Understanding the stereospecific interactions of 3-deoxyphosphatidylinositol derivatives with the PTEN phosphatase domain

Journal of Molecular Graphics and Modelling

Volumn 29, Issue 1, 2010, Pages 102-114

  Wang, Qin ^a   Wei, Yang ^a   Mottamal, Madhusoodanan ^a   Roberts, Mary F ^a   Krilov, Goran ^a  

^a BOSTON COLLEGE   (United States)

Author keywords

Apoptosis; Cancer; Molecular dynamics; Phosphatidylinositol; PI3K AKT; PTEN

Indexed keywords

APOPTOSIS; CANCER; PHOSPHATIDYLINOSITOL; PI3K/AKT; PTEN;

BINDING ENERGY; CELL DEATH; CHIRALITY; ENANTIOMERS; HYDROGEN BONDS; LEAD COMPOUNDS; MOLECULAR DYNAMICS; PHOSPHATASES; PROTEINS; STEREOCHEMISTRY; SUGARS;

LIGANDS;

3 DEOXYPHOSPHATIDYLINOSITOL DERIVATIVE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BINDING AFFINITY; CHIRALITY; COMPLEX FORMATION; COMPUTER MODEL; DRUG STRUCTURE; ENZYME ACTIVE SITE; GENE OVEREXPRESSION; GENE TARGETING; HYDROGEN BOND; HYDROPHOBICITY; LIGAND BINDING; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STEREOSPECIFICITY;

BINDING SITES; COMPUTER SIMULATION; INOSITOL; LIGANDS; MODELS, MOLECULAR; PHOSPHATIDYLINOSITOLS; PROTEIN STRUCTURE, TERTIARY; PTEN PHOSPHOHYDROLASE; REPRODUCIBILITY OF RESULTS; STATIC ELECTRICITY; STEREOISOMERISM; SUBSTRATE SPECIFICITY; THERMODYNAMICS;

EID: 77955842614     PISSN: 10933263     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmgm.2010.05.004     Document Type: Article

References (53)

1. Li D.M., Sun H. TEP1, encoded by a candidate tumor suppressor locus, is a novel protein tyrosine phosphatase regulated by transforming growth factor beta. Cancer Res. 1997, 57:2124-2129.
2. Li J., Yen C., Liaw D., Podsypanina K., Bose S., Wang S.I., et al. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 1997, 275:1943-1947.
3. Maehama T., Dixon J.E. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 1998, 273:13375-13378.
4. Myers M.P., Pass I., Batty I.H., Van der Kaay J., Stolarov J.P., Hemmings B.A., et al. The lipid phosphatase activity of PTEN is critical for its tumor suppressor function. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:13513-13518.
5. Steck P.A., Pershouse M.A., Jasser S.A., Yung W.K.A., Lin H., Ligon A.H., et al. Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nat. Genet. 1997, 15:356-362.
6. Barnett S.F., Ledder L.M., Stirdivant S.M., Ahern J., Conroy R.R., Heimbrook D.C. Interfacial catalysis by phosphoinositide 3'-hydroxykinase. Biochemistry 1995, 34:14254-14262.
7. Seufferlein T. Novel protein kinases in pancreatic cell growth and cancer. Int. J. Gastrointest. Cancer 2002, 31:15-21.
8. Vivanco I., Sawyers C.L. The phosphatidylinositol 3-kinase-AKT pathway in human cancer. Nat. Rev. Cancer 2002, 2:489-501.
9. Ghosh P.M., Malik S., Bedolla R., Kreisberg J.I. Akt in prostate cancer: possible role in androgen-independence. Curr. Drug Metab. 2003, 4:487-496.
10. Kim D., Dan H.C., Park S., Yang L., Liu Q.Y., Kaneko S., et al. Akt/PKB signaling mechanisms in cancer and chemoresistance. Front. Biosci. 2005, 10:975-987.
11. Stokoe D.P. Curr. Biol. 2001, 11:R502.
12. Du K., Herzig S., Kulkarni R.N., Montminy M. TRB3: a tribbles homolog that inhibits Akt/PKB activation by insulin in liver. Science 2003, 300:1574-1577.
13. Iida S., Ono A., Sayama K., Hamaguchi T., Fujii H., Nakajima H., et al. Accelerated decline of blood glucose after intravenous glucose injection in a patient with Cowden disease having a heterozygous germline mutation of the PTEN/MMAC1 gene. Anticancer Res. 2000, 20:1901-1904.
14. Stiles B., Wang Y., Stahl A., Bassilian S., Lee W.P., Kim Y.-J., et al. Liver-specific deletion of negative regulator Pten results in fatty liver and insulin hypersensitivity. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:2082-2087.
15. Stiles B.L., Kuralwalla-Martinez C., Guo W., Gregorian C., Wang Y., Tian J., et al. Selective deletion of Pten in pancreatic {beta} cells leads to increased islet mass and resistance to STZ-induced diabetes. Mol. Cell. Biol. 2006, 26:2772-2781.
16. Lai J.P., Shengying B., Ian C.D., Daren L.K. Inhibition of the phosphatase PTEN protects mice against oleic acid-induced acute lung injury. Br. J. Pharmacol. 2009, 156:189-200.
17. Wang Y.K., Chen W., Blair D., Pu M., Xu Y., Miller S.J., et al. Insights into the structural specificity of the cytotoxicity of 3-deoxyphosphatidylinositols. J. Am. Chem. Soc. 2008, 130:7746-7755.
18. Castillo S.S., Brognard J., Petukhov P.A., Zhang C.Y., Tsurutani J., Granville C.A., et al. Preferential inhibition of Akt and killing of Akt-dependent cancer cells by rationally designed phosphatidylinositol ether lipid analogues. Cancer Res. 2004, 64:2782-2792.
19. Lemieux R.U. How water provides the impetus for molecular recognition in aqueous solution. Acc. Chem. Res. 1996, 29:373-380.
20. Tor Y. Targeting RNA with small molecules. ChemBioChem 2003, 4:998-1007.
21. Lee J.-O., Yang H., Georgescu M.-M., Di Cristofano A., Maehama T., Shi Y., et al. Crystal structure of the PTEN tumor suppressor: implications for its phosphoinositide phosphatase activity and membrane association. Cell 1999, 99:323-334.
22. Andresen T.L., Skytte D.M., Madsen R. Synthesis of anti-tumour phosphatidylinositol analogues from glucose by the use of ring-closing olefin metathesis. Org. Biomol. Chem. 2004, 2:2951-2957.
23. Gills J.J., Dennis P.A. The development of phosphatidylinositol ether lipid analogues as inhibitors of the serine/threonine kinase, Akt. Exp. Opin. Invest. Drugs 2004, 13:787-797.
24. Kozikowski A.P., Sun H., Brognard J., Dennis P.A. Novel PI analogues selectively block activation of the pro-survival serine/threonine kinase Akt. J. Am. Chem. Soc. 2003, 125:1144-1145.
25. Campbell R.B., Liu F.H., Ross A.H. Allosteric activation of PTEN phosphatase by phosphatidylinositol 4,5-bisphosphate. J. Biol. Chem. 2003, 278:33617-33620.
26. McConnachie G., Pass I., Walker S.M., Downes P.C. Interfacial kinetic analysis of the tumour suppressor phosphatase. PTEN: evidence for activation by anionic phospholipids. Biochem. J. 2003, 371:947-955.
27. Berendsen H.J.C., Vanderspoel D., Vandrunen R. Gromacs-a message-passing parallel molecular-dynamics implementation. Comput. Phys. Commun. 1995, 91:43-56.
28. Lindahl E., Hess B., van der Spoel D. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. 2001, 7:306-317.
29. Van der Spoel D., Lindahl E., Hess B., Groenhof G., Mark A.E., Berendsen H.J.C. GROMACS: fast, flexible, and free. J. Comput. Chem. 2005, 26:1701-1718.
30. Maestro, Maestro, Schrodinger, LLC, New York, 2008.
31. Jorgensen W.L., Maxwell D.S., TiradoRives J. Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J. Am. Chem. Soc. 1996, 118:11225-11236.
32. Kaminski G.A., Friesner R.A., Tirado-Rives J., Jorgensen W.L. Evaluation and reparametrization of the OPLS-AA force field for proteins via comparison with accurate quantum chemical calculations on peptides. J. Phys. Chem. B 2001, 105:6474-6487.
33. Jorgensen W.L., Chandrasekhar J., Madura J.D., Impey R.W., Klein M.L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 1983, 79:926-935.
34. Essmann U., Perera L., Berkowitz M.L., Darden T., Lee H., Pedersen L.G. A smooth particle mesh ewald method. J. Chem. Phys. 1995, 103:8577-8593.
35. Hoover W.G. Canonical dynamics-equilibrium phase-space distributions. Phys. Rev. A 1985, 31:1695-1697.
36. Berendsen H.J.C., Postma J.P.M., Vangunsteren W.F., Dinola A., Haak J.R. Molecular-dynamics with coupling to an external bath. J. Chem. Phys. 1984, 81:3684-3690.
37. Ghosh A., Rapp C.S., Friesner R.A. Generalized born model based on a surface integral formulation. J. Phys. Chem. B 1998, 102:10983-10990.
38. Prime, Prime, Schrodinger, LLC, New York, 2008.
39. Jaguar, Jaguar, Schrodinger, LLC, New York, 2008.
40. Das S., Dixon J.E., Cho W. Membrane-binding and activation mechanism of PTEN. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:7491-7496.
41. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
42. Jones G., Willett P., Glen R.C., Leach A.R., Taylor R. Development and validation of a genetic algorithm for flexible docking. J. Mol. Biol. 1997, 267:727-748.
43. Novak W., Wang H., Krilov G. Role of protein flexibility in the design of Bcl-XL targeting agents: insight from molecular dynamics. J. Comput. Aided Mol. Des. 2009, 23:49-61.
44. Mancinelli F., Caraglia M., Budillon A., Abbruzzese A., Bismuto E. Molecular dynamics simulation and automated docking of the pro-apoptotic Bax protein and its complex with a peptide designed from the Bax-binding domain of anti-apoptotic Ku70. J. Cell. Biochem. 2006, 99:305-318.
45. Dastidar S.G., Lane D.P., Verma C.S. Multiple peptide conformations give rise to similar binding affinities: molecular simulations of p53-MDM2. J. Am. Chem. Soc. 2008, 130:13514-13515.
46. Huang N., Kalyanaraman C., Bernacki K., Jacobson M.P. Molecular mechanics methods for predicting protein-ligand binding. Phys. Chem. Chem. Phys. 2006, 8:5166-5177.
47. Holger G., David A.C. Converging free energy estimates: MM-PB(GB)SA studies on the protein-protein complex Ras-Raf. J. Comput. Chem. 2004, 25:238-250.
48. Kuhn B., Gerber P., Schulz-Gasch T., Stahl M. Validation and use of the MM-PBSA approach for drug discovery. J. Med. Chem. 2005, 48:4040-4048.
49. Abel R., Young T., Farid R., Berne B.J., Friesner R.A. Role of the active-site solvent in the thermodynamics of factor Xa ligand binding. J. Am. Chem. Soc. 2008, 130:2817-2831.
50. Guimaraes C.R.W., Cardozo M. MM-GB/SA rescoring of docking poses in structure-based lead optimization. J. Chem. Inf. Model. 2008, 48:958-970.
51. Pearlman D.A. Evaluating the molecular mechanics poissonâ' Boltzmann surface area free energy method using a congeneric series of ligands to p38 MAP kinase. J. Med. Chem. 2005, 48:7796-7807.
52. Weis A., Katebzadeh K., Soderhjelm P., Nilsson I., Ryde U. Ligand affinities predicted with the MM/PBSA method: dependence on the simulation method and the force field. J. Med. Chem. 2006, 49:6596-6606.
53. Young T., Abel R., Kim B., Berne B.J., Friesner R.A. Motifs for molecular recognition exploiting hydrophobic enclosure in proteinâ" ligand binding. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:808-813.