Class i phospho-inositide-3-kinases (PI3Ks) isoform-specific inhibition study by the combination of docking and molecular dynamics simulation

Journal of Chemical Information and Modeling

Volumn 50, Issue 1, 2010, Pages 136-145

  Han, Ming ^a   Zhang, John Z H ^b,c  

^a NANJING UNIVERSITY   (China)

^b EAST CHINA NORMAL UNIVERSITY   (China)

^c NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMES;

CLUSTERING ANALYSIS; COMPARATIVE ANALYSIS; DYNAMIC BEHAVIORS; LIPID KINASE; MOLECULAR DYNAMICS SIMULATIONS; PHARMACOPHORE MODELING; PROTEIN FLEXIBILITY; SPECIFIC SELECTIVITY;

MOLECULAR DYNAMICS;

2 MORPHOLINO 8 PHENYLCHROMONE; 2-(4-MORPHOLINYL)-8-PHENYL-4H-1-BENZOPYRAN-4-ONE; APOENZYME; CHROMONE DERIVATIVE; ENZYME INHIBITOR; ISOENZYME; MORPHOLINE DERIVATIVE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE GAMMA; PHOSPHATIDYLINOSITOL 3-KINASE GAMMA; PYRIDINE; PYRIDINE DERIVATIVE; WATER;

ARTICLE; CHEMISTRY; DRUG ANTAGONISM; ENZYME SPECIFICITY; HUMAN; METABOLISM; MOLECULAR DYNAMICS; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; SOLUTION AND SOLUBILITY; X RAY CRYSTALLOGRAPHY;

1-PHOSPHATIDYLINOSITOL 3-KINASE; APOENZYMES; CHROMONES; CRYSTALLOGRAPHY, X-RAY; ENZYME INHIBITORS; HUMANS; ISOENZYMES; MOLECULAR DYNAMICS SIMULATION; MORPHOLINES; PROTEIN STRUCTURE, TERTIARY; PYRIDINES; SEQUENCE HOMOLOGY, AMINO ACID; SOLUTIONS; SUBSTRATE SPECIFICITY; WATER;

EID: 75749088885     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci900175n     Document Type: Article

References (54)

1. Stein, R. C.; Waterfield, M. D. PI3-kinase inhibition: a target for drag development. Mol. Med. Today 2000, 6, 347-358.
2. Framan, D. A.; Meyers, R. E.; Cantley, L. C. Phosphoinositide Kinases. Annu. Rev. Biochem. 1998, 67, 481-507.
3. Rodriguez-Viciana, P.; Warne, P. H.; Dhand, R.; Vanhaesebroeck, B.; Gout, I.; Fry, M. J.; Waterfield, M. D.; Downward, J. Phosphatidylinositol-3-OH kinase direct target of Ras. Nature 1994, 370, 527-532. (Pubitemid 24264918)
4. Vivanco, I.; Sawyers, C. L. The phosphatidylinositol 3-Kinase-AKT pathway in human cancer. Nat. Rev. Cancer 2002, 2, 489-501.
5. Vanhaesebroeck, B.; Waterfield, M. D. Signaling by Distinct Classes of Phosphoinositide 3-Kinases. Exp. Cell Res. 1999, 253, 239-254.
6. Domin, J.; Waterfield, M. D. Using structure to define the function of phosphoinositide 3-kinase family members. FEBS Lett. 1997, 410, 91-95. (Pubitemid 27283391)
7. Chang, H. W.; Aoki, M.; Framan, D.; Auger, K. R.; Bellacosa, A.; Tsichlis, P. N.; Cantley, L. C.; Roberts, T. M.; Vogt, P. K. Transformation of Chicken Cells by the Gene Encoding the Catalytic Subunit of PI 3-Kinase. Science 1997, 276, 1848-1850. (Pubitemid 27443659)
8. Li, J.; Yen, C.; Liaw, D.; Podsypanina, K.; Bose, S.; Wang, S. I.; Puc, J.; Miliaresis, C.; Rodgers, L.; McCombie, R.; Bigner, S. H.; Giovanella, B. C.; Ittmann, M.; Tycko, B.; Hibshoosh, H.; Wigler, M. H.; Parsons, R. PTEN a Putative Protein Tyrosine Phosphatase Gene Mutated in Human Brain, Breast, and Prostate Cancer. Science 1997, 275, 1943-1947.
9. Sansal, I.; Sellers, W. R. The Biology and Clinical Relevance of the PTEN Tumor Suppressor Pathway. J. Clin. Oncol. 2004, 22, 2954-2963.
10. Steck, P. A.; Pershouse, M. A.; Jasser, S. A.; Yung, W. K. A.; Lin, H.; Ligon, A. H.; Langford, L. A.; Baumgard, M. L.; Hattier, T.; Davis, T.; Frye, C.; Hu, R.; Swedlund, B.; Teng, D. H. R.; Tavtigian, S. V. Identification of a candidate tumour suppressor gene, MMACl, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nat. Genet. 1997, 15, 356-362.
11. Samuels, Y.; Diaz Jr, L. A.; Schmidt-Kittler, O.; Cummins, J. M.; DeLong, L.; Cheong, I.; Rago, C.; Huso, D. L.; Lengauer, C.; Kinzler, K. W.; Vogelstein, B.; Velculescu, V. E. Mutant PIK3CA promotes cell growth and invasion of human cancer cells. Cancer Cell 2005, 7, 561-573. (Pubitemid 40799249)
12. Samuels, Y.; Wang, Z.; Bardelli, A.; Silliman, N.; Ptak, J.; Szabo, S.; Yan, H.; Gazdar, A.; Powell, S. M.; Riggins, G. J.; Willson, J. K. V.; Markowitz, S.; Kinzler, K. W.; Vogelstein, B.; Velculescu, V. E. High Frequency of Mutations of the PIK3CA Gene in Human Cancers. Science 2004, 304, 554.
13. Marone, R.; Cmiljanovic, V.; Giese, B.; Wymann, M. P. Targeting phosphoinositide 3-kinase-Moving towards therapy. BBA 2008, 1784, 159-185.
14. Knight, Z. A.; Gonzalez, B.; Feldman, M. E.; Zunder, E. R.; Goldenberg, D. D.; Williams, O.; Loewith, R.; Stokoe, D.; Baila, A.; Toth, B.; Baila, T.; Weiss, W. A.; Williams, R. L.; Shokat, K. M. A Pharmacological Map of the PI3-K Family Defines a Role for p110α in Insulin Signaling. Cell 2006, 125, 733-747.
15. Knight, Z. A.; Shokat, K. M. Chemically targeting the PI3K family. Biochem. Soc. Trans. 2007, 35, 245-249.
16. Amzel, L. M.; Huang, C.-H.; Mandelker, D.; Lengauer, C.; Gabelli, S. B.; Vogelstein, B. Structural comparisons of class I phosphoinositide 3-kinases. Nat. Rev. Cancer 2008, 8, 665-669.
17. Zvelebil, M. J.; Waterfield, M. D.; Shuttleworth, S. J. Structural analysis of PI3-kinase isoforms: Identification of residues enabling selective inhibition by small molecule ATP-competitive inhibitors. Arch. Biochem. Biophys. 2008, 477, 404-410.
18. Frederick, R.; Denny, W. A. Phosphoinositide-3-kinases (PDKs): Combined Comparative Modeling and 3D-QSAR to Rationalize the Inhibition of p110α. Chem. Inf. Model. 2008, 48, 629-638.
19. Cheng, L. S.; Amaro, R. E.; Xu, D.; Li, W. W.; Arzberger, P. W.; McCammon, J. A. Ensemble-Based Virtual Screening Reveals Potential Novel Antiviral Compounds for Avian Influenza Neuraminidase. J. Med. Chem. 2008, 51, 3878-3894.
20. Carlson, H. A.; Masukawa, K. M.; Rubins, K.; Bushman, F. D.; Jorgensen, W. L.; Lins, R. D.; Briggs, J. M.; McCammon, J. A. Developing a dynamic pharmacophore model for HIV-1 integrase. J. Med. Chem. 2000, 43 (11), 2100-2114.
21. Kua, J.; Zhang, Y.; McCammon, J. A. Studying enzyme binding specificity in acetylcholinesterase using a combined molecular dynamics and multiple docking approach. J. Am. Chem. Soc. 2002, 124 (28), 8260-8267.
22. Lin, J. H.; Perryman, A. L.; Schames, J. R.; McCammon, J. A. Computational drug design accommodating receptor flexibility: the relaxed complex scheme.J. Am. Chem. Soc. 2002, 124 (20), 5632-5633.
23. Cavasotto, C. N.; Abagyan, R. A. Protein flexibility in ligand docking and virtual screening to protein kinases.J. Mol. Biol. 2004, 337 (1), 209-225. (Pubitemid 38270258)
24. Cavasotto, C. N.; Kovacs, J. A.; Abagyan, R. A. Representing receptor flexibility in ligand docking through relevant normal modes.J. Am. Chem. Soc. 2005, 127 (26), 9632-9640.
25. Sherman, W.; Day, T.; Jacobson, M. P.; Friesner, R. A.; Farid, R. Novel procedure for modeling ligand/receptor induced fit effects. J. Med. Chem. 2006, 49 (2), 534-553. (Pubitemid 43157487)
26. Damm, K. L.; Carlson, H. A. Exploring experimental sources of multiple protein conformations in structure-based drag design.J. Am. Chem. Soc. 2007, 129 (26), 8225-8235.
27. Walker, E. H.; Pacold, M. E.; Perisic, O.; Stephens, L.; Hawkins, P. T.; Wymann, M. P.; Williams, R. L. Structural Determinants of Phosphoinositide 3-Kinase Inhibition by Wortmannin, LY294002, Quercetin, Myricetin, and Staurosporine. Mol. Cell. 2000, 6, 909-919.
28. Apsel, B.; Blair, J. A.; Gonzalez, B.; Nazif, T. M.; Feldman, M. E.; Aizenstein, B.; Hoffman, R.; Williams, R. L.; Shokat, K. M.; Knight, Z. A. Targeted polypharmacology: discovery of dual inhibitors of tyrosine and phosphoinositide kinases. Nat. Chem. Biol. 2008, 4, 691-699.
29. Huang, C.-H.; Mandelker, D.; Schmidt-Kittler, O.; Samuels, Y.; Velculescu, V. E.; Kinzler, K. W.; Vogelstein, B.; Gabelli, S. B.; Amzel, L. M. The Structure of a Human p110α/p85α Complex Elucidates the Effects of Oncogenic PI3Kα Mutations. Science 2007, 318, 1744-1748.
30. Hayakawa, M.; Kawaguchi, K.-i.; Kaizawa, H.; Koizumi, T.; Ohishi, T.; Yamano, M.; Okada, M.; Ohta, M.; Tsukamoto, S.-i.; Raynaud, F. I.; Parker, P.; Workman, P.; Waterfield, M. D. Synthesis and biological evaluation of sulfonylhydrazone-substituted imidazo[1,2-a]pyridines as novel PI3 kinase p110[alpha] inhibitors. Bioorgan. Med. Chem. 2007, 15, 5837-5844.
31. Sali, A.; Blundell, T. L. Comparative Protein Modelling by Satisfaction of Spatial Restraints.J. Mol. Biol. 1993, 234, 779-815.
32. Andrάs, F.; Richard Kinh Gian, D.; Andrej, S. Modeling of loops in protein structures. Protein Sci. 2000, 9, 1753-1773.
33. Gaussian 03, Revision D.01; Gaussian, Inc.: Wallingford, CT, 2004.
34. Garrett, M. M.; David, S. G.; Robert, S. H.; Ruth, H.; William, E. H.; Richard, K. B.; Arthur, J. O. Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J. Comput. Chem. 1998, 19, 1639-1662.
35. Ruth, H.; Garrett, M. M.; Arthur, J. O.; David, S. G. A semiempirical free energy force field with charge-based desolvation.J. Comput. Chem. 2001, 28, 1145-1152.
36. Michel, F. Sanner. Python: A Programming Language for Software Integration and Development.J. Mol. Graph. Model. 1999, 17, 57-61.
37. Gasteiger, J.; Marsili, M. Iterative partial equalization of orbital electronegativity--a rapid access to atomic charges. Tetrahedron 1980, 36 (22), 3219-3228.
38. Case, D. A.; Darden, T. A.; Cheatham, T. E., III; Simmerling, C. L.; Wang, J.; Duke, R. E.; Luo, R.; Crowley, M.; Walker, R. C.; Zhang, W.; Merz, K. M.; Wang, B.; Hayik, S.; Roitberg, A.; Seabra, G.; Kolossváry, I.; Wong, K. F.; Paesani, F.; Vanicek, J.; Wu, X.; Brozell, S. R.; Steinbrecher, T.; Gohlke, H.; Yang, L.; Tan, C.; Mongan, J.; Hornak, V.; Cui, G.; Mathews, D. H. Seetin, M. G.; Sagui, C.; Babin, V.; Kollman, P. A. AMBER 10; University of California: San Francisco, 2008.
39. Viktor, H.; Robert, A.; Asim, O.; Bentley, S.; Adrian, R.; Carlos, S. Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 2006, 65, 712-725.
40. Junmei, W.; Romain, M. W.; James, W. C.; Peter, A. K.; David, A. C. Development and testing of a general amber force field. J. Comput. Chem. 2004, 25, 1157-1174.
41. Jakalian, A.; Bush, B. L.; Jack, D. B.; Bayly, C. I. Fast, efficient generation of high-quality atomic charges. AM1-BCC model: I. Method. J. Comput. Chem. 2000, 21, 132-146.
42. Jakalian, A.; Jack, D. B.; Bayly, C. I. Fast, efficient generation of high-quality atomic charges. AM1-BCC model: II. Parameterization and Validation. J. Comput. Chem. 2002, 23, 1623-1641.
43. Darden, T.; York, D.; Pedersen, L. Particle mesh Ewald: An N-log(N) method for Ewald sums in large systems. J. Chem. Phys. 1993, 98, 10089-10092.
44. Pastor, R. W.; Brooks, B. R.; Szabo, A. An analysis of the accuracy of Langevin and molecular dynamics algorithms. Mol. Phys. 1988, 65, 1409-1419.
45. Loncharich, R. J.; Brooks, B. R.; Pastor, R. W. Langevin dynamics of peptides: The frictional dependence of isomerization rates of N-actylananyl-N'-methylamide. Biopolymers 1992, 32, 523-535.
46. Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.; DiNola, A.; Haak, J. R. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 1984, 81, 3684-3690.
47. Ryckaert, J.-P.; Ciccotti, G.; Berendsen, H. J. C. Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys. 1977, 23, 327-341.
48. Miyamoto, S.; Kollman, P. A. Settle: An analytical version of the SHAKE and RATTLE algorithm for rigid water models. J. Comput. Chem. 1992, 13, 952-962.
49. Kendall, J. D.; Rewcastle, G. W.; Frederick, R.; Mawson, C.; Denny, W. A.; Marshall, E. S.; Baguley, B. C.; Chaussade, C.; Jackson, S. P.; Shepherd, P. R. Synthesis, biological evaluation and molecular modelling of sulfonohydrazides as selective PI3K p110α inhibitors. Bioorg. Med. Chem. 2007, 15, 7677-7687.
50. Brunger, A. T.; Adams, P. D.; Clore, G. M.; DeLano, W. L.; Gros, P.; Grosse-Kunstleve, R. W.; Jiang, J. S.; Kuszewski, J.; Nilges, M.; Pannu, N. S.; Read, R. J.; Rice, L. M.; Simonson, T.; Warren, G. L. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr., Sect. D 1998, 54, 905-921.
51. Camps, M.; Ruckle, T.; Ji, H.; Ardissone, V.; Rintelen, F.; Shaw, J.; Ferrandi, C.; Chabert, C.; Gillieron, C.; Francon, B.; Martin, T.; Gretener, D.; Perrin, D.; Leroy, D.; Vitte, P.-A.; Hirsch, E.; Wymann, M. P.; Cirillo, R.; Schwarz, M. K.; Rommel, C. Blockade of PI3Kγ suppresses joint inflammation and damage in mouse models of rheumatoid arthritis. Nat. Med. 2005, 11, 936-943.
52. Yung-Chi, C.; Prasoff, W. H. Relationship between the inhibition constant (KI) and the concentration of inhibitor which causes 50% inhibition (150) of an enzymatic reaction. Biochem. Pharmacol. 1973, 22, 3099-3108.
53. Chaussade, C.; Rewcastle, G. W.; Kendall, J. D.; Denny, W. A.; Cho, K.; Gronning, L. M.; Chong, M. L.; Anagnostou, S. H.; Jackson, S. P.; Daniele, N.; Shepherd, P. R. Evidence for functional redundancy of class IA PI3K isoforms in insulin signalling. Biochem. J. 2007, 404, 449-458.
54. Vulpetti, A.; Bosotti, R. Sequence and structural analysis of kinase ATP pocket residues. Il Farmaco 2004, 59, 759-765. CI900175N