Levin N.A., and Christman M.F. The topoisomerase-related function gene TRF4 affects cellular sensitivity to the antitumor agent camptothecin. J. Biol. Chem. 274 (1999) 7302-7308
29. Wang Z., Castano I.B., Adams C., Vu C., Fitzhugh D., and Christman M.F. Structure/function analysis of the Saccharomyces cerevisiae Trf4/Pol sigma DNA polymerase. Genetics 160 (2002) 381-391
30. Castano I.B., Brzoska P.M., Sadoff B.U., Chen H., and Christman M.F. Mitotic chromosome condensation in the rDNA requires TRF4 and DNA topoisomerase I in Saccharomyces cerevisiae. Genes Dev. 10 (1996) 2564-2576
31. Carson D.R., and Christman M.F. Evidence that replication fork components catalyze establishment of cohesion between sister chromatids. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 8270-8275
32. Uhlmann F. Chromosome cohesion: a polymerase for chromosome bridges. Curr. Biol. 10 (2000) R698-R700
33. Wang Z., Castano I.B., De Las Penas A., Adams C., and Christman M.F. Pol kappa: a DNA polymerase required for sister chromatid cohesion. Science 289 (2000) 774-779
34. Haracska L., Johnson R.E., Prakash L., and Prakash S. Trf4 and Trf5 proteins of Saccharomyces cerevisiae exhibit poly(A) RNA polymerase activity but no DNA polymerase activity. Mol. Cell. Biol. 25 (2005) 10183-10189
35. Saitoh S., Chabes A., McDonald W.H., Thelander L., Yates J.R., and Russell P. Cid13 is a cytoplasmic poly(A) polymerase that regulates ribonucleotide reductase mRNA. Cell 109 (2002) 563-573
36. Kadaba S., Wang X., and Anderson J.T. Nuclear RNA surveillance in Saccharomyces cerevisiae: Trf4p-dependent polyadenylation of nascent hypomethylated tRNA and an aberrant form of 5S rRNA. Rna 12 (2006) 508-521
37. LaCava J., Houseley J., Saveanu C., Petfalski E., Thompson E., Jacquier A., and Tollervey D. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121 (2005) 713-724
38. Vanacova S., Wolf J., Martin G., Blank D., Dettwiler S., Friedlein A., Langen H., Keith G., and Keller W. A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol. 3 (2005) e189
39. Wyers F., Rougemaille M., Badis G., Rousselle J.C., Dufour M.E., Boulay J., Regnault B., Devaux F., Namane A., Seraphin B., Libri D., and Jacquier A. Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121 (2005) 725-737
40. Sherman F. Getting started with yeast. Methods Enzymol. 194 (1991) 3-21
41. Longtine M.S., McKenzie III A., Demarini D.J., Shah N.G., Wach A., Brachat A., Philippsen P., and Pringle J.R. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14 (1998) 953-961
42. Levin J.D., Johnson A.W., and Demple B. Homogeneous Escherichia coli endonuclease IV. Characterization of an enzyme that recognizes oxidative damage in DNA. J. Biol. Chem. 263 (1988) 8066-8071
43. Wong D., and Demple B. Modulation of the 5′-deoxyribose-5-phosphate lyase and DNA synthesis activities of mammalian DNA polymerase beta by apurinic/apyrimidinic endonuclease 1. J. Biol. Chem. 279 (2004) 25268-25275
44. DeMott M.S., Beyret E., Wong D., Bales B.C., Hwang J.T., Greenberg M.M., and Demple B. Covalent trapping of human DNA polymerase beta by the oxidative DNA lesion 2-deoxyribonolactone. J. Biol. Chem. 277 (2002) 7637-7640
45. Hoffman G.A., Garrison T.R., and Dohlman H.G. Analysis of RGS proteins in Saccharomyces cerevisiae. Methods Enzymol. 344 (2002) 617-631
46. Piersen C.E., McCullough A.K., and Lloyd R.S. AP lyases and dRPases: commonality of mechanism. Mutat. Res. 459 (2000) 43-53
47. Piersen C.E., Prasad R., Wilson S.H., and Lloyd R.S. Evidence for an imino intermediate in the DNA polymerase beta deoxyribose phosphate excision reaction. J. Biol. Chem. 271 (1996) 17811-17815
48. Faure V., Saparbaev M., Dumy P., and Constant J.F. Action of multiple base excision repair enzymes on the 2′-deoxyribonolactone. Biochem. Biophys. Res. Commun. 328 (2005) 1188-1195
49. Hashimoto M., Greenberg M.M., Kow Y.W., Hwang J.T., and Cunningham R.P. The 2-deoxyribonolactone lesion produced in DNA by neocarzinostatin and other damaging agents forms cross-links with the base-excision repair enzyme endonuclease III. J. Am. Chem. Soc. 123 (2001) 3161-3162
50. Haracska L., Prakash L., and Prakash S. A mechanism for the exclusion of low-fidelity human Y-family DNA polymerases from base excision repair. Genes Dev. 17 (2003) 2777-2785
51. Gellon L., Barbey R., Auffret van der Kemp P., Thomas D., and Boiteux S. Synergism between base excision repair, mediated by the DNA glycosylases Ntg1 and Ntg2, and nucleotide excision repair in the removal of oxidatively damaged DNA bases in Saccharomyces cerevisiae. Mol. Genet. Genomics 265 (2001) 1087-1096
52. Hanna M., Chow B.L., Morey N.J., Jinks-Robertson S., Doetsch P.W., and Xiao W. Involvement of two endonuclease III homologs in the base excision repair pathway for the processing of DNA alkylation damage in Saccharomyces cerevisiae. DNA Repair (Amst.) 3 (2004) 51-59
53. Thomas D., Scot A.D., Barbey R., Padula M., and Boiteux S. Inactivation of OGG1 increases the incidence of G. C-->T. A transversions in Saccharomyces cerevisiae: evidence for endogenous oxidative damage to DNA in eukaryotic cells. Mol. Gen. Genet. 254 (1997) 171-178
54. Koc A., Wheeler L.J., Mathews C.K., and Merrill G.F. Hydroxyurea arrests DNA replication by a mechanism that preserves basal dNTP pools. J. Biol. Chem. 279 (2004) 223-230
55. Wu X., and Wang Z. Relationships between yeast Rad27 and Apn1 in response to apurinic/apyrimidinic (AP) sites in DNA. Nucleic Acids Res. 27 (1999) 956-962
56. Wang Z., Wu X., and Friedberg E.C. Molecular mechanism of base excision repair of uracil-containing DNA in yeast cell-free extracts. J. Biol. Chem. 272 (1997) 24064-24071
57. Wu X., Braithwaite E., and Wang Z. DNA ligation during excision repair in yeast cell-free extracts is specifically catalyzed by the CDC9 gene product. Biochemistry 38 (1999) 2628-2635
58. Boiteux S., and Guillet M. Abasic sites in DNA: repair and biological consequences in Saccharomyces cerevisiae. DNA Repair (Amst.) 3 (2004) 1-12
59. Guzder S.N., Torres-Ramos C., Johnson R.E., Haracska L., Prakash L., and Prakash S. Requirement of yeast Rad1-Rad10 nuclease for the removal of 3′-blocked termini from DNA strand breaks induced by reactive oxygen species. Genes Dev. 18 (2004) 2283-2291
60. Swanson R.L., Morey N.J., Doetsch P.W., and Jinks-Robertson S. 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 (1999) 2929-2935
61. Sun X., Thrower D., Qiu J., Wu P., Zheng L., Zhou M., Bachant J., Wilson III D.M., and Shen B. Complementary functions of the Saccharomyces cerevisiae Rad2 family nucleases in Okazaki fragment maturation, mutation avoidance, and chromosome stability. DNA Repair (Amst.) 2 (2003) 925-940
62. Johnson R.E., Kovvali G.K., Prakash L., and Prakash S. Role of yeast Rth1 nuclease and its homologs in mutation avoidance, DNA repair, and DNA replication. Curr. Genet. 34 (1998) 21-29
63. Saxowsky T.T., Matsumoto Y., and Englund P.T. The mitochondrial DNA polymerase beta from Crithidia fasciculata has 5′-deoxyribose phosphate (dRP) lyase activity but is deficient in the release of dRP. J. Biol. Chem. 277 (2002) 37201-37206
64. Bailly V., and Verly W.G. The multiple activities of Escherichia coli endonuclease IV and the extreme lability of 5′-terminal base-free deoxyribose 5-phosphates. Biochem. J. 259 (1989) 761-768
65. Shen X., Woodgate R., and Goodman M.F. Lyase activities intrinsic to Escherichia coli polymerases IV and V. DNA Repair (Amst.) 4 (2005) 1368-1373
66. Pinz K.G., and Bogenhagen D.F. Characterization of a catalytically slow AP lyase activity in DNA polymerase gamma and other family A DNA polymerases. J. Biol. Chem. 275 (2000) 12509-12514
67. Graves R.J., Felzenszwalb I., Laval J., and O'Connor T.R. Excision of 5′-terminal deoxyribose phosphate from damaged DNA is catalyzed by the Fpg protein of Escherichia coli. J. Biol. Chem. 267 (1992) 14429-14435
68. Girard P.M., Guibourt N., and Boiteux S. The Ogg1 protein of Saccharomyces cerevisiae: a 7,8-dihydro-8-oxoguanine DNA glycosylase/AP lyase whose lysine 241 is a critical residue for catalytic activity. Nucleic Acids Res. 25 (1997) 3204-3211
69. Tchou J., Bodepudi V., Shibutani S., Antoshechkin I., Miller J., Grollman A.P., and Johnson F. Substrate specificity of Fpg protein. Recognition and cleavage of oxidatively damaged DNA. J. Biol. Chem. 269 (1994) 15318-15324
70. Houseley J., and Tollervey D. Yeast Trf5p is a nuclear poly(A) polymerase. EMBO Rep. 7 (2006) 205-211
71. Pinz K.G., and Bogenhagen D.F. The influence of the DNA polymerase gamma accessory subunit on base excision repair by the catalytic subunit. DNA Repair (Amst.) 5 (2006) 121-128
72. Lundin C., North M., Erixon K., Walters K., Jenssen D., Goldman A.S., and Helleday T. Methyl methanesulfonate (MMS) produces heat-labile DNA damage but no detectable in vivo DNA double-strand breaks. Nucleic Acids Res. 33 (2005) 3799-3811
73. Corpet F. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16 (1988) 10881-10890