Phenethyl isothiocyanate inhibited tumor migration and invasion via suppressing multiple signal transduction pathways in human colon cancer HT29 cells

Journal of Agricultural and Food Chemistry

Volumn 58, Issue 20, 2010, Pages 11148-11155

  Lai, Kuang Chi ^a,b   Hsu, Shu Chun ^c   Kuo, Chao Lin ^d   Ip, Siu Wan ^d   Yang, Jai Sing ^d   Hsu, Yuan Man ^d   Huang, Hui Ying ^d   Wu, Shin Hwar ^e   Chung, Jing Gung ^d,f  

^a CHINA MEDICAL UNIVERSITY BEIGANG HOSPITAL   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

^c HSIUPING INSTITUTE OF TECHNOLOGY   (Taiwan)

^d CHINA MEDICAL UNIVERSITY   (Taiwan)

^e CHANGHUA CHRISTIAN HOSPITAL   (Taiwan)

^f ASIA UNIVERSITY   (Taiwan)

Author keywords

Human colon cancer HT29 cells; Invasion; Migration; MMP 2; MMP 9; PEITC

Indexed keywords

HUMAN COLON CANCER HT29 CELLS; INVASION; MIGRATION; MMP-2; MMP-9; PEITC;

CELL PROLIFERATION; GENE EXPRESSION; SIGNAL TRANSDUCTION;

DISEASES;

ANTINEOPLASTIC AGENT; ISOTHIOCYANIC ACID DERIVATIVE; PHENETHYL ISOTHIOCYANATE; PLANT EXTRACT;

CELL MOTION; CHEMISTRY; COLONIC NEOPLASMS; DOWN REGULATION; DRUG EFFECTS; HT 29 CELL LINE; HUMAN; PATHOLOGY; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION; TUMOR INVASION; VEGETABLE;

ANTINEOPLASTIC AGENTS; CELL MOVEMENT; COLONIC NEOPLASMS; DOWN-REGULATION; HT29 CELLS; HUMANS; ISOTHIOCYANATES; NEOPLASM INVASIVENESS; PLANT EXTRACTS; SIGNAL TRANSDUCTION; VEGETABLES;

EID: 78049262629     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf102384n     Document Type: Article

References (46)

1. Wingo, P. A.; Tong, T.; Bolden, S. Cancer statistics, 1995. Ca;Cancer J. Clin. 1995, 45 (1), 8-30.
2. Conaway, C. C.; Yang, Y. M.; Chung, F. L. Isothiocyanates as cancer chemopreventive agents: Their biological activities and metabolism in rodents and humans. Curr. Drug Metab. 2002, 3 (3), 233-255.
3. Potter, J. D. Nutrition and colorectal cancer. Cancer, Causes Control 1996, 7 (1), 127-146.
4. Stoner, G. D.; Morrissey, D. T.; Heur, Y. H.; Daniel, E. M.; Galati, A. J.; Wagner, S. A. Inhibitory effects of phenethyl isothiocyanate on N-nitrosobenzylmethylamine carcinogenesis in the rat esophagus. Cancer Res. 1991, 51 (8), 2063-2068.
5. Zhang, Y.; Talalay, P. Anticarcinogenic activities of organic isothiocyanates: Chemistry andmechanisms.CancerRes. 1994, 54 (7 Suppl.), 1976s-1981s.
6. Hu, R.; Kim, B. R.; Chen, C.; Hebbar, V.; Kong, A. N. The roles of JNK and apoptotic signaling pathways in PEITC-mediated responses in human HT-29 colon adenocarcinoma cells. Carcinogenesis 2003, 24 (8), 1361-1367.
7. Zhang, Y. Cancer-preventive isothiocyanates: Measurement of human exposure and mechanism of action. Mutat. Res. 2004, 555 (1-2), 173-190.
8. Wu, X.; Kassie, F.; Mersch-Sundermann, V. Induction of apoptosis in tumor cells by naturally occurring sulfur-containing compounds. Mutat. Res. 2005, 589 (2), 81-102.
9. Morse, M. A.; Amin, S. G.; Hecht, S. S.; Chung, F. L. Effects of aromatic isothiocyanates on tumorigenicity, O6-methylguanine formation, and metabolism of the tobacco-specific nitrosamine 4-(methylnitrosamino)-1-(3-pyridyl)-1- butanone in A/J mouse lung. Cancer Res. 1989, 49 (11), 2894-2897.
10. Zhang, Y.; Kensler, T. W.; Cho, C. G.; Posner, G. H.; Talalay, P. Anticarcinogenic activities of sulforaphane and structurally related synthetic norbornyl isothiocyanates. Proc.Natl. Acad. Sci. U.S.A. 1994, 91 (8), 3147-3150.
11. Kilian, M.; Gregor, J. I.; Heukamp, I.; Hanel, M.; Ahlgrimm, M.; Schimke, I.; Kristiansen, G.; Ommer, A.; Walz, M. K.; Jacobi, C. A.; Wenger, F. A. Matrix metalloproteinase inhibitor RO 28-2653 decreases liver metastasis by reduction of MMP-2 and MMP-9 concentration in BOP-induced ductal pancreatic cancer in Syrian Hamsters: Inhibition of matrix metalloproteinases in pancreatic cancer. Prostaglandins, Leukotrienes Essent. Fatty Acids 2006, 75 (6), 429-434.
12. Mizutani, K.; Kofuji, K.; Shirouzu, K. The significance of MMP-1 and MMP-2 in peritoneal disseminated metastasis of gastric cancer. Surg. Today 2000, 30 (7), 614-621.
13. Gullu, I. H.; Kurdoglu, M.; Akalin, I. The relation of gelatinase (MMP-2 and -9) expression with distant site metastasis and tumour aggressiveness in colorectal cancer. Br. J. Cancer 2000, 82 (1), 249.
14. Donadio, A. C.; Remedi, M. M.; Susperreguy, S.; Frede, S.; Gilardoni, M. B.; Tang, Y.; Pellizas, C. G.; Yan, L. Extracellular matrix metalloproteinase inducer (EMMPRIN) and matrix metalloproteinases (MMPs) as regulators of tumor-host interaction in a spontaneous metastasis model in rats. Histochem. Cell Biol. 2008, 130 (6), 1155-1164.
15. CorteşReynosa, P.; Robledo, T.; MaciaşSilva, M.; Wu, S. V.; Salazar, E. P. Src kinase regulates metalloproteinase-9 secretion induced by type IV collagen in MCF-7 human breast cancer cells. Matrix Biol. 2008, 27 (3), 220-231.
16. Okuducu, A. F.; Zils, U.; Michaelis, S. A.; Michaelides, S.; von Deimling, A. Ets-1 is up-regulated together with its target gene products matrix metalloproteinase-2 and matrix metalloproteinase-9 in atypical and anaplastic meningiomas. Histopathology 2006, 48 (7), 836-845.
17. Ho, C. C.; Lin, S. Y.; Yang, J. S.; Liu, K. C.; Tang, Y. J.; Yang, M. D.; Chiang, J. H.; Lu, C. C.; Wu, C. L.; Chiu, T. H.; Chung, J. G. Gallic acid inhibits murine leukemia WEHI-3 cells in vivo and promotes macrophage phagocytosis. In Vivo 2009, 23 (3), 409-413.
18. Lin, J. P.; Yang, J. S.; Lu, C. C.; Chiang, J. H.; Wu, C. L.; Lin, J. J.; Lin, H. L.; Yang, M. D.; Liu, K. C.; Chiu, T. H.; Chung, J. G. Rutin inhibits the proliferation of murine leukemia WEHI-3 cells in vivo and promotes immune response in vivo. Leuk. Res. 2009, 33 (6), 823-828.
19. Yun, J. W.; Lee, W. S.; Kim, M. J.; Lu, J. N.; Kang, M. H.; Kim, H. G.; Kim, D. C.; Choi, E. J.; Choi, J. Y.; Lee, Y. K.; Ryu, C. H.; Kim, G.; Choi, Y. H.; Park, O. J.; Shin, S. C. Characterization of a profile of the anthocyanins isolated from Vitis coignetiae Pulliat and their anti-invasive activity on HT-29 human colon cancer cells. Food Chem. Toxicol. 2010, 48 (3), 903-909.
20. Fishman, D. A.; Liu, Y.; Ellerbroek, S. M.; Stack, M. S. Lysophosphatidic acid promotes matrix metalloproteinase (MMP) activation and MMP-dependent invasion in ovarian cancer cells. Cancer Res. 2001, 61 (7), 3194-3199.
21. Chen, Y. Y.; Chiang, S. Y.; Lin, J. G.; Ma, Y. S.; Liao, C. L.; Weng, S. W.; Lai, T. Y.; Chung, J. G. Emodin, aloe-emodin and rhein inhibit migration and invasion in human tongue cancer SCC-4 cells through the inhibition of gene expression of matrix metalloproteinase-9. Int. J. Oncol. 2010, 36 (5), 1113-1120.
22. Lin, C. C.; Chen, J. T.; Yang, J. S.; Lu, H. F.; Hsu, S. C.; Tan, T. W.; Lin, Y. T.; Ma, Y. S.; Ip, S. W.; Wu, J. J.; Li, Y. C.; Chung, J. G. Danthron inhibits the migration and invasion of human brain glioblastoma multiforme cells through the inhibition of mRNA expression of focal adhesion kinase, Rho kinaseş1 and metalloproteinase-9. Oncol. Rep. 2009, 22 (5), 1033-1037.
23. Lu, C. C.; Yang, J. S.; Huang, A. C.; Hsia, T. C.; Chou, S. T.; Kuo, C. L.; Lu, H. F.; Lee, T. H.; Wood, W. G.; Chung, J. G. Chrysophanol induces necrosis through the production of ROS and alteration of ATP levels in J5 human liver cancer cells. Mol. Nutr. Food Res. 2010, 54 (7), 967-976.
24. Ji, B. C.; Hsu, W. H.; Yang, J. S.; Hsia, T. C.; Lu, C. C.; Chiang, J. H.; Yang, J. L.; Lin, C. H.; Lin, J. J.; Suen, L. J.; Gibson Wood, W.; Chung, J. G. Gallic acid induces apoptosis via caspase-3 and mitochondrion-dependent pathways in vitro and suppresses lung xenograft tumor growth in vivo. J. Agric. Food Chem. 2009, 57 (16), 7596-7604.
25. Lai, K. C.; Huang, A. C.; Hsu, S. C.; Kuo, C. L.; Yang, J. S.; Wu, S. H.; Chung, J. G. Benzyl isothiocyanate (BITC) inhibits migration and invasion of human colon cancer HT29 cells by inhibiting matrix metalloproteinase-2/-9 and urokinase plasminogen (uPA) through PKC and MAPK signaling pathway. J. Agric. Food Chem. 2010, 58 (5), 2935-2942.
26. Jones, P. F.; Jakubowicz, T.; Pitossi, F. J.; Maurer, F.; Hemmings, B. A. Molecular cloning and identification of a serine/threonine protein kinase of the second-messenger subfamily. Proc. Natl. Acad. Sci. U.S.A. 1991, 88 (10), 4171-4175.
27. Enomoto, A.; Murakami, H.; Asai, N.; Morone, N.; Watanabe, T.; Kawai, K.;Murakumo,Y.; Usukura, J.;Kaibuchi, K.; Takahashi,M. Akt/PKB regulates actin organization and cell motility via Girdin/ APE. Dev. Cell 2005, 9 (3), 389-402.
28. Economou, M. A. Uveal melanoma and macular degeneration: Molecular biology and potential therapeutic applications. Acta Ophthalmol. 2008, 86 (8), 930-931.
29. Guruvayoorappan, C.; Kuttan, G. Amentoflavone inhibits experimental tumor metastasis through a regulatory mechanism involving MMP-2, MMP-9, prolyl hydroxylase, lysyl oxidase, VEGF, ERK-1, ERK-2, STAT-1, nm23 and cytokines in lung tissues of C57BL/6 mice. Immunopharmacol. Immunotoxicol. 2008, 30 (4), 711-727.
30. Waas, E. T.; Wobbes, T.; Lomme, R. M.; DeGroot, J.; Ruers, T.; Hendriks, T. Matrix metalloproteinase 2 and 9 activity in patients with colorectal cancer liver metastasis. Br. J. Surg. 2003, 90 (12), 1556-1564.
31. Okada, N.; Ishida, H.; Murata, N.; Hashimoto, D.; Seyama, Y.; Kubota, S. Matrix metalloproteinase-2 and -9 in bile as a marker of liver metastasis in colorectal cancer. Biochem. Biophys. Res. Commun. 2001, 288 (1), 212-216.
32. Nee, L.; Tuite, N.; Ryan, M. P.; McMorrow, T. TNF-alpha and IL-1 beta-mediated regulation of MMP-9 and TIMP-1 in human glomerular mesangial cells. Nephron. Exp. Nephrol. 2007, 107 (2), e73-86.
33. Hollborn, M.; Stathopoulos, C.; Steffen, A.; Wiedemann, P.; Kohen, L.; Bringmann, A. Positive feedback regulation between MMP-9 and VEGF in human RPE cells. Invest. Ophthalmol. Vis. Sci. 2007, 48 (9), 4360-4367.
34. Cowden Dahl, K.D.; Symowicz, J.; Ning, Y.; Gutierrez, E.; Fishman, D. A.; Adley, B. P.; Stack, M. S.; Hudson, L. G. Matrix metalloproteinase 9 is a mediator of epidermal growth factor-dependent e-cadherin loss in ovarian carcinoma cells. Cancer Res. 2008, 68 (12), 4606-4613.
35. Zeisberg, M.; Maeshima, Y.; Mosterman, B.; Kalluri, R. Renal fibrosis. Extracellular matrix microenvironment regulates migratory behavior of activated tubular epithelial cells. Am. J. Pathol. 2002, 160 (6), 2001-2008.
36. Thant, A. A.; Sein, T. T.; Liu, E.; Machida, K.; Kikkawa, F.; Koike, T.; Seiki, M.; Matsuda, S.; Hamaguchi, M. Ras pathway is required for the activation of MMP-2 secretion and for the invasion of src-transformed 3Y1. Oncogene 1999, 18 (47), 6555-6563.
37. Moon, A.; Kim, M. S.; Kim, T. G.; Kim, S. H.; Kim, H. E.; Chen, Y. Q.; Kim, H. R. H-ras, but not N-ras, induces an invasive phenotype in human breast epithelial cells: A role for MMP-2 in the H-raşinduced invasive phenotype. Int. J. Cancer 2000, 85 (2), 176-181.
38. Zhang, S.; Li, Z.; Wu, X.; Huang, Q.; Shen, H. M.; Ong, C. N. Methyl-3-indolylacetate inhibits cancer cell invasion by targeting the MEK1/2-ERK1/2 signaling pathway. Mol. Cancer Ther. 2006, 5 (12), 3285-3293.
39. Chung, T. W.; Lee, Y. C.; Kim, C. H. Hepatitis B viral HBx induces matrix metalloproteinase-9 gene expression through activation of ERK and PI-3K/AKT pathways: Involvement of invasive potential. FASEB J. 2004, 18 (10), 1123-1125.
40. Chakraborti, S.; Mandal, M.; Das, S.; Mandal, A.; Chakraborti, T. Regulation of matrix metalloproteinases: An overview. Mol. Cell. Biochem. 2003, 253 (1-2), 269-285.
41. Simon, C.; Simon, M.; Vucelic, G.; Hicks, M. J.; Plinkert, P. K.; Koitschev, A.; Zenner, H. P. The p38 SAPK pathway regulates the expression of the MMP-9 collagenase via AP-1-dependent promoter activation. Exp. Cell Res. 2001, 271 (2), 344-355.
42. Carpenter, C. L.; Cantley, L. C. Phosphoinositide kinases. Curr. Opin. Cell Biol 1996, 8 (2), 153-158.
43. Woo, J. H.; Lim, J. H.; Kim, Y. H.; Suh, S. I.; Min, D. S.; Chang, J. S.; Lee, Y. H.; Park, J. W.; Kwon, T. K. Resveratrol inhibits phorbol myristate acetate-induced matrix metalloproteinase-9 expression by inhibiting JNK and PKC delta signal transduction. Oncogene 2004, 23 (10), 1845-1853.
44. Andreasen, P. A.; Kjoller, L.; Christensen, L.; Duffy, M. J. The urokinase-type plasminogen activator system in cancer metastasis: A review. Int. J. Cancer 1997, 72 (1), 1-22.
45. Kwaan, H. C. The plasminogen-plasmin system in malignancy. Cancer Metastasis Rev. 1992, 11 (3-4), 291-311.
46. Duffy, M. J.; Maguire, T. M.; McDermott, E. W.; O'Higgins, N. Urokinase plasminogen activator: A prognostic marker in multiple types of cancer. J. Surg. Oncol. 1999, 71 (2), 130-135.