Modeling studies on the structural determinants for the DAG/phorbol ester binding to C1 domain

Journal of Biomolecular Structure and Dynamics

Volumn 33, Issue 1, 2015, Pages 219-232

  Rahman, Ghazi M ^a   Das, Joydip ^a  

^a UNIVERSITY OF HOUSTON   (United States)

Author keywords

C1 domain; diacylglycerol; molecular dynamics; molecular modeling; phorbol ester; protein kinase C; protomol; Sybyl

Indexed keywords

DIACYLGLYCEROL; PHORBOL ESTER; PROTEIN KINASE C; ISOENZYME; PROTEIN BINDING; WATER;

ALPHA HELIX; ARTICLE; BETA SHEET; BINDING AFFINITY; BINDING SITE; C1 DOMAIN; CONTROLLED STUDY; CRYSTAL STRUCTURE; LIGAND BINDING; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE SEQUENCE; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; RESIDUE ANALYSIS; SEQUENCE ANALYSIS; SOLVATION; STRUCTURAL HOMOLOGY; STRUCTURE ANALYSIS; SURFACE PROPERTY; X RAY CRYSTALLOGRAPHY; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOLECULAR DOCKING; MOLECULAR GENETICS; MUTATION; PLIABILITY; PROCEDURES; PROTEIN TERTIARY STRUCTURE; THERMODYNAMICS;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; DIGLYCERIDES; HUMANS; ISOENZYMES; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MUTATION; PHORBOL ESTERS; PLIABILITY; PROTEIN BINDING; PROTEIN KINASE C; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; THERMODYNAMICS; WATER;

EID: 84908566281     PISSN: 07391102     EISSN: 15380254     Source Type: Journal    
DOI: 10.1080/07391102.2014.895679     Document Type: Article

References (48)

1. Ananthanarayanan, B., Stahelin, R. V., Digman, M. A., & Cho, W. (2003). Activation mechanisms of conventional protein kinase C isoforms are determined by the ligand affinity and conformational flexibility of their C1 domains. Journal of Biological Chemistry, 278, 46886-46894.
2. Billas, I. M., Iwema, T., Garnier, J. M., Mitschler, A., Rochel, N., & Moras, D. (2003). Structural adaptability in the ligand-binding pocket of the ecdysone hormone receptor. Nature, 426, 91-96.
3. Blumberg, P. M., Kedei, N., Lewin, N. E., Yang, D., Czifra, G., Pu, Y., ... Marquez, V. E. (2008). Wealth of opportunity - The C1 domain as a target for drug development. Current Drug Targets, 9, 641-652.
4. Boije af Gennas, G., Talman, V., Yli-Kauhaluoma, J., K Tuominen, R. K., & Ekokoski, E. (2011). Current status and future prospects of c1 domain ligands as drug candidates. Current Topics in Medicinal Chemistry, 11, 1370-1392.
5. Buchan, D. W., Minneci, F., Nugent, T. C., Bryson, K., & Jones, D. T. (2013). Scalable web services for the PSIPRED protein analysis workbench. Nucleic Acids Research, 41, W349-W357.
6. Chrencik, J. E., Orans, J., Moore, L. B., Xue, Y., Peng, L., Collins, J. L., ... Redinbo, M. R. (2005). Structural disorder in the complex of human pregnane X receptor and the macrolide antibiotic rifampicin. Molecular Endocrinology, 19, 1125-1134.
7. Colon-Gonzalez, F., & Kazanietz, M. G. (2006). C1 domains exposed: From diacylglycerol binding to protein-protein interactions. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, 1761, 827-837.
8. Corbalán-García, S., & Gómez-Fernández, J. C. (2006). Protein kinase C regulatory domains: The art of decoding many different signals in membranes. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, 1761, 633-654.
9. Dries, D. R., Gallegos, L. L., & Newton, A. C. (2007). A single residue in the C1 domain sensitizes novel protein kinase C isoforms to cellular diacylglycerol production. Journal of Biological Chemistry, 282, 826-830.
10. Farnegardh, M., Bonn, T., Sun, S., Ljunggren, J., Ahola, H., Wilhelmsson, A., ... Carlquist, M. (2003). The threedimensional structure of the liver X receptor beta reveals a flexible ligand-binding pocket that can accommodate fundamentally different ligands. Journal of Biological Chemistry, 278, 38821-38828.
11. Geczy, T., Peach, M. L., El Kazzouli, S., Sigano, D. M., Kang, J. H., Valle, C. J., ... Blumberg, P. M. (2012). Molecular basis for failure of "atypical" C1 domain of Vav1 to bind diacylglycerol/phorbol ester. Journal of Biological Chemistry, 287, 13137-13158.
12. Giorgione, J. R., Lin, J. H., McCammon, J. A., & Newton, A. C. (2006). Increased membrane affinity of the C1 domain of protein kinase Cdelta compensates for the lack of involvement of its C2 domain in membrane recruitment. Journal of Biological Chemistry, 281, 1660-1669.
13. Henzler-Wildman, K. A., Thai, V., Lei, M., Ott, M., Wolf-Watz, M., Fenn, T., ... Kern, D. (2007). Intrinsic motions along an enzymatic reaction trajectory. Nature, 450, 838-844.
14. House, C., & Kemp, B. E. (1987). Protein kinase C contains a pseudosubstrate prototope in its regulatory domain. Science, 238, 1726-1728.
15. Hurley, J. H., Newton, A. C., Parker, P. J., Blumberg, P. M., & Nishizuka, Y. (1997). Taxonomy and function of C1 protein kinase C homology domains. Protein Science, 6, 477-480.
16. Irie, K., Nakagawa, Y., & Ohigashi, H. (2004). Indolactam and benzolactam compounds as new medicinal leads with binding selectivity for C1 domains of protein kinase C isozymes. Current Pharmaceutical Design, 10, 1371-1385.
17. Irie, K., Nakagawa, Y., & Ohigashi, H. (2005). Toward the development of new medicinal leads with selectivity for protein kinase C isozymes. The Chemical Record, 5, 185-195.
18. Irie, K., Nakahara, A., Nakagawa, Y., Ohigashi, H., Shindo, M., Fukuda, H., ... Saito, N. (2002). Establishment of a binding assay for protein kinase C isozymes using synthetic C1 peptides and development of new medicinal leads with protein kinase C isozyme and C1 domain selectivity. Pharmacology & Therapeutics, 93, 271-281.
19. Irie, K., Oie, K., Nakahara, A., Yanai, Y., Ohigashi, H., Wender, P. A., ... Kikkawa, U. (1998). Molecular basis for protein kinase C isozyme-selective binding: The synthesis, folding, and phorbol ester binding of the cysteine-rich domains of all protein kinase C isozymes. Journal of the American Chemical Society, 120, 9159-9167.
20. Jones, D. T. (1999). Protein secondary structure prediction based on position-specific scoring matrices. Journal of Molecular Biology, 292, 195-202.
21. Kahraman, A., Morris, R. J., Laskowski, R. A., & Thornton, J. M. (2007). Shape variation in protein binding pockets and their ligands. Journal of Molecular Biology, 368, 283-301.
22. Kazanietz, M. G. (2000). Eyes wide shut: Protein kinase C isozymes are not the only receptors for the phorbol ester tumor promoters. Molecular Carcinogenesis, 28, 5-11.
23. Kirwan, A. F., Bibby, A. C., Mvilongo, T., Riedel, H., Burke, T., Millis, S. Z., & Parissenti, A. M. (2003). Inhibition of protein kinase C catalytic activity by additional regions within the human protein kinase Cα-regulatory domain lying outside of the pseudosubstrate sequence. Biochemical Journal, 373, 571-581.
24. Lange, O. F., Lakomek, N. A., Fares, C., Schroder, G. F., Walter, K. F., Becker, S., ... de Groot, B. L. (2008). Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution. Science, 320, 1471-1475.
25. Ma, D. (2001). Recent advances in the discovery of protein kinase C modulators based on the structures of natural protein kinase C activators. Current Medicinal Chemistry, 8, 191-202.
26. Melowic, H. R., Stahelin, R. V., Blatner, N. R., Tian, W., Hayashi, K., Altman, A., & Cho, W. (2007). Mechanism of diacylglycerol-induced membrane targeting and activation of protein kinase C . Journal of Biological Chemistry, 282, 21467-21476.
27. Milne, J. S., Mayne, L., Roder, H., Wand, A. J., & Englander, S. W. (1998). Determinants of protein hydrogen exchange studied in equine cytochrome c. Protein Science, 7, 739-745.
28. Milne, J. S., Xu, Y., Mayne, L. C., & Englander, S. W. (1999). Experimental study of the protein folding landscape: Unfolding reactions in cytochrome c. Journal of Molecular Biology, 290, 811-822.
29. Mittermaier, A., & Kay, L. E. (2006). New tools provide new insights in NMR studies of protein dynamics. Science, 312, 224-228.
30. Mobley, D. L., & Dill, K. A. (2009). Binding of small-molecule ligands to proteins: "what you see" is not always "what you get". Structure, 17, 489-498.
31. Newton, A. C. (2001). Protein kinase C: Structural and spatial regulation by phosphorylation, cofactors, and macromolecular interactions. Chemical Reviews, 101, 2353-2364.
32. Newton, A. C. (2010). Protein kinase C: Poised to signal. AJP: Endocrinology and Metabolism, 298, E395-E402.
33. Orr, J. W., & Newton, A. C. (1994). Intrapeptide regulation of protein kinase C. Journal of Biological Chemistry, 269, 8383-8387.
34. Pu, Y., Peach, M. L., Garfield, S. H., Wincovitch, S., Marquez, V. E., & Blumberg, P. M. (2006). Effects on ligand interaction and membrane translocation of the positively charged arginine residues situated along the C1 domain binding cleft in the atypical protein kinase C isoforms. Journal of Biological Chemistry, 281, 33773-33788.
35. Rahman, G. M., Shanker, S., Lewin, N. E., Kedei, N., Hill, C. S., Prasad, B. V., ... Das, J. (2013). Identification of the activator-binding residues in the second cysteine-rich regulatory domain of protein kinase Cθ (PKCθ). Biochemical Journal, 451, 33-44.
36. Shanmugasundararaj, S., Das, J., Sandberg, W. S., Zhou, X., Wang, D., Messing, R. O., ... Miller, K. W. (2012). Structural and functional characterization of an anesthetic binding site in the second cysteine-rich domain of protein kinase Cδ. Biophysical Journal, 103, 2331-2340.
37. Shen, N., Guryev, O., & Rizo, J. (2005). Intramolecular occlusion of the diacylglycerol-binding site in the C1 domain of munc13-1. Biochemistry, 44, 1089-1096.
38. Shindo, M., Irie, K., Nakahara, A., Ohigashi, H., Konishi, H., Kikkawa, U., ... Wender, P. A. (2001). Toward the identification of selective modulators of protein kinase C (PKC) isozymes: Establishment of a binding assay for PKC isozymes using synthetic C1 peptide receptors and identification of the critical residues involved in the phorbol ester binding. Bioorganic & Medicinal Chemistry, 9, 2073-2081.
39. Simon, Z., Vigh-Smeller, M., Peragovics, A, Csukly, G., ZahoranszkyKohalmi, G., Rauscher, A. A., ... Czobor, P. (2010). Relating the shape of protein binding sites to binding affinity profiles: Is there an association? BMC Structural Biology, 10, 32.
40. Slater, S. J., Seiz, J. L., Cook, A. C., Buzas, C. J., Malinowski, S. A., Kershner, J. L., ... Stubbs, C. D. (2002). Regulation of PKCalpha activity by C1-C2 domain interactions. Journal of Biological Chemistry, 277, 15277-15285.
41. Stahelin, R. V., Digman, M. A., Medkova, M., Ananthanarayanan, B., Melowic, H. R., Rafter, J. D., & Cho, W. (2005a). Diacylglycerol-induced membrane targeting and activation of protein kinase Cepsilon: Mechanistic differences between protein kinases Cdelta and Cepsilon. Journal of Biological Chemistry, 280, 19784-19793.
42. Stahelin, R. V., Digman, M. A., Medkova, M., Ananthanarayanan, B., Rafter, J. D., Melowic, H. R., & Cho, W. (2004). Mechanism of diacylglycerol-induced membrane targeting and activation of protein kinase C. Journal of Biological Chemistry, 279, 29501-29512.
43. Stahelin, R. V., Wang, J., Blatner, N. R., Rafter, J. D., Murray, D., & Cho, W. (2005b). The origin of C1A-C2 interdomain interactions in protein kinase C. Journal of Biological Chemistry, 280, 36452-36463.
44. Suino-Powell, K., Xu, Y., Zhang, C., Tao, Y. G., Tolbert, W. D., Simons, S. S., Jr., & Xu, H. E. (2008). Doubling the size of the glucocorticoid receptor ligand binding pocket by deacylcortivazol. Molecular and Cellular Biology, 28, 1915-1923.
45. Teague, S. J. (2003). Implications of protein flexibility for drug discovery. Nature Reviews Drug Discovery, 2, 527-541.
46. Timm, D. E., Baker, L. J., Mueller, H., Zidek, L., & Novotny, M. V. (2001). Structural basis of pheromone binding to mouse major urinary protein (MUP-I). Protein Science, 10, 997-1004.
47. Xu, H. E., Stanley, T. B., Montana, V. G., Lambert, M. H., Shearer, B. G., Cobb, J. E., ... Stimmel, J. B. (2002). Structural basis for antagonist-mediated recruitment of nuclear co-repressors by PPARα. Nature, 415, 813-817.
48. Zhang, G., Kazanietz, M. G., Blumberg, P. M., & Hurley, J. H. (1995). Crystal structure of the Cys2 activator-binding domain of protein kinase Cδ in complex with phorbol ester. Cell, 81, 917-924.