Histone mimics: digging down under

Abstract

Epigenetic deregulation is intimately associated with the development of human diseases. Intensive studies are currently underway to clarify the mechanism for the sake of achieving ideal diagnostic and therapeutic goals. It has been demonstrated that enzymes with histone-modifying activities can also target non-histone proteins, with the underlying mechanism remaining obscure. In this review, we focus on a novel histone mimicry strategy that may be wildly adapted during the non-histone substrate recognition process. Its potential clinical implications are also discussed.

Keywords

epigenetics / histone mimicry

References

[1] Adcock I M, Ito K, Barnes P J (2005). Histone deacetylation: an important mechanism in inflammatory lung diseases. COPD, 2(4): 445-455

[2] Arents G, Burlingame R W, Wang B C, Love W E, Moudrianakis E N (1991). The nucleosomal core histone octamer at 3.1 A resolution: a tripartite protein assembly and a left-handed superhelix. Proc Natl Acad Sci USA, 88(22): 10148-10152

[3] Arents G, Moudrianakis E N (1995). The histone fold: a ubiquitous architectural motif utilized in DNA compaction and protein dimerization. Proc Natl Acad Sci USA, 92(24): 11170-11174

[4] Baron R, Binda C, Tortorici M, McCammon J A, Mattevi A (2011). Molecular mimicry and ligand recognition in binding and catalysis by the histone demethylase LSD1-CoREST complex. Structure, 19(2): 212-220

[5] Batlle E, Sancho E, Francí C, Domínguez D, Monfar M, Baulida J, García De Herreros A (2000). The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol, 2(2): 84-89

[6] Baxevanis A D, Arents G, Moudrianakis E N, Landsman D (1995). A variety of DNA-binding and multimeric proteins contain the histone fold motif. Nucleic Acids Res, 23(14): 2685-2691

[7] Cano A, Pérez-Moreno M A, Rodrigo I, Locascio A, Blanco M J, del Barrio M G, Portillo F, Nieto M A (2000). The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol, 2(2): 76-83

[8] Chan D W, Wang Y, Wu M, Wong J, Qin J, Zhao Y (2009). Unbiased proteomic screen for binding proteins to modified lysines on histone H3. Proteomics, 9(9): 2343-2354

[9] Chang Y, Ganesh T, Horton J R, Spannhoff A, Liu J, Sun A, Zhang X, Bedford M T, Shinkai Y, Snyder J P, Cheng X (2010). Adding a lysine mimic in the design of potent inhibitors of histone lysine methyltransferases. J Mol Biol, 400(1): 1-7

[10] Egger G, Liang G, Aparicio A, Jones P A (2004). Epigenetics in human disease and prospects for epigenetic therapy. Nature, 429(6990): 457-463

[11] Egorova K S, Olenkina O M, Olenina L V (2010). Lysine methylation of nonhistone proteins is a way to regulate their stability and function. Biochemistry (Mosc), 75(5): 535-548

[12] Elsässer S J, Allis C D, Lewis P W (2011). Cancer. New epigenetic drivers of cancers. Science, 331(6021): 1145-1146

[13] Esteller M (2008). Epigenetics in cancer. N Engl J Med, 358(11): 1148-1159

[14] Feinberg A P, Vogelstein B (1983). Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature, 301(5895): 89-92

[15] Henkels C H, Khorasanizadeh S (2007). Implications of a histone code mimic in epigenetic signaling. Mol Cell, 27(4): 521-522

[16] Issa J P, Kantarjian H M, Kirkpatrick P (2005). Azacitidine. Nat Rev Drug Discov, 4(4): 275-276

[17] Jenuwein T, Allis C D (2001). Translating the histone code. Science, 293(5532): 1074-1080

[18] Jeyaprakash A A, Basquin C, Jayachandran U, Conti E (2011). Structural basis for the recognition of phosphorylated histone h3 by the survivin subunit of the chromosomal passenger complex. Structure, 19(11): 1625-1634

[19] Jiao Y, Shi C, Edil B H, de Wilde R F, Klimstra D S, Maitra A, Schulick R D, Tang L H, Wolfgang C L, Choti M A, Velculescu V E, Diaz L A Jr, Vogelstein B, Kinzler K W, Hruban R H, Papadopoulos N (2011). DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science, 331(6021): 1199-1203

[20] Jones P A, Baylin S B (2007). The epigenomics of cancer. Cell, 128(4): 683-692

[21] Kayne P S, Kim U J, Han M, Mullen J R, Yoshizaki F, Grunstein M (1988). Extremely conserved histone H4 N terminus is dispensable for growth but essential for repressing the silent mating loci in yeast. Cell, 55(1): 27-39

[22] Kelly A E, Ghenoiu C, Xue J Z, Zierhut C, Kimura H, Funabiki H (2010b). Survivin reads phosphorylated histone H3 threonine 3 to activate the mitotic kinase Aurora B. Science, 330(6001): 235-239

[23] Kelly T K, De Carvalho D D, Jones P A (2010a). Epigenetic modifications as therapeutic targets. Nat Biotechnol, 28(10): 1069-1078

[24] Kouzarides T (2007). Chromatin modifications and their function. Cell, 128(4): 693-705

[25] Lee Y H, Stallcup M R (2009). Minireview: protein arginine methylation of nonhistone proteins in transcriptional regulation. Mol Endocrinol, 23(4): 425-433

[26] Lim S, Janzer A, Becker A, Zimmer A, Schüle R, Buettner R, Kirfel J (2010). Lysine-specific demethylase 1 (LSD1) is highly expressed in ER-negative breast cancers and a biomarker predicting aggressive biology. Carcinogenesis, 31(3): 512-520

[27] Lin Y, Wu Y, Li J, Dong C, Ye X, Chi Y I, Evers B M, Zhou B P (2010). The SNAG domain of Snail1 functions as a molecular hook for recruiting lysine-specific demethylase 1. EMBO J, 29(11): 1803-1816

[28] Marks P A, Breslow R (2007). Dimethyl sulfoxide to vorinostat: development of this histone deacetylase inhibitor as an anticancer drug. Nat Biotechnol, 25(1): 84-90

[29] Morgunkova A, Barlev N A (2006). Lysine methylation goes global. Cell Cycle, 5(12): 1308-1312

[30] Nicodeme E, Jeffrey K L, Schaefer U, Beinke S, Dewell S, Chung C W, Chandwani R, Marazzi I, Wilson P, Coste H, White J, Kirilovsky J, Rice C M, Lora J M, Prinjha R K, Lee K, Tarakhovsky A (2010). Suppression of inflammation by a synthetic histone mimic. Nature, 468(7327): 1119-1123

[31] Nieto M A (2002). The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol, 3(3): 155-166

[32] Peng L, Seto E (2011). Deacetylation of nonhistone proteins by HDACs and the implications in cancer. Handb Exp Pharmacol, 206: 39-56

[33] Rodenhiser D, Mann M (2006). Epigenetics and human disease: translating basic biology into clinical applications. CMAJ, 174(3): 341-348

[34] Ruchaud S, Carmena M, Earnshaw W C (2007). Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol, 8(10): 798-812

[35] Sampath S C, Marazzi I, Yap K L, Sampath S C, Krutchinsky A N, Mecklenbräuker I, Viale A, Rudensky E, Zhou M M, Chait B T, Tarakhovsky A (2007). Methylation of a histone mimic within the histone methyltransferase G9a regulates protein complex assembly. Mol Cell, 27(4): 596-608

[36] Savagner P (2001). Leaving the neighborhood: molecular mechanisms involved during epithelial-mesenchymal transition. Bioessays, 23(10): 912-923

[37] Shi Y, Lan F, Matson C, Mulligan P, Whetstine J R, Cole P A, Casero R A, Shi Y (2004). Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell, 119(7): 941-953

[38] Shima K, Nosho K, Baba Y, Cantor M, Meyerhardt J A, Giovannucci E L, Fuchs C S, Ogino S (2011). Prognostic significance of CDKN2A (p16) promoter methylation and loss of expression in 902 colorectal cancers: Cohort study and literature review. Int J Cancer, 128(5): 1080-1094

[39] Shook D, Keller R (2003). Mechanisms, mechanics and function of epithelial-mesenchymal transitions in early development. Mech Dev, 120(11): 1351-1383

[40] Singh B N, Zhang G, Hwa Y L, Li J, Dowdy S C, Jiang S W (2010). Nonhistone protein acetylation as cancer therapy targets. Expert Rev Anticancer Ther, 10(6): 935-954

[41] Spannhoff A, Hauser A T, Heinke R, Sippl W, Jung M (2009). The emerging therapeutic potential of histone methyltransferase and demethylase inhibitors. ChemMedChem, 4(10): 1568-1582

[42] Tarakhovsky A (2010). Tools and landscapes of epigenetics. Nat Immunol, 11(7): 565-568

[43] Thiery J P (2002). Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer, 2(6): 442-454

[44] Thiery J P, Acloque H, Huang R Y, Nieto M A (2009). Epithelial-mesenchymal transitions in development and disease. Cell, 139(5): 871-890

[45] Turner B M (2007). Defining an epigenetic code. Nat Cell Biol, 9(1): 2-6

[46] Urdinguio R G, Sanchez-Mut J V, Esteller M (2009). Epigenetic mechanisms in neurological diseases: genes, syndromes, and therapies. Lancet Neurol, 8(11): 1056-1072

[47] Villeneuve L M, Natarajan R (2010). The role of epigenetics in the pathology of diabetic complications. Am J Physiol Renal Physiol, 299(1): F14-F25

[48] Waddington C H (2011). The Epigenotype. Int J Epidemiol, online available December 20, 2011

[49] Wang Y, Fischle W, Cheung W, Jacobs S, Khorasanizadeh S (2004). Beyond the double helix: writing and reading the histone code. Novartis Found Symp, 259: 3-17

[50] Yang J, Weinberg R A (2008). Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell, 14(6): 818-829

[51] Yoo C B, Jones P A (2006). Epigenetic therapy of cancer: past, present and future. Nat Rev Drug Discov, 5(1): 37-50

[52] Zhou B P, Deng J, Xia W, Xu J, Li Y M, Gunduz M, Hung M C (2004). Dual regulation of Snail by GSK-3beta-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat Cell Biol, 6(10): 931-940

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