GRID and docking analyses reveal a molecular basis for flavonoid inhibition of Src family kinase activity

Journal of Nutritional Biochemistry

Volumn 26, Issue 11, 2015, Pages 1156-1165

  Wright, Bernice ^a   Watson, Kimberly A ^a   McGuffin, Liam J ^a   Lovegrove, Julie A ^b   Gibbins, Jonathan M ^a  

^a Institute for Cardiovascular and Metabolic Research   (United Kingdom)

^b UNIVERSITY OF READING   (United Kingdom)

Author keywords

Anti platelet agents and flavonoids; Cardiovascular disease and flavonoids; Flavonoid computational studies; Flavonoid molecular templates; GRID; Selective flavonoid based analogues; Sybyl docking

Indexed keywords

APIGENIN; CATECHIN; FLAVONOID; HEMATOPOIETIC CELL KINASE; PROTEIN KINASE FYN; PROTEIN KINASE LYN; PROTEIN TYROSINE KINASE; QUERCETIN; ADENOSINE TRIPHOSPHATE; HCK PROTEIN, HUMAN; LYN PROTEIN-TYROSINE KINASE; PROTEIN KINASE INHIBITOR;

ALGORITHM; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HYDROGEN BOND; IN VITRO STUDY; MOLECULAR DOCKING; MOLECULAR INTERACTION; NORMAL HUMAN; X RAY CRYSTALLOGRAPHY; ANTAGONISTS AND INHIBITORS; BINDING SITE; CHEMISTRY; METABOLISM; PRECLINICAL STUDY; PROCEDURES; PROTEIN DOMAIN; STRUCTURE ACTIVITY RELATION;

ADENOSINE TRIPHOSPHATE; APIGENIN; BINDING SITES; CATECHIN; DRUG EVALUATION, PRECLINICAL; FLAVONOIDS; HUMANS; MOLECULAR DOCKING SIMULATION; PROTEIN DOMAINS; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-HCK; QUERCETIN; SRC-FAMILY KINASES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84946485084     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2015.05.004     Document Type: Article

References (64)

1. Oak M.H., Chataigneau M., Keravis T., Chataigneau T., Beretz A., Andriantsitohaina R, et al. Red wine polyphenolic compounds inhibit vascular endothelial growth factor expression in vascular smooth muscle cells by preventing the activation of the p38 mitogen-activated protein kinase pathway. Arterioscler Thromb Vasc Biol 2003, 23:1001-1007.
2. Lang Y., Chen D., Li D., Zhu M., Xu T., Zhang T, et al. Luteolin inhibited hydrogen peroxide-induced vascular smooth muscle cells proliferation and migration by suppressing the Src and Akt signalling pathways. J Pharm Pharmacol 2012, 64:597-603.
3. Kobuchi H., Roy S., Sen C.K., Nguyen H.G., Packer L. Quercetin inhibits inducible ICAM-1 expression in human endothelial cells through the JNK pathway. Am J Physiol 1999, 277:C403-C411.
4. Peng A., Ye T., Rakheja D., Tu Y., Wang T., Du Y, et al. The green tea polyphenol (-)-epigallocatechin-3-gallate ameliorates experimental immune-mediated glomerulonephritis. Kidney Int 2011, 80:601-611.
5. Babu P.V., Si H., Fu Z., Zhen W., Liu D. Genistein prevents hyperglycemia-induced monocyte adhesion to human aortic endothelial cells through preservation of the cAMP signaling pathway and ameliorates vascular inflammation in obese diabetic mice. J Nutr 2012, 142:724-730.
6. Wu C.H., Wu C.F., Huang H.W., Jao Y.C., Yen G.C. Naturally occurring flavonoids attenuate high glucose-induced expression of proinflammatory cytokines in human monocytic THP-1 cells. Mol Nutr Food Res 2009, 53:984-995.
7. Maeda-Yamamoto M., Inagaki N., Kitaura J., Chikumoto T., Kawahara H., Kawakami Y, et al. O-Methylated catechins from tea leaves inhibit multiple protein kinases in mast cells. J Immunol 2004, 172:4486-4492.
8. Bucki R., Pastore J.J., Giraud F., Sulpice J.C., Janmey P.A. Flavonoid inhibition of platelet procoagulant activity and phosphoinositide synthesis. J Thromb Haemost 2003, 1:1820-1828.
9. Briggs W.H., Folts J.D., Osman H.E., Goldman I.L. Administration of raw onion inhibits platelet-mediated thrombosis in dogs. J Nutr 2001, 131:2619-2622.
10. Navarro-Nuñez L., Lozano M.L., Palomo M., Martinez C., Vicente V., Castillo J, et al. Apigenin inhibits platelet adhesion and thrombus formation and synergises with aspirin in the suppression of the arachidonic acid pathway. J Agric Food Chem 2008, 56:2970-2976.
11. Sano T., Oda E., Yamashita T., Naemura A., Ijiri Y., Yamakoshi J, et al. Anti-thrombotic effect of proanthocyanidin, a purified ingredient of grape seed. Thromb Res 2005, 115:115-121.
12. Pawlikowska-Pawlega B., Gruszecki W.I., Misiak L., Paduch R., Piersiak T., Zarzyka B, et al. Modification of membranes by quercetin, a naturally occurring flavonoid, via its incorporation into the polar head group. Biochim Biophys Acta 1768, 2007:2195-2204.
13. Wright B., Moraes L.A., Kemp C.F., Mullen W., Crozier A., Lovegrove JA, et al. A structural basis for the inhibition of collagen-stimulated platelet function by quercetin and structurally related flavonoids. Br J Pharmacol 2010, 159:1312-1325.
14. Wright B., Gibson T., Spencer J., Lovegrove J.A., Gibbins J.M. Platelet-mediated metabolism of the common dietary flavonoid, quercetin. PLoS One 2010, 5:e9673.
15. Gryglewski R.J., Korbut R., Robak J., Swies J. On the mechanism of antithrombotic action of flavonoids. Biochem Pharmacol 1987, 36:317-322.
16. Fiorani M., Accorsi A., Cantoni O. Human red blood cells as a natural flavonoid reservoir. Free Radic Res 2003, 37:1331-1338.
17. Lill G., Voit S., Schror K., Weber A.A. Complex effects of different green tea catechins on human platelets. FEBS Lett 2003, 546:265-270.
18. Hubbard G.P., Stevens J.M., Cicmil M., Sage T., Jordan P.A., Williams CM, et al. Quercetin inhibits collagen-stimulated platelet activation through inhibition of multiple components of the glycoprotein VI signalling pathway. J Thromb Haemost 2003, 1:1079-1088.
19. Zhang Y., Han G., Fan B., Zhou Y., Zhou X., Wei L, et al. Green tea (-)-epigallocatechin-3-gallate down-regulates VASP expression and inhibits breast cancer cell migration and invasion by attenuating Rac1 activity. Eur J Pharmacol 2009, 606:172-179.
20. Peluso M.R. Flavonoids attenuate cardiovascular disease, inhibit phosphodiesterase, and modulate lipid homeostasis in adipose tissue and liver. Exp Biol Med 2006, 231:1287-1299.
21. Deana R., Turetta L., Donella-Deana A., Donà M., Brunati A.M., De Michiel L, et al. Green tea epigallocatechin-3-gallate inhibits platelet signalling pathways triggered by both proteolytic and non-proteolytic agonists. Thromb Haemost 2003, 89:866-874.
22. Agullo G., Gamet-Payrastre L., Manenti S., Viala C., Remesy C., Chap H, et al. Relationship between flavonoids structure and inhibition of phosphatidylinositol 3-kinase: A comparison with tyrosine kinase and protein kinase C inhibition. Biochem Pharmacol 1997, 53:1649-1657.
23. Gamet-Payrastre L., Manenti S., Gratacap M.P., Tulliez J., Chap H., Payrastre B Flavonoids and the inhibition of PKC and PI 3-kinase. Gen Pharmacol 1999, 32:279-286.
24. Holder S., Zemskova M., Zhang C., Tabrizizad M., Bremer R., Neidigh JW, et al. Characterisation of a potent and selective small-molecule inhibitor of the PIM1 kinase. Mol Cancer Ther 2007, 6:163-172.
25. Hagiwara M., Inoue S., Tanaka T., Nunoki K., Ito M., Hidaka H Differential effects of flavonoids as inhibitors of tyrosine protein kinases and serine/threonine protein kinases. Biochem Pharmacol 1988, 37:2987-2992.
26. Cochet C., Feige J.J., Pirollet F., Keramidas M., Chambaz E.M. Selective inhibition of a cyclic nucleotide independent protein kinase (G-type casein kinase) by quercetin and related polyphenols. Biochem Pharmacol 1982, 31:157-1361.
27. Walker E.H., Pacold M.E., Perisic O., Stephens L., Hawkins P.T., Wymann MP, et al. Structural determinants of phosphoinositide 3-kinase inhibition by wortmannin, LY294002, quercetin, myricetin and staurosporine. Mol Cell 2000, 6:909-919.
28. Jung S.K., Lee K.W., Kim H.Y., Oh M.H., Byun S., Lim SH, et al. Myricetin suppresses UVB-induced wrinkle formation and MMP-9 expression by inhibiting Raf. Biochem Pharmacol 2010, 79:1455-1461.
29. Davies S.P., Reddy H., Caivano M., Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 2000, 351:95-105.
30. Hubbard G.P., Wolffram S., Lovegrove J.A., Gibbins J.M. Ingestion of quercetin inhibits platelet aggregation and essential components of the collagen-stimulated platelet activation pathway in humans. J Thromb Haemost 2004, 2:2138-2145.
31. Hubbard G.P., Wolffram S., Gibbins J.M., Lovegrove J.A. Ingestion of onion soup high in quercetin inhibits platelet aggregation and essential components of the collagen-stimulated platelet activation pathways in man: A pilot study. Br J Nutr 2006, 96:482-488.
32. Freedman J.E., Parker C., Li L., Perlman J.A., Frei B., Ivanov V, et al. Select flavonoids and whole juice from purple grapes inhibit platelet function and enhance nitric oxide release. Circulation 2001, 103:2792-2798.
33. Pignatelli P., Ghiselli A., Buchetti B., Carnevale R., Natella F., Germanò G, et al. Polyphenols synergistically inhibit oxidative stress in subjects given red and white wine. Atherosclerosis 2006, 188:77-83.
34. Pignatelli P., Pulcinelli F.M., Celestini A., Lenti L., Ghiselli A., Gazzaniga PP, et al. The flavonoids quercetin and catechin synergistically inhibit platelet function by antagonizing the intracellular production of hydrogen peroxide. Am J Clin Nutr 2000, 72:1150-1155.
35. Sicheri F., Moarefi I., Kuriyan J. Crystal structure of the Src family tyrosine kinase Hck. Nature 1997, 385:602-609.
36. Plaper A., Golob M., Hafner I., Oblak M., Solmajer T., Jerala R, et al. Characterization of quercetin binding site on DNA gyrase. Biochem Biophys Res Commun 2003, 306:530-536.
37. Cuccioloni M., Mozzicafreddo M., Bonfili L., Cecarini V., Eleuteri A.M., Angeletti M, et al. Natural occurring polyphenols as template for drug design. Focus on serine proteases. Chem Biol Drug Des 2009, 74:1-15.
38. Lambert C., Leonard N., De Bolle X., Depiereux E. ESyPred3D: Prediction of proteins 3D structures. Bioinformatics 2002, 18:1250-1256.
39. Park H., Bhattarai B.R., Ham S.W., Cho H. Structure-based virtual screening approach to identify novel classes of PTP1B inhibitors. Eur J Med Chem 2009, 44:3280-3284.
40. McGuffin L.J. Prediction of global and local model quality in CASP8 using the ModFOLD server. Proteins Struct Funct Bioinform 2009, 77:185-190.
41. Pastor M., Cruciani G. A novel strategy for improving ligand selectivity in receptor-based drug design. J Med Chem 1995, 38:4637-4647.
42. McGuffin L.J., Buenavista M.T., Roche D.B. The ModFOLD4 server for the quality assessment of 3D protein models. Nucleic Acids Res 2013, 10.1093/nar/gkt294.
43. Pettitt C.S., McGuffin L.J., Jones D.T. Improving sequenced based fold recognition by use of 3D model quality assessment. Bioinformatics 2005, 21:3509-3515.
44. Park H., Li M., Choi J., Cho H., Ham S.W. Structure-based virtual screening approach to identify novel classes of Cdc25B phosphatase inhibitors. Bioorg Med Chem Lett 2009, 19:4372-4375.
45. Howlin B.J., Tomkinson N.P., Chen J., Webb G.A. Design of potential angiogenin inhibitors. J Comput Aided Mol Des 1994, 8:223-230.
46. Ahmed A., Choo H., Cho Y.S., Park W.K., Pae A.N. Identification of novel serotonin 2C receptor ligands by sequential virtual screening. Bioorg Med Chem 2009, 17:4559-4568.
47. Takeda-Shitaka M., Takaya D., Chiba C., Tanaka H., Umeyama H. Protein structure prediction in structure based drug design. Curr Med Chem 2004, 11:551-558.
48. Goodford P.J. A computational procedure for determining energetically favorable binding sites on biologically important macromolecules. J Med Chem 1985, 28:849-857.
49. Hevener K.E., Zhao W., Ball D.M., Babaoglu K., Qi J., White SW, et al. Validation of molecular docking programs for virtual screening against dihydropteroate synthase. J Chem Inf Model 2009, 49:444-460.
50. Lu H., Chang D.J., Baratte B., Meijer L., Schulze-Gahmen U. Crystal structure of a human cyclin-dependent kinase 6 complex with a flavonol inhibitor, fisetin. J Med Chem 2005, 48:737-743.
51. Byun S., Park J., Lee E., Lim S., Yu J.G., Lee SJ, et al. Src kinase is a direct target of apigenin against UVB-induced skin inflammation. Carcinogenesis 2012, 34:397-405.
52. Gradisar H., Pristovsek P., Plaper A., Jerala R. Green tea catechins inhibit bacterial DNA gyrase by interaction with its ATP binding site. J Med Chem 2007, 50:264-271.
53. Kim J.A., Formoso G., Li Y., Potenza M.A., Marasciulo F.L., Montagnani M, et al. Epigallocatechin gallate, a green tea polyphenol, mediates NO-dependent vasodilation using signaling pathways in vascular endothelium requiring reactive oxygen species and Fyn. J Biol Chem 2007, 282:13736-13745.
54. He Z., Tang F., Ermakova S., Li M., Zhao Q., Cho YY, et al. Fyn is a novel target of (-)-epigallocatechin gallate in the inhibition of JB6 C141 cell transformation. Mol Carcinog 2008, 47:172-183.
55. Liu Y.C., Yang Z.Y., Du J., Yao X.J., Lei R.X., Zheng XD, et al. Study of the interactions of kaempferol and quercetin with intravenous immunoglobulin by fluorescence quenching, fourier transformation infrared spectroscopy and circular dichroism spectroscopy. Chem Pharm Bull (Tokyo) 2008, 56:443-445.
56. Hou D.X., Kumamoto T. Flavonoids as protein kinase inhibitors for cancer chemoprevention: Direct binding and molecular modeling. Antioxid Redox Signal 2010, 13:691-719.
57. Johnson J.L., Rupasinghe S.G., Stefani F., Schuler M.A., Gonzalez de Mejia E. Citrus flavonoids luteolin, apigenin, and quercetin inhibit glycogen synthase kinase-3β enzymatic activity by lowering the interaction energy within the binding cavity. J Med Food 2011, 14:325-333.
58. Matter W.F., Brown R.F., Vlahos C.J. The inhibition of phosphatidylinositol 3-kinase by quercetin and analogs. Biochem Biophys Res Commun 1992, 186:624-631.
59. Huang H., Jia Q., Ma J., Qin G., Chen Y., Xi Y, et al. Discovering novel quercetin-3-O-amino acid-esters as a new class of Src tyrosine kinase inhibitors. Eur J Med Chem 2009, 44:1982-1989.
60. Vlahos C.J., Matter W.F., Hui K.Y., Brown R.F. A specific inhibitor of phosphatidylinositol-3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J Biol Chem 1994, 269:5241-5248.
61. Goettert M., Schattel V., Koch P., Merfort I., Laufer S. Biological evaluation and structural determinants of p38α mitogen-activated-protein kinase and c-Jun-N-terminal kinase 3 inhibition by flavonoids. Chembiochem 2010, 11:2579-2588.
62. Hwang M.K., Kang N.J., Heo Y.S., Lee K.W., Lee H.J. Fyn kinase is a direct molecular target of delphinidin for the inhibition of cyclooxygenase-2 expression induced by tumor necrosis factor-alpha. Biochem Pharmacol 2009, 77:1213-1222.
63. Traxler P., Green J., Mett H., Sequin U., Furet P. Use of a pharmacophore model for the design of EGFR tyrosine kinase inhibitors: Isoflavones and 3-phenyl-4(1H)-quinolines. J Med Chem 1999, 42:1018-1026.
64. McGuffin L.J. The ModFOLD server for the quality assessment of protein structural models. Bioinformatics 2008, 24:586-587.