Understanding the role of the Q338H MUTYH variant in oxidative damage repair

Nucleic Acids Research

Volumn 41, Issue 7, 2013, Pages 4093-4103

  Turco, Eleonora ^a   Ventura, Ilenia ^a   Minoprio, Anna ^a   Russo, Maria Teresa ^a   Torreri, Paola ^a   Degan, Paolo ^b   Molatore, Sara ^c   Ranzani, Guglielmina Nadia ^c   Bignami, Margherita ^a   Mazzei, Filomena ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c UNIVERSITY OF PAVIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

7,8 DIHYDRO 8 OXO 2' DEOXYGUANINE; COMPLEMENTARY DNA; DNA GLYCOSYLASE MUTY; GUANINE DERIVATIVE; OXIDIZING AGENT; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ARTICLE; COLON POLYPOSIS; COLORECTAL CANCER; CONTROLLED STUDY; EMBRYO; EXCISION REPAIR; FIBROBLAST; GENE EXPRESSION; GENE MUTATION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; MUTYH ASSOCIATED POLYPOSIS; MUTYH GENE; NONHUMAN; OXIDATIVE STRESS; PENETRANCE; PRIORITY JOURNAL; REPLICATION SENSOR; S PHASE CELL CYCLE CHECKPOINT; SENSOR; TUMOR GENE; WILD TYPE;

AMINO ACID SUBSTITUTION; ANIMALS; CELL CYCLE PROTEINS; CELLS, CULTURED; DNA GLYCOSYLASES; DNA REPAIR; MICE; MICE, KNOCKOUT; MUTATION; OXIDATIVE STRESS; RECOMBINANT PROTEINS;

EID: 84876552334     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt130     Document Type: Article

References (52)

1. Barnes, D.E. and Lindahl, T. (2004) Repair and genetic consequences of endogeneous DNA base damage in mammalian cells. Annu. Rev. Genet., 38, 445-476. (Pubitemid 40013735)
2. Fortini, P. and Dogliotti, E. (2006) Base damage and single-strand break repair: mechanisms and functional significance of short and long-patch repair subpathways. DNA Repair, 6, 398-409. (Pubitemid 46357049)
3. Slupska, M.M., Luther, W.M., Chiang, J.H., Yang, H. and Miller, J.H. (1999) Functional expression of hMYH, a human homolog of the Escherichia coli MutY protein. J. Bacteriol., 181, 6210-6213. (Pubitemid 29459939)
4. Parker, A.R. and Eshleman, J.R. (2003) Human MutY: gene structure, protein functions and interactions, and role in carcinogenesis. Cell. Mol. Life Sci., 60, 2064-2083. (Pubitemid 37357417)
5. Parker, A., Gu, Y., Mahoney, W., Lee, S.H., Singh, K.K. and Lu, A.L. (2001) Human homolog of the MutY repair protein (hMYH) physically interacts with proteins involved in long patch DNA base excision repair. J. Biol. Chem., 276, 5547-5555.
6. Balakrishanan, L., Brandt, P.D., Lindsey-Boltz, L.A., Sancar, A. and Bambara, R.A. (2009) Long patch base excision repair proceeds via coordinated stimulation of the multienzyme DNA repair complex. J. Biol. Chem., 284, 15158-15172.
7. van Loon, B. and Hubscher, U. (2009) An 8-oxo-guanine repair pathway coordinated by MUTYH glycosylase and DNA polymerase lambda. Proc. Natl Acad. Sci. USA, 106, 18201-18206.
8. Boldogh, I., Milligan, D., Lee, M.S., Bassett, H., Lloyd, R.S. and McCullough, A.K. (2001) hMYH cell cycle dependent expression, subcellular localization and association with replication foci: evidence suggesting replication-coupled repair of adenine:8-oxoguanine mispairs. Nucleic Acids Res., 29, 2802-2809. (Pubitemid 32685044)
9. Gu, Y., Parker, A., Wilson, T.M., Bai, H., Chang, D.Y. and Lu, A.L. (2002) Human MutY homolog, a DNA glycosylase involved in base excision repair, physically and functionally interacts with mismatch repair proteins human MutS homolog 2/human MutS homolog 6. J. Biol. Chem., 277, 11135-11142. (Pubitemid 34952874)
10. Chang, D.Y. and Lu, A.L. (2002) Functional interaction of MutY homolog with proliferating cell nuclear antigen in fission yeast Schizosaccharomyces pombe. J. Biol. Chem., 277, 11853-11858.
11. Al-Tassan, N., Chmiel, N.H., Maynard, J., Fleming, N., Livingston, A.L., Williams, G.T., Hodges, A.K., Davies, D.R., David, S.S., Sampson, J.R. et al. (2002) Inherited variants of MYH associated with somatic G:C->T:A mutations in colorectal tumors. Nat. Genet., 30, 227-232.
12. Sieber, O.M., Lipton, L., Crabtree, M., Heinimann, K., Fidalgo, P., Phillips, R.K., Bisgaard, M.L., Orntoft, T.F., Aaltonen, L.A., Hodgson, S.V. et al. (2003) Multiple colorectal adenomas, classic adenomatous polyposis, and germ-line mutations in MYH. N. Engl. J. Med., 348, 791-799. (Pubitemid 36245755)
13. Out, A.A., Tops, C.M., Nielsen, M., Weiss, M.M., van Minderhout, I.J., Fokkema, I.F., Buisine, M.P., Claes, K., Colas, C., Fodde, R. et al. (2010) Leiden open variation database of the MUTYH gene. Hum. Mutat., 31, 1205-1215.
14. Bai, H., Jones, S., Guan, X., Wilson, T.M., Sampson, J.R., Cheadle, J.P. and Lu, A.L. (2005) Functional characterization of two human MutY homolog (hMYH) missense mutations (R227 and V232F) that lie within the putative hMSH6 binding domain and are associated with MYH polyposis. Nucleic Acids Res., 33, 597-604. (Pubitemid 40360989)
15. Bai, S., Grist, J., Gardner, G., Suthers, G., Wilson, T.M. and Lu, A.L. (2007) Functional characterization of human MutY homolog (hMYH) missense mutation (R231L) that is linked with hMYH-associated polyposis. Cancer Lett., 250, 74-81. (Pubitemid 46483844)
16. Ali, M., Kim, H., Cleary, S., Cupples, C., Gallinger, S. and Bristow, R. (2008) Characterization of mutant MUTYH proteins associated with familial colorectal cancer. Gastroenterology, 135, 499-507.
17. Kundu, S., Brinkmeyer, M.K., Livingston, A.L. and David, S.S. (2009) Adenine removal activity and bacterial complementation with the human MutY homologue (MUTYH) and Y165C, G382D, P391L and Q324R variants associates with colorectal cancer. DNA Repair, 8, 1400-1410.
18. D'Agostino, V.G., Minoprio, A., Torreri, P., Marinoni, I., Bossa, C., Petrucci, T.C., Albertini, A.M., Ranzani, G.M., Bignami, M. and Mazzei, F. (2010) Functional analysis of MUTYH mutated proteins associated with familial adenomatous polyposis. DNA Repair, 9, 700-707.
19. Goto, M., Shinmura, K., Nakabeppu, Y., Tao, H., Yamada, H., Tsuneyoshi, T. and Sugimura, H. (2010) Adenine DNA glycosylase activity of 14 human MutY homolog (MUTYH) variant proteins found in patients with colorectal polyposis and cancer. Hum. Mutat., 31, E1861-E1874.
20. Pope, M.A., Chmiel, N. and David, S.S. (2005) 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, 4, 315-325. (Pubitemid 40126995)
21. Ushijima, Y., Tominaga, Y., Miura, T., Tsuchimoto, D., Sakumi, K. and Nakabeppu, Y. (2005) A functional analysis of the DNA glycosylase activity of mouse MUTYH protein excising 2-hydroxyadenine opposite guanine in DNA. Nucleic Acids Res., 33, 672-682. (Pubitemid 40360997)
22. Yanaru-Fujisawa, R., Matsumoto, T., Ushijima, Y., Esaki, M., Hirahashi, M., Gushima, M., Yao, T., Nakabeppu, Y. and Iida, M. (2008) Genomic and functional analyses of MUTYH in Japanese patients with adenomatous polyposis. Clin. Genet., 73, 545-553. (Pubitemid 351663935)
23. Alhopuro, P., Parker, A., Lehtonen, R., Enholm, S., Jarvinen, H.J., Mecklin, J.P., Karhu, A., Eshleman, J.R. and Aaltonen, L.A. (2005) A novel functionally deficient MYH variant in individuals with colorectal adenomatous polyposis. Hum. Mutat., 26, 393-402.
24. Parker, A.R., Sieber, O.M., Shi, C., Hua, L., Takao, M., Tomlinson, I.P. and Eshleman, J.R. (2005) Cells with pathogenic biallelic mutations in the human MUTYH gene are defective in DNA damage binding and repair. Carcinogenesis, 26, 2010-2018. (Pubitemid 41631275)
25. Bartek, J., Lukas, C. and Lukas, J. (2004) Checking on DNA damage in S phase. Nat. Rev. Mol. Cell Biol., 5, 792-804. (Pubitemid 39336273)
26. Dorè, A.S., Kilkenny, M.L., Rzechorzek, N.J. and Pearl, L.H. (2009) Crystal structure of the RAD9-RAD1-HUS1 DNA damage checkpoint complex-implications for clamp loading and regulation. Mol. Cell., 34, 735-745.
27. Sohn, S.Y. and Cho, Y. (2009) Crystal structure of human rad9-hus1-rad1 clamp. J. Mol. Biol., 390, 490-502.
28. Shi, G., Chang, D.Y., Cheng, C.C., Cuan, X., Venclovas, C. and Lu, A.L. (2006) Physical and functional interactions between MutY glycosylase homologue (MYH) and checkpoint proteins RAD9-RAD1-HUS1. Biochem. J., 400, 53-62. (Pubitemid 44763819)
29. Luncsford, P.J., Chang, D.Y., Shi, G., Bernstein, J., Madabushi, A., Patterson, D.N., Lu, A.L. and Toth, E.A. (2010) A structural hinge in eukaryotic MUTY homologues mediates catalytic activity and RAD9-RAD1-HUS1 checkpoint complex interactions. J. Mol. Biol., 403, 351-370.
30. Gembka, A., Toueille, M., Smirnova, E., Poltz, R., Ferrari, E., Villani, G. and Hubscher, U. (2007) The checkpoint clamp, RAD9-RAD1-HUS1 complex, preferentially stimulates the activity of apurinic/apyrimidinic endonuclease 1 and DNA polymerase b in long patch base excision repair. Nucleic Acids Res., 35, 2596-2608. (Pubitemid 47073673)
31. Toueille, M., El-Andaloussi, N., Frouin, I., Freire, R., Funk, D., Shevelev, I., Friedrich-Heineken, E., Villani, G., Hottiger, M.O. and Hubscher, U. (2004) The human RAD9/RAD1/HUS1 damage sensor clamp interacts with DNA polymerase beta and increases its DNA substrate utilization efficiency: implications for DNA repair. Nucleic Acids Res., 32, 3316-3324. (Pubitemid 39117448)
32. Friedrich-Heineken, E., Toueille, M., Tannler, B., Burki, C., Ferrari, E., Hottiger, M.O. and Hubscher, U. (2005) The two DNA clamps RAD9/RAD1/HUS1 complex and proliferating cell nuclear antigen differentially regulate flap endonuclease 1 activity. J. Mol. Biol., 353, 980-989. (Pubitemid 41503266)
33. Wang, W., Brandt, P., Rossi, M.L., Lindsey-Boltz, L., Podust, V., Fanning, E., Sancar, A. and Bambara, R.A. (2004) The human RAD9-RAD1-HUS1 checkpoint complex stimulates flap endonuclease1. Proc. Natl Acad. Sci. USA, 101, 16762-16767. (Pubitemid 39601312)
34. Smirnova, E., Toueille, M., Markkanen, E. and Hubscher, U. (2005) The human checkpoint sensor and alternative DNA clamp RAD9-RAD1-HUS1 modulates the activity of DNA ligase I, a component of the long-patch base excision repair machinery. Biochem. J., 389, 13-17. (Pubitemid 40978002)
35. Wang, W., Lindsey-Boltz, L.A., Sancar, A. and Bambara, R.A. (2006) Mechanism of stimulation of human DNA ligase I by the RAD9-RAD1-HUS1 checkpoint complex. J. Biol. Chem., 281, 20865-20872. (Pubitemid 44115427)
36. Park, M.J., Park, J.H., Hahm, S.H., Ko, S.I., Lee, Y.R., Chung, J.H., Sohn, S.Y., Cho, Y., Kang, L.W. and Han, Y.S. (2009) Repair activities of human 8-oxoguanine DNA glycosylase are stimulated by the interaction with human checkpoint sensor RAD9-RAD1-HUS1 complex. DNA Repair, 8, 1190-1200.
37. Guan, X., Madabushi, A., Chang, D.Y., Fitzgerald, M.E., Shi, G., Drohat, A.C. and Lu, A.L. (2007) The human checkpoint sensor RAD9-RAD1-HUS1 interacts with and stimulates DNA repair enzyme TDG glycosylase. Nucleic Acids Res., 35, 6207-6218. (Pubitemid 350018582)
38. Guan, X., Bai, H., Shi, G., Theriot, C.A., Hazra, T.K., Mitra, S. and Lu, A.L. (2007) The human checkpoint sensor RAD9-RAD1-HUS1 interacts with and stimulates Neil1 glycosylase. Nucleic Acids Res., 35, 2463-2472. (Pubitemid 47073661)
39. Wu, X., Shell, S.M. and Zou, Y. (2005) Interaction and colocalization of Rad9/Rad1/Hus1 checkpoint complex with replication protein A in human cells. Oncogene, 24, 4728-4735. (Pubitemid 41032609)
40. He, W., Zhao, Y., Zhang, C., An, L., Hu, Z. and Lui, Y. (2008) RAD9 plays an important role in DNA mismatch repair through physical interaction with MLH1. Nucleic Acids Res., 36, 6406-6417.
41. Shinmura, K., Yamaguchi, S., Saitoh, T., Takeuchi-Sasaki, M., Kim, S.R., Nohmi, T. and Yokota, J. (2000) Adenine excisional repair function of MYH protein on the adenine:8-hydroxyguanine base pair in double-stranded DNA. Nucleic Acids Res., 28, 4912-4918. (Pubitemid 32014261)
42. Raetz, A.G., Xie, Y., Kundu, S., Brinkmeyer, M.K., Chang, C. and David, S.S. (2012) Cancer-associated variants and a common polymorphism of MUTYH exhibit reduced repair of oxidative DNA damage using a GFP-based assay in mammalian cells. Carcinogenesis, 33, 2301-2309.
43. Fromme, J.C., Banerjee, A., Huang, S.J. and Verdine, G. (2004) Structural basis for removal of adenine mispaired with 8-oxoguanine by MutY adenine DNA glycosylase. Nature, 427, 652-656. (Pubitemid 38248487)
44. Klungland, A., Rosewell, I., Hollenbach, S., Larsen, E., Daly, G., Epe, B., Seeberg, E., Lindahl, T. and Barnes, D.E. (1999) Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage. Proc. Natl Acad. Sci. USA, 96, 13300-12305.
45. Russo, M.T., De Luca, G., Casorelli, I., Degan, P., Molatore, S., Barone, F., Mazzei, F., Pannellini, T., Musiani, P. and Bignami, M. (2009) Role of MUTYH and MSH2 in the control of oxidative DNA damage, genetic instability and tumorigenesis. Cancer Res., 69, 4372-4379.
46. Molatore, S., Russo, M.T., D'Agostino, V.G., Barone, F., Matsumoto, Y., Albertini, A.M., Minoprio, A., Degan, P., Mazzei, F., Bignami, M. et al. (2010) MUTYH mutations associated with familial adenomatous polyposis: functional characterization by a mammalian cell-based assay. Hum. Mutat., 31, 159-166.
47. Porello, S.L., Leyes, A.E. and David, S.S. (1998) Single-turnover and pre-steady-state kinetics of the reaction of the adenine glycosylase MutY with mismatch-containing DNA substrates. Biochemistry, 37, 14756-14764. (Pubitemid 28487583)
48. Tominaga, Y., Ushijima, Y., Tsuchimoto, D., Mishima, M., Shirakawa, M., Hirano, S., Sakumi, K. and Nakabeppu, Y. (2004) MUTYH prevents OGG1 or APEX1 from inappropriately processing its substrate or reaction product with its C-terminal domain. Nucleic Acids Res., 32, 3198-3211. (Pubitemid 39028860)
49. Yang, H., Clendenin, W.M., Wong, D., Demple, B., Slupska, M.M., Chiang, J.H. and Miller, J.H. (2001) 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, 743-752. (Pubitemid 32124386)
50. Gorgens, H., Kruger, S., Kuhlisch, E., Pagenstecher, C., Hohl, R., Schackert, H.K. and Muller, A. (2006) Microsatellite stable colorectal cancers in clinically suspected hereditary nonpolyposis colorectal cancer patients without vertical transmission of disease are unlikely to be caused by biallelic germline mutations in MYH. J. Mol. Diagn., 8, 178-182. (Pubitemid 43811240)
51. Picelli, S., Zajac, P., Zhou, X.L., Edler, D., Lenander, C., Dalen, J., Hjern, F., Lundqvist, N., Lindforss, U., Pa hlman, L. et al. (2010) Common variants in human CRC genes as low-risk alleles. Eur. J. Cancer., 46, 1041-1048.
52. Casper, M., Plotz, G., Juengling, B., Zeuzem, S., Lammert, F. and Raedle, J. (2012) MUTYH hotspot mutations in unselected colonoscopy patients. Colorectal Dis., 14, e238-e244.