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Genes  2011 

SET/MYND Lysine Methyltransferases Regulate Gene Transcription and Protein Activity

DOI: 10.3390/genes2010210

Keywords: SET, MYND, Smyd1, Smyd2, Smyd3, transcriptional regulation, chromatin modifications, epigenetics, tumorigenesis

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Abstract:

The SET and MYND (SMYD) family of lysine methyltransferases is defined by a SET domain that is split into two segments by a MYND domain, followed by a cysteine-rich post-SET domain. While members of the SMYD family are important in the SET-mediated regulation of gene transcription, pathological consequences have also been associated with aberrant expression of SMYD proteins. The last decade has witnessed a rapid increase in the studies and corresponding understanding of these highly impactful enzymes. Herein, we review the current body of knowledge related to the SMYD family of?lysine methyltransferases and their role in transcriptional regulation, epigenetics, and?tumorigenesis.

References

[1]  Turner, B.M. Cellular memory and the histone code. Cell?2002, 111, 285–291.
[2]  Bonasio, R.; Tu, S.; Reinberg, D. Molecular signals of epigenetic states. Science?2010, 330, 612–616.
[3]  Lee, J.S.; Smith, E.; Shilatifard, A. The language of histone crosstalk. Cell?2010, 142, 682–685.
[4]  Felsenfeld, G.; Groudine, M. Controlling the double helix. Nature?2003, 421, 448–453.
[5]  Richmond, T.J. Genomics: Predictable packaging. Nature?2006, 442, 750–752.
[6]  Kornberg, R.D.; Lorch, Y. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell?1999, 98, 285–294.
[7]  Hayes, J.J.; Clark, D.J.; Wolffe, A.P. Histone contributions to the structure of DNA in the nucleosome. Proc. Natl. Acad. Sci. USA?1991, 88, 6829–6833.
[8]  Rister, J.; Desplan, C. Deciphering the genome's regulatory code: The many languages of DNA. Bioessays?2010, 32, 381–384.
[9]  Vitolo, J.M.; Thiriet, C.; Hayes, J.J. The H3-H4 N-terminal tail domains are the primary mediators of transcription factor IIIA access to 5S DNA within a nucleosome. Mol. Cell Biol.?2000, 20, 2167–2175.
[10]  Hager, G.L.; McNally, J.G.; Misteli, T. Transcription dynamics. Mol. Cell?2009, 35, 741–753.
[11]  Jenuwein, T. The epigenetic magic of histone lysine methylation. FEBS J.?2006, 273, 3121–3135.
[12]  Lennartsson, A.; Ekwall, K. Histone modification patterns and epigenetic codes. Biochim. Biophys. Acta.?2009, 1790, 863–868.
[13]  Khorasanizadeh, S. The nucleosome: from genomic organization to genomic regulation. Cell?2004, 116, 259–272.
[14]  Jenuwein, T.; Allis, C.D. Translating the histone code. Science?2001, 293, 1074–1080.
[15]  Strahl, B.D.; Allis, C.D. The language of covalent histone modifications. Nature?2000, 403, 41–45.
[16]  Dutnall, R.N.; Denu, J.M. Methyl magic and HAT tricks. Nat. Struct. Biol.?2002, 9, 888–891.
[17]  McManus, K.J.; Hendzel, M.J. The relationship between histone H3 phosphorylation and acetylation throughout the mammalian cell cycle. Biochem. Cell Biol.?2006, 84, 640–657.
[18]  Daujat, S.; Bauer, U.M.; Shah, V.; Turner, B.; Berger, S.; Kouzarides, T. Crosstalk between CARM1 methylation and CBP acetylation on histone H3. Curr. Biol.?2002, 12, 2090–2097.
[19]  Dillon, N.; Festenstein, R. Unravelling heterochromatin: Competition between positive and negative factors regulates accessibility. Trends Genet.?2002, 18, 252–258.
[20]  Tsukada, Y.; Fang, J.; Erdjument-Bromage, H.; Warren, M.E.; Borchers, C.H.; Tempst, P.; Zhang, Y. Histone demethylation by a family of JmjC domain-containing proteins. Nature?2006, 439, 811–816.
[21]  Zhang, Y.; Reinberg, D. Transcription regulation by histone methylation: Interplay between different covalent modifications of the core histone tails. Genes Dev.?2001, 15, 2343–2360.
[22]  Lachner, M.; Jenuwein, T. The many faces of histone lysine methylation. Curr. Opin. Cell Biol.?2002, 14, 286–298.
[23]  Kouzarides, T. Histone methylation in transcriptional control. Curr. Opin. Genet. Dev.?2002, 12, 198–209.
[24]  Wang, H.; An, W.; Cao, R.; Xia, L.; Erdjument-Bromage, H.; Chatton, B.; Tempst, P.; Roeder, R.G.; Zhang, Y. mAM facilitates conversion by ESET of dimethyl to trimethyl lysine 9 of histone H3 to cause transcriptional repression. Mol. Cell?2003, 12, 475–487.
[25]  Santos-Rosa, H.; Schneider, R.; Bannister, A.J.; Sherriff, J.; Bernstein, B.E.; Emre, N.C.; Schreiber, S.L.; Mellor, J.; Kouzarides, T. Active genes are tri-methylated at K4 of histone H3. Nature?2002, 419, 407–411.
[26]  O'Carroll, D.; Erhardt, S.; Pagani, M.; Barton, S.C.; Surani, M.A.; Jenuwein, T. The polycomb-group gene Ezh2 is required for early mouse development. Mol. Cell Biol.?2001, 21, 4330–4336.
[27]  Sims, R.J., III; Nishioka, K.; Reinberg, D. Histone lysine methylation: A signature for chromatin function. Trends Genet.?2003, 19, 629–639.
[28]  Sims, R.J., III; Chen, C.F.; Santos-Rosa, H.; Kouzarides, T.; Patel, S.S.; Reinberg, D. Human but not yeast CHD1 binds directly and selectively to histone H3 methylated at lysine 4 via its tandem chromodomains. J. Biol. Chem.?2005, 280, 41789–41792.
[29]  Shi, Y.; Lan, F.; Matson, C.; Mulligan, P.; Whetstine, J.R.; Cole, P.A.; Casero, R.A.; Shi, Y. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell?2004, 119, 941–953.
[30]  Gottlieb, P.D.; Pierce, S.A.; Sims, R.J.; Yamagishi, H.; Weihe, E.K.; Harriss, J.V.; Maika, S.D.; Kuziel, W.A.; King, H.L.; Olson, E.N.; et al. Bop encodes a muscle-restricted protein containing MYND and SET domains and is essential for cardiac differentiation and morphogenesis. Nat. Genet.?2002, 31, 25–32.
[31]  Brown, M.A.; Sims, R.J., III; Gottlieb, P.D.; Tucker, P.W. Identification and characterization of Smyd2: A split SET/MYND domain-containing histone H3 lysine 36-specific methyltransferase that interacts with the Sin3 histone deacetylase complex. Mol. Cancer?2006, 5, 26.
[32]  Trievel, R.C.; Beach, B.M.; Dirk, L.M.; Houtz, R.L.; Hurley, J.H. Structure and catalytic mechanism of a SET domain protein methyltransferase. Cell?2002, 111, 91–103.
[33]  Zhang, X.; Tamaru, H.; Khan, S.I.; Horton, J.R.; Keefe, L.J.; Selker, E.U.; Cheng, X. Structure of the Neurospora SET domain protein DIM-5, a histone H3 lysine methyltransferase. Cell?2002, 111, 117–127.
[34]  Wilson, J.R.; Jing, C.; Walker, P.A.; Martin, S.R.; Howell, S.A.; Blackburn, G.M.; Gamblin, S.J.; Xiao, B. Crystal structure and functional analysis of the histone methyltransferase SET7/9. Cell?2002, 111, 105–115.
[35]  Kwon, T.; Chang, J.H.; Kwak, E.; Lee, C.W.; Joachimiak, A.; Kim, Y.C.; Lee, J.; Cho, Y. Mechanism of histone lysine methyl transfer revealed by the structure of SET7/9-AdoMet. EMBO J.?2003, 22, 292–303.
[36]  Couture, J.F.; Collazo, E.; Brunzelle, J.S.; Trievel, R.C. Structural and functional analysis of SET8, a histone H4 Lys-20 methyltransferase. Genes Dev.?2005, 19, 1455–1465.
[37]  Min, J.; Zhang, X.; Cheng, X.; Grewal, S.I.; Xu, R.M. Structure of the SET domain histone lysine methyltransferase Clr4. Nat. Struct. Biol.?2002, 9, 828–832.
[38]  Hamamoto, R.; Furukawa, Y.; Morita, M.; Iimura, Y.; Silva, F.P.; Li, M.; Yagyu, R.; Nakamura, Y. SMYD3 encodes a histone methyltransferase involved in the proliferation of cancer cells. Nat. Cell Biol.?2004, 6, 731–740.
[39]  Tan, X.; Rotllant, J.; Li, H.; de Deyne, P.; Du, S.J. SmyD1, a histone methyltransferase, is required for myofibril organization and muscle contraction in zebrafish embryos. Proc. Natl. Acad. Sci. USA?2006, 103, 2713–2718.
[40]  Erickson, P.; Gao, J.; Chang, K.S.; Look, T.; Whisenant, E.; Raimondi, S.; Lasher, R.; Trujillo, J.; Rowley, J.; Drabkin, H. Identification of breakpoints in t(8;21) acute myelogenous leukemia and isolation of a fusion transcript, AML1/ETO, with similarity to Drosophila segmentation gene, runt. Blood?1992, 80, 1825–1831.
[41]  Veraksa, A.; Kennison, J.; McGinnis, W. DEAF-1 function is essential for the early embryonic development of Drosophila. Genesis?2002, 33, 67–76.
[42]  Sims, R.J., III; Weihe, E.K.; Zhu, L.; O'Malley, S.; Harriss, J.V.; Gottlieb, P.D. m-Bop, a repressor protein essential for cardiogenesis, interacts with skNAC, a heart- and muscle-specific transcription factor. J. Biol. Chem.?2002, 277, 26524–26529.
[43]  Shago, M.; Giguere, V. Isolation of a novel retinoic acid-responsive gene by selection of genomic fragments derived from CpG-island-enriched DNA. Mol. Cell Biol.?1996, 16, 4337–4348.
[44]  Phan, D.; Rasmussen, T.L.; Nakagawa, O.; McAnally, J.; Gottlieb, P.D.; Tucker, P.W.; Richardson, J.A.; Bassel-Duby, R.; Olson, E.N. BOP, a regulator of right ventricular heart development, is a direct transcriptional target of MEF2C in the developing heart. Development?2005, 132, 2669–2678.
[45]  Sirinupong, N.; Brunzelle, J.; Ye, J.; Pirzada, A.; Nico, L.; Yang, Z. Crystal structure of cardiac specific histone methyltransferase SmyD1 reveals unusual active site architecture. J. Biol. Chem.?2010, 285, 40635–40644.
[46]  Keogh, M.C.; Kurdistani, S.K.; Morris, S.A.; Ahn, S.H.; Podolny, V.; Collins, S.R.; Schuldiner, M.; Chin, K.; Punna, T.; Thompson, N.J.; et al. Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell?2005, 123, 593–605.
[47]  Carrozza, M.J.; Li, B.; Florens, L.; Suganuma, T.; Swanson, S.K.; Lee, K.K.; Shia, W.J.; Anderson, S.; Yates, J.; Washburn, M.P.; et al. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell?2005, 123, 581–592.
[48]  Diehl, F.; Brown, M.A.; van Amerongen, M.J.; Novoyatleva, T.; Wietelmann, A.; Harriss, J.; Ferrazzi, F.; Bottger, T.; Harvey, R.P.; Tucker, P.W.; et al. Cardiac deletion of Smyd2 is dispensable for mouse heart development. PLoS One?2010, 5, e9748.
[49]  Huang, J.; Perez-Burgos, L.; Placek, B.J.; Sengupta, R.; Richter, M.; Dorsey, J.A.; Kubicek, S.; Opravil, S.; Jenuwein, T.; Berger, S.L. Repression of p53 activity by Smyd2-mediated methylation. Nature?2006, 444, 629–632.
[50]  Saddic, L.A.; West, L.E.; Aslanian, A.; Yates, J.R., III; Rubin, S.M.; Gozani, O.; Sage, J. Methylation of the retinoblastoma tumor suppressor by SMYD2. J. Biol. Chem.?2010, 285, 37733–37740.
[51]  Hamamoto, R.; Silva, F.P.; Tsuge, M.; Nishidate, T.; Katagiri, T.; Nakamura, Y.; Furukawa, Y. Enhanced SMYD3 expression is essential for the growth of breast cancer cells. Cancer Sci.?2006, 97, 113–118.
[52]  Apergis, G.A.; Crawford, N.; Ghosh, D.; Steppan, C.M.; Vorachek, W.R.; Wen, P.; Locker, J. A novel nk-2-related transcription factor associated with human fetal liver and hepatocellular carcinoma. J. Biol. Chem.?1998, 273, 2917–2925.
[53]  Sims, J.R., III; Reinberg, D. From chromatin to cancer: a new histone lysine methyltransferase enters the mix. Nat. Cell Biol.?2004, 6, 685–687.
[54]  Lin, Y.M.; Furukawa, Y.; Tsunoda, T.; Yue, C.T.; Yang, K.C.; Nakamura, Y. Molecular diagnosis of colorectal tumors by expression profiles of 50 genes expressed differentially in adenomas and carcinomas. Oncogene?2002, 21, 4120–4128.
[55]  Okabe, H.; Satoh, S.; Kato, T.; Kitahara, O.; Yanagawa, R.; Yamaoka, Y.; Tsunoda, T.; Furukawa, Y.; Nakamura, Y. Genome-wide analysis of gene expression in human hepatocellular carcinomas using cDNA microarray: Identification of genes involved in viral carcinogenesis and tumor progression. Cancer Res.?2001, 61, 2129–2137.

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