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Research Article

Insights into intermolecular interactions, electrostatic properties and the stability of C646 in the binding pocket of p300 histone acetyltransferase enzyme: a combined molecular dynamics and charge density study

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Pages 3246-3264 | Received 06 Jul 2017, Accepted 13 Sep 2017, Published online: 30 Oct 2017

References

  • Bader, R. F. W., Tal, Y., Anderson, S. G., & Nguyen-Dang, T. T. (1980). Quantum topology: Theory of molecular structure and its change. Israel Journal of Chemistry, 19, 8–29. doi:10.1002/ijch.198000003
  • Balasubramanyam, K., Varier, R. A., Altaf, M., Swaminathan, V., Siddappa, N. B., Ranga, U., & Kundu, T. K. (2004). Curcumin, a Novel p300/CREB-binding protein-specific inhibitor of acetyltransferase, represses the acetylation of histone/nonhistone proteins and histone acetyltransferase-dependent chromatin transcription. Journal of Biological Chemistry, 279, 51163–51171. doi:10.1074/jbc.m409024200
  • Bannister, A. J., & Kouzarides, T. (2011). Regulation of chromatin by histone modifications. Cell Research, 21, 381–395. doi:10.1038/cr.2011.22
  • Barnes, P. J., Adcock, I. M., & Ito, K. (2005). Histone acetylation and deacetylation: Importance in inflammatory lung diseases. European Respiratory Journal, 25, 552–563. doi:10.1183/09031936.05.00117504
  • Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., & Haak, J. R. (1984). Molecular dynamics with coupling to an external bath. The Journal of Chemical Physics, 81, 3684–3690. doi:10.1063/1.448118
  • Berndsen, C. E., & Denu, J. M. (2008). Catalysis and substrate selection by histone/protein lysine acetyltransferases. Current Opinion in Structural Biology, 18, 682–689. doi:10.1016/j.sbi.2008.11.004
  • Bowers, E. M., Yanb, G., Mukherjee, C., Orry, A., Wang, L., Holbert, M. A., … Cole, P. A. (2010). Virtual ligand screening of the p300/CBP histone acetyltransferase: Identification of a selective small molecule inhibitor. Chemistry & Biology, 17(5), 471–482. doi:10.1016/j.chembiol.2010.03.006
  • Case, D. A., Babin, V., Berryman, J. T., Betz, R. M., Cai, Q., Cerutti, D. S., … Kollman, P. A. (2014). AMBER 14. San Francisco: University of California.
  • Chan, H. M., & La Thangue, N. B. (2001). p300/CBP proteins: HATs for transcriptional brifges and scaffolds. Journal of Cell Science, 114, 2363–2373.
  • Cheeseman, J., Keith, T. A., & Bader, R. F. W. (1992). AIMPAC program package. Hamilton, ON: McMaster University.
  • Cohen, I., Poreba, E., Kamieniarz, K., & Schneider, R. (2011). Histone modifiers in cancer: Friends or foes? Genes Cancer, 2(6), 631–647. doi:10.1177/1947601911417176
  • Costi, R., Santo, R. D., Artico, M., Miele, G., Valentini, P., Novellino, E., & Cereseto, A. (2007). Cinnamoyl compounds as simple molecules that inhibit p300 histone acetyltransferase. Journal of Medicinal Chemistry, 50, 1973–1977. doi:10.1021/jm060943s
  • Das, C., Lucia, M. S., Hansen, K. C., & Tyler, J. K. (2009). CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature, 459, 113–117. doi:10.1038/nature07861
  • Dassault Systems BIOVIA. (2017). Discovery studio modeling environment, release. San Diego, CA: Author.
  • Davie, J. R. (1998). Covalent modifications of histones: Expression from chromatin templates. Current Opinion in Genetics & Development, 8, 173–178. doi:10.1016/S0959-437X(98)80138-X
  • Dekker, F. J., & Haisma, H. J. (2009). Histone acetyl transferases as emerging drug targets. Drug Discovery Today, 14, 942–948. doi:10.1016/j.drudis.2009.06.008
  • Delano, W. L. (2002). PyMol molecular graphics system. San Carlos, CA: Delano Scientific.
  • Devipriya, B., & Kumaradhas, P. (2012). Probing the effect of intermolecular interaction and understanding the electrostatic moments of anacardic acid in the active site of p300 enzyme via DFT and charge density analysis. Journal of Molecular Graphics and Modelling, 34, 57–66. doi:10.1016/j.jmgm.2011.12.003 10.1016/j.jmgm.2011.12.003
  • Devipriya, B., & Kumaradhas, P. (2013a). Molecular flexibility and the electrostatic moments of curcumin and its derivatives in the active site of p300: A theoretical charge density study. Chemico-Biological Interactions, 204(3), 153–165. doi:10.1016/j.cbi.2013.05.002
  • Devipriya, B., & Kumaradhas, P. (2013b). Charge density distribution and the electrostatic moments of CTPB in the active site of p300 enzyme: A DFT and charge density study. Journal of Theoretical Biology, 335, 119–129. doi:10.1016/j.jtbi.2013.06.001
  • Devipriya, B., Parameswari, A., Rajalakshmi, G., & Kumaradhas, P. (2012). Charge density distribution and electrostatic moments of N-(4-chloro-3- trifluromethyl-phenyl)-2-ethoxy-benzamide molecule at the active site of p300 enzyme: A quantum chemical and theoretical charge density study. International Journal of Quantum Chemistry, 112, 1185–1197. doi:10.1002/qua.23109
  • Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., … Pople, J.A. (2004). Wallingford, CT: Gaussian.
  • Geerlings, P., De Proft, F. D., & Langenaeker, W. (2003). Conceptual density functional theory. Chemical Reviews, 103, 1793–1874. doi:10.1021/cr990029p
  • Goodman, R. H., & Smolik, S. (2000). CBP/p300 in cell growth, transformation, and development. Genes & Development, 14, 1553–1577. doi:10.1101/gad.14.13.1553
  • Grant, P. A. (2001). A tale of histone modifications. Genome Biology, 2(4). reviews/0003.1–0003.6.
  • Grunstein, M. (1997). Histone acetylation in chromatin structure and transcription. Nature, 389, 349–352. doi:10.1038/38664
  • Happel, N., & Doenecke, D. (2009). Histone H1 and its isoforms: Contribution to chromatin structure and function. Gene, 431, 1–12. doi:10.1016/j.gene.2008.11.003
  • Harrach, M. F., & Drossel, B. (2014). Structure and dynamics of TIP3P, TIP4P, and TIP5P water near smooth and atomistic walls of different hydroaffinity. The Journal of Chemical Physics, 140(1–14), 174501. doi:10.1063/1.4872239
  • He, H., Yu, F., Sun, C., & Luo, Y. (2011). CBP/p300 and SIRT1 are involved in transcriptional regulation of S-phase specific histone genes. PLoS ONE, 6, 1–14. doi:10.1371/journal.pone.0022088
  • Hong, J., Kwon, S. J., Sang, S., Ju, J., Zhou, J., Ho, C., … Yang, C. S. (2007). Effects of garcinol and its derivatives on intestinal cell growth: Inhibitory effects and autoxidation-dependent growth-stimulatory effects. Free Radical Biology and Medicine, 42, 1211–1221. doi:10.1016/j.freeradbiomed.2007.01.016
  • Iyer, N. G., Özdag, H., & Caldas, C. (2004). p300/CBP and cancer. Oncogene, 23, 4225–4231. doi:10.1038/sj.onc.1207118
  • Jenuwein, T., & Allis, C. D. (2001). Translating the histone code. Science, 293, 1074–1080. doi:10.1126/science.1063127
  • Johnson, C. A., & Turner, B. M. (1999). Histone deacetylases: Complex transducers of nuclear signals. Seminars in Cell & Developmental Biology, 10, 179–188. doi:10.1006/scdb.1999.0299
  • Jones, A., & Leimkuhler, B. (2011). Adaptive stochastic methods for sampling driven molecular systems. The Journal of Chemical Physics, 135(1–11), 084125. doi:10.1063/1.3626941
  • Kadiyala, C. S. R., Zheng, L., Du, Y., Yohannes, E., Kao, H., Miyagi, M., & Kern, T. S. (2012). Acetylation of retinal histones in diabetes increases inflammatory proteins. Journal of Biological Chemistry, 287, 25869–25880. doi:10.1074/jbc.m112.375204
  • Kalkhoven, E. (2004). CBP and p300: HATs for different occasions. Biochemical Pharmacology, 68, 1145–1155. doi:10.1016/j.bcp.2004.03.045
  • Koritsanszky, T., Richter, T., Macci, P., Gatti, C., Farruugia, L. J., Mallinson, P. R., … Richter, T. (2007). XD-2006. A computer program package for multipole refinement and topological analysis of charge densities and evaluation of intermolecular energies from experimental or theoretical structure factors (Version 5.33). Berlin: Freie University.
  • Koritsanszky, T., Richter, T., Macci, P., Gatti, C., Howard, S., Mallison, P. R., … Hansen, N. K. (2003). XD – A computer program package for multipole refinement and analysis of electron densities from diffraction data. Berlin: Freie University.
  • Kurdistani, S. K., & Grunstein, M. (2003). Histone acetylation and deacetylation in yeast. Nature Reviews Molecular Cell Biology, 4, 276–284. doi:10.1038/nrm1075
  • Labanowski, J. K., & Andzelm, J. W. (1991). Density functional methods in chemistry. New York, NY: Springer.10.1007/978-1-4612-3136-3
  • Liu, X., Wang, L., Zhao, K., Thompson, P. R., Hwang, Y., Marmorstein, R., & Cole, P. A. (2008). The structural basis of protein acetylation by the p300/CBP transcriptional coactivator. Nature, 451, 846–850. doi:10.1038/nature06546
  • Luger, K. (2001). Nucleosomes: Structure and function, encyclopedia of life sciences. Nature Publishing Group. Retrieved from www.els.net
  • Maier, J. A., Martinez, C., Kasavajhala, K., Wickstrom, L., Hauser, K., & Simmerling, C. (2015). ff14SB: Improving the accuracy of protein side chain and backbone parameters from ff99SB. Journal of Chemical Theory and Computation, 11, 3696–3713. doi:10.1021/acs.jctc.5b00255
  • Maksimoska, J., Segura-Peña, D., Cole, P. A., & Marmorstein, R. (2014). Structure of the p300 histone acetyltransferase bound to acetyl-coenzyme A and its analogues. Biochemistry, 53, 3415–3422. doi:10.1021/bi500380f
  • Mark, P., & Nilsson, L. (2001). Structure and dynamics of the TIP3P, SPC, and SPC/E water models at 298 K. The Journal of Physical Chemistry A, 105, 9954–9960. doi:10.1021/jp003020w
  • Marmorstein, R. (2001). Structure and function of histone acetyltransferases. Cellular and Molecular Life Sciences, 58, 693–703.10.1007/PL00000893
  • Marmorstein, R., Liu, X., Cole, P.A., Wang, L., Bowers, E. M., Meyers, D.J, & Mukherjee, C. (2013, December 26). Methods and compositions for modulating p300/CBP activity, united state patent application Pub. No: US 2013/0345267 A1.
  • Martyna, G. J., & Hughes, A. (1999). Molecular dynamics algorithms for path integrals at constant pressure. The Journal of Chemical Physics, 110, 3275–3290. doi:10.1063/1.478193
  • Oike, T., Komachi, M., Ogiwara, H., Amornwichet, N., Saitoh, Y., Torikai, K., … Kohno, T. (2014). C646, a selective small molecule inhibitor of histone acetyltransferase p300, radiosensitizes lung cancer cells by enhancing mitotic catastrophe. Radiotherapy and Oncology, 111, 222–227. doi:10.1016/j.radonc.2014.03.015
  • Parr, R. G., Donnelly, R. A., Levy, M., & Palke, W. E. (1978). Electronegativity: The density functional viewpoint. The Journal of Chemical Physics, 68, 3801–3807. doi:10.1063/1.436185
  • Parr, R. G., & Pearson, R. G. (1983). Absolute hardness: Companion parameter to absolute electronegativity. Journal of the American Chemical Society, 105, 7512–7516. doi:10.1021/ja00364a005
  • Parr, R. G., Szentpály, L. V., & Liu, S. (1999). Electrophilicity Index. Journal of the American Chemical Society, 121, 1922–1924. doi:10.1021/cr040109f
  • Parr, R. G., & Yang, W. (1989). Density functional theory of atoms and molecules. New York, NY: Oxford.
  • Renuga Parameswari, A., Rajalakshmi, G., & Kumaradhas, P. (2015). A combined molecular docking and charge density analysis is a new approach for medicinal research to understand drug–receptor interaction: Curcumin–AChE model. Chemico-Biological Interactions, 225, 21–31. doi:10.1016/j.cbi.2014.09.011
  • Roe, D. R., & Cheatham, T. E. (2013). PTRAJ and CPPTRAJ: Software for processing and analysis of molecular dynamics trajectory data. Journal of Chemical Theory and Computation, 9, 3084–3095. doi:10.1021/ct400341p
  • Roy, D. R., Sarkar, U., Chattaraj, P. K., Mitra, A., Padmanabhan, J., Parthasarathi, R., … Bultinck, P. (2006). Analyzing toxicity through electrophilicity. Molecular Diversity, 10, 119–131. doi:10.1007/s11030-005-9009-x
  • Ryckaert, J., Ciccotti, G., & Berendsen, H. J. C. (1977). Numerical integration of the Cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes. Journal of Computational Physics, 23, 321–341. doi:10.1016/0021-9991(77)90098-5
  • Sadoul, K., Boyault, C., Pabion, M., & Khochbin, S. (2008). Regulation of protein turnover by acetyltransferases and deacetylases. Biochimie, 90, 306–312. doi:10.1016/j.biochi.2007.06.009
  • Saravanan, K., Kalaiarasi, Chinnasamy, & Kumaradhas, P. (2017). Understanding the conformational flexibility and electrostatic properties of curcumin in the active site of rhAChE via molecular docking, molecular dynamics, and charge density analysis. Journal of Biomolecular Structure and Dynamics, 2, 1–21. doi:10.1080/07391102.2016.1264891
  • Schreiber, S. L., & Bernstein, B. E. (2002). Signaling network model of chromatin. Cell, 111, 771–778. doi:10.1016/S0092-8674(02)01196-0
  • Schrodinger release. 2014-2. New York, NY: Schrödinger, LLC.
  • Schrodinger release 2014-2. (2014). Maestro (Version 9.8). New York, NY: Schrödinger, LLC.
  • Schrödinger Suite. 2014-2. Protein Preparation Wizard. New York, NY: Schrödinger, LLC.
  • Schrödinger Suite 2014-2. (2014). Ligprep (Version 2.5). New York, NY: Schrödinger, LLC.
  • Shiio, Y., & Eisenman, R. N. (2011). Histone sumoylation is associated with transcriptional repression. Proceedings of the National Academy of Sciences, 100, 13225–13230. doi: 10.1073/pnas.1735528100
  • Shilatifard, A. (2006). Chromatin modifications by methylation and ubiquitination: Implications in the regulation of gene expression. Annual Review of Biochemistry, 75, 243–269. doi:10.1146/annurev.biochem.75.103004.142422
  • Small-molecular Drug Discovery suite 2014-2. (2014). Induced Fit docking protocol. New York, NY: Schrödinger, LLC.
  • Stash, A., & Tsirelson, V. (2002). WinXPRO: A program for calculating crystal and molecular properties using multipole parameters of the electron density. Journal of Applied Crystallography, 35, 371–373. doi:10.1107/s0021889802003230
  • Strahl, B. D., & Allis, C. D. (2000). The language of covalent histone modifications. Nature, 403, 41–45. doi:10.1038/47412
  • Turner, B. M. (2000). Histone acetylation and an epigenetic code. BioEssays, 22, 836–845. doi:10.1002/1521-1878(200009)22:9<836::aid-bies9>3.0.co;2-x
  • Valor, L. M., Viosca, J., Lopez-Atalaya, J. P., & Barco, A. (2013). Lysine acetyltransferases CBP and p300 as therapeutic targets in cognitive and neurodegenerative disorders. Current Pharmaceutical Design, 19, 5051–5064. doi:10.2174/13816128113199990382
  • Verdone, L., Agricola, E., Caserta, M., & Mauro, E. D. (2006). Histone acetylation in gene regulation. Briefings in Functional Genomics and Proteomics, 5, 209–221. doi:10.1093/bfgp/ell028
  • Wang, J., Wang, W., Kollman, P. A., & Case, D. A. (2006). Automatic atom type and bond type perception in molecular mechanical calculations. Journal of Molecular Graphics and Modelling, 25, 247–260. doi:10.1016/j.jmgm.2005.12.005
  • Wang, J., Wolf, R. M., Caldwell, J. M., Kollman, P. A., & Case, D. A. (2004). Development and testing of a general amber force field. Journal of Computational Chemistry, 25, 1157–1174. doi:10.1002/jcc.20035
  • Wang, F., Marshall, C. B., & Ikura, M. (2013). Transcriptional/epigenetic regulator CBP/p300 in tumorigenesis: Structural and functional versatility in target recognition. Cellular and Molecular Life Sciences, 70, 3989–4008. doi:10.1007/s00018-012-1254-4
  • Wang, Y., Miao, X., Liu, Y., Li, F., Liu, Q., Sun, J., & Cai, L. (2014). Dysregulation of histone acetyltransferases and deacetylases in cardiovascular diseases. Oxidative Medicine and Cellular Longevity, 2014, 1–11. doi:10.1155/2014/641979
  • Zhang, X., Ouyang, S., Kong, X., Liang, Z., Lu, J., Zhu, K., … Luo, C. (2014). The catalytic mechanism of histone acetyltransferase p300: From the proton transfer to acetylation reaction. The Journal of Physical Chemistry B, 118(8), 2009–2019. doi:10.1021/jp409778e

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