Product specificity and mechanism of protein lysine methyltransferases: Insights from the histone lysine methyltransferase SET8

Biochemistry

Volumn 47, Issue 25, 2008, Pages 6671-6677

  Zhang, Xiaodong ^a   Bruice, Thomas C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FORCE FIELD (FF); HISTONE H4; LYSINE 20; METHYLATION REACTION; METHYLTRANSFERASE (MTASE); METHYLTRANSFERASES; MOLECULAR DYNAMICS SIMULATIONS (MDS); MOLECULAR MECHANICS (MM); NEUTRAL PH; PRODUCT SPECIFICITY; PROTONATED; QUANTUM MECHANICS (QM);

ALKYLATION; DYNAMICS; ENZYMES; FOOD ADDITIVES; MECHANICS; MECHANISMS; METHOD OF MOMENTS; METHYLATION; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MOLECULES; OPTICS; QUANTUM CHEMISTRY; QUANTUM THEORY; REACTION KINETICS; TARGETS;

AMINO ACIDS;

HISTONE LYSINE METHYLTRANSFERASE;

ARTICLE; CHEMICAL REACTION; ELECTRICITY; ENZYME SPECIFICITY; METHYLATION; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTON TRANSPORT; QUANTUM MECHANICS; SIMULATION;

CATALYSIS; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; KINETICS; LYSINE; METHYLATION; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR STRUCTURE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; QUANTUM THEORY; S-ADENOSYLHOMOCYSTEINE; S-ADENOSYLMETHIONINE; STATIC ELECTRICITY; SUBSTRATE SPECIFICITY;

EID: 45749140396     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800244s     Document Type: Article

References (44)

1. Strahl, B. D., and Allis, C. D. (2000) The language of covalent histone modifications. Nature 403, 41-45.
2. Feng, Q., Wang, H., Ng, H. H., Erdjument-Bromage, H., Tempst, P., Struhl, K., and Zhang, Y. (2002) Methylation of H3-lysine 79 is mediated by a new family of HMTases without a SET domain. Curr. Biol. 12, 1052-1058.
3. Min, J., Feng, Q., Li, Z. Z., Zhang, Y., and Xu, R. M. (2003) Structure of the catalytic domain of human DOT1L: A non-SET domain nucleosomal histone methy!transferase. Cell 112, 711-723.
4. Jacobs, S. A., Harp, J. M., Devarakonda, S., Kim, Y., Rastinejad, F., and Khorasanizadeh, S. (2002) The active site of the SET domain is constructed on a knot. Nat. Struct. Biol. 9, 833-838.
5. Xiao, B., Jing, C., Wilson, J. R., and Gamblin, S. J. (2003) SET Domain and Histone Metylation. Curr. Opin. Struct. Biol. 13, 699-705.
6. Xiao, B., Jing, C., Wilson, J. R., Walker, P. A., Vasisht, N., Kelly, G., Howell, S., Taylor, I. A., Blackburn, G. M., and Gamblin, S. J. (2003) Structure and Catalytic Mechanism of the Human Histone Methyltransferase SET 7/9. Nature 421, 652-656.
7. Kwon, T., Chang, J. H., Kwak, E., Lee, C. W., Joachimiak, A., Kim, Y. C., Lee, J., and Cho, Y. (2002) Mechanism of histone lysine methyl transfer revealed by the structure of SET7/9-AdoMet. EMBO J. 22, 292-303.
8. Couture, J., Collazo, E., Hauk, G., and Trievel, R. C. (2006) Structural Basis for the Methylation Site Specificity of SET7/9. Nat. Struct. Mol. 13, 140-146.
9. Couture, J., Collazo, E., Brunzelle, J. S., and Trievel, R. C. (2005) Structural and functional analysis of SET8, a histone H4 Lys-20 methyltransferase. Genes Dev. 19, 1455-1465.
10. Xiao, B., Jing, C., Kelly, G., Walker, P. A., Muskett, F. W., Frenkiel, T. A., Martin, S. R., Sarma, K., Reinberg, D., Gamblin, S. J., and Wilson, J. R. (2005) Specificity and mechanism of the histone methyltransferase Pr-Set7. Genes Dev. 19, 1444-1454.
11. Zhang, X., Yang, Z., Khan, S. I., Horton, J. R., Tamarn, H., Selker, E. U., and Cheng, X. (2003) Structural basis for the product specificity of histone lysine methyltransferase. Mol. Cell 12, 177-185.
12. Min, J., Zhang, X., Cheng, X., Grewal, S. I., and Xu, R. M. (2002) Structure of the SET domain histone lysine methyltransferase Clr4. Nat. Struct. Biol. 9, 828-832.
13. Qian, C., Wang, X., Manzur, K., Farooq, S. A., Zeng, L., Wang, R., and Zhou, M. (2006) Structural Insights of the Specificity and Catalysis of a Viral Histone H3 Lysine 27 Methyltransferase. J. Mol. Biol. 359, 86-96.
14. Manzur, K. L., Farooq, A., Zeng, L., Plotnikova, O., Koch, A. W., Sachchildanand, and Zhou, M. M. (2003) A dimeric viral SET domain methyltransferase specific to Lys27 of histone H3. Nat. Struct. Biol. 10, 187-196.
15. Trivel, R. C., Flynn, E. M., Houtz, R. L., and Hurley, J. H. (2003) Mechanism of Multiple Lysine Methylation by the SET Domain Enzyme Rubisco LSMT. Nat. Struct. Biol. 10, 545-552.
16. Couture, J., Hauk, G., Thompson, M. J., Blackburn, G. M., and Trievel, R. C. (2006) Catalytic Roles for Carbon-Oxygen Hydrogen Bonding in SET Domain Lysine Methyltransferases. J. Biol. Chem. 281, 19280-19287.
17. Zhang, X. D., and Bruice, T. C. (2007) Catalytic Mechanism and Product Specificity of Rubisco Large Subunit Methyltransferase: QM/MM and MD Investigations. Biochemistry 46, 5505-5014.
18. Zhang, X.-D., and Bruice, T. C. (2007) Histone Lysine Methyl-transferase SET7/9: Formation of a Water Channel Precedes Each Methyl Transfer. Biochemistry 46, 14838-14844.
19. Zhang, X.-D., and Bruice, T. C. (2007) A QM/MM Study on the Catalytic Mechanism and Product Specificity of viral Histone Lysine Methyltransferase. Biochemistry 46, 9743-9751.
20. Schotta, G., Lachner, M., Sarma, K., Ebert, A., Sengupta, R., Reuter, G., Reinberg, D., and Jenuwein, T. (2004) A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitute heterochromatin. Genes Dev. 18, 1251-1262.
21. Rayasam, G. V., Wendling, O., Angrand, P. O., Mark, M., Niederreither, K., Song, L., Lerouge, T., Hager, G. L., Chambon, P., and Losson, R. (2003) NSD1 is essential for early post-implantation development and has a catalytically active SET domain. EMBO J. 22, 3153-3168.
22. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, K. L. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-935.
23. Brooks, B. R., Bruccoleri, R. E., Olafson, B. D., States, D. J., Swaminathan, S., and Karplus, M. (1983) CHARMM: A Program for Macromolecular Energy, Minimization, and Dynamics Calculations. J. Comput. Chem. 4, 187-217.
24. MacKerell, A. D., Feig, M., and Brooks, C. L. (2004) Extending the treatment of backbone energetics in protein force fields: Limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J. Comput. Chem. 25, 1400-1415.
25. MacKerell, A. D., Jr., Bashford, D., Bellott, M., Dunbrack, R. L., Evanseck, J. D., Field, M. J., Fischer, S., Gao, J., Guo, H., Ha, S., Joseph-McCarthy, D., Kuchnir, L., Kuczera, K., Lau, F. T. K., Mattos, C, Michnick, S., Ngo, T., Nguyen, D. T., Prodhom, B., Reiher, W. E., Roux, B., Schlenkrich, M., Smith, J. C., Stote, R., Straub, J., Watanabe, M., Wiorkiewicz-Kuczera, J., Yin, D., and Karplus, M. (1998) All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins. J. Phys. Chem. B 102, 3586-3616.
26. Brunger, A. T., Brooks, C. L., III, and Karplus, M. (1985) Active Site Dynamics of Ribonuclease. Proc. Natl. Acad. Sci. U.S.A. 82, 8458-8462.
27. Brooks, C. L., and Karplus, M. (1989) Solvent Effects on Protein Motion and Protein Effects on Solvent Motion: Dynamics of the Active Site Region of Lysozyme. J. Mol. Biol. 208, 159-181.
28. Ryckaert, J. P., Ciccotti, G., and Berendsen, H. J. C. (1977) Numerical integration of the cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes. J. Comput. Phys. 23, 327-341.
29. Cui, Q., Elstner, M., Kaxiras, E., Frauesheim, Th., and Karplus, M. (2001) A QM/MM Implementation of the Self-Consistent Charge Density Functional Tight Binding (SCC-DFTB) Method. J. Phys. Chem. B 105, 569-585.
30. Elstner, M., Porezag, D., Jungnickel, G., Elsner, J., Haugk, M., Frauenheim, Th., Suhai, S., and Seifert, G. (1998) Self-Consistent-Charge Density-Functional Tight-Binding Method for Simulation of Complex Materials Properties. Phys. Rev. B 58, 7260-7268.
31. Fischer, S., and Karplus, M. (1992) Conjugate Peak Refinement: An Algorithm for Finding Reaction Paths and Accurate Transition States in Systems with Many Degrees of Freedom. Chem. Phys. Lett. 194, 252-261.
32. Hu, P., and Zhang, Y. (2006) Catalytic Mechanism and Product Specificity of the Histone Lysine Methyltransferase SET 7/9: An ab initio QM/MM-FE study with Multiple Initial Structures. J. Am. Chem. Soc. 128, 1272-1278.
33. Wiberg, K. B. (1968) Application of the Pople-Santry-Segal complete neglect of differential overlap method to the cyclopropyl-carbinyl and cyclobutyl cation and to bicyclobutane. Tetrahedron 24, 1083-1096.
34. Schmidt, M. W., Baldridge, K. K., Boatz, J. A., Elbert, S. T., Gorden, M. S., Jensen, J. H., Koseki, S., Matsunage, N., Nguyen, K. A., Su, S. J., Windus, T. L., Dupuis, M., and Montgomery, J. A. (1993) General atomic and molecular electronic-structure system. J. Comput. Chem. 14, 1347-1363.
35. McQuarrie, D. A. (1973) Statistical Thermodynamics, Harper and Row, New York.
36. Takusagawa, F., Fujioba, M., Spies, A., and Schowen, R. L. (1998) S-Adenosylmethionine (AdoMet)-dependent Methyltransferases, in Comprehensive Biological Catalysis: A Mechanistic Reference (Sinnott, M., Ed.) pp 1-30, Academic Press, New York.
37. Wang, S., Hu, P., and Zhang, Y. (2007) Ab Initio Quantum mechanical/Molecular Mechanism Molecular Dynamics Simulations of Enzyme Catalysis: The Case of Histone Lysine Methyl-transferase SET7/9. J. Phys. Chem. B 111, 3758-3764.
38. Bruice, T. C. (2002) A view at the millennium: The efficiency of enzyme catalysis. Acc. Chem. Res. 35, 139-148.
39. Bruice, T. C., and Benhovic, S. J. (2000) Chemical basis for enzyme catalysis. Biochemistry 39, 6267-6274.
40. Bruice, T. C. (2006) Computational approaches: Reaction trajectories, structures, and atomic motions. Enzyme reactions and proficiency. Chem. Rev. 106, 3119-3139.
41. Zhang, X.-D., and Bruice, T. C. (2008) Mechanism of product specificity of AdoMet methylation catalyzed by lysine methyltransferases: Transcriptional factor p53 methylation by histone lysine methyltransferase SET7/9. Biochemistry 47, 2743-2748.
42. Lu, J., Yu, J., Chen, X., Cheng, P., Zhang, X., and Xu, J. (2005) Novel Self-Assembled Chain of Water Molecules in a Metal-Organic Framework Structure of Co(II) with Tartrate Acid. Inorg. Chem. 44, 5978-5980.
43. Jin, Y., Che, Y., and Zheng, J. (2007) Supramolecularly assembled decameric water cluster stabilized by dichromate anions in complex of Ni(II). Inorg. Chem. Commun. 10, 514-516.
44. Cheng, X., Collins, R., and Zhang, X. (2005) Structural and Sequence Motifs of Protein (Histone) Methylation Enzymes. Annu. Rev. Biophys. Biomol. Struct. 34, 267-294.