Mismatch repair proteins recruit DNA methyltransferase 1 to sites of oxidative DNA damage

Journal of Molecular Cell Biology

Volumn 8, Issue 3, 2016, Pages 244-254

  Ding, Ning ^a   Bonham, Emily M ^a   Hannon, Brooke E ^a   Amick, Thomas R ^a   Baylin, Stephen B ^b   O'Hagan, Heather M ^a,c  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

DNA repair; DNMT1; epigenetics; mismatch repair; oxidative damage; SIRT1; transcription

Indexed keywords

DNA METHYLTRANSFERASE 1; HYDROGEN PEROXIDE; MISMATCH REPAIR PROTEIN; PROTEIN MSH2; PROTEIN MSH6; CHROMATIN; CYCLINE; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA BINDING PROTEIN; G-T MISMATCH-BINDING PROTEIN; MSH2 PROTEIN, HUMAN; PROTEIN BINDING;

ARTICLE; BINDING AFFINITY; CHROMATIN; CONTROLLED STUDY; CPG ISLAND; DNA DAMAGE; EPIGENETICS; GENETIC TRANSCRIPTION; OXIDATIVE STRESS; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; DRUG EFFECTS; GENE SILENCING; GENETICS; HUMAN; METABOLISM; MISMATCH REPAIR; OXIDATION REDUCTION REACTION; TUMOR CELL LINE;

CELL LINE, TUMOR; CHROMATIN; CPG ISLANDS; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA DAMAGE; DNA MISMATCH REPAIR; DNA-BINDING PROTEINS; GENE KNOCKDOWN TECHNIQUES; HUMANS; HYDROGEN PEROXIDE; MUTS HOMOLOG 2 PROTEIN; OXIDATION-REDUCTION; PROLIFERATING CELL NUCLEAR ANTIGEN; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; TRANSCRIPTION, GENETIC;

EID: 84978871086     PISSN: 16742788     EISSN: 17594685     Source Type: Journal    
DOI: 10.1093/jmcb/mjv050     Document Type: Article

References (39)

1. Christmann M., and Kaina B. (2000). Nuclear translocation of mismatch repair proteins MSH2 and MSH6 as a response of cells to alkylating agents. J. Biol. Chem. 275, 36256-36262
2. Chuang L.S.H., Ian H.I., Koh T.W., et al. (1997). Human DNA (cytosine-5) methyltransferase PCNA complex as a target for p21(WAF1). Science 277, 1996-2000
3. Clements E.G., Mohammad H.P., Leadem B.R., et al. (2012). Dnmt1 modulates gene expression without its catalytic activity partially through its interactions with histone-modifying enzymes. Nucleic Acids Res. 40, 4334-4346
4. Colussi C., Parlanti E., Degan P., et al. (2002). The mammalian mismatch repair pathway removesDNA 8-oxodGMPincorporated from the oxidized dNTP pool. Curr. Biol. 12, 912-918
5. DeWeese T.L., Shipman J.M., Larrier N.A., et al. (1998). Mouse embryonic stem cells carrying one or two defective Msh2 alleles respond abnormally to oxidative stress inflicted by low-level radiation. Proc. Natl Acad. Sci. USA 95, 11915-11920
6. Edelbrock M.A., Kaliyaperumal S., and Williams K.J. (2013). Structural, molecular and cellular functions of MSH2 and MSH6 during DNA mismatch repair, damage signaling and other noncanonical activities. Mutat. Res. 743-744, 53-66
7. Egger G., Jeong S., Escobar S.G., et al. (2006). Identification of DNMT1 (DNA methyltransferase 1) hypomorphs in somatic knockouts suggests an essential role for DNMT1 in cell survival. Proc. Natl Acad. Sci. USA 103, 14080-14085
8. Gassman N.R., Clodfelter J.E., McCauley A.K., et al. (2011). Cooperative nuclear localization sequences lend a novel role to the N-terminal region of MSH6. PLoS One 6, e17907
9. Groth A., Rocha W., Verreault A., et al. (2007). Chromatin challenges during DNA replication and repair. Cell 128, 721-733
10. Guo G., Wang W., and Bradley A. (2004). Mismatch repair genes identified using genetic screens in Blm-deficient embryonic stem cells. Nature 429, 891-895
11. Ha K., Lee G.E., Palii S.S., et al. (2010). Rapid and transient recruitment of DNMT1 to DNA double-strand breaks is mediated by its interaction with multiple components of the DNA damage response machinery. Hum. Mol. Genet. 20, 126-140
12. Havugimana P.C., Hart G.T., Nepusz T., et al. (2012).Acensus ofhumansoluble protein complexes. Cell 150, 1068-1081
13. Hong Z., Jiang J., Hashiguchi K., et al. (2008). Recruitment of mismatch repair proteins to the site ofDNAdamage inhuman cells. J. Cell Sci. 121, 3146-3154
14. Jass J.R. (2007). Classification of colorectal cancer based on correlation of clinical, morphological and molecular features. Histopathology 50, 113-130
15. Jung I., Kim S.K., Kim M., et al. (2012). H2B monoubiquitylation is a 5'-enriched active transcription mark and correlates with exon-intron structure in human cells. Genome Res. 22, 1026-1035
16. Kim M., Trinh B.N., Long T.I., et al. (2004). Dnmt1 deficiency leads to enhanced microsatellite instability in mouse embryonic stem cells. Nucleic Acids Res. 32, 5742-5749
17. Kohli R.M., and Zhang Y. (2013). TET enzymes, TDG and the dynamics of DNA demethylation. Nature 502, 472-479
18. Koi M., Umar A., Chauhan D.P., et al. (1994). Human chromosome 3 corrects mismatch repair deficiency and microsatellite instability and reduces N-methyl-N?-nitro-N-nitrosoguanidine tolerance in colon tumor cells with homozygous hMLH1 mutation. Cancer Res. 54, 4308-4312
19. Lao V.V., and Grady W.M. (2011). Epigenetics and colorectal cancer. Nat. Rev. Gastroenterol. Hepatol. 8, 686-700
20. Leonhardt H., Page A.W., Weier H.U., et al. (1992).Atargeting sequence directs DNA methyltransferase to sites of DNA replication in mammalian nuclei. Cell 71, 865-873
21. Lindahl T. (1982). DNA repair enzymes. Annu. Rev. Biochem. 51, 61-87
22. Loughery J.E., Dunne P.D., O?Neill K.M., et al. (2011). DNMT1 deficiency triggers mismatch repair defects in human cells through depletion of repair protein levels in a process involving the DNA damage response. Hum. Mol. Genet. 20, 3241-3255
23. Mortusewicz O., Schermelleh L., Walter J., et al. (2005). Recruitment of DNA methyltransferase I to DNA repair sites. Proc. Natl Acad. Sci. USA 102, 8905-8909
24. Muzny D.M., Chang K., Dinh H.H., et al. (2012). Comprehensive molecular characterization of human colon and rectal cancer. Nature 487, 330-337
25. Neeley W.L., and Essigmann J.M. (2006). Mechanisms of formation, genotoxicity, and mutation of guanine oxidation products. Chem. Res. Toxicol. 19, 491-505
26. Niwa T., and Ushijima T. (2010). Induction of epigenetic alterations by chronic inflammation and its significance on carcinogenesis. Adv. Genet. 71, 41-56
27. O'Hagan H.M. (2014). Chromatin modifications during repair of environmental exposure-induced DNA damage: A potential mechanism for stable epigenetic alterations. Environ. Mol. Mutagen. 55, 278-291
28. O'Hagan H.M., Mohammad H.P., and Baylin S.B. (2008). Double strand breaks can initiate gene silencing and SIRT1-dependent onset of DNA methylation in an exogenous promoter CpG island. PLoS Genet. 4, e1000155
29. O'Hagan H.M., Wang W., Sen S., et al. (2011). Oxidative damage targets complexes containing DNA methyltransferases, SIRT1, and polycomb members to promoter CpG islands. Cancer Cell 20, 606-619
30. Palles C., Cazier J.-B., Howarth K.M., et al. (2013). Germline mutations affecting the proofreading domains of POLE and POLD1 predispose to colorectal adenomas and carcinomas. Nat. Genet. 45, 136-144
31. Pena-Diaz J., Bregenhorn S., Ghodgaonkar M., et al. (2012). Noncanonical mismatch repair as a source of genomic instability in human cells. Mol. Cell 47, 669-680
32. Rhee I., Bachman K.E., Park B.H., et al. (2002). DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature 416, 552-556
33. Schroering A.G., and Williams K.J. (2008). Rapid induction of chromatinassociated DNA mismatch repair proteins after MNNG treatment. DNA Repair 7, 951-969
34. Soria G., Polo S.E., and Almouzni G. (2012). Prime, repair, restore: the active role of chromatin in the DNA damage response. Mol. Cell 46, 722-734
35. Umar A., Koi M., Risinger J.I., et al. (1997). Correction of hypermutability, N-methyl-N?-nitro-N-nitrosoguanidine resistance, and defective DNA mismatch repair by introducing chromosome 2 into human tumor cells with mutations in MSH2 and MSH6. Cancer Res. 57, 3949-3955
36. Wang K.Y., and James Shen C.K. (2004).DNAmethyltransferaseDnmt1 and mismatch repair. Oncogene 23, 7898-7902
37. Yan S., Sorrell M., and Berman Z. (2014). Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress. Cell. Mol. Life Sci. 71, 3951-3967
38. Yanamadala S., and Ljungman M. (2003). Potential role of MLH1 in the induction of p53 and apoptosis by blocking transcription on damaged DNA templates. Mol. Cancer Res. 1, 747-754
39. Zlatanou A., Despras E., Braz-Petta T., et al. (2011). The hMsh2-hMsh6 complex acts in concert with monoubiquitinated PCNA and Pol eta in response to oxidative DNA damage in human cells. Mol. Cell 43, 649-662