Transinactivation of the epidermal growth factor receptor tyrosine kinase and focal adhesion kinase phosphorylation by dietary flavonoids: Effect on invasive potential of human carcinoma cells

Biochemical Pharmacology

Volumn 67, Issue 11, 2004, Pages 2103-2114

  Lee, Lung Ta ^a,f   Huang, Ying Tang ^a   Hwang, Jiuan Jiuan ^b   Lee, Amy Y L ^c   Ke, Ferng Chun ^d   Huang, Chang Jen ^a   Kandaswami, Chithan ^e   Lee, Ping Ping H ^a   Lee, Ming Ting ^a  

^a INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c DUKE UNIVERSITY   (United States)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^e UNIVERSITY AT BUFFALO   (United States)

^f TOKO UNIVERSITY   (Taiwan)

Author keywords

dimethyl sulphoxide; DMSO; ECL; EGF; enhanced chemiluminescence; epidermal growth factor; FAK; focal adhesion kinase; matrix metalloproteinase; MMP; protein tyrosine kinase; PTK; SDS PAGE; sodium dodecyl sulphate polyacrylamide gel electrophoresis

Indexed keywords

ANTINEOPLASTIC AGENT; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE; FLAVONOID; FOCAL ADHESION KINASE; LUTEOLIN; MATRIX METALLOPROTEINASE; PROTEIN TYROSINE KINASE INHIBITOR; QUERCETIN; WOGONIN;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER INVASION; CARCINOMA CELL; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MOLECULAR BIOLOGY; PRIORITY JOURNAL; PROTEIN SECRETION; SIGNAL TRANSDUCTION; TARGET CELL DESTRUCTION;

CARCINOMA; CELL MOVEMENT; DIET; EPIDERMAL GROWTH FACTOR; FLAVONOIDS; FOCAL ADHESION KINASE 1; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GENE EXPRESSION; HUMANS; LUTEOLIN; MATRIX METALLOPROTEINASES; NEOPLASM INVASIVENESS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; QUERCETIN; RECEPTOR, EPIDERMAL GROWTH FACTOR; SUBCELLULAR FRACTIONS; TRANS-ACTIVATION (GENETICS); TUMOR CELLS, CULTURED; TYROSINE;

EID: 2342543194     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2004.02.023     Document Type: Article

References (46)

1. Liotta L.A., Steeg P.S., Stetler-Stevenson W.G. Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell. 64:1991;327-336
2. Schneider M.R., Schirner M. Antimetastatic prostacyclin analog. Drugs Future. 18:1993;29-48
3. Liabakk N.B., Talbot I., Smith R.A., Wilkinson K., Balkwill F.R. Matrix metalloproteinases 2 (MMP-2) and matrix metalloproteinase 9 (MMP-9) type IV collagenases in colorectal cancer. Cancer Res. 56:1996;190-196
4. Naylor M.S., Stamp G.W., Davies B.D., Balkwill F.R. Expression and activity of MMPs and their regulators in ovarian cancer. Int. J. Cancer. 58:1994;50-56
5. Benaud C., Dickson R.B., Thompson E.W. Roles of the matrix metalloproteinases in mammary gland development and cancer. Breast Cancer Res. Treat. 50:1998;97-116
6. Hua J., Muschel R. Inhibition of matrix metalloproteinase nine expression by a ribozyme blocks metastasis in a rat sarcoma model system. Cancer Res. 56:1996;5279-5284
7. Watson S.A., Morris T.M., Robinson G., Crimmin M.J., Brown P.D., Hardcastle J.D. Inhibition of organ invasion by the metalloproteinase inhibitor Batimastat (BB-94) in two human colon carcinoma metastasis models. Cancer Res. 55:1995;3629-3633
8. Zhang L., Lau Y.K., Xi L., Hong R.L., Kim D.S.H.L., Chang C.J., et al. Tyrosine kinase inhibitors, emodin and its derivative repress Her-2/neu-induced cellular transformation and metastasis-associated properties. Oncogene. 16:1998;2855-2863
9. Llic D., Damsky E., Yamamoto T. Focal adhesion kinase: at the crossroads of a signal transduction. J. Cell Sci. 110:1997;401-407
10. Owens L.V., Xu L., Craven R.J., Dent G.A., Weiner T.M., Kornberg L., et al. Over expression of the focal adhesion kinase (p125FAK) in invasive human tumors. Cancer Res. 55:1995;2752-2755
11. Parsons J.T., Martin K.H., Slack J.K., Taylor J.M., Weed S.A. Focal adhesion kinase: a regulator of focal adhesion dynamics and cell movement. Oncogene. 19:2000;5606-5613
12. Sieg D.J., Hauck C.R., Llic D., Klingbeil C.K., Schaefer E., Damsky C.H., et al. FAK integrates growth-factor and integrin signals to promote cell migration. Nature Cell Biol. 2:2000;249-256
13. Tamura M., Gu J., Matsumoto K., Aota S.I., Parsons R., Yamada K.M. Inhibition of cell migration, spreading, and focal adhesion by tumor suppressor PTEN. Science. 280:1998;1614-1617
14. Gu J., Tamura M., Pankov R., Takino T., Matsumoto K., Yamada K.M. Shc and FAK differentially regulate cell motility and directionality modulated by PTEN. J. Cell Biol. 146:1999;389-404
15. Hsia D.A., Mitra S.K., Hauck C.R., Streblow D.N., Nelson J.A., Ilic D., et al. Differential regulation of cell motility and invasion by FAK. J. Cell Biol. 160:2003;753-767
16. 2-Terminal FAK in the nuclei of apoptotic glioblastoma cells. Cancer Res. 61:2001;4978-4981
17. Harborne JB. The flavonoids: advances in research since 1980. London: Chapman and Hall, 1998.
18. Huang Y.T., Hwang J.J., Lee P.P.H., Ke F.C., Huang J.H., Huang C.J., et al. Effects of luteolin and quercetin, inhibitors of tyrosine kinase, on growth and metastasis-associated properties in A431 cells overexpressing epidermal growth factor receptor. Br. J. Pharmacol. 128:1999;999-1010
19. Hertog M.G.L., Hollom P.C.H., Katan M.B., Kromhout D. Intake of potential anticarcinogenic flavonoids and their determinants in adults in The Netherlands. Nutr. Cancer. 20:1995;21-29
20. Middleton E. Jr., Kandaswami C., Theoharidis T.C. The impact of plant flavonoids on mammalian biology: implications for inflammations. Pharmacol. Rev. 52:2000;673-751
21. Kandaswami C, Middleton E, Jr. Flavonoids as antioxidants. In: Shahihi E, editors. Natural antioxidants. Champagne, Illinois: ACS Press, 1997, pp. 174-203.
22. Sieg D.J., Hauck C.R., Llic D., Klingbeil C.K., Schaefer E., Damsky C.H., Schlaepfer D.D. FAK integrates growth-factor and integrin signals to promote cell migration. Nature Cell Biol. 2:2000;249-256
23. Kappagoda C.T., Karim M., McCormic K., Kandaswami C. Unraveling the French paradox. Chem. Innov. 30(9):2000;26-31
24. Kandaswami C., Perkins E., Soloniuk D.S., Drzewiecki G., Middleton E. Jr. Antiproliferative effects of citrus flavonoids on a human squamous cell carcinoma in vitro. Cancer Lett. 56:1991;147-152
25. Constantinou A., Kiguchi K., Huberman E. Induction of differentiation and DNA strand breakage in human HL-60 and K-562 leukemia cells by genistein. Cancer Res. 50:1990;2618-2624
26. Akiyama T., Ishida J., Nakagawa S., Ogawara H., Watanabe S., Itoh N., et al. Genistein, a specific inhibitor of tyrosine kinases. J. Biol. Chem. 262:1987;5592-5595
27. Sato F., Matsukawa Y., Matsumoto K., Nishino H., Sakai T. Apegenin induces morphological differentiation and G2/M arrest in rat neuronal cells. Biochem. Biophys. Res. Commun. 204:1994;578-584
28. Wei Y.Q., Zhao X., Kariya Y., Fukata H., Teshigawara K., Uchida A. Induction of apoptosis by quercetin: involvement of heat shock protein. Cancer Res. 54:1994;4952-4957
29. Lee L.T., Huang Y.T., Hwang J.J., Lee H.P.P., Ke F.C., Nair M.P., et al. Blockade of the epidermal growth factor receptor tyrosine kinase activity by quercetin and luteolin leads to growth inhibition and apoptosis of pancreatic tumor cells. Anticancer Res. 22:2002;1615-1628
30. Weyant M.J., Carothers A.M., Dannenberg A.J., Bertagnolli M.M. (+)-Catechin inhibits tumor formation and suppresses focal adhesion kinase activation in the min/+mouse. Cancer Res. 61:2001;118-125
31. Lu Z., Jiang G., Blume-Jensen P., Hunter T. Epidermal growth factor-induced tumor cell invasion and metastasis initiated by dephosphorylation and downregulation of focal adhesion kinase. Mol. Cell Biol. 21:2001;4016-4031
32. Mosmann T.J. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity. J. Immunol. Methods. 65:1993;55-63
33. Samuels M.L., Weber M.J., Bishop J.M., McMahon M. Conditional transformation of cells and rapid activation of the mitogen-activated protein kinase cascade by an estradiol-dependent human raf-1 protein kinase. Mol. Cell Biol. 13:1993;6241-6252
34. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the protein-dye binding. Anal Biochem. 72:1976;248-254
35. Lee M.T., Liebow C., Kamer A., Schally A.V. Effect of epidermal growth factor and analogue of luteinizing hormone releasing hormone and somatostatin on phosphorylation and dephosphorylation of tyrosine residues of specific protein substrates in various tumors. Proc. Natl. Acad. Sci. U.S.A. 88:1991;1656-1660
36. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4a. Nature. 227:1970;680-685
37. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from poly-acrylamide gels to nitrocellular sheets: procedure and some application. Proc. Natl. Acad. Sci. U.S.A. 76:1976;4350-4354
38. Heussen C., Dowdle E.B. Electrophoretic analysis of plasminogen activators in polyacrylamide gels containing sodium dodecyl sulfate and copolymerized substrate. Anal Biochem. 102:1980;196-202
39. Saiki K.H., Fuji H., Yoneda J., Abe F., Nakajima M., Tsuruo T., et al. Role of aminopeptidase N(CD13) in tumor-cell invasion and extracellular matrix degradation. Int. J. Cancer. 54:1993;137-143
40. Sieg D.J., Hauck C.R., Schlaepfer D.D. Required role of focal adhesion kinases (FAK) for integrin-stimulated cell migration. J. Cell Sci. 112:1999;2677-2691
41. Hunter T. Oncoprotein networks. Cell. 88:1997;333-346
42. Hauck C.R., Hsia D.A., Schalaepfer D.D. FAK facilitates PDGF-BB stimulated ERK2 activation required for chemotaxis migration of vascular smooth muscle cells. J. Biol. Chem. 275:2000;41092-41099
43. Kyle E., Neckers L., Takimoto C., Curt G., Bergan R. Genistein-induced apoptosis of prostate cancer cells is preceded by a specific decrease in focal adhesion kinase activity. Mol. Pharmacol. 51:1997;193-200
44. Hauck C.R., Sieg D.J., Hsia D.A., Loftus J.C., Garrde W.A., Monia B.P., et al. Inhibition of Focal Adhesion kinase expression or activity disrupts epidermal growth factor-stimulated signaling promoting the migration of invasive human carcinoma cells. Cancer Res. 61:2001;7079-7090
45. Scholar E.M., Toews M.L. Inhibition of invasion of murine mammary carcinoma cells by the tyrosine kinase inhibitor genistein. Cancer Lett. 87:1994;159-162
46. Liu Y., Kyle E., Lieberman R., Crowell J., Kelloff G., Bergan R.C. Focal adhesion kinase (FAK) phosphorylation is not required for genistein-induced FAK-β-1-integrin complex formation. Clin. Exp. Meta. 18:2000;203-212