Insight into the functional consequences of hMYH variants associated with colorectal cancer: Distinct differences in the adenine glycosylase activity and the response to AP endonucleases of Y150C and G365D murine MYH

DNA Repair

Volumn 4, Issue 3, 2005, Pages 315-325

  Pope, Mary Ann ^a   Chmiel, Nikolas H ^a   David, Sheila S ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

8 Oxoguanine; Adenine glycosylase; Base excision repair; Colorectal cancer; MYH associated polyposis

Indexed keywords

DEOXYADENOSINE DERIVATIVE; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; DNA BINDING PROTEIN; DNA GLYCOSYLTRANSFERASE;

ARTICLE; BINDING AFFINITY; COLORECTAL CANCER; CONTROLLED STUDY; CORRELATION ANALYSIS; DNA BINDING; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME BINDING; ENZYME MECHANISM; ENZYME SUBSTRATE; EXAMINATION; GENE FUNCTION; GENE TARGETING; GENETIC VARIABILITY; MISMATCH REPAIR; NONHUMAN; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; TURNOVER TIME; WILD TYPE;

ANIMALS; BASE SEQUENCE; COLORECTAL NEOPLASMS; DNA GLYCOSYLASES; DNA PRIMERS; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; HUMANS; MICE; SUBSTRATE SPECIFICITY;

ESCHERICHIA COLI; EUKARYOTA; MURINAE;

EID: 12344258702     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2004.10.003     Document Type: Article

References (52)

1. A. Yarnell Doing DNA damage assessment Chem. Eng. News 81 2003 33 35
2. S. Shibutani, M. Takeshita, and A.P. Grollman Insertion of specific bases during DNA synthesis past the oxidative damaged base 8-oxodG Nature 349 1991 431 434
3. A.P. Grollman, and M. Moriya Mutagenesis by 8-oxoguanine: an enemy within Trends Genet. 9 1993 246 249
4. M.L. Wood, A. Esteve, M.L. Morningstar, G.M. Kuziemko, and J.M. Essigmann Genetic effects of oxidative DNA damage: comparative mutagenesis of 7,8-dihydro-8-oxoguanine and 7,8-dihydro-8-oxoadenine in Escherichia coli Nucleic Acids Res. 20 1992 6023 6032
5. T. Tajiri, H. Maki, and M. Sekiguchi Functional cooperation of MutT, MutM, and MutY proteins in preventing mutations caused by spontaneous oxidation of guanine nucleotides in Escherichia coli Mutat. Res. 366 1995 257 267
6. J.Y. Mo, H. Maki, and M. Sekiguchi Hydrolytic elimination of a mutagenic nucleotide, 8-oxodGTP, by human 18-kDa protein, sanitization of nucleotide pool Proc. Natl. Acad. Sci. U.S.A. 89 1992 11021 11025
7. K. Sakumi, M. Furuichi, T. Tsuzuki, T. Kakuma, S.I. Kawabata, H. Maki, and M. Sekiguchi Cloning and expression of cDNA for a human enzyme that hydrolyzes 8-oxo-dGTP, a mutagenic substrate for DNA synthesis J. Biol. Chem. 268 1993 23524 23530
8. T. Kakuma, J.I. Nishida, T. Tsuzuki, and M. Sekiguchi Mouse MTH1 protein with 8-oxo-7,8-dihydro-2′-deoxyguanosine 5′-triphosphatase activity that prevents transversion mutation J. Biol. Chem. 270 1995 25942 25948
9. T. Bessho, K. Tano, H. Kasai, E. Ohtsuka, and S. Nishimura Evidence for two DNA repair enzymes for 8-hydroxyguanine (7,8-dihydro-8-oxoguanine) in human cells J. Biol. Chem. 268 1993 19416 19421
10. T.A. Rosenquist, D.O. Zharkov, and A.P. Grollman Cloning and characterization of a mammalian 8-oxoguanine DNA glycosylase Proc. Natl. Acad. Sci. U.S.A. 94 1997 7429 7434
11. R. Lu, H.M. Nash, and G.L. Verdine A mammalian DNA repair enzyme that excises oxidatively damaged guanines maps to a locus frequently lost in lung cancer Curr. Biol. 7 1997 397 407
12. Y.C. Yeh, D.-Y. Chang, J. Masin, and A.-L. Lu Two nicking enzymes systems specific for mismatch-containing DNA in nuclear extracts from human cells J. Biol. Chem. 266 1991 6480 6484
13. M.M. Slupska, C. Baikalov, W.M. Luther, J.-H. Chiang, Y.-F. Wei, and J.H. Miller Cloning and sequencing a human homolog (hMYH) of the Escherichia coli mutY gene whose function is required for the repair of oxidative DNA damage J. Bacteriol. 178 1996 3885 3892
14. H. Yang, W.M. Clendenin, D. Wong, B. Demple, M.M. Slupska, J.-H. Chiang, and J.H. Miller Enhanced activity of adenine-DNA glycosylase (Myh) by apurinic-apyrimidinic endonuclease (Ape1) in mammalian base excision repair of an A/GO mismatch Nucleic Acids Res. 29 2001 743 752
15. S.S. David, and S.D. Williams Chemistry of glycosylases and endonucleases involved in base-excision repair Chem. Rev. 98 1998 1221 1261
16. E.C. Friedberg, G.C. Walker, and W. Siede DNA Repair and Mutagenesis 1995 ASM Press Washington, DC
17. N. Al-Tassan, N.H. Chmiel, J. Maynard, N. Fleming, A.L. Livingston, G.T. Williams, A.K. Hodges, D.R. Davies, S.S. David, J.R. Sampson, and J.P. Cheadle Inherited variants of MYH associated with somatic G:C to T:A mutations in colorectal tumors Nature Genet. 30 2002 227 232
18. J.R. Sampson, S. Dolwani, S. Jones, D. Eccles, A. Ellis, D.G. Evan, I. Frayling, F. Pigatto, S. Jordan, T. Mak, E.R. Maher, J. Maynard, J. Shaw, and J.P. Cheadle MYH Polyposis: a new autosomal recessive form of familial adenomatous polyposis demanding reappraisal of genetic risk and family management Lancet 362 2003 39 41
19. O.M. Sieber, L. Lipton, M. Crabtree, K. Heinimann, P. Fidalgo, R.K.S. Philips, M.-L. Bisgaard, T.F. Orntoft, L.A. Aaltonen, S.V. Hodgson, H.J.W. Thomas, and I.P.M. Tomlinson Multiple colorectal adenomas, classic adenomatous polyposis, and germ-line mutations in MYH N. Engl. J. Med. 348 2003 791 799
20. S. Jones, P. Emmerson, J. Maynard, J.M. Best, S. Jordan, G.T. Williams, J.R. Sampson, and J.P. Cheadle Biallelic germline mutations in MYH predispose to multiple colorectal adenoma and somatic G:C to T:A mutations Human Mol. Gen. 11 2002 2961 2967
21. J.P. Cheadle, and J.R. Sampson Exposing the MYtH about base excision repair and human inherited disease Human Mol. Gen. 12 2003 R159 R165
22. N.H. Chmiel, A.L. Livingston, and S.S. David Insights into the functional consequences of inherited variants of the hMYH adenine glycosylase associated with colorectal cancer: complementation assays with hMYH variants and pre-steady-state kinetics of the corresponding mutated E. coli enzymes J. Mol. Biol. 327 2003 431 443
23. D.G. Rothwell, and I.D. Hickson Base Excision Repair of DNA Damage 1997 Chapman and Hall New York
24. D.M. Wilson, and D. Barsky The major human abasic endonuclease: formation, consequences and repair of abasic lesions in DNA Mutat. Res. 485 2001 283 307
25. T.R. Waters, P. Gallinari, J. Jiricny, and P.F. Swann Human thymine DNA glycosylase binds to apurinic sites in DNA but is displaced by human apurinic endonuclease 1 J. Biol. Chem. 274 1999 67 74
26. T.R. Waters, and P.F. Swann Kinetics of the action of thymine DNA glycosylase J. Biol. Chem. 273 1998 20007 20014
27. S.S. Parikh, C.D. Mol, G. Slupphaug, S. Bharati, H.E. Krokan, and J.A. Tainer Base excision repair initiation revealed by crystal structures and binding kinetics of human uracil-DNA glycosylase with DNA EMBO J. 17 1998 5214 5226
28. A.E. Vidal, I.D. Hickson, S. Boiteux, and J.P. Radicella Mechanism of stimulation of the DNA glycosylase activity of hOGG1 by the major human AP endonuclease: bypass of the AP lyase activity step Nucleic Acids Res. 29 2001 1285 1292
29. J.W. Hill, T.K. Hazra, T. Izumi, and S. Mitra Stimulation of human 8-oxoguanine-DNA glycosylase by AP-endonuclease: potential coordination of the initial steps in base excision repair Nucleic Acids Res. 29 2001 430 438
30. F. Petronzelli, A. Riccio, G.D. Markham, S.H. Seeholzer, J. Stoerker, M. Genuardi, A.T. Yeung, Y. Matsumoto, and A. Bellacosa Biphasic kinetics of the human DNA repair protein MED1(MBD4), a mismatch-specific DNA N-glycosylase J. Biol. Chem. 275 2000 32422 32429
31. J.-S. Sung, and D.W. Mosbaugh Escherichia coli double-strand uracil-DNA glycosylase: involvement in uracil-mediated DNA base excision repair and stimulation of activity by endonuclease IV Biochemistry 39 2000 10224 10235
32. S.L. Porello, A.E. Leyes, and S.S. David Single-turnover and pre-steady-state kinetics of the reaction of the adenine glycosylase MutY with mismatch-containing DNA substrates Biochemistry 37 1998 14756 14764
33. J. Tchou, V. Bodepudi, S. Shibutani, I. Antoshechkin, J.H. Miller, and A.P. Grollman Substrate specificity of Fpg protein. Recognition and cleavage of oxidatively damaged DNA J. Biol. Chem. 269 1994 15318
34. M.A. Pope, S.L. Porello, and S.S. David Escherichia coli apurinic-apyrimidinic endonuclease enhances the turnover of the adenine glycosylase MutY with G:A substrates J. Biol. Chem. 277 2002 22605 22615
35. M.A. Pope, S.S. David (2005). DNA Damage recognition and repair by murine MutY homolog, DNA repair 4, 91-102.
36. J.H. Miller A Short Course in Bacterial Genetics 1992 Cold Spring Harbor Laboratory Press Cold Spring Harbor N.Y.
37. J. Sambrook, and T. Maniatis Molecular Cloning, a Laboratory Manual second ed. 1989 Cold Spring Harbor Laboratory Press Cold Spring Harbor, N.Y.
38. D.G. Rothwell, B. Hang, M.A. Gorman, P.S. Freemont, B. Singer, and I.D. Hickson Substitution of Asp-210 in HAP1 (APE/Ref-1) eliminates endonuclease activity but stabilizes substrate binding Nucleic Acids Res. 28 2000 2207 2213
39. M.M. Bradford A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
40. C.L. Chepanoske, S.L. Porello, T. Fujiwara, H. Sugiyama, and S.S. David Substrate recognition by Escherichia coli MutY using substrate analogs Nucleic Acids Res. 27 1999 3197 3204
41. J.A.B. McCaan, and P.J. Berti Adenine release is fast in MutY-catalyzed hydrolysis of G:A amd 8-oxo-G:A DNA mismatches J. Biol. Chem. 278 2003 29587 29592
42. N.H. Chmiel, M.-P. Golinelli, A.W. Francis, and S.S. David Efficient recognition of substrates and substrate analogs by the adenine glycosylase MutY requires the C-terminal domain Nucleic Acids Res. 29 2001 553 564
43. D.M. Wilson III, M. Takeshita, and B. Demple Abasic site binding by the human apurinic endonuclease, Ape, and determination of the DNA contact sites Nucleic Acids Res. 25 1997 933 939
44. Y. Masuda, R.A.O. Bennett, and B. Demple Rapid dissociation of human apurinic endonuclease (Ape1) from incised DNA induced by magnesium J. Biol. Chem. 273 1998 30360 30365
45. Y. Tominaga, Y. Ushijima, D. Tsuchimoto, M. Mishima, M. Shirakawa, S. Hirano, K. Sakumi, and Y. Nakabeppu MUTYH prevents OGG1 or APEX1 from inappropriately processing its substrate or reaction product with its C-terminal domain Nucleic Acids Res. 32 2004 3198 3211
46. S.H. Wooden, H.M. Bassett, T.G. Wood, and A.K. McCullough Identification of critical residues required for the mutation avoidance function of human MutY (hMYH) and implications in colorectal cancer Cancer Lett. 205 2004 89 95
47. J.C. Fromme, A. Banerjee, S.J. Huang, and G.L. Verdine Structural basis for removal of adenine mispaired with 8-oxoguanine by MutY adenine DNA glycosylase Nature 427 2004 652 656
48. D.E. Volk, P.G. House, V. Thiviyanathan, B.A. Luxon, S. Zhang, R.S. Lloyd, and D.G. Gorenstein Structural similarities between MutT and the C-terminal domain of MutY Biochemistry 39 2000 7331 7336
49. D.M. Noll, A. Gogos, J.A. Granek, and N.D. Clarke The C-terminal domain of the adenine-DNA glycosylase MutY confers specificity for 8-oxoguanine:adenine mispairs and may have evolved from MutT, an 8-oxo-dGTPase Biochemistry 38 1999 6374 6379
50. A. Parker, Y. Gu, W. Mahoney, S.-H. Lee, K.K. Singh, and A.-L. Lu Human homolog of the MutY repair protein (hMYH) physically interacts with proteins involved in long patch DNA base excision repair J. Biol. Chem. 276 2001 5547 5555
51. S. Seki, K. Akiyama, S. Watanabe, M. Hatsushika, S. Ikeda, and K. Tsutsui cDNA and deduced amino acid sequence of mouse DNA repair enzyme (APEX nuclease) with significant homology to Escherichia coli Exonuclease III J. Biol. Chem. 266 1991 20797 20802
52. A.W. Francis, and S.S. David Escherichia coli MutY and Fpg utilize a processive mechanism for target location Biochemistry 42 2002 801 810