Role of MUTYH in human cancer

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 743-744, Issue , 2013, Pages 33-43

  Mazzei, Filomena ^a   Viel, Alessandra ^b   Bignami, Margherita ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b CENTRO DI RIFERIMENTO ONCOLOGICO   (Italy)

Author keywords

8 Hydroxyguanine; Colorectal cancer; DNA repair; MAP; Mutagenesis; MUTYH

Indexed keywords

DNA GLYCOSYLASE MUTY;

CANCER RISK; COLORECTAL CANCER; DISEASE MODEL; DNA GLYCOSYLASE MUTY GENE; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME MECHANISM; ENZYME SPECIFICITY; ENZYME STRUCTURE; GENE INACTIVATION; GENE MUTATION; GENETIC POLYMORPHISM; GENETIC RISK; GENETIC VARIABILITY; HETEROZYGOSITY; HUMAN; MALIGNANT NEOPLASTIC DISEASE; MOLECULAR PATHOLOGY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; STRUCTURE ACTIVITY RELATION;

ANIMALS; DNA GLYCOSYLASES; DNA REPAIR; HUMANS; MUTATION; NEOPLASMS; PHENOTYPE;

MAMMALIA;

EID: 84877926368     PISSN: 00275107     EISSN: 09218262     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2013.03.003     Document Type: Review

References (139)

1. Cheng K.C., Cahill D.S., Kasai H., Nishimura S., Loeb L.A. 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G->T and A->C substitutions. J. Biol. Chem. 1992, 267:166-172.
2. Michaels M.L., Cruz C., Grollman A.P., Miller J.H. Evidence that MutM and MutY combine to prevent mutations by an oxidatively damaged form of guanine in DNA. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:7022-7025.
3. Nghiem Y., Cabrera M., Cupples C.G., Miller J.H. The mutY gene: a mutator locus in Escherichia coli that generates G.C->T.A. transversions. Proc. Natl. Acad. Sci. U.S.A. 1988, 85:2709-2713.
4. Maki H., Sekiguchi M. MutT protein specifically hydrolyzes a potent mutagenic substrate for DNA synthesis. Nature (London) 1992, 355:273-275.
5. Fowler R.G., White S.J., Koyama C., Moore S.C., Dunn R.L., Schaaper R.M. Interactions among the Escherichia coli mutT, mutM, and mutY damage prevention pathways. DNA Repair (Amst.) 2003, 2:159-173.
6. Michaels M.L., Miller J.H. The GO system protects organisms from the mutagenic effect of the spontaneous lesion 8-hydroxyguanine (7, 8-dihydro-8-oxoguanine). J. Bacteriol. 1992, 174:6321-6325.
7. Jansson K., Blomberg A., Sunnerhagen P., Alm Rosenblad M. Evolutionary loss of 8-oxo-G repair components among eukaryotes. Genome Integr. 2010, 1:12.
8. Macpherson P., Barone F., Maga G., Mazzei F., Karran P., Bignami M. 8-oxoguanine incorporation into DNA repeats in vitro and mismatch recognition by MutSalpha. Nucleic Acids Res. 2005, 33:5094-5105.
9. Barone F., McCulloch S.D., Macpherson P., Maga G., Yamada M., Nohmi T., Minoprio A., Mazzei F., Kunkel T.A., Karran P., Bignami M. Replication of 2-hydroxyadenine-containing DNA and recognition by human MutSalpha. DNA Repair (Amst.) 2007, 6:355-366.
10. Russo M.T., De Luca G., Casorelli I., Degan P., Molatore S., Barone F., Mazzei F., Pannellini T., Musiani P., Bignami M. Role of MUTYH and MSH2 in the control of oxidative DNA damage, genetic instability, and tumorigenesis. Cancer Res. 2009, 69:4372-4379.
11. Russo M.T., Blasi M.F., Chiera F., Fortini P., Degan P., Macpherson P., Furuichi M., Nakabeppu Y., Karran P., Aquilina G., Bignami M. The oxidized deoxynucleoside triphosphate pool is a significant contributor to genetic instability in mismatch repair-deficient cells. Mol. Cell. Biol. 2004, 24:465-474.
12. 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., Cheadle J.P. Inherited variants of MYH associated with somatic G:C-->T:A mutations in colorectal tumors. Nat. Genet. 2002, 30:227-232.
13. Jones S., Emmerson P., Maynard J., Best J.M., Jordan S., Williams G.T., Sampson J.R., Cheadle J.P. Biallelic germline mutations in MYH predispose to multiple colorectal adenoma and somatic G:C-->T:A mutations. Hum. Mol. Genet. 2002, 11:2961-2967.
14. 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., Thomas H.J., Tomlinson I.P. Multiple colorectal adenomas, classic adenomatous polyposis, and germ-line mutations in MYH. N. Engl. J. Med. 2003, 348:791-799.
15. Lynch H.T., Lynch P.M., Lanspa S.J., Snyder C.L., Lynch J.F., Boland C.R. Review of the Lynch syndrome: history, molecular genetics, screening, differential diagnosis, and medicolegal ramifications. Clin. Genet. 2009, 76:1-18.
16. David S.S., O'Shea V.L., Kundu S. Base-excision repair of oxidative DNA damage. Nature 2007, 447:941-950.
17. van Loon B., Markkanen E., Hübscher U. Oxygen as a friend and enemy: how to combat the mutational potential of 8-oxo-guanine. DNA Repair (Amst.) 2010, 9:604-616.
18. Wallace S.S., Murphy D.L., Sweasy J.B. Base excision repair and cancer. Cancer Lett. 2012, 327(1-2):73-89.
19. Zeibell K., Aguila S., Yan Shi V., Chan A., Yang H., Miller J.H. Mutagenesis and repair in Bacillus anthracis: the effect of mutators. J. Bacteriol. 2007, 189:2331-2338.
20. Debora B.N., Vidales L.E., Ramírez R., Ramírez M., Robleto E.A., Yasbin R.E., Pedraza-Reyes M. Mismatch repair modulation of MutY activity drives Bacillus subtilis stationary-phase mutagenesis. J. Bacteriol. 2011, 193:236-245.
21. Oliver A., Cantón R., Campo P., Baquero F., Blázquez J. High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 2000, 288:1251-1254.
22. Sanders L.H., Sudhakaran J., Sutton M.D. The GO system prevents ROS-induced mutagenesis and killing in Pseudomonas aeruginosa. FEMS Microbiol. Lett. 2009, 294:89-96.
23. Mandsberg L.F., Ciofu O., Kirkby N., Christiansen L.E., Poulsen H.E., Høiby N. Antibiotic resistance in Pseudomonas aeruginosa strains with increased mutation frequency due to inactivation of the DNA oxidative repair system. Antimicrob. Agents Chemother. 2009, 53:2483-2491.
24. Mandsberg L.F., Maciá M.D., Bergmann K.R., Christiansen L.E., Alhede M., Kirkby N., Høiby N., Oliver A., Ciofu O. Development of antibiotic resistance and up-regulation of the antimutator gene pfpI in mutator Pseudomonas aeruginosa due to inactivation of two DNA oxidative repair genes (mutY, mutM). FEMS Microbiol. Lett. 2011, 324:28-37.
25. Ciofu O., Mandsberg L.F., Bjarnsholt T., Wassermann T., Høiby N. Genetic adaptation of Pseudomonas aeruginosa during chronic lung infection of patients with cystic fibrosis: strong and weak mutators with heterogeneous genetic backgrounds emerge in mucA and/or lasR mutants. Microbiology 2010, 156:1108-1119.
26. Davidsen T., Bjørås M., Seeberg E.C., Tønjum T. Antimutator role of DNA glycosylase MutY in pathogenic Neisseria species. J. Bacteriol. 2005, 187:2801-2809.
27. Davidsen T., Tuven H.K., Bjørås M., Rødland E.A., Tønjum T. Genetic interactions of DNA repair pathways in the pathogen Neisseria meningitidis. J. Bacteriol. 2007, 189:5728-5737.
28. Huang S., Kang J., Blaser M.J. Antimutator role of the DNA glycosylase mutY gene in Helicobacter pylori. J. Bacteriol. 2006, 188:6224-6234.
29. Kulick S., Moccia C., Kraft C., Suerbaum S. The Helicobacter pylori mutY homologue HP0142 is an antimutator gene that prevents specific C to A transversions. Arch. Microbiol. 2008, 189:263-270.
30. Eutsey R., Wang G., Maier R.J. Role of a MutY DNA glycosylase in combating oxidative DNA damage in Helicobacter pylori. DNA Repair (Amst.) 2007, 6:19-26.
31. Chang D.Y., Gu Y., Lu A.L. Fission yeast (Schizosaccharomyces pombe) cells defective in the MutY-homologous glycosylase activity have a mutator phenotype and are sensitive to hydrogen peroxide. Mol. Genet. Genomics 2001, 266:336-342.
32. Hirano S., Tominaga Y., Ichinoe A., Ushijima Y., Tsuchimoto D., Honda-Ohnishi Y., Ohtsubo T., Sakumi K., Nakabeppu Y. Mutator phenotype of MUTYH-null mouse embryonic stem cells. J. Biol. Chem. 2003, 278:38121-38124.
33. Russo M.T., De Luca G., Degan P., Parlanti E., Dogliotti E., Barnes D.E., Lindahl T., Yang H., Miller J.H., Bignami M. Accumulation of the oxidative base lesion 8-hydroxyguanine in DNA of tumor-prone mice defective in both the Myh and Ogg1 DNA glycosylases. Cancer Res. 2004, 64:4411-4414.
34. Xie Y., Yang H., Cunanan C., Okamoto K., Shibata D., Pan J., Barnes D.E., Lindahl T., McIlhatton M., Fishel R., Miller J.H. Deficiencies in mouse Myh and Ogg1 result in tumor predisposition and G to T mutations in codon 12 of the K-ras oncogene in lung tumors. Cancer Res. 2004, 64:3096-3102.
35. Sakamoto K., Tominaga Y., Yamauchi K., Nakatsu Y., Sakumi K., Yoshiyama K., Egashira A., Kura S., Yao T., Tsuneyoshi M., Maki H., Nakabeppu Y., Tsuzuki T. MUTYH-null mice are susceptible to spontaneous and oxidative stress induced intestinal tumorigenesis. Cancer Res. 2007, 67:6599-6604.
36. Sieber O.M., Howarth K.M., Thirlwell C., Rowan A., Mandir N., Goodlad R.A., Gilkar A., Spencer-Dene B., Stamp G., Johnson V., Silver A., Yang H., Miller J.H., Ilyas M., Tomlinson I.P. Myh deficiency enhances intestinal tumorigenesis in multiple intestinal neoplasia (ApcMin/+) mice. Cancer Res. 2004, 64:8876-8881.
37. Casorelli I., Pannellini T., De Luca G., Degan P., Chiera F., Iavarone I., Giuliani A., Butera A., Boirivant M., Musiani P., Bignami M. The Mutyh base excision repair gene influences the inflammatory response in a mouse model of ulcerative colitis. PLoS ONE 2010, 5(8):e12070.
38. Guan Y., Manuel R.C., Arvai A.S., Parikh S.S., Mol C.D., Miller J.H., Lloyd S., Tainer J.A. MutY catalytic core, mutant and bound adenine structures define specificity for DNA repair enzyme superfamily. Nat. Struct. Biol. 1998, 5:1058-1064.
39. Fromme J.C., Banerjee A., Huang S.J., Verdine G.L. Structural basis for removal of adenine mispaired with 8-oxoguanine by MutY adenine DNA glycosylase. Nature 2004, 427:652-656.
40. Luncsford P.J., Chang D.Y., Shi G., Bernstein J., Madabushi A., Patterson D.N., Lu A.L., Toth E.A. A structural hinge in eukaryotic MutY homologues mediates catalytic activity and Rad9-Rad1-Hus1 checkpoint complex interactions. J. Mol. Biol. 2010, 403:351-370.
41. Van Loom B., Hubscher U. An 8-oxo-guanine repair pathway coordinated by MUTYH glycosylase and DNA polymerase lambda. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:18201-18206.
42. Maga G., Villani G., Crespan E., Wimmer U., Ferrari E., Bertocci B., Hubscher U. 8-oxo-guanine bypass by human DNA polymerases in the presence of auxiliary proteins. DNA glycosylase. Nature 2004, 427:652-656.
43. Fortini P., Dogliotti E. Base damage and single-strand break repair: mechanisms and functional significance of short- and long-patch repair subpathways. DNA Repair (Amst.) 2007, 6:398-409.
44. Parlanti E., Fortini P., Macpherson P., Laval J., Dogliotti E. Base excision repair of adenine/8-oxoguanine mispairs by an aphidicolin-sensitive DNA polymerase in human cell extracts. Oncogene 2002, 21:5204-5212.
45. Parker A., Gu Y., Mahoney W., Lee S.-H., Singh K.K., Lu A.-L. Human Homolog of the MutY repair protein (hMYH) physically interacts with proteins involved in long patch DNA base excision repair. J. Biol. Chem. 2001, 276:5547-5555.
46. Balakrishanan L., Brant P.D., Lindsey-Boltz L.A., Sancar A., Bambara R.A. Long patch base excision repair proceeds via coordinated stimulation of the multienzyme DNA repair complex. J. Biol. Chem. 2009, 284:15158-15172.
47. Slupska M.M., Baihalov C., Luther W.M., Chiang J.M., Wei Y.F., Miller J.H. 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. 1996, 178:3885-3892.
48. Slupska M.M., Luther W.M., Chiang J.H., Yang H., Miller J.H. Functional expression of hMYH, a human homolog of the Escherichia coli MutY protein. J. Bacteriol. 1999, 181:6210-6213.
49. Hashiguchi K., Zhang Q.M., Sugiyama H., Ikeda H.S., Yonei S. Characterization of 2-hydroxyadenine DNA glycosylase activity of Escherichia coli MutY protein. Int. J. Radiat. Biol. 2002, 78:585-592.
50. Ohtsubo T., Nishioka K., Imaiso Y., Iwai S., Shimokawa H., Oda H., Fujiwara T., Nakabeppu Y. Identification of human MutY homolog (hMYH) as a repair enzyme for 2-hydroxyadenine in DNA and detection of multiple forms of hMYH located in nuclei and mitochondria. Nucleic Acids Res. 2000, 28:1355-1364.
51. Noll D.M., Gogos A., Granek J.A., Clarke N.D. The C-terminal domain of the adenine DNA glycosylase MutY confers specificity for 8-oxoguanine, adenine mispair and may be evolved from mutT, an 8-oxo-dGTPase. Biochemistry 1999, 38:6374-6379.
52. Volk D.E., House P.G., Thiviyanathan V., Luxon B.A., Zhang S., Lloyd R.S., Gorenstein D.G. Structural similarities between MutT and the C terminal domain of MutY. Biochemistry 2000, 39:7331-7336.
53. Gogos A., Cilllo J., Clarke N.D., Lu A. Specific recognition of A/G and A/7 8-dihydro-8-oxoguanine (8-oxoG) mismatches by Escherichia coli MutY: removal of the C terminal domain preferentially affects A/8-oxoG recognition. Biochemistry 1996, 35:16665-16671.
54. Chmiel N.H., Golinelli M.P., Francis A.W., David S.S. Efficient recognition of substrates and substrate analogs by the adenine glycosylase MutY require the C terminal domain. Nucleic Acids Res. 2001, 29:553-564.
55. Li L., Wright P.M., Lu A.L. The C-terminal Domain of MUTY glycosylase determines the 7.8-dihydro-8-oxo-guanine specificity and is crucial for mutation avoidance. J. Biol. Chem. 2000, 275:8448-8455.
56. Li L., Lu A.L. The C-terminal domain of Escherichia coli MutY is involved in DNA binding and glycosylase activities. Nucleic Acids Res. 2003, 31:3038-3049.
57. Kundu S., Brinkmeyer M.K., Eigenheer R.A., David S.S. Ser524 is a phosphorilation site in MUTYH and Ser524 mutations alter 8-oxoguanine: a mismatch recognition. DNA Repair (Amst.) 2010, 9:1026-1037.
58. Boal A.K., Yavin E., Barton J.K. DNA repair glycosilases with a (4Fe-4S) cluster: a redox cofactor for DNA-mediated charge transport?. J. Inorg. Biochem. 2007, 101:1913-1921.
59. Yang H., Clendenin W.M., Wong D., Demple B., Slupska M.M., Chiang J.H., Miller J.H. Enhanced activity of Adenine DNA glycosylase (Myh) by apurinic/apyrimidinic endonuclease (Ape1) in mammalian based excision repair o fan A/GO mismatch. Nucleic Acids Res. 2001, 29:743-752.
60. Gu Y., Parker A., Wilson T.M., Bai H., Chang D.Y., Lu A.L. Human MutY homolog, a DNA glycosylase involved in base excision repair, physically and functionally interacts with mismatch repair proteins human MutS homolog2/human MutS homolog 6. J. Biol. Chem. 2002, 277:11135-11142.
61. Pope M.A., Chmiel N.H., David S.S. Insight into the functional consequences of hMYH variants associated with colorectal cancer: distinct differences in the adenine glycosylase activity and the response to AP endonuclease of Y150 C and G365D murine MYH. DNA Repair 2005, 4:315-325.
62. Parker A.R., Eshleman J.R. Human MutY: gene structure, protein functions and interactions, and role in carcinogenesis. Cell Mol. Life Sci. 2003, 60:2064-2083.
63. Shi G., Chang D.Y., Cheng C.C., Guan X., Venclovas C., Lu A.L. Physical and functional interactions between MutY glycosylase homologue (MYH) and checkpoint proteins Rad9-Rad1-Hus1. Biochem. J. 2006, 400:53-62.
64. Gu Y., Lu A.L. Differential recognition and glycosylase activity of the native human MutY homolog (hMYH) and recombinant hMYH expressed in bacteria. Nucleic Acids Res. 2001, 29:2666-2674.
65. Ali M., Kim H., Cleary S., Cupples C., Gallinger S., Bristow R. Characterization of mutant MUTYH proteins associated with familial colorectal cancer. Gastroenterology 2008, 135:499-507.
66. Goto M., Shinmura K., Nakabeppu Y., Tao H., Yamada H., Tsuneyoshi T., Sugimura H. Adenine DNA glycosylase activity of 14 human MutY homolog (MUTYH) variant proteins found in patients with colorectal polyposis and cancer. Hum. Mutat. 2010, 31:1861-1874.
67. Kundu S., Brinkmeyer M.K., Livingston A.L., David S.S. Adenine removal activity and bacterial complementation with the human MutY homologue (MUTYH) and Y165 C, G382D, P391L and Q324R variants associated with colorectal cancer. DNA Repair (Amst.) 2009, 8:1400-1410.
68. Chmiel N.H., Livingston A.L., David S.S. Insight 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. 2003, 327:431-443.
69. Livingston A.L., Kundu S., Henderson Pozzi M., Anderson D.W., David S.S. Insight into the roles of tyrosine 82 and glycine 253 in the Escherichia coli adenine glycosylase MutY. Biochemistry 2005, 44:14179-14190.
70. Porello S.L., Leyes A.E., David S.S. Single turnover-state kinetics of the reaction of the adenine glycosylase MutY with mismatch-containing DNA substrates. Biochemistry 1998, 37:14756-14764.
71. Pope M.A., David S.S. DNA damage recognition and repair by the murine MutY homologue. DNA Repair 2005, 4:91-102.
72. Ushijima Y., Tominaga Y., Miura T., Tsuchimoto D., Sakumi K., Nagabeppu Y. A functional analysis of the DNA glycosylase activity of mouse MUTYH protein excising 2-hydroxyadenine opposite guanine in DNA. Nucleic Acids Res. 2005, 33:672-682.
73. Bai H., Jones S., Guan X., Wilson T.M., Sampson J.R., Cheadle J.P., Lu A.-L. Functional characterization of two human MutY homolog (hMYH) missense mutations (R227 and 232F) that lie within the putative hMSH6 binding domain and are associated with MYH polyposis. Nucleic Acids Res. 2005, 33:597-604.
74. Bai H., Grist S., Gardner J., Suthers G., Wilson T.M., Lu A.L. Functional characterization of human MutY homolog (hMYH) missense mutation (R231L) that is linked with hMYH-associated polyposis. Cancer Lett. 2007, 250:74-81.
75. D'Agostino V.G., Minoprio A., Torreri P., Marinoni I., Bossa C., Petrucci T.C., Albertini A.M., Ranzani G.N., Bignami M., Mazzei F. Functional analysis of MUTYH mutated proteins associated with familial adenomatous polyposis. DNA Repair (Amst.) 2010, 9:700-707.
76. Forsbring M., Vik E.S., Dalhus B., Karlsen T.H., Bergquist A., Schrumpf E., Bjoras M., Boberg K.M., Alseth I. Catalytically impaired hMYH and Neil1 mutant proteins identified in patients with primary sclerosing cholangitis and cholangiocarcinoma. Carcinogenesis 2009, 30:1147-1154.
77. Shinmura K., Yamaguchi S., Saitoh T., Takeuchi-Sasaki M., Kim S.R., Nohmi T., Yokota J. Adenine excisional repair function of MYH protein on the adenine: 8-hydroxyguanine base pair in double stranded DNA. Nucleic Acids Res. 2000, 28:4912-4918.
78. Raetz A.G., Xie Y., Kundu S., Brinkmeyer M.K., Chang C., David S.S. 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 2012, 33:2301-2319.
79. Out A.A., Tops C.M.J., Nielsen M., Weiss M.M., van Minderhout I.J.H.M., Fokkema I.F.A.C., Buisine M.-P., Claes K., Colas C., Fodde R., Fostira F., Franken P.F., Gaustadnes M., Heinimann K., Hodgson S.V., Hogervorst F.B.L., Holinski-Feder E., Lagerstedt-Robinson K., Olschwang S., van den Ouweland A.M.W., Redeker E.J.W., Scott R.J., Vankeirsbilck B., Grønlund R.V., Wijnen J.T., Wikman F.P., Aretz S., Sampson J.R., Devilee P., den Dunnen J.T., Hes F.J. Leiden open variation database of the MUTYH gene. Hum. Mutat. 2010, 31:1205-1215.
80. Turco E., Ventura I., Minoprio A., Russo M.T., Torreri P., Degan P., Molatore S., Ranzani G.N., Bignami M., Mazzei F. Understanding the role of the Q338H MUTYH variant in oxidative damage repair. Nucleic Acids Rep. 2013, 10.1093/nar/gkt130.
81. Oka S., Ohno M., Tsuchimoto D., Sakumi K., Furuichi M., Nakabeppu Y. Two distinct pathways of cell death triggered by oxidative damage to nuclear and mitochondrial DNAs. EMBO J. 2008, 27:421-432.
82. Molatore S., Russo M.T., D'Agostino V.G., Barone F., Matsumoto Y., Albertini A.M., Minoprio A., Degan P., Mazzei F., Bignami M., Ranzani G.N. MUTYH mutations associated with familial adenomatous polyposis: functional characterization by a mammalian cell-based assay. Hum. Mutat. 2010, 31:159-166.
83. Xie Y., Yang H., Miller J.H., Shih D.M., Hicks G.G., Xie J., Shiu R.P. Cells deficient in oxidative DNA damage repair genes Myh and Ogg1 are sensitive to oxidants with increased G2/M arrest and multinucleation. Carcinogenesis 2008, 29:722-728.
84. Ruggieri V., Pin E., Russo M.T., Barone F., Degan P., Sanchez M., Quaia M., Minoprio A., Turco E., Mazzei F., Viel A., Bignami M. Loss of MUTYH function in human cells leads to accumulation of oxidative damage and genetic instability. Oncogene 2012, 479. 10.1038/onc. 2012.
85. Parker A.R., Sieber O.M., Shi C., Hua L., Takao M., Tomlinson I.P., Eshleman J.R. Cells with pathogenic biallelic mutations in the human MUTYH gene are defective in DNA damage binding and repair. Carcinogenesis 2005, 26:2010-2018.
86. Alhopuro P., Parker A.R., Lehtonen R., Enholm S., Järvinen H.J., Mecklin J.P., Karhu A., Eshleman J.R., Aaltonen L.A. A novel functionally deficient MYH variant in individuals with colorectal adenomatous polyposis. Hum. Mutat. 2005, 26:393-402.
87. Shinmura K., Goto M., Suzuki M., Tao H., Yamada H., Igarashi H., Matsuura S., Maeda M., Konno H., Matsuda T., Sugimura H. Reduced expression of MUTYH with suppressive activity against mutations caused by 8-hydroxyguanine is a novel predictor of a poor prognosis in human gastric cancer. J. Pathol. 2011, 225:414-423.
88. Lubbe S.J., Di Bernardo M.C., Chandler I.P., Houlston R.S. Clinical implications of the colorectal cancer risk associated with MUTYH mutation. J. Clin. Oncol. 2009, 27:3975-3980.
89. O'Shea A.M., Cleary S.P., Croitoru M.A., Kim H., Berk T., Monga N., Riddell R.H., Pollett A., Gallinger S. Pathological features of colorectal carcinomas in MYH-associated polyposis. Histopathology 2008, 53:184-194.
90. Cleary S.P., Cotterchio M., Jenkins M.A., Kim H., Bristow R., Green R., Haile R., Hopper J.L.J.L., LeMarchand L., Lindor N., Parfrey P., Potter J., Younghusband B., Gallinger S. Germline MutY human homologue mutations and colorectal cancer: a multisite case-control study. Gastroenterology 2009, 136:1251-1260.
91. Nieuwenhuis M.H., Vogt S., Jones N., Nielsen M., Hes F.J., Sampson J.R., Aretz S., Vasen H.F. Evidence for accelerated colorectal adenoma--carcinoma progression in MUTYH-associated polyposis?. Gut 2012, 61:734-738.
92. Farrington S.M., Tenesa A., Barnetson R., Wiltshire A., Prendergast J., Porteous M., Campbell H., Dunlop M.G. Germline susceptibility to colorectal cancer due to base-excision repair gene defects. Am. J. Hum. Genet. 2005, 77:112-119.
93. Aretz S., Tricarico R., Papi L., Spier I., Pin E., Horpaopan S., Lucci-Cordisco E., Pedroni M., Stienen D., Gentile A., Panza A., Piepoli A., Ponz de Leon M., Friedl W., Viel A., Genuardi M. MUTYH-associated polyposis (MAP): evidence for the origin of the common European mutations p.Tyr179Cys and p.Gly396Asp by founder events. Eur. J. Hum. Genet. 2013, 309. 10.1038/ejhg. 2012.
94. Nielsen M., Joerink-van de Beld M.C., Jones N., Vogt S., Tops C.M., Vasen H.F., Sampson J.R., Aretz S., Hes F.J. Analysis of MUTYH genotypes and colorectal phenotypes in patients with MUTYH-associated polyposis. Gastroenterology 2009, 136:471-476.
95. Pin E., Pastrello C., Tricarico R., Papi L., Quaia M., Fornasarig M., Carnevali I., Oliani C., Fornasin A., Agostini M., Maestro R., Barana D., Aretz S., Genuardi M., Viel A. MUTYH c.933+3A>C, associated with a severely impaired gene expression, is the first Italian founder mutation in MUTYH-associated polyposis. Int. J. Cancer 2013, 132:1060-1069.
96. Tao H., Shinmura K., Hanaoka T., Natsukawa S., Shaura K., Koizumi Y., Kasuga Y., Ozawa T., Tsujinaka T., Li Z., Yamaguchi S., Yokota J., Sugimura H., Tsugane S. A novel splice-site variant of the base excision repair gene MYH is associated with production of an aberrant mRNA transcript encoding a truncated MYH protein not localized in the nucleus. Carcinogenesis 2004, 25:1859-1866.
97. Plotz G., Casper M., Raedle J., Hinrichsen I., Heckel V., Brieger A., Trojan J., Zeuzem S. MUTYH gene expression and alternative splicing in controls and polyposis patients. Hum. Mutat. 2012, 33:1067-1074.
98. Fornasarig M., Minisini A.M., Viel A., Quaia M., Canzonieri V., Veronesi A. Twelve years of endoscopic surveillance in a family carrying biallelic Y165 C MYH defect: report of a case. Dis. Colon Rectum 2006, 49:272-275.
99. Vasen H.F., Möslein G., Alonso A., Aretz S., Bernstein I., Bertario L., Blanco I., Bülow S., Burn J., Capella G., Colas C., Engel C., Frayling I., Friedl W., Hes F.J., Hodgson S., Järvinen H., Mecklin J.P., Møller P., Myrhøi T., Nagengast F.M., Parc Y., Phillips R., Clark S.K., de Leon M.P., Renkonen-Sinisalo L., Sampson J.R., Stormorken A., Tejpar S., Thomas H.J., Wijnen J. Guidelines for the clinical management of familial adenomatous polyposis (FAP). Gut 2008, 57:704-713.
100. Buecher B., Bonaïti C., Buisine M.P., Colas C., Saurin J.C. French experts report on MUTYH-associated polyposis (MAP). Fam. Cancer 2012, 11:321-328.
101. Jenkins M.A., Croitoru M.E., Monga N., Cleary S.P., Cotterchio M., Hopper J.L., Gallinger S. Risk of colorectal cancer in monoallelic and biallelic carriers of MYH mutations: a population-based case-family study. Cancer Epidemiol. Biomarkers Prev. 2006, 15:312-314.
102. Theodoratou E., Campbell H., Tenesa A., Houlston R., Webb E., Lubbe S., Broderick P., Gallinger S., Croitoru E.M., Jenkins M.A., Win A.K., Cleary S.P., Koessler T., Pharoah P.D., Küry S., Bézieau S., Buecher B., Ellis N.A., Peterlongo P., Offit K., Aaltonen L.A., Enholm S., Lindblom A., Zhou X.L., Tomlinson I.P., Moreno V., Blanco I., Capellà G., Barnetson R., Porteous M.E., Dunlop M.G., Farrington S.M. A large-scale meta-analysis to refine colorectal cancer risk estimates associated with MUTYH variants. Br. J. Cancer 2010, 103:1875-1884.
103. Jones N., Vogt S., Nielsen M., Christian D., Wark P.A., Eccles D., Edwards E., Evans D.G., Maher E.R., Vasen H.F., Hes F.J., Aretz S., Sampson J.R. Increased colorectal cancer incidence in obligate carriers of heterozygous mutations in MUTYH. Gastroenterology 2009, 137:489-494.
104. Win A.K., Cleary S.P., Dowty J.G., Baron J.A., Young J.P., Buchanan D.D., Southey M.C., Burnett T., Parfrey P.S., Green R.C., Le Marchand L., Newcomb P.A., Haile R.W., Lindor N.M., Hopper J.L., Gallinger S., Jenkins M.A. Cancer risks for monoallelic MUTYH mutation carriers with a family history of colorectal cancer. Int. J. Cancer 2011, 129:2256-2262.
105. Avezzù A., Agostini M., Pucciarelli S., Lise M., Urso E.D., Mammi I., Maretto I., Enzo M.V., Pastrello C., Lise M., Nitti D., Viel A. The role of MYH gene in genetic predisposition to colorectal cancer: another piece of the puzzle. Cancer Lett. 2008, 268:308-313.
106. Thorstensen L., Qvist H., Heim S., Liefers G.J., Nesland J.M., Giercksky K.E., Lothe R.A. Evaluation of 1p losses in primary carcinomas, local recurrences and peripheral metastases from colorectal cancer patients. Neoplasia 2000, 2:514-522.
107. Croitoru M.E., Cleary S.P., Di Nicola N., Manno M., Selander T., Aronson M., Redston M., Cotterchio M., Knight J., Gryfe R., Gallinger S. Association between biallelic and monoallelic germline MYH gene mutations and colorectal cancer risk. J. Natl. Cancer Inst. 2004, 96:1631-1634.
108. Kambara T., Whitehall V.L., Spring K.J., Barker M.A., Arnold S., Wynter C.V., Matsubara N., Tanaka N., Young J.P., Leggett B.A., Jass J.R. Role of inherited defects of MYH in the development of sporadic colorectal cancer. Genes Chromosomes Cancer 2004, 40:1-9.
109. Niessen R.C., Sijmons R.H., Ou J., Olthof S.G., Osinga J., Ligtenberg M.J., Hogervorst F.B., Weiss M.M., Tops C.M., Hes F.J., de Bock G.H., Buys C.H., Kleibeuker J.H., Hofstra R.M. MUTYH and the mismatch repair system: partners in crime?. Hum Genet. 2006, 119:206-211.
110. Steinke V., Rahner N., Morak M., Keller G., Schackert H.K., Görgens H., Schmiegel W., Royer-Pokora B., Dietmaier W., Kloor M., Engel C., Propping P., Aretz S. German HNPCC Consortium, No association between MUTYH and MSH6 germline mutations in 64 HNPCC patients. Eur. J. Hum. Genet. 2008, 16:587-592.
111. Morak M., Massdorf T., Sykora H., Kerscher M., Holinski-Feder E. First evidence for digenic inheritance in hereditary colorectal cancer by mutations in the base excision repair genes. Eur. J. Cancer 2011, 47:1046-1055.
112. Vogt S., Jones N., Christian D., Engel C., Nielsen M., Kaufmann A., Steinke V., Vasen H.F., Propping P., Sampson J.R., Hes F.J., Aretz S. Expanded extracolonic tumor spectrum in MUTYH-associated polyposis. Gastroenterology 2009, 137:1976-1985.
113. Ponti G., Ponz de Leon M., Maffei S., Pedroni M., Losi L., Di Gregorio C., Gismondi V., Scarselli A., Benatti P., Roncari B., Seidenari S., Pellacani G., Varotti C., Prete E., Varesco L., Roncucci L. Attenuated familial adenomatous polyposis and Muir-Torre syndrome linked to compound biallelic constitutional MYH gene mutations. Clin. Genet. 2005, 68:442-447.
114. Ajith Kumar V.K., Gold J.A., Mallon E., Thomas S., Hodgson S.V. Sebaceous adenomas in an MYH associated polyposis patient of Indian (Gujarati) origin. Fam. Cancer 2008, 7:187-189.
115. de Ferro S.M., Suspiro A., Fidalgo P., Lage P., Rodrigues P., Fragoso S., Vitoriano I., Baltazar C., Albuquerque C., Bettencourt A., Leitão C.N. Aggressive phenotype of MYH-associated polyposis with jejunal cancer and intra-abdominal desmoid tumor: report of a case. Dis. Colon Rectum 2009, 52:742-745.
116. Beiner M.E., Zhang W.W., Zhang S., Gallinger S., Sun P., Narod S.A. Mutations of the MYH gene do not substantially contribute to the risk of breast cancer. Breast Cancer Res. Treat. 2009, 114:575-578.
117. Out A.A., Wasielewski M., Huijts P.E., van Minderhout I.J., Houwing-Duistermaat J.J., Tops C.M., Nielsen M., Seynaeve C., Wijnen J.T., Breuning M.H., van Asperen C.J., Schutte M., Hes F.J., Devilee P. MUTYH gene variants and breast cancer in a Dutch case-control study. Breast Cancer Res. Treat. 2012, 134(1):219-227.
118. Barnetson R.A., Devlin L., Miller J., Farrington S.M., Slater S., Drake H., Campbell M.G., Dunlop M.E., Porteous Germline mutation prevalence in the base excision repair gene, MYH, in patients with endometrial cancer. Clin. Genet. 2007, 72:551-555.
119. Tricarico R., Bet P., Ciambotti B., Di Gregorio C., Gatteschi B., Gismondi V., Toschi B., Tonelli F., Varesco L., Genuardi M. Endometrial cancer and somatic G>T KRAS transversion in patients with constitutional MUTYH biallelic mutations. Cancer Lett. 2009, 274:266-270.
120. Wasielewski M., Out A.A., Vermeulen J., Nielsen M., van den Ouweland A., Tops C.M., Wijnen J.T., Vasen H.F., Weiss M.M., Klijn J.G., Devilee P., Hes F.J., Schutte M. Increased MUTYH mutation frequency among Dutch families with breast cancer and colorectal cancer. Breast Cancer Res. Treat. 2010, 124:635-641.
121. Kasahara M., Osawa K., Yoshida K., Miyaishi A., Osawa Y., Inoue N., Tsutou A., Tabuchi Y., Tanaka K., Yamamoto M., Shimada E., Takahashi J. Association of MUTYH Gln324His and APEX1 Asp148Glu with colorectal cancer and smoking in a Japanese population. J. Exp. Clin. Cancer Res. 2008, 27:49.
122. Picelli S., Zajac P., Zhou X.L., Edler D., Lenander C., Dalén J., Hjern F., Lundqvist N., Lindforss U., Påhlman L., Smedh K., Törnqvist A., Holm J., Janson M., Andersson M., Ekelund S., Olsson L., Lundeberg J., Lindblom A. Common variants in human CRC genes as low-risk alleles. Eur. J. Cancer 2010, 46:1041-1048.
123. Tao H., Shinmura K., Suzuki M., Kono S., Mibu R., Tanaka M., Kakeji Y., Maehara Y., Okamura T., Ikejiri K., Futami K., Yasunami Y., Maekawa T., Takenaka K., Ichimiya H., Imaizumi N., Sugimura H. Association between genetic polymorphisms of the base excision repair gene MUTYH and increased colorectal cancer risk in a Japanese population. Cancer Sci. 2008, 99:355-360.
124. Casper M., Plotz G., Juengling B., Zeuzem S., Lammert F., Raedle J. MUTYH hotspot mutations in unselected colonoscopy patients. Colorectal Dis. 2012, 14:e238-e244.
125. Miyaishi A., Osawa K., Osawa Y., Inoue N., Yoshida K., Kasahara M., Tsutou A., Tabuchi Y., Sakamoto K., Tsubota N., Takahashi J. MUTYH Gln324His gene polymorphism and genetic susceptibility for lung cancer in a Japanese population. J. Exp. Clin. Cancer Res. 2009, 28:10.
126. Sun C., Chen H., Guo W., Zhang K., Qi Q., Gu X., Zhu D., Wang Y. A common mutation of the MYH gene is associated with increased DNA oxidation and age-related diseases. Free Radic. Biol. Med. 2010, 48:430-436.
127. Zhu M., Chen X., Zhang H., Xiao N., Zhu C., He Q., Guo W., Cai Z., Shen H., Wang Y. AluYb8 insertion in the MUTYH gene and risk of early-onset breast and gastric cancers in the Chinese population. Asian Pac. J. Cancer Prev. 2011, 12:1451-1455.
128. Lipton L., Halford S.E., Johnson V., Novelli M.R., Jones A., Cummings C., Barclay E., Sieber O., Sadat A., Bisgaard M.L., Hodgson S.V., Aaltonen L.A., Thomas H.J., Tomlinson I.P. Carcinogenesis in MYH-associated polyposis follows a distinct genetic pathway. Cancer Res. 2003, 63:7595-7599.
129. Jones S., Lambert S., Williams G.T., Best J.M., Sampson J.R., Cheadle J.P. Increased frequency of the k-ras G12 C mutation in MYH polyposis colorectal adenomas. Br. J. Cancer 2004, 90:1591-1593.
130. van Puijenbroek M., Nielsen M., Tops C.M., Halfwerk H., Vasen H.F., Weiss M.M., van Wezel T., Hes F.J., Morreau H. Identification of patients with (atypical) MUTYH-associated polyposis by KRAS2 c.34G>T prescreening followed by MUTYH hotspot analysis in formalin-fixed paraffin-embedded tissue. Clin. Cancer Res. 2008, 14:139-142.
131. Middeldorp A., van Puijenbroek M., Nielsen M., Corver W.E., Jordanova E.S., ter Haar N., Tops C.M., Vasen H.F., Lips E.H., van Eijk R., Hes F.J., Oosting J., Wijnen J., van Wezel T., Morreau H. High frequency of copy-neutral LOH in MUTYH-associated polyposis carcinomas. J. Pathol. 2008, 216:25-31.
132. Bougatef K., Marrakchi R., Kourda N., Ben Lahely Y.B., Jileni S.B., El Khil H.K., Soubrier F.F., Ammar Elgaaied A.B. Somatic mutation of MutYH in Tunisian patients with sporadic colorectal cancer. J. Clin. Lab. Anal. 2007, 21:372-374.
133. Halford S.E., Rowan A.J., Lipton L., Sieber O.M., Pack K., Thomas H.J., Hodgson S.V., Bodmer W.F. I.P. Tomlinson Germline mutations but not somatic changes at the MYH locus contribute to the pathogenesis of unselected colorectal cancers. Am. J. Pathol. 2003, 162:1545-1548.
134. Vasovcak P., Pavlikova K., Sedlacek Z., Skapa P., Kouda M., Hoch J., Krepelova A. Molecular genetic analysis of 103 sporadic colorectal tumours in Czech patients. PLoS One 2011, 6:e24114.
135. Kuno T., Matsubara N., Tsuda S., Kobayashi M., Hamanaka M., Yamagishi D., Tsukamoto K., Yamano T., Noda M., Ikeuchi H., Kim S., Tamura K., Tomita N. Alterations of the base excision repair gene MUTYH in sporadic colorectal cancer. Oncol. Rep. 2012, 28:473M-480M.
136. Gushima M., Hirahashi T., Matsumoto K., Fujita R., Fujisawa K., Mizumoto Y., Nakabeppu M., Iida T., Yao M. Tsuneyoshi Altered expression of MUTYH and an increase in 8-hydroxydeoxyguanosine are early events in ulcerative colitis-associated carcinogenesis. J. Pathol. 2009, 219:77-86.
137. Oka S., Nakabeppu Y. DNA glycosylase encoded by MUTYH functions as a molecular switch for programmed cell death under oxidative stress to suppress tumorigenesis. Cancer Sci. 2011, 102:677-682.
138. de Miranda N.F., Nielsen M., Pereira D., van Puijenbroek M., Vasen H.F., Hes F.J., van Wezel T., Morreau H. MUTYH-associated polyposis carcinomas frequently lose HLA class I expression - a common event amongst DNA-repair-deficient colorectal cancers. J. Pathol. 2009, 219:69-76.
139. de Miranda N.F., Hes F.J., van Wezel T., Morreau H. Role of the microenvironment in the tumourigenesis of microsatellite unstable and MUTYH-associated polyposis colorectal cancers. Mutagenesis 2012, 27:247-253.