Characterization of a mammalian homolog of the Escherichia coli MutY mismatch repair protein

Molecular and Cellular Biology

Volumn 15, Issue 2, 1995, Pages 989-996

  Mcgoldrick, John P ^a   Yeh, Yang Chen ^a,c   Solomon, Marjorie ^b   Essigmann, John M ^b   Lu, A Lien ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA GLYCOSYLTRANSFERASE;

ARTICLE; DNA BINDING; DNA REPLICATION; ENZYME ACTIVITY; ESCHERICHIA COLI; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PURIFICATION; SEQUENCE HOMOLOGY;

ESCHERICHIA COLI; EUKARYOTA; MAMMALIA;

EID: 0028831129     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.15.2.989     Document Type: Article

References (75)

1. Aaltonen, L. A., P. Peltomäki, F. S. Leach, P. Sistonen, L. Rylkkänen, J. P. Mecklin, H. Järvinen, S. M. Powell, J. Jen, S. R. Hamilton, G. M. Petersen, K. W. Kinzler, B. Vogelstein, and A. de la Chapelle. 1993. Clues to the pathogenesis of familial colorectal cancer. Science 260:812-816.
2. Ames, B. N., and L. S. Gold. 1991. Endogenous mutagens and the causes of aging and cancer. Mutat. Res. 250:3-16.
3. Au, K. G., M. Cabrera, J. H. Miller, and P. Modrich. 1988. Escherichia coli mutY gene product is required for specific A-G to C · G mismatch correction. Proc. Natl. Acad. Sci. USA 85:9163-9166.
4. Au, K. G., S. Clark, J. H. Miller, and P. Modrich. 1989. Escherichia coli mutY gene encodes an adenine glycosylase active on G/A mispairs. Proc. Natl. Acad. Sci. USA 86:8877-8881.
5. Beinert, H., and A. J. Thomson. 1983. Three iron clusters in iron-sulfur proteins. Arch. Biochem. Biophys. 222:333-361.
6. Bessho, T., K. Tano, H. Kasai, E. Ohtsuka, and S. Nishimura. 1993. Evidence for two DNA repair enzymes for 8-hydroxyguanine (7,8-dihydro-8-oxoguanine) in human cells. J. Biol. Chem. 268:19416-19421.
7. Bishop, D. K., M. S. Williamson, S. Fogel, and R. D. Kolodner. 1987. The role of heteroduplex correction in gene conversion in Saccharomyces cerevisiae. Nature (London) 238:362-364.
8. Bodepudi, V., S. Shibutani, and F. Johnson. 1992. Synthesis of 2′-deoxy-7,8-dihydro-8-oxoguanosine and their incorporation into oligomeric DNA. Chem. Res. Toxicol. 5:608-617.
9. Bradford, M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
10. Bronner, C. E., S. M. Baker, P. T. Morrison, G. Warren, L. G. Smith, M. K. Lescoe, M. Kane, C. Earabino, J. Lipford, A. Lindblom, P. Tannergard, R. J. Bollag, A. R. Godwin, D. C. Ward, M. Nordenskjøld, R. Fishel, R. Kolodner, and R. M. Liskay. 1994. Mutation in the DNA mismatch repair gene homologue hMLH1 is associated with hereditary non-polyposis colon cancer. Nature (London) 368:258-261.
11. Brown, T. C., and J. Jiricny. 1987. A specific mismatch repair event protects mammalian cells from loss of 5-methylcytosine. Cell 50:945-950.
12. Cheng, K. C., D. S. Cahill, H. Kasai, S. Nishimura, and L. A. Loeb. 1991. 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G-T and A-C substitutions. J. Biol. Chem. 267:166-172.
13. Chetsanga, C. J., and T. Lindahl. 1979. Release of 7-methylguanine residues whose imidazole rings have been opened from damaged DNA by a DNA glycosylase from Escherichia coli. Nucleic Acids Res. 6:3673-3683.
14. Claverys, J.-P., and S. A. Lacks. 1986. Heteroduplex deoxyribonucleic acid base mismatch repair in bacteria. Microbiol. Rev. 50:133-165.
15. Cunningham, R. P., H. Asahara, J. F. Bank, C. P. Scholes, H. C. Salerno, K. Surerus, E. Münck, J. McCracken, J. Peisach, and M. H. Emptage. 1989. Endonuclease III is an iron-sulfur protein. Biochemistry 28:4450-4455.
16. Desiraju, V., W. G. Shanabruch, and A.-L. Lu. 1993. Nucleotide sequence of the Salmonella typhimurium mutB gene, the homolog of Escherichia coli mutY. J. Bacteriol. 175:541-543.
17. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription inhibition by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
18. Fishel, R., M. K. Lescoe, M. R. S. Rao, N. G. Copeland, N. A. Jenkins, J. Garber, M. Kane, and R. Kolodner. 1993. The human mutator gene homolog MSH2 and its association with hereditary nonpolyposis colon cancer. Cell 75:1027-1038.
19. Friedberg, E. C. 1985. DNA repair. W. H. Freeman, New York.
20. Fujii, H., and T. Shimada. 1989. Isolation and characterization of cDNA clones derived from the divergently transcribed gene in the region upstream from the human dihydrofolate reductase gene. J. Biol. Chem. 264:10057-10064.
21. Hollstein, M., D. Sidransky, B. Vogelstein, and C. C. Harris. 1991. p53 mutations in human cancers. Science 253:49-53.
22. Holmes, J., Jr., S. Clark, and P. Modrich. 1990. Strand-specific mismatch correction in nuclear extracts of human and Drosophila melanogaster cell lines. Proc. Natl. Acad. Sci. USA 87:5837-5841.
23. Jiricny, J., M. Hughes, N. Corman, and B. B. Rudkin. 1988. A human 200-kDa protein binds selectively to DNA fragments containing G/T mismatches. Proc. Natl. Acad. Sci. USA 85:8860-8864.
24. Jones, M., R. Wagner, and M. Radman. 1987. Repair of a mismatch is influenced by the base composition of the surrounding nucleotide sequence. Genetics 115:605-610.
25. Kasai, H., and S. Nishimura. 1991. Formation of 8-hydroxydeoxyguanosine in DNA by oxygen radicals and its biological significance, p. 99-116. In H. Sies (ed.), Oxidative stress: oxidants and antioxidants. Academic Press, London.
26. Kramer, W., B. Kramer, M. S. Williamson, and S. Fogel. 1989. Cloning and nucleotide sequence of DNA mismatch repair gene PMS1 from Saccharomyces cerevisiae: homology of PMS1 to procaryotic MutL and HexB. J. Bacteriol. 171:5339-5346.
27. Laemmli, U. K. 1970. Cleavage of structural protein during the assembly of the head of bacteriophage T4. Nature (London) 227:680-685.
28. Leach, F. S., N. C. Nicolaides, N. Papadopoulos, B. Liu, H. Hen, R. Parsons, P. Peltomaki, P. Sistonen, L. A. Aaltonen, M. Nystrom-Lahti, X.-Y. Guan, J. Zhang, P. S. Meltzer, J.-W. Yu, F.-T. Kao, D. J. Chen, K. M. Cerosaletti, R. E. K. Fournier, S. Todd, T. Lewis, R. J. Leach, S. L. Naylor, J. Weisenbach, J.-P. Mecklin, H. Jarvinen, G. M. Petersen, S. R. Hamilton, J. Green, J. Jas, P. Watson, H. T. Lynch, J. M. Trent, A. de la Chapelle, K. W. Kinzler, and B. Vogelstein. 1993. Mutations of a mutS homolog in hereditary non-polyposis colorectal cancer. Cell 75:1215-1225.
29. Lerner, R. A., N. Green, H. Alexander, F. T. Liu, J. G. Sutcliffe, and T. M. Shinnick. 1981. Chemically synthesized peptides predicted from the nucleotide sequence of the hepatitis B virus genome elicit antibodies reactive with the native envelope protein of Dane particles. Proc. Natl. Acad. Sci. USA 78:3403-3407.
30. Lieb, M. 1983. Specific mismatch correction in bacteriophage lambda crosses by very short patch repair. Mol. Gen. Genet. 181:118-125.
31. Lieb, M., E. Allen, and D. Read. 1986. Very short patch mismatch repair in phage lambda: repair sites and length of repair tracts. Genetics 114:1041-1060.
32. Linton, J. P., J.-Y. J. Yen, E. Selby, Z. Chen, J. M. Chinsky, K. Liu, R. E. Kellems, and G. F. Crouse. 1989. Dual bidirectional promoters at the mouse dhfr locus: cloning and characterization of two mRNA classes of the divergently transcribed Rep-1 gene. Mol. Cell. Biol. 9:3058-3072.
33. Lu, A.-L., and D.-Y. Chang. 1988. Repair of single base-pair transversion mismatches of Escherichia coli in vitro: correction of certain A/G mismatches is independent of dam methylation and host mutHLS gene functions. Genetics 118:593-600.
34. Lu, A.-L., and D.-Y. Chang. 1988. A novel nucleotide excision repair for the conversion of an A/G mismatch to C/G base pair in E. coli. Cell 54:805-812.
35. Lu, A.-L., H.-F. Liu, C. P. Scholes, K. K. Surerus, and E. Münck. 1994. Unpublished data.
36. Maki, H., and M. Sekiguchi. 1992. MutT protein specifically hydrolyses a potent mutagenic substrate for DNA synthesis. Nature (London) 355:273-275.
37. Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
38. Marginson, G. P., and A. E. Pegg. 1981. Enzymatic release of 7-methylguanine from methylated DNA by rodent liver extracts. Proc. Natl. Acad. Sci. USA 78:861-865.
39. Maxam, A. M., and W. Gilbert. 1980. Sequencing end-labelled DNA with base-specific chemical cleavage. Methods Enzymol. 65:499-560.
40. Michaels, M. L., C. Cruz, A. P. Grollman, and J. H. Miller. 1992. Evidence that MutM and MutY combine to prevent mutations by an oxidatively damaged form of guanine in DNA. Proc. Natl. Acad. Sci. USA 89:7022-7025.
41. Michaels, M. L., and J. H. Miller. 1992. The GO repair system protects organisms from the mutagenesis effect of 8-hydroxyguanine (7,8-dihydro-8-oxo-guanine). J. Bacteriol. 174:6321-6325.
42. Michaels, M. L., L. Pham, Y. Ngheim, C. Cruz, and J. H. Miller. 1990. MutY, an adenine glycosylase active on G-A mispairs, has homology to endonuclease III. Nucleic Acids Res. 18:3841-3845.
43. Michaels, M. L., J. Tchou, A. P. Grollman, and J. H. Miller. 1992. A repair system for 8-oxo-7,8-dihydrodeoxyguanine (8-hydroxyguanine). Biochemistry 31:10964-10968.
44. Mo, J.-Y., H. Maki, and M. Sekiguchi. 1992. Hydrolytic elimination of a mutagenic nucleotide, 8-oxodGTP, by human 18-kilodalton protein: sanitization of nucleotide pool. Proc. Natl. Acad. Sci. USA 89:11021-11025.
45. Modrich, P. 1991. Mechanisms and biological effects of mismatch repair. Annu. Rev. Genet. 25:229-253.
46. Moriya, M. 1993. Single-stranded shuttle phagemid for mutagenesis studies in mammalian cells: 8-oxoguanine in DNA induces targeted G · C → T · A transversions in simian kidney cells. Proc. Natl. Acad. Sci. USA 90:1122-1126.
47. Moriya, M., C. Ou, V. Bodepudi, F. Johnson, M. Takeshita, and A. P. Grollman. 1991. Site-specific mutagenesis using a gapped duplex vector: a study of translesion synthesis past 8-oxodeoxyguanosine in Escherichia coli. Mutat. Res. 254:281-288.
48. New, L., K. Liu, and G. F. Crouse. 1993. The yeast gene MSH3 defines a new class of eukaryotic MutS homologues. Mol. Gen. Genet. 239:97-108.
49. Papadopoulos, N., N. C. Nicolaides, Y.-F. Wei, S. M. Ruben, K. C. Carter, C. A. Rosen, W. A. Haseltine, R. K. Fleischmann, C. M. Graser, M. D. Adams, J. C. Venter, S. R. Hamilton, G. M. Petersen, P. Watson, H. T. Lynch, P. Peltomaki, J.-P. Mecklin, A. de la Chapelle, K. W. Kinzler, and B. Vogelstein. 1994. Mutation of a mutL homolog in hereditary colon cancer. Science 263:1625-1629.
50. + tumor cells. Cell 75: 1227-1236.
51. Prolla, T. A., D.-M. Christie, and R. M. Liskay. 1994. Dual requirement in yeast DNA mismatch repair for MLH1 and PMS1, two homologs of the bacterial mutL gene. Mol. Cell. Biol. 14:407-415.
52. Radicella, J. P., E. A. Clark, S. Chen, and M. S. Fox. 1993. Patch length of localized repair event: role of DNA polymerase I in mutY-dependent mismatch repair. J. Bacteriol. 175:7732-7736.
53. Radicella, J. P., E. A. Clark, and M. S. Fox. 1988. Some mismatch repair activities in Escherichia coli. Proc. Natl. Acad. Sci. USA 85:9674-9678.
54. Radman, M., and R. Wagner. 1986. Mismatch repair in Escherichia coli. Annu. Rev. Genet. 20:523-528.
55. Raposa, S., and M. S. Fox. 1987. Some features of base pair mismatch and heterology repair in Escherichia coli. Genetics 117:381-390.
56. Reenan, R. A., and R. D. Kolodner. 1992. Isolation and characterization of two Saccharomyces cerevisiae genes encoding homologs of the bacterial HexA and MutS mismatch repair proteins. Genetics 132:963-973.
57. Reenan, R. A., and R. D. Kolodner. 1992. Characterization of insertion mutations in Saccharomyces cerevisiae MSH1 and MSH2 genes: evidence for separate mitochondrial and nuclear functions. Genetics 132:975-985.
58. Roelen, H. C. P. F., C. P. Saris, H. F. Brugghe, H. van den Elst, J. G. Westra, G. A. van der Marel, and J. H. van Boom. 1991. Solid-phase synthesis of DNA fragments containing the modified base 7-hydro-8-oxo-2′-deoxyguanosine. Nucleic Acids Res. 19:4361-4369.
59. Sakumi, K., M. Furuichi, T. Tsuzuki, T. Kakuma, S.-I. Kawabata, H. Maki, and M. Sekiguchi. 1993. Cloning and expression of cDNA for a human enzyme that hydrolyzes 8-oxo-dGTP, a mutagenic substrate for DNA synthesis. J. Biol. Chem. 268:23524-23530.
60. Shibutani, S., M. Takeshita, and A. P. Grollman. 1991. Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature (London) 349:431-434.
61. Strand, M., T. A. Prolla, R. M. Liskay, and T. Petes. 1993. Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair. Nature (London) 365:274-276.
62. Su, S.-S., R. S. Lahue, K. G. Au, and P. Modrich. 1988. Mispair specificity of methyl-directed DNA mismatch correction in vitro. J. Biol. Chem. 263:6829-6835.
63. Tchou, J., and A. P. Grollman. 1993. Repair of DNA containing the oxidatively-damaged base 8-hydroxyguanine. Mutat. Res. 299:277-287.
64. Tchou, J., H. Kasai, S. Shibutani, M.-H. Chung, A. P. Grollman, and S. Nishimura. 1991. 8-Oxoguanine (8-hydroxyguanine) DNA glycosylase and its substrate specificity. Proc. Natl. Acad. Sci. USA 88:4690-4694.
65. Thomas, D. C., J. D. Roberts, and T. A. Kunkel. 1991. Heteroduplex repair in extracts of human HeLa cells. J. Biol. Chem. 266:3744-3751.
66. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76:4350-4354.
67. Tsai-Wu, J.-J., H.-F. Liu, and A.-L. Lu. 1992. Escherichia coli MutY protein has both N-glycosylase and apurinic/apyrimidinic endonuclease activities on A · C and A · G mispairs. Proc. Natl. Acad. Sci. USA 89:8779-8783.
68. Tsai-Wu, J.-J., and A.-L. Lu. 1994. Escherichia coli mutY-dependent mismatch repair involves DNA polymerase I and a short repair tract. Mol. Gen. Genet. 244:444-450.
69. Tsai-Wu, J.-J., J. P. Radicella, and A.-L. Lu. 1991. Nucleotide sequence of the Escherichia coli micA gene required for A/G-specific mismatch repair: identity of MicA and MutY. J. Bacteriol. 173:1902-1910.
70. Varlet, I., M. Radman, and B. Brooks. 1990. DNA mismatch repair in Xenopus egg extracts: repair efficiency and DNA repair synthesis for all single base-pair mismatches. Proc. Natl. Acad. Sci. USA 87:7883-7887.
71. Wiebauer, K., and J. Jiricny. 1989. In vitro correction of G · T mispairs to G · C pairs in nuclear extracts from human cells. Nature (London) 339:234-236.
72. Wiebauer, K., and J. Jiricny. 1990. Mismatch-specific thymine DNA glycosylase and DNA polymerase β mediate the correction of G · T mispairs in nuclear extracts from human cells. Proc. Natl. Acad. Sci. USA 87:5842-5845.
73. Williamson, M., J. Game, and S. Fogel. 1985. Meiotic gene conversion mutants in Saccharomyces cerevisiae. I. Isolation and characterization of pms1-1 and pms1-2. Genetics 110:609-646.
74. Wood, M. L., M. Dizdaroglu, E. Gajewski, and J. M. Essigmann. 1990. Mechanistic studies of ionizing radiation and oxidative mutagenesis: genetic effects of single 8-hydroxylguanine (7-hydro-8-oxoguanine) residue inserted at a unique site in a viral genome. Biochemistry 29:7024-7032.
75. Yeh, Y.-C., D.-Y. Chang, J. Masin, and A.-L. Lu. 1991. Two nicking enzyme systems specific for mismatch-containing DNA in nuclear extracts from human cells. J. Biol. Chem. 266:6480-6484.