Butein inhibits the migration and invasion of SK-HEP-1 human hepatocarcinoma cells through suppressing the ERK, JNK, p38, and uPA signaling multiple pathways

Journal of Agricultural and Food Chemistry

Volumn 59, Issue 16, 2011, Pages 9032-9038

  Ma, Chia Yu ^a   Ji, Wei Ting ^b   Chueh, Fu Shin ^c   Yang, Jai Sing ^b   Chen, Po Yuan ^b   Yu, Chien Chih ^b   Chung, Jing Gung ^b,c  

^a TECHNOLOGY AND SCIENCE INSTITUTE OF NORTHERN TAIWAN   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

^c ASIA UNIVERSITY   (Taiwan)

Author keywords

Butein; invasion; MAPKs pathway; matrix metalloproteinase; migration; SK HEP 1 human hepatocarcinoma cells

Indexed keywords

BUTEIN; INVASION; MAPKS PATHWAY; MATRIX METALLOPROTEINASES; MIGRATION; SK-HEP-1;

BLOOD VESSELS; CELL DEATH; ELECTROPHORETIC MOBILITY; ENZYME INHIBITION;

DISEASES;

ANTINEOPLASTIC AGENT; BUTEIN; CHALCONE DERIVATIVE; UROKINASE;

ARTICLE; CANCER INVASION; CELL MOTION; DRUG ANTAGONISM; DRUG EFFECT; HUMAN; LIVER CELL CARCINOMA; LIVER TUMOR; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL MOVEMENT; CHALCONES; HUMANS; LIVER NEOPLASMS; MAP KINASE SIGNALING SYSTEM; NEOPLASM INVASIVENESS; UROKINASE-TYPE PLASMINOGEN ACTIVATOR;

EID: 80051750075     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf202027n     Document Type: Article

References (48)

1. Zimonjic, D. B.; Keck, C. L.; Thorgeirsson, S. S.; Popescu, N. C. Novel recurrent genetic imbalances in human hepatocellular carcinoma cell lines identified by comparative genomic hybridization Hepatology 1999, 29 (4) 1208-1214 (Pubitemid 29168756)
2. Nowak, A. K.; Chow, P. K.; Findlay, M. Systemic therapy for advanced hepatocellular carcinoma: A review Eur. J. Cancer 2004, 40 (10) 1474-1484 (Pubitemid 38757734)
3. Wang, X. W.; Hussain, S. P.; Huo, T. I.; Wu, C. G.; Forgues, M.; Hofseth, L. J.; Brechot, C.; Harris, C. C. Molecular pathogenesis of human hepatocellular carcinoma Toxicology 2002, 181-182, 43-47 (Pubitemid 36015671)
4. Rao, J. S. Molecular mechanisms of glioma invasiveness: The role of proteases Nat. Rev. Cancer 2003, 3 (7) 489-501 (Pubitemid 37328837)
5. Werb, Z. ECM and cell surface proteolysis: regulating cellular ecology Cell 1997, 91 (4) 439-442 (Pubitemid 27508232)
6. Fang, J.; Shing, Y.; Wiederschain, D.; Yan, L.; Butterfield, C.; Jackson, G.; Harper, J.; Tamvakopoulos, G.; Moses, M. A. Matrix metalloproteinase-2 is required for the switch to the angiogenic phenotype in a tumor model Proc. Natl. Acad. Sci. U.S.A. 2000, 97 (8) 3884-3889 (Pubitemid 30226056)
7. Sternlicht, M. D.; Werb, Z. How matrix metalloproteinases regulate cell behavior Annu. Rev. Cell Dev. Biol. 2001, 17, 463-516 (Pubitemid 33096184)
8. Mignatti, P.; Tsuboi, R.; Robbins, E.; Rifkin, D. B. In vitro angiogenesis on the human amniotic membrane: Requirement for basic fibroblast growth factor-induced proteinases J. Cell Biol. 1989, 108 (2) 671-682 (Pubitemid 19065862)
9. Cornelius, L. A.; Nehring, L. C.; Roby, J. D.; Parks, W. C.; Welgus, H. G. Human dermal microvascular endothelial cells produce matrix metalloproteinases in response to angiogenic factors and migration J. Invest. Dermatol. 1995, 105 (2) 170-176
10. Hanemaaijer, R.; Koolwijk, P.; le Clercq, L.; de Vree, W. J.; van Hinsbergh, V. W. Regulation of matrix metalloproteinase expression in human vein and microvascular endothelial cells. Effects of tumour necrosis factor alpha, interleukin 1 and phorbol ester Biochem. J. 1993, 296 (Part 3) 803-809 (Pubitemid 24008200)
11. Unemori, E. N.; Bouhana, K. S.; Werb, Z. Vectorial secretion of extracellular matrix proteins, matrix-degrading proteinases, and tissue inhibitor of metalloproteinases by endothelial cells J. Biol. Chem. 1990, 265 (1) 445-451
12. Kim, N. Y.; Pae, H. O.; Oh, G. S.; Kang, T. H.; Kim, Y. C.; Rhew, H. Y.; Chung, H. T. Butein, a plant polyphenol, induces apoptosis concomitant with increased caspase-3 activity, decreased Bcl-2 expression and increased Bax expression in HL-60 cells Pharmacol. Toxicol. 2001, 88 (5) 261-266
13. Wang, Y.; Chan, F. L.; Chen, S.; Leung, L. K. The plant polyphenol butein inhibits testosterone-induced proliferation in breast cancer cells expressing aromatase Life Sci. 2005, 77 (1) 39-51 (Pubitemid 40546375)
14. Samoszuk, M.; Tan, J.; Chorn, G. The chalcone butein from Rhus verniciflua Stokes inhibits clonogenic growth of human breast cancer cells co-cultured with fibroblasts BMC Complementary Altern. Med. 2005, 5, 5
15. Iwashita, K.; Kobori, M.; Yamaki, K.; Tsushida, T. Flavonoids inhibit cell growth and induce apoptosis in B16 melanoma 4A5 cells Biosci., Biotechnol., Biochem. 2000, 64 (9) 1813-1820
16. Lee, J. C.; Lee, K. Y.; Kim, J.; Na, C. S.; Jung, N. C.; Chung, G. H.; Jang, Y. S. Extract from Rhus verniciflua Stokes is capable of inhibiting the growth of human lymphoma cells Food Chem. Toxicol. 2004, 42 (9) 1383-1388 (Pubitemid 38844855)
17. Ramanathan, R.; Tan, C. H.; Das, N. P. Cytotoxic effect of plant polyphenols and fat-soluble vitamins on malignant human cultured cells Cancer Lett. 1992, 62 (3) 217-224
18. Kang, H. M.; Kim, J. H.; Lee, M. Y.; Son, K. H.; Yang, D. C.; Baek, N. I.; Kwon, B. M. Relationship between flavonoid structure and inhibition of farnesyl protein transferase Nat. Prod. Res. 2004, 18 (4) 349-356 (Pubitemid 38787023)
19. Yit, C. C.; Das, N. P. Cytotoxic effect of butein on human colon adenocarcinoma cell proliferation Cancer Lett. 1994, 82 (1) 65-72 (Pubitemid 24211073)
20. Jang, H. S.; Kook, S. H.; Son, Y. O.; Kim, J. G.; Jeon, Y. M.; Jang, Y. S.; Choi, K. C.; Kim, J.; Han, S. K.; Lee, K. Y.; Park, B. K.; Cho, N. P.; Lee, J. C. Flavonoids purified from Rhus verniciflua Stokes actively inhibit cell growth and induce apoptosis in human osteosarcoma cells Biochim. Biophys. Acta 2005, 1726 (3) 309-316 (Pubitemid 41668540)
21. Lee, S. H.; Seo, G. S.; Kim, H. S.; Woo, S. W.; Ko, G.; Sohn, D. H. 2′,4′,6′-Tris(methoxymethoxy) chalcone attenuates hepatic stellate cell proliferation by a heme oxygenase-dependent pathway Biochem. Pharmacol. 2006, 72 (10) 1322-1333 (Pubitemid 44572190)
22. Zhang, L.; Chen, W.; Li, X. A novel anticancer effect of butein: inhibition of invasion through the ERK1/2 and NF-kappa B signaling pathways in bladder cancer cells FEBS Lett. 2008, 582 (13) 1821-1828
23. Huang, W. W.; Ko, S. W.; Tsai, H. Y.; Chung, J. G.; Chiang, J. H.; Chen, K. T.; Chen, Y. C.; Chen, H. Y.; Chen, Y. F.; Yang, J. S. Cantharidin induces G2/M phase arrest and apoptosis in human colorectal cancer colo 205 cells through inhibition of CDK1 activity and caspase-dependent signaling pathways Int. J. Oncol. 2011, 38 (4) 1067-1073
24. Wu, P. P.; Liu, K. C.; Huang, W. W.; Ma, C. Y.; Lin, H.; Yang, J. S.; Chung, J. G. Triptolide induces apoptosis in human adrenal cancer NCI-H295 cells through a mitochondrial-dependent pathway Oncol. Rep. 2011, 25 (2) 551-557
25. Oh, S. J.; Santy, L. C. Differential effects of cytohesins 2 and 3 on beta1 integrin recycling J. Biol. Chem. 2010, 285 (19) 14610-14616
26. Li, G.; Luna, C.; Qiu, J.; Epstein, D. L.; Gonzalez, P. Targeting of integrin beta1 and kinesin 2alpha by microRNA 183 J. Biol. Chem. 2010, 285 (8) 5461-5471
27. Barhoumi, R.; Bowen, J. A.; Stein, L. S.; Echols, J.; Burghardt, R. C. Concurrent analysis of intracellular glutathione content and gap junctional intercellular communication Cytometry 1993, 14 (7) 747-756 (Pubitemid 23290356)
28. Suh, H. N.; Han, H. J. Laminin regulates mouse embryonic stem cell migration: involvement of Epac1/Rap1 and Rac1/cdc42 Am. J. Physiol. Cell Physiol. 2010, 298 (5) C1159-C1169
29. 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
30. Lu, K. W.; Chen, J. C.; Lai, T. Y.; Yang, J. S.; Weng, S. W.; Ma, Y. S.; Lu, P. J.; Weng, J. R.; Chueh, F. S.; Wood, W. G.; Chung, J. G. Gypenosides inhibits migration and invasion of human oral cancer SAS cells through the inhibition of matrix metalloproteinase-2/-9 and urokinase-plasminogen by ERK1/2 and NF-kappa B signaling pathways Hum. Exp. Toxicol. 2011, 30, 406-415
31. Hsu, S. C.; Yang, J. S.; Kuo, C. L.; Lo, C.; Lin, J. P.; Hsia, T. C.; Lin, J. J.; Lai, K. C.; Kuo, H. M.; Huang, L. J.; Kuo, S. C.; Wood, W. G.; Chung, J. G. Novel quinolone CHM-1 induces apoptosis and inhibits metastasis in a human osterogenic sarcoma cell line J. Orthop. Res. 2009, 27 (12) 1637-1644
32. Sathya, S.; Sudhagar, S.; Vidhya Priya, M.; Bharathi Raja, R.; Muthusamy, V. S.; Niranjali Devaraj, S.; Lakshmi, B. S. 3beta-Hydroxylup-20(29)-ene-27,28- dioic acid dimethyl ester, a novel natural product from Plumbago zeylanica inhibits the proliferation and migration of MDA-MB-231 cells Chem.-Biol. Interact. 2010, 188, 412-420
33. Pan, B.; Zhao, M. H.; Chen, Z.; Lu, L.; Wang, Y.; Shi, D. W.; Han, P. Z. Inhibitory effects of resistin-13-peptide on the proliferation, adhesion, and invasion of MDA-MB-231 in human breast carcinoma cells Endocr. Relat. Cancer 2007, 14 (4) 1063-1071 (Pubitemid 351252437)
34. Lin, S. Y.; Lai, W. W.; Ho, C. C.; Yu, F. S.; Chen, G. W.; Yang, J. S.; Liu, K. C.; Lin, M. L.; Wu, P. P.; Fan, M. J.; Chung, J. G. Emodin induces apoptosis of human tongue squamous cancer SCC-4 cells through reactive oxygen species and mitochondria-dependent pathways Anticancer Res. 2009, 29 (1) 327-335
35. 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
36. Chiang, J. H.; Yang, J. S.; Ma, C. Y.; Yang, M. D.; Huang, H. Y.; Hsia, T. C.; Kuo, H. M.; Wu, P. P.; Lee, T. H.; Chung, J. G. Danthron, an Anthraquinone Derivative, Induces DNA Damage and Caspase Cascades-Mediated Apoptosis in SNU-1 Human Gastric Cancer Cells through Mitochondrial Permeability Transition Pores and Bax-Triggered Pathways Chem. Res. Toxicol. 2011, 24 (1) 20-29
37. 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 (Pubitemid 21914501)
38. 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 (Pubitemid 41235808)
39. Coffer, P. J.; Woodgett, J. R. Molecular cloning and characterisation of a novel putative protein-serine kinase related to the cAMP-dependent and protein kinase C families Eur. J. Biochem. 1991, 201 (2) 475-481
40. Jazirehi, A. R.; Vega, M. I.; Bonavida, B. Development of rituximab-resistant lymphoma clones with altered cell signaling and cross-resistance to chemotherapy Cancer Res. 2007, 67 (3) 1270-1281
41. Harada, H.; Takahashi, E.; Itoh, S.; Harada, K.; Hori, T. A.; Taniguchi, T. Structure and regulation of the human interferon regulatory factor 1 (IRF-1) and IRF-2 genes: Implications for a gene network in the interferon system Mol. Cell. Biol. 1994, 14 (2) 1500-1509
42. Jazirehi, A. R.; Vega, M. I.; Chatterjee, D.; Goodglick, L.; Bonavida, B. Inhibition of the Raf-MEK1/2-ERK1/2 signaling pathway, Bcl-xL down-regulation, and chemosensitization of non-Hodgkin's lymphoma B cells by Rituximab Cancer Res. 2004, 64 (19) 7117-7126 (Pubitemid 39331025)
43. Kuo, T. C.; Yang, J. S.; Lin, M. W.; Hsu, S. C.; Lin, J. J.; Lin, H. J.; Hsia, T. C.; Liao, C. L.; Yang, M. D.; Fan, M. J.; Wood, W. G.; Chung, J. G. Emodin has cytotoxic and protective effects in rat C6 glioma cells: roles of Mdr1a and nuclear factor kappaB in cell survival J. Pharmacol. Exp. Ther. 2009, 330 (3) 736-744
44. Zhao, J.; Guan, J. L. Signal transduction by focal adhesion kinase in cancer Cancer Metastasis Rev. 2009, 28 (1-2) 35-49
45. Finn, R. S. Targeting Src in breast cancer Ann. Oncol. 2008, 19 (8) 1379-1386
46. Meng, X. N.; Jin, Y.; Yu, Y.; Bai, J.; Liu, G. Y.; Zhu, J.; Zhao, Y. Z.; Wang, Z.; Chen, F.; Lee, K. Y.; Fu, S. B. Characterisation of fibronectin-mediated FAK signalling pathways in lung cancer cell migration and invasion Br. J. Cancer 2009, 101 (2) 327-334
47. Schlaepfer, D. D.; Hanks, S. K.; Hunter, T.; van der Geer, P. Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase Nature 1994, 372 (6508) 786-791
48. Zhao, L.; Xu, G.; Zhou, J.; Xing, H.; Wang, S.; Wu, M.; Lu, Y. P.; Ma, D. The effect of RhoA on human umbilical vein endothelial cell migration and angiogenesis in vitro Oncol. Rep. 2006, 15 (5) 1147-1152