Apple polyphenol inhibits colon carcinoma metastasis via disrupting Snail binding to focal adhesion kinase

Journal of Functional Foods

Volumn 12, Issue , 2015, Pages 80-91

  Hung, Chia Hung ^a   Huang, Chi Chou ^a,b   Hsu, Li Sung ^a,b   Kao, Shao Hsuan ^a,b   Wang, Chau Jong ^a,b  

^a CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^b CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

Apple polyphenol; Colon cancer; Focal adhesion kinase; Metastasis

Indexed keywords

GASTROPODA; MALUS X DOMESTICA;

EID: 84920747411     PISSN: 17564646     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jff.2014.10.031     Document Type: Article

References (43)

1. Abbi S., Guan J.L. Focal adhesion kinase: Protein interactions and cellular functions. Histology and Histopathology 2002, 17:1163-1171.
2. Avizienyte E., Frame M.C. Src and FAK signalling controls adhesion fate and the epithelial-to-mesenchymal transition. Current Opinion in Cell Biology 2005, 17:542-547.
3. Azios N.G., Dharmawardhane S.F. Resveratrol and estradiol exert disparate effects on cell migration, cell surface actin structures, and focal adhesion assembly in MDA-MB-231 human breast cancer cells. Neoplasia (New York, N.Y.) 2005, 7:128-140.
4. Chang F., Lemmon C.A., Park D., Romer L.H. FAK potentiates Rac1 activation and localization to matrix adhesion sites: A role for betaPIX. Molecular Biology of the Cell 2007, 18:253-264.
5. Chen J.S., Huang X.H., Wang Q., Chen X.L., Fu X.H., Tan H.X., Zhang L.J., Li W., Bi J. FAK is involved in invasion and metastasis of hepatocellular carcinoma. Clinical and Experimental Metastasis 2010, 27:71-82.
6. Deng Y.T., Lin J.K. EGCG inhibits the invasion of highly invasive CL1-5 lung cancer cells through suppressing MMP-2 expression via JNK signaling and induces G2/M arrest. Journal of Agricultural and Food Chemistry 2011, 59:13318-13327.
7. Deramaudt T.B., Dujardin D., Noulet F., Martin S., Vauchelles R., Takeda K., Ronde P. Altering FAK-paxillin interactions reduces adhesion, migration and invasion processes. PLoS ONE 2014, 9. e92059.
8. Elloul S., Elstrand M.B., Nesland J.M., Trope C.G., Kvalheim G., Goldberg I., Reich R., Davidson B. Snail, Slug, and Smad-interacting protein 1 as novel parameters of disease aggressiveness in metastatic ovarian and breast carcinoma. Cancer 2005, 103:1631-1643.
9. Faerden A.E., Sjo O.H., Bukholm I.R., Andersen S.N., Svindland A., Nesbakken A., Bakka A. Lymph node micrometastases and isolated tumor cells influence survival in stage I and II colon cancer. Diseases of the Colon and Rectum 2011, 54:200-206.
10. Fujiwara K., Nakashima S., Sami M., Kanda T. Ninety-day dietary toxicity study of apple polyphenol extracts in Crl: CD (SD) rats. Food and Chemical Toxicology: An International Journal Published for the British Industrial Biological Research Association 2013, 56:214-222.
11. González-Sarrías A., Li L., Seeram N.P. Anticancer effects of maple syrup phenolics and extracts on proliferation, apoptosis, and cell cycle arrest of human colon cells. Journal of Functional Foods 2012, 4:185-196.
12. Gosse F., Guyot S., Roussi S., Lobstein A., Fischer B., Seiler N., Raul F. Chemopreventive properties of apple procyanidins on human colon cancer-derived metastatic SW620 cells and in a rat model of colon carcinogenesis. Carcinogenesis 2005, 26:1291-1295.
13. Gupta G.P., Massague J. Cancer metastasis: Building a framework. Cell 2006, 127:679-695.
14. Hall A. Rho family GTPases. Biochemical Society Transactions 2012, 40:1378-1382.
15. Haraguchi M., Okubo T., Miyashita Y., Miyamoto Y., Hayashi M., Crotti T.N., McHugh K.P., Ozawa M. Snail regulates cell-matrix adhesion by regulation of the expression of integrins and basement membrane proteins. The Journal of Biological Chemistry 2008, 283:23514-23523.
16. Hibasami H., Shohji T., Shibuya I., Higo K., Kanda T. Induction of apoptosis by three types of procyanidin isolated from apple (Rosaceae Malus pumila) in human stomach cancer KATO III cells. International Journal of Molecular Medicine 2004, 13:795-799.
17. Hill A.R., McQuellon R.P., Russell G.B., Shen P., Stewart J.H., Levine E.A. Survival and quality of life following cytoreductive surgery plus hyperthermic intraperitoneal chemotherapy for peritoneal carcinomatosis of colonic origin. Annals of Surgical Oncology 2011, 18:3673-3679.
18. Hsu H.Y., Lin T.Y., Hwang P.A., Tseng L.M., Chen R.H., Tsao S.M., Hsu J. Fucoidan induces changes in the epithelial to mesenchymal transition and decreases metastasis by enhancing ubiquitin-dependent TGFbeta receptor degradation in breast cancer. Carcinogenesis 2013, 34:874-884.
19. Hu X.W., Meng D., Fang J. Apigenin inhibited migration and invasion of human ovarian cancer A2780 cells through focal adhesion kinase. Carcinogenesis 2008, 29:2369-2376.
20. Ji H.F., Pang D., Fu S.B., Jin Y., Yao L., Qi J.P., Bai J. Overexpression of focal adhesion kinase correlates with increased lymph node metastasis and poor prognosis in non-small-cell lung cancer. Journal of Cancer Research and Clinical Oncology 2013, 139:429-435.
21. Kaur M., Deep G., Jain A.K., Raina K., Agarwal C., Wempe M.F., Agarwal R. Bitter melon juice activates cellular energy sensor AMP-activated protein kinase causing apoptotic death of human pancreatic carcinoma cells. Carcinogenesis 2013, 34:1585-1592.
22. Korb T., Schluter K., Enns A., Spiegel H.U., Senninger N., Nicolson G.L., Haier J. Integrity of actin fibers and microtubules influences metastatic tumor cell adhesion. Experimental Cell Research 2004, 299:236-247.
23. Luo M., Guan J.L. Focal adhesion kinase: A prominent determinant in breast cancer initiation, progression and metastasis. Cancer Letters 2010, 289:127-139.
24. Megison M.L., Stewart J.E., Nabers H.C., Gillory L.A., Beierle E.A. FAK inhibition decreases cell invasion, migration and metastasis in MYCN amplified neuroblastoma. Clinical and Experimental Metastasis 2013, 30:555-568.
25. Mitra S.K., Hanson D.A., Schlaepfer D.D. Focal adhesion kinase: In command and control of cell motility. Nature Reviews. Molecular Cell Biology 2005, 6:56-68.
26. Miura T., Chiba M., Kasai K., Nozaka H., Nakamura T., Shoji T., Kanda T., Ohtake Y., Sato T. Apple procyanidins induce tumor cell apoptosis through mitochondrial pathway activation of caspase-3. Carcinogenesis 2008, 29:585-593.
27. Miyoshi A., Kitajima Y., Kido S., Shimonishi T., Matsuyama S., Kitahara K., Miyazaki K. Snail accelerates cancer invasion by upregulating MMP expression and is associated with poor prognosis of hepatocellular carcinoma. British Journal of Cancer 2005, 92:252-258.
28. Nam E.H., Lee Y., Park Y.K., Lee J.W., Kim S. ZEB2 upregulates integrin alpha5 expression through cooperation with Sp1 to induce invasion during epithelial-mesenchymal transition of human cancer cells. Carcinogenesis 2012, 33:563-571.
29. Nieto M.A. The snail superfamily of zinc-finger transcription factors. Nature Reviews. Molecular Cell Biology 2002, 3:155-166.
30. Osada K., Suzuki T., Kawakami Y., Senda M., Kasai A., Sami M., Ohta Y., Kanda T., Ikeda M. Dose-dependent hypocholesterolemic actions of dietary apple polyphenol in rats fed cholesterol. Lipids 2006, 41:133-139.
31. Park J.H., Lee B.L., Yoon J., Kim J., Kim M.A., Yang H.K., Kim W.H. Focal adhesion kinase (FAK) gene amplification and its clinical implications in gastric cancer. Human Pathology 2010, 41:1664-1673.
32. Rizzi F., Naponelli V., Silva A., Modernelli A., Ramazzina I., Bonacini M., Tardito S., Gatti R., Uggeri J., Bettuzzi S. Polyphenon E (R), a standardized green tea extract, induces endoplasmic reticulum stress, leading to death of immortalized PNT1a cells by anoikis and tumorigenic PC3 by necroptosis. Carcinogenesis 2014, 35:828-839.
33. Shoji T., Akazome Y., Kanda T., Ikeda M. The toxicology and safety of apple polyphenol extract. Food and Chemical Toxicology: An International Journal Published for the British Industrial Biological Research Association 2004, 42:959-967.
34. Singh T., Katiyar S.K. Green tea catechins reduce invasive potential of human melanoma cells by targeting COX-2, PGE2 receptors and epithelial-to-mesenchymal transition. PLoS ONE 2011, 6. e25224.
35. Sugiyama H., Akazome Y., Shoji T., Yamaguchi A., Yasue M., Kanda T., Ohtake Y. Oligomeric procyanidins in apple polyphenol are main active components for inhibition of pancreatic lipase and triglyceride absorption. Journal of Agricultural and Food Chemistry 2007, 55:4604-4609.
36. Thiery J.P. Epithelial-mesenchymal transitions in tumor progression. Nature Reviews. Cancer 2002, 2:442-454.
37. Ward K.K., Tancioni I., Lawson C., Miller N.L., Jean C., Chen X.L., Uryu S., Kim J., Tarin D., Stupack D.G., Plaxe S.C., Schlaepfer D.D. Inhibition of focal adhesion kinase (FAK) activity prevents anchorage-independent ovarian carcinoma cell growth and tumor progression. Clinical and Experimental Metastasis 2013, 30:579-594.
38. Weyant M.J., Carothers A.M., Dannenberg A.J., Bertagnolli M.M. (+)-Catechin inhibits intestinal tumor formation and suppresses focal adhesion kinase activation in the Min/+ mouse. Cancer Research 2001, 61:118-125.
39. Yamazaki D., Kurisu S., Takenawa T. Regulation of cancer cell motility through actin reorganization. Cancer Science 2005, 96:379-386.
40. Zhang A., Wang Q., Han Z., Hu W., Xi L., Gao Q., Wang S., Zhou J., Xu G., Meng L., Chen G., Ma D. Reduced expression of Snail decreases breast cancer cell motility by downregulating the expression and inhibiting the activity of RhoA GTPase. Oncology Letters 2013, 6:339-346.
41. Zhao J., Guan J.L. Signal transduction by focal adhesion kinase in cancer. Cancer Metastasis Reviews 2009, 28:35-49.
42. Zhong Y., Chiou Y.S., Pan M.H., Ho C.T., Shahidi F. Protective effects of epigallocatechin gallate (EGCG) derivatives on azoxymethane-induced colonic carcinogenesis in mice. Journal of Functional Foods 2012, 4:323-330.
43. Zhou J., Roh J.W., Bandyopadhyay S., Chen Z., Munkarah A.R., Hussein Y., Alosh B., Jazaerly T., Hayek K., Semaan A., Sood A.K., Ali-Fehmi R. Overexpression of enhancer of zeste homolog 2 (EZH2) and focal adhesion kinase (FAK) in high grade endometrial carcinoma. Gynecologic Oncology 2013, 128:344-348.