The study of the chemical synthesis and preparation of histone with post-translational modifications

Current Organic Synthesis

Volumn 12, Issue 2, 2015, Pages 150-162

  Wang, Zhi Peng ^a,b   Wang, Ye Hai ^a   Chu, Guo Chao ^c   Shi, Jing ^c   Li, Yi Ming ^a  

^a HEFEI UNIVERSITY OF TECHNOLOGY   (China)

^b TEXAS A AND M UNIVERSITY   (United States)

^c UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

Histone; Post translational modification; Protein; Protein expression; Protein semi synthesis; Total synthesis; Unnatural amino acid incorporation

Indexed keywords

EID: 84931025395     PISSN: 15701794     EISSN: None     Source Type: Journal    
DOI: 10.2174/1570179411666141125215343     Document Type: Article

References (85)

1. [1] Luger, K., Mäder, A.W., Richmond, R.K., Sargent, D.F., Richmond, T.J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature, 1997, 389, 251-260.
2. [2] Boyer, L.A., Plath, K., Zeitlinger, J., Brambrink, T., Medeiros, L.A., Lee, T.I., Levine, S.S., Wernig, M., Tajonar, A., Ray, M.K. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature, 2006, 441, 349-353.
3. [3] Shogren-Knaak, M., Ishii, H., Sun, J.-M., Pazin, M.J., Davie, J.R., Peterson, C.L. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science, 2006, 311, 844-847.
4. [4] Latham, J.A., Dent, S.Y.R. Cross-regulation of histone modifications. Nature structural & molecular biology, 2007, 14, 1017-1024.
5. [5] Shechter, D., Dormann, H.L., Allis, C.D., Hake, S.B. Extraction, purification and analysis of histones. Nature protocols, 2007, 2, 1445-1457.
6. [6] Simon, M.D., Chu, F., Racki, L.R., de la Cruz, C.C., Burlingame, A.L., Panning, B., Narlikar, G.J., Shokat, K.M. The site-specific installation of methyl-lysine analogs into recombinant histones. Cell, 2007, 128, 1003-1012.
7. [7] Yang, Y.Y., Hang, H.C. Chemical approaches for the detection and synthesis of acetylated proteins. Chembiochem, 2011, 12, 314-322.
8. [8] Peng, C., Lu, Z., Xie, Z., Cheng, Z., Chen, Y., Tan, M., Luo, H., Zhang, Y., He, W., Yang, K. The first identification of lysine malonylation substrates and its regulatory enzyme. Mol. Cell. Proteomics, 2011, 10, M111. 012-658.
9. [9] Tan, M., Luo, H., Lee, S., Jin, F., Yang, J.S., Montellier, E., Buchou, T., Cheng, Z., Rousseaux, S., Rajagopal, N. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell, 2011, 146, 1016-1028.
10. [10] Zhang, Z., Tan, M., Xie, Z., Dai, L., Chen, Y., Zhao, Y. Identification of lysine succinylation as a new post-translational modification. Nature chemical biology, 2011, 7, 58-63.
11. [11] Tan, M., Peng, C., Anderson, K.A., Chhoy, P., Xie, Z., Dai, L., Park, J., Chen, Y., Huang, H., Zhang, Y. Lysine Glutarylation Is a Protein Posttranslational Modification Regulated by SIRT5. Cell Metabol., 2014, 19, 605-617.
12. [12] Dai, L., Peng, C., Montellier, E., Lu, Z., Chen, Y., Ishii, H., Debernardi, A., Buchou, T., Rousseaux, S., Jin, F., Benjamin, R.S., Deng, Z., Allis, C.D., Ren, B., Khochbin, S., Zhao, Y. Lysine 2-hydroxyisobutyrylation is a widely distributed active histone mark. Nat. Chem. Biol., 2014, 10, 365-370
13. [13] Du, J., Zhou, Y., Su, X., Yu, J.J., Khan, S., Jiang, H., Kim, J., Woo, J., Kim, J.H., Choi, B.H. Sirt5 is a NAD-dependent protein lysine demalonylase and desuccinylase. Science, 2011, 334, 806-809.
14. [14] Galligan, J.J., Rose, K.L., Beavers, W.N., Hill, S., Tallman, K.A., Tansey, W.P., Marnett, L.J. Stable Histone Adduction by 4-Oxo-2-nonenal: A Potential Link between Oxidative Stress and Epigenetics. J Am Chem Soc., 2014,136, 11864-11866.
15. [15] Voigt, P., Reinberg, D. Histone tails: ideal motifs for probing epigenetics through chemical biology approaches. Chembiochem, 2011, 12, 236-252.
16. [16] Krieger, D.E., Levine, R., Merrifield, R.B., Vidali, G., Allfrey, V.G. Chemical Studies of Histone Acetylation substrate specificity of a histone deacetylase from calf thymus nuclei. J. Biol. Chem., 1974, 249, 332-334.
17. [17] Krieger, D.E., Vidali, G., Erickson, B.W., Allfrey, V.G., Merrifield, R.B. The synthesis of diacetylated histone H4-(1–37) for studies on the mechanism of histone deacetylation. Bioorg. Chem., 1979, 8, 409-427.
18. [18] Kervabon, A., Mery, J., Parello, J. Enzymatic deacetylation of a synthetic peptide fragment of histone H4. FEBS letters, 1979, 106, 93-96.
19. [19] Dhalluin, C., Carlson, J.E., Zeng, L., He, C., Aggarwal, A.K., Zhou, M.-M., Zhou, M.-M. Structure and ligand of a histone acetyltransferase bromodomain. Nature, 1999, 399, 491-496.
20. [20] Jacobson, R.H., Ladurner, A.G., King, D.S., Tjian, R. Structure and function of a human TAFII250 double bromodomain module. Science, 2000, 288, 1422-1425.
21. [21] Carmen, A.A., Milne, L., Grunstein, M. Acetylation of the yeast histone H4 N terminus regulates its binding to heterochromatin protein SIR3. J. Biol. Chem., 2002, 277, 4778-4781.
22. [22] Wysocka, J., Swigut, T., Milne, T.A., Dou, Y., Zhang, X., Burlingame, A.L., Roeder, R.G., Brivanlou, A.H., Allis, C.D. WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell, 2005, 121, 859-872.
23. [23] Trievel, R.C., Shilatifard, A. WDR5, a complexed protein. Nat Struct Mol Biol., 2009, 16, 678-680.
24. [24] Bua, D.J., Kuo, A.J., Cheung, P., Liu, C.L., Migliori, V., Espejo, A., Casadio, F., Bassi, C., Amati, B., Bedford, M.T. Epigenome microarray platform for proteome-wide dissection of chromatin-signaling networks. PloS one, 2009, 4, e6789.
25. [25] Rathert, P., Zhang, X., Freund, C., Cheng, X., Jeltsch, A. Analysis of the substrate specificity of the Dim-5 histone lysine methyltransferase using peptide arrays.Chem. Biol., 2008, 15, 5-11.
26. [26] Frank, R. The SPOT-synthesis technique: synthetic peptide arrays on membrane supports-principles and applications. J. Immunol. Methods, 2002, 267, 13-26.
27. [27] Garske, A.L., Craciun, G., Denu, J.M. A Combinatorial H4 Tail Library for Exploring the Histone Code†. Biochemistry, 2008, 47, 8094-8102.
28. [28] Poveda, A., Sendra, R. An easy assay for histone acetyltransferase activity using a PhosphorImager. Anal. Biochem., 2008,383, 296-300.
29. [29] Wynne Aherne, G., Rowlands, M.G., Stimson, L., Workman, P. Assays for the identification and evaluation of histone acetyltransferase inhibitors. Methods, 2002, 26, 245-253.
30. [30] Kee, J.-M., Villani, B., Carpenter, L.R., Muir, T.W. Development of stable phosphohistidine analogues. J. Am. Chem. Soc., 2010, 132, 14327-14329.
31. [31] Moyle, P.M., Muir, T.W. Method for the synthesis of mono-ADP-ribose conjugated peptides. J. Am. Chem. Soc., 2010, 132, 15878-15880.
32. [32] Merrifield, R.B. Solid phase peptide synthesis. I. The synthesis of a tetrapeptide. J. Am. Chem. Soc., 1963, 85, 2149-2154.
33. [33] Dawson, P.E., Muir, T.W., Clark-Lewis, I., Kent, S.B. Synthesis of proteins by native chemical ligation. Science, 1994, 266, 776-779.
34. [34] Fang, G.M., Li, Y.M., Shen, F., Huang, Y.C., Li, J.B., Lin, Y., Cui, H.K., Liu, L. Protein chemical synthesis by ligation of peptide hydrazides. Angew. Chem. Int. Ed. Engl., 2011,50, 7645-7649.
35. [35] Fang, G.M., Wang, J.X., Liu, L. Convergent chemical synthesis of proteins by ligation of peptide hydrazides. Angew. Chem. Int. Ed. Engl., 2012, 51, 10347-10350.
36. [36] Zheng, J.-S., Tang, S., Huang, Y.-C., Liu, L. Development of New Thioester Equivalents for Protein Chemical Synthesis. Acc. Chem. Res., 2013,46, 2475-2484.
37. [37] Zheng, J.-S., Tang, S., Qi, Y.-K., Wang, Z.-P., Liu, L. Chemical synthesis of proteins using peptide hydrazides as thioester surrogates. Nature Protocols, 2013,8, 2483-2495.
38. [38] Zheng, J.-S., Chang, H.-N., Wang, F.-L., Liu, L. Fmoc synthesis of peptide thioesters without post-chain-assembly manipulation. J. Am. Chem. Soc., 2011, 133, 11080-11083.
39. [39] Wan, Q., Danishefsky, S.J. Free-radical-based, specific desulfurization of cysteine: a powerful advance in the synthesis of polypeptides and glycopolypeptides. Angew. Chem. Int. Ed. Engl., 2007, 46, 9248-9252.
40. [40] Pentelute, B.L., Kent, S.B.H. Selective desulfurization of cysteine in the presence of Cys (Acm) in polypeptides obtained by native chemical ligation. Org. Lett., 2007, 9, 687-690.
41. [41] Shimko, J.C., North, J.A., Bruns, A.N., Poirier, M.G., Ottesen, J.J. Preparation of fully synthetic histone H3 reveals that acetyl-lysine 56 facilitates protein binding within nucleosomes. J. Mol. Biol., 2011, 408, 187-204.
42. [42] Simon, M., North, J.A., Shimko, J.C., Forties, R.A., Ferdinand, M.B., Manohar, M., Zhang, M., Fishel, R., Ottesen, J.J., Poirier, M.G. Histone fold modifications control nucleosome unwrapping and disassembly. Proceedings of the National Academy of Sciences, 2011, 108, 12711-12716.
43. [43] North, J.A., Shimko, J.C., Javaid, S., Mooney, A.M., Shoffner, M.A., Rose, S.D., Bundschuh, R., Fishel, R., Ottesen, J.J., Poirier, M.G. Regulation of the nucleosome unwrapping rate controls DNA accessibility.Nucleic acids research, 2012,gks747.
44. [44] Mahto, S.K., Howard, C.J., Shimko, J.C., Ottesen, J.J. A Reversible Protection Strategy To Improve Fmoc-SPPS of Peptide Thioesters by the N-Acylurea Approach. ChemBioChem, 2011,12, 2488-2494.
45. [45] Kawakami, T., Akai, Y., Fujimoto, H., Kita, C., Aoki, Y., Konishi, T., Waseda, M., Takemura, L., Aimoto, S. Sequential Peptide Ligation by Combining the Cys–Pro Ester (CPE) and Thioester Methods and Its Application to the Synthesis of Histone H3 Containing a Trimethyl Lysine Residue. Bull. Chem. Soc. Jpn. 2013,86, 690-697.
46. [46] Li, J., Li, Y., He, Q., Li, Y., Li, H., Liu, L. One-pot native chemical ligation of peptide hydrazides enables total synthesis of modified histones. Org. Biomol. Chem., 2014, 12, 5435-5441.
47. [47] Kumar, K.S.A., Spasser, L., Ohayon, S., Erlich, L.A., Brik, A. Expeditious chemical synthesis of ubiquitinated peptides employing orthogonal protection and native chemical ligation. Bioconjug. Chem. 2011, 22, 137-143.
48. [48] Siman, P., Karthikeyan, S.V., Nikolov, M., Fischle, W., Brik, A. Convergent Chemical Synthesis of Histone H2B Protein for the Site-Specific Ubiquitination at Lys34. Angew. Chem. Int. Ed. Engl. 2013, 52, 8059-8063.
49. [49] Xu, M.Q., Southworth, M.W., Mersha, F.B., Hornstra, L.J., Perler, F.B. In-Vitro Protein Splicing of Purified Precursor and the Identification of a Branched Intermediate. Cell, 1993, 75, 1371-1377.
50. [50] Muir, T.W., Sondhi, D., Cole, P.A. Expressed protein ligation: A general method for protein engineering. Proceedings of the National Academy of Sciences of the United States of America, 1998, 95, 6705-6710.
51. [51] Evans, T.C., Benner, J., Xu, M.Q. Semisynthesis of cytotoxic proteins using a modified protein splicing element. Protein Science, 1998, 7, 2256-2264.
52. [52] Shah, N.H., Vila-Perello, M., Muir, T.W. Kinetic Control of One-Pot Trans-Splicing Reactions by Using a Wild-Type and Designed Split Intein. Angew. Chem. Int. Ed. Engl., 2011, 50, 6511-6515.
53. [53] Vila-Perello, M., Liu, Z.H., Shah, N.H., Willis, J.A., Idoyaga, J., Muir, T.W. Streamlined Expressed Protein Ligation Using Split Inteins. J. Am. Chem. Soc., 2013, 135, 286-292.
54. [54] Vila-Perello, M., Muir, T.W. Biological Applications of Protein Splicing. Cell, 2010, 143, 191-200.
55. [55] Li, Y. M., Li, Y. T., Pan, M., Kong, X. Q., Huang, Y.C., Hong, Z.Y., Liu, L. Irreversible site-specific hydrazinolysis of protein by use of sortase. Angew. Chem. Int. Ed., 2014, 53, 2198-2202.
56. [56] Li, Y.-M., Yang, M.-Y., Huang, Y.-C., Li, Y.-T., Chen, P.R., Liu, L. Ligation of expressed protein α-hydrazides via genetic incorporation of an α-hydroxy acid. ACS Chem. Biol., 2012, 7, 1015-1022.
57. [57] Shogren-Knaak, M.A., Fry, C.J., Peterson, C.L. A native peptide ligation strategy for deciphering nucleosomal histone modifications. J. Biol. Chem., 2003, 278, 15744-15748.
58. [58] He, S., Bauman, D., Davis, J.S., Loyola, A., Nishioka, K., Gronlund, J.L., Reinberg, D., Meng, F., Kelleher, N., McCafferty, D.G. Facile synthesis of site-specifically acetylated and methylated histone proteins: reagents for evaluation of the histone code hypothesis. Proceedings of the National Academy of Sciences, 2003, 100, 12033-12038.
59. [59] Smith, C.M., Gafken, P.R., Zhang, Z., Gottschling, D.E., Smith, J.B., Smith, D.L. Mass spectrometric quantification of acetylation at specific lysines within the amino-terminal tail of histone H4. Anal. Biochem., 2003,316, 23-33.
60. [60] Ferreira, H., Flaus, A., Owen-Hughes, T. Histone modifications influence the action of Snf2 family remodelling enzymes by different mechanisms. J. Mol. Biol., 2007, 374, 563-579.
61. [61] Chiang, K.P., Jensen, M.S., McGinty, R.K., Muir, T.W. A semisynthetic strategy to generate phosphorylated and acetylated histone H2B. ChemBioChem, 2009, 10, 2182-2187.
62. [62] Goldknopf, I.L., French, M.F., Musso, R., Busch, H. Presence of protein A24 in rat liver nucleosomes. Proceedings of the National Academy of Sciences, 1977, 74, 5492-5495.
63. [63] West, M.H.P., Bonner, W.M. Histone 2B can be modified by the attachment of ubiquitin. Nucleic Acids Res., 1980,8, 4671-4680.
64. [64] McGinty, R.K., Kim, J., Chatterjee, C., Roeder, R.G., Muir, T.W. Chemically ubiquitylated histone H2B stimulates hDot1L-mediated intranucleosomal methylation. Nature, 2008, 453, 812-816.
65. [65] McGinty, R.K., Kohn, M., Chatterjee, C., Chiang, K.P., Pratt, M.R., Muir, T.W. Structure–activity analysis of semisynthetic nucleosomes: mechanistic insights into the stimulation of Dot1L by ubiquitylated histone H2B. ACS Chem. Biol., 2009, 4, 958-968.
66. [66] Kim, J., Guermah, M., McGinty, R.K., Lee, J.-S., Tang, Z., Milne, T.A., Shilatifard, A., Muir, T.W., Roeder, R.G. RAD6-Mediated transcriptioncoupled H2B ubiquitylation directly stimulates H3K4 methylation in human cells. Cell, 2009,137, 459-471.
67. [67] Chatterjee, C., McGinty, R.K., Fierz, B., Muir, T.W. Disulfide-directed histone ubiquitylation reveals plasticity in hDot1L activation. Nat. Chem. Biol., 2010,6, 267-269.
68. [68] Fierz, B., Chatterjee, C., McGinty, R.K., Bar-Dagan, M., Raleigh, D.P., Muir, T.W. Histone H2B ubiquitylation disrupts local and higher-order chromatin compaction. Nat. Chem. Biol., 2011, 7, 113-119.
69. [69] Wang, L., Xie, J., Schultz, P.G. Expanding the genetic code. Annu. Rev. Biophys. Biomol. Struct., 2006,35, 225-249.
70. [70] Wang, L., Brock, A., Herberich, B., Schultz, P.G. Expanding the genetic code of Escherichia coli. Science, 2001, 292, 498-500.
71. [71] Chin, J.W. Expanding and reprogramming the genetic code of cells and animals. Ann. Rev. Biochem., 2014,83, 379-408.
72. [72] Li, Y., Pan, M., Li, Y., Huang, Y., Guo, Q. Thiol–yne radical reaction mediated site-specific protein labeling via genetic incorporation of an alkynyl-l-lysine analogue. Organ. Biomol. Chem., 2013, 11, 2624-2629.
73. [73] Li, Y., Yang, M., Huang, Y., Song, X., Liu, L., Chen, P.R. Genetically encoded alkenyl–pyrrolysine analogues for thiol–ene reaction mediated sitespecific protein labeling. Chem. Sci., 2012, 3, 2766-2770.
74. [74] Guo, J., Wang, J., Lee, J.S., Schultz, P.G. Site-Specific Incorporation of methyl-and acetyl-lysine analogues into recombinant proteins. Angewandte Chemie, 2008, 120, 6499-6501.
75. [75] Neumann, H., Peak-Chew, S.Y., Chin, J.W. Genetically encoding Nε-acetyllysine in recombinant proteins. Nat. Chem. Biol., 2008, 4, 232-234.
76. [76] Nguyen, D.P., Garcia Alai, M.M., Kapadnis, P.B., Neumann, H., Chin, J.W. Genetically Encoding N-Methyl-l-lysine in Recombinant Histones. J. Am. Chem. Soc., 2009, 131, 14194-14195.
77. [77] Ai, H.-W., Lee, J.W., Schultz, P.G. A method to site-specifically introduce methyllysine into proteins in E. coli. Chem. Commun., 2010, 46, 5506-5508.
78. [78] Wang, Y.-S., Wu, B., Wang, Z., Huang, Y., Wan, W., Russell, W.K., Pai, P.-J., Moe, Y.N., Russell, D.H., Liu, W.R. A genetically encoded photocaged Nε-methyl-L-lysine. Mol. BioSyst., 2010,6, 1557-1560.
79. [79] Nguyen, D.P., Alai, M.M.G., Virdee, S., Chin, J.W. Genetically directing ε-N, N-dimethyl-l-Lysine in recombinant histones. Chem. Biol., 2010, 17, 1072-1076.
80. [80] Huang, R., Holbert, M.A., Tarrant, M.K., Curtet, S., Colquhoun, D.R., Dancy, B.M., Dancy, B.C., Hwang, Y., Tang, Y., Meeth, K. Site-specific introduction of an acetyl-lysine mimic into peptides and proteins by cysteine alkylation. J. Am. Chem. Soc., 2010,132, 9986-9987.
81. [81] Allahverdi, A., Yang, R., Korolev, N., Fan, Y., Davey, C.A., Liu, C.-F., Nordenskiöld, L. The effects of histone H4 tail acetylations on cationinduced chromatin folding and self-association. Nucleic Acids Res., 2011,39, 1680-1691.
82. [82] Patel, D.J., Wang, Z. Readout of epigenetic modifications. Annu. Rev. Biochem., 2013, 82, 81-118.
83. [83] Dhall, A., Chatterjee, C. Chemical approaches to understand the language of histone modifications. ACS Chem. Biol. 2011, 6, 987-999.
84. [84] Wang, Z., Ding, X., Li, S., Shi, J., Li, Y. Engineered fluorescence tags for in vivo protein labelling. RSC Advances, 2014, 4, 7235-7245.
85. [85] Rodriguez-Collazo, P., Leuba, S.H., Zlatanova, J. Robust methods for purification of histones from cultured mammalian cells with the preservation of their native modifications. Nucleic Acids. Res., 2009, 37, e81-e81.