HDAC6 deacetylates and ubiquitinates MSH2 to maintain proper levels of MutSα

Molecular Cell

Volumn 55, Issue 1, 2014, Pages 31-46

  Zhang, Mu ^a   Xiang, Shengyan ^a   Joo, Heui Yun ^b   Wang, Lei ^a   Williams, Kendra A ^a   Liu, Wei ^a   Hu, Chen ^a   Tong, Dan ^c   Haakenson, Joshua ^a   Wang, Chuangui ^d   Zhang, Shengping ^d   Pavlovicz, Ryan E ^e   Jones, Amanda ^b   Schmidt, Kristina H ^f,g   Tang, Jinfu ^a   Dong, Huiqin ^a   Shan, Bin ^h   Fang, Bin ^g   Radhakrishnan, Rangasudhagar ^g   Glazer, Peter M ⁱ   Matthias, Patrick ^j   Koomen, John ^g   Seto, Edward ^g   Bepler, Gerold ^k   Nicosia, Santo V ^a,g   Chen, Jiandong ^g   Li, Chenglong ^e   Gu, Liya ^c   Li, Guo Min ^c   Bai, Wenlong ^a,g   Wang, Hengbin ^b   Zhang, Xiaohong ^a,g   more..

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

^d CHINA MEDICAL UNIVERSITY   (China)

^e OHIO STATE UNIVERSITY   (United States)

^f UNIVERSITY OF SOUTH FLORIDA   (United States)

^g H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^h WASHINGTON STATE UNIVERSITY   (United States)

ⁱ YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^j FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^k KARMANOS CANCER INSTITUTE   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

HETERODIMER; HISTONE DEACETYLASE 6; MISMATCH REPAIR PROTEIN; NUCLEOTIDE DERIVATIVE; PROTEASOME; PROTEIN MSH2; PROTEIN MUTS; PROTEIN MUTS ALPHA; UBIQUITIN; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; DEACETYLATION; DNA ADDUCT; DNA DAMAGE; DOWN REGULATION; HUMAN; HUMAN CELL; MICROSATELLITE INSTABILITY; MISMATCH REPAIR; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PROTEIN DEGRADATION; UBIQUITINATION;

ACETYLATION; ANIMALS; CELLS, CULTURED; HEK293 CELLS; HELA CELLS; HISTONE DEACETYLASES; HUMANS; MICE; MUTS HOMOLOG 2 PROTEIN; PROTEIN STABILITY; UBIQUITINATION;

EID: 84903796100     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.04.028     Document Type: Article

References (38)

1. Bertos N.R., Gilquin B., Chan G.K., Yen T.J., Khochbin S., Yang X.J. Role of the tetradecapeptide repeat domain of human histone deacetylase 6 in cytoplasmic retention. J.Biol. Chem. 2004, 279:48246-48254.
2. Boyault C., Gilquin B., Zhang Y., Rybin V., Garman E., Meyer-Klaucke W., Matthias P., Müller C.W., Khochbin S. HDAC6-p97/VCP controlled polyubiquitin chain turnover. EMBO J. 2006, 25:3357-3366.
3. Carmen A.A., Rundlett S.E., Grunstein M. HDA1 and HDA3 are components of a yeast histone deacetylase (HDA) complex. J.Biol. Chem. 1996, 271:15837-15844.
4. Chang D.K., Ricciardiello L., Goel A., Chang C.L., Boland C.R. Steady-state regulation of the human DNA mismatch repair system. J.Biol. Chem. 2000, 275:29178.
5. Christmann M., Kaina B. Nuclear translocation of mismatch repair proteins MSH2 and MSH6 as a response of cells to alkylating agents. J.Biol. Chem. 2000, 275:36256-36262.
6. Constantin N., Dzantiev L., Kadyrov F.A., Modrich P. Human mismatch repair: reconstitution of a nick-directed bidirectional reaction. J.Biol. Chem. 2005, 280:39752-39761.
7. Drummond J.T., Li G.M., Longley M.J., Modrich P. Isolation of an hMSH2-p160 heterodimer that restores DNA mismatch repair to tumor cells. Science 1995, 268:1909-1912.
8. Fink D., Aebi S., Howell S.B. The role of DNA mismatch repair in drug resistance. Clin. Cancer Res. 1998, 4:1-6.
9. Gammie A.E., Erdeniz N., Beaver J., Devlin B., Nanji A., Rose M.D. Functional characterization of pathogenic human MSH2 missense mutations in Saccharomyces cerevisiae. Genetics 2007, 177:707-721.
10. Genschel J., Littman S.J., Drummond J.T., Modrich P. Isolation of MutSbeta from human cells and comparison of the mismatch repair specificities of MutSbeta and MutSalpha. J.Biol. Chem. 1998, 273:19895-19901.
11. Grozinger C.M., Hassig C.A., Schreiber S.L. Three proteins define a class of human histone deacetylases related to yeast Hda1p. Proc. Natl. Acad. Sci. USA 1999, 96:4868-4873.
12. Guerrette S., Wilson T., Gradia S., Fishel R. Interactions of human hMSH2 with hMSH3 and hMSH2 with hMSH6: examination of mutations found in hereditary nonpolyposis colorectal cancer. Mol. Cell. Biol. 1998, 18:6616-6623.
13. Hayes A.P., Sevi L.A., Feldt M.C., Rose M.D., Gammie A.E. Reciprocal regulation of nuclear import of the yeast MutSalpha DNA mismatch repair proteins Msh2 and Msh6. DNA Repair (Amst.) 2009, 8:739-751.
14. Hernandez-Pigeon H., Laurent G., Humbert O., Salles B., Lautier D. Degadration of mismatch repair hMutSalpha heterodimer by the ubiquitin-proteasome pathway. FEBS Lett. 2004, 562:40-44.
15. Hook S.S., Orian A., Cowley S.M., Eisenman R.N. Histone deacetylase 6 binds polyubiquitin through its zinc finger (PAZ domain) and copurifies with deubiquitinating enzymes. Proc. Natl. Acad. Sci. USA 2002, 99:13425-13430.
16. Hubbert C., Guardiola A., Shao R., Kawaguchi Y., Ito A., Nixon A., Yoshida M., Wang X.F., Yao T.P. HDAC6 is a microtubule-associated deacetylase. Nature 2002, 417:455-458.
17. Karran P. Thiopurines, DNA damage, DNA repair and therapy-related cancer. Br. Med. Bull. 2006, 79-80:153-170.
18. Kawaguchi Y., Kovacs J.J., McLaurin A., Vance J.M., Ito A., Yao T.P. The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 2003, 115:727-738.
19. Kim A.H., Puram S.V., Bilimoria P.M., Ikeuchi Y., Keough S., Wong M., Rowitch D., Bonni A. A centrosomal Cdc20-APC pathway controls dendrite morphogenesis in postmitotic neurons. Cell 2009, 136:322-336.
20. Kolodner R.D. Mismatch repair: mechanisms and relationship to cancer susceptibility. Trends Biochem. Sci. 1995, 20:397-401.
21. Kovacs J.J., Murphy P.J., Gaillard S., Zhao X., Wu J.T., Nicchitta C.V., Yoshida M., Toft D.O., Pratt W.B., Yao T.P. HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol. Cell 2005, 18:601-607.
22. Li G.M. The role of mismatch repair in DNA damage-induced apoptosis. Oncol. Res. 1999, 11:393-400.
23. Li G.M. Mechanisms and functions of DNA mismatch repair. Cell Res. 2008, 18:85-98.
24. Matthias P., Yoshida M., Khochbin S. HDAC6 a new cellular stress surveillance factor. Cell Cycle 2008, 7:7-10.
25. Modrich P. Mismatch repair, genetic stability, and cancer. Science 1994, 266:1959-1960.
26. Namdar M., Perez G., Ngo L., Marks P.A. Selective inhibition of histone deacetylase 6 (HDAC6) induces DNA damage and sensitizes transformed cells to anticancer agents. Proc. Natl. Acad. Sci. USA 2010, 107:20003-20008.
27. Nomura S., Sugano K., Kashiwabara H., Taniguchi T., Fukayama N., Fujita S., Akasu T., Moriya Y., Ohhigashi S., Kakizoe T., Sekiya T. Enhanced detection of deleterious and other germline mutations of hMSH2 and hMLH1 in Japanese hereditary nonpolyposis colorectal cancer kindreds. Biochem. Biophys. Res. Commun. 2000, 271:120-129.
28. North B.J., Marshall B.L., Borra M.T., Denu J.M., Verdin E. The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase. Mol. Cell 2003, 11:437-444.
29. Pandey U.B., Nie Z., Batlevi Y., McCray B.A., Ritson G.P., Nedelsky N.B., Schwartz S.L., DiProspero N.A., Knight M.A., Schuldiner O., et al. HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 2007, 447:859-863.
30. Sadoul K., Boyault C., Pabion M., Khochbin S. Regulation of protein turnover by acetyltransferases and deacetylases. Biochimie 2008, 90:306-312.
31. Seigneurin-Berny D., Verdel A., Curtet S., Lemercier C., Garin J., Rousseaux S., Khochbin S. Identification of components of the murine histone deacetylase 6 complex: link between acetylation and ubiquitination signaling pathways. Mol. Cell. Biol. 2001, 21:8035-8044.
32. Tsai S.C., Seto E. Regulation of histone deacetylase 2 by protein kinase CK2. J.Biol. Chem. 2002, 277:31826-31833.
33. Verdel A., Khochbin S. Identification of a new family of higher eukaryotic histone deacetylases. Coordinate expression of differentiation-dependent chromatin modifiers. J.Biol. Chem. 1999, 274:2440-2445.
34. Verdel A., Curtet S., Brocard M.P., Rousseaux S., Lemercier C., Yoshida M., Khochbin S. Active maintenance of mHDA2/mHDAC6 histone-deacetylase in the cytoplasm. Curr. Biol. 2000, 10:747-749.
35. Wang L., Xiang S., Williams K.A., Dong H., Bai W., Nicosia S.V., Khochbin S., Bepler G., Zhang X. Depletion of HDAC6 enhances cisplatin-induced DNA damage and apoptosis in non-small cell lung cancer cells. PLoS ONE 2012, 7:e44265.
36. Warren J.J., Pohlhaus T.J., Changela A., Iyer R.R., Modrich P.L., Beese L.S. Structure of the human MutSalpha DNA lesion recognition complex. Mol. Cell 2007, 26:579-592.
37. Zhang Y., Yuan F., Presnell S.R., Tian K., Gao Y., Tomkinson A.E., Gu L., Li G.M. Reconstitution of 5'-directed human mismatch repair in a purified system. Cell 2005, 122:693-705.
38. Zhang X., Yuan Z., Zhang Y., Yong S., Salas-Burgos A., Koomen J., Olashaw N., Parsons J.T., Yang X.J., Dent S.R., et al. HDAC6 modulates cell motility by altering the acetylation level of cortactin. Mol. Cell 2007, 27:197-213.