Long-term ethanol exposure-induced hepatocellular carcinoma cell migration and invasion through lysyl oxidase activation are attenuated by combined treatment with pterostilbene and curcumin analogues

Journal of Agricultural and Food Chemistry

Volumn 61, Issue 18, 2013, Pages 4326-4335

  Huang, Ching Shui ^a,b   Ho, Chi Tang ^c   Tu, Shih Hsin ^a,b   Pan, Min Hsiung ^d   Chuang, Chien Hui ^a   Chang, Hui Wen ^e   Chang, Chien Hsi ^e   Wu, Chih Hsiung ^a,f,g   Ho, Yuan Soon ^a,e  

^a TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^b CATHAY GENERAL HOSPITAL   (Taiwan)

^c RUTGERS UNIVERSITY   (United States)

^d NATIONAL KAOHSIUNG UNIVERSITY OF APPLIED SCIENCES   (Taiwan)

^e TAIPEI MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^f TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^g TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

alcoholism; hepatocellular carcinoma; lysyl oxidase; metastasis; pterostilbene

Indexed keywords

ALCOHOLISM; HEPATOCELLULAR CARCINOMA; LYSYL OXIDASE; METASTASIS; PTEROSTILBENE;

CELLS; ETHANOL; PATHOLOGY; PROTEINS;

CYTOLOGY;

ALCOHOL; ANTINEOPLASTIC AGENT; COLLAGEN; CURCUMIN; ELASTIN; MESSENGER RNA; PROTEIN LYSINE 6 OXIDASE; PTEROSTILBENE; STILBENE DERIVATIVE;

ADULT; AGED; ALCOHOLISM; ARTICLE; CELL MOTION; DRUG EFFECT; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LASER CAPTURE MICRODISSECTION; LIVER CELL CARCINOMA; LIVER TUMOR; MALE; METABOLISM; MIDDLE AGED; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

ADULT; AGED; ALCOHOLISM; ANTINEOPLASTIC AGENTS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL MOVEMENT; COLLAGEN; CURCUMIN; ELASTIN; ETHANOL; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION REGULATION; HUMANS; LASER CAPTURE MICRODISSECTION; LIVER NEOPLASMS; MALE; MIDDLE AGED; PROTEIN-LYSINE 6-OXIDASE; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; STILBENES;

EID: 84877262131     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf4004175     Document Type: Article

References (58)

1. Parkin, D. M. Global cancer statistics in the year 2000 Lancet Oncol. 2001, 2, 533-543
2. Di Bisceglie, A. M.; Rustgi, V. K.; Hoofnagle, J. H.; Dusheiko, G. M.; Lotze, M. T. NIH conference. Hepatocellular carcinoma Ann. Intern. Med. 1988, 108, 390-401
3. Wu, H. C.; Wang, Q.; Yang, H. I.; Ahsan, H.; Tsai, W. Y.; Wang, L. Y.; Chen, S. Y.; Chen, C. J.; Santella, R. M. Aflatoxin B1 exposure, hepatitis B virus infection, and hepatocellular carcinoma in Taiwan Cancer Epidemiol. Biomarkers Prev. 2009, 18, 846-853
4. Korourian, S.; Hakkak, R.; Ronis, M. J.; Shelnutt, S. R.; Waldron, J.; Ingelman-Sundberg, M.; Badger, T. M. Diet and risk of ethanol-induced hepatotoxicity: carbohydrate-fat relationships in rats Toxicol. Sci. 1999, 47, 110-117
5. Parkin, D. M.; Bray, F.; Ferlay, J.; Pisani, P. Global cancer statistics, 2002 CA: Cancer J. Clin. 2005, 55, 74-108
6. Barderas, R.; Bartolome, R. A.; Fernandez-Acenero, M. J.; Torres, S.; Casal, J. I. High expression of IL-13 receptor α2 in colorectal cancer is associated with invasion, liver metastasis, and poor prognosis Cancer Res. 2012, 72, 2780-2790
7. Bellizzi, A.; Sebastian, S.; Ceglia, P.; Centonze, M.; Divella, R.; Manzillo, E. F.; Azzariti, A.; Silvestris, N.; Montemurro, S.; Caliandro, C.; De Luca, R.; Cicero, G.; Rizzo, S.; Russo, A.; Quaranta, M.; Simone, G.; Paradiso, A. Co-expression of CD133(+)/CD44(+) in human colon cancer and liver metastasis J. Cell. Physiol. 2013, 228, 408-415
8. El-Serag, H. B.; Rudolph, K. L. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis Gastroenterology 2007, 132, 2557-2576
9. Erler, J. T.; Bennewith, K. L.; Nicolau, M.; Dornhofer, N.; Kong, C.; Le, Q. T.; Chi, J. T.; Jeffrey, S. S.; Giaccia, A. J. Lysyl oxidase is essential for hypoxia-induced metastasis Nature 2006, 440, 1222-1226
10. Behmoaras, J.; Slove, S.; Seve, S.; Vranckx, R.; Sommer, P.; Jacob, M. P. Differential expression of lysyl oxidases LOXL1 and LOX during growth and aging suggests specific roles in elastin and collagen fiber remodeling in rat aorta Rejuvenation Res. 2008, 11, 883-889
11. Levental, K. R.; Yu, H.; Kass, L.; Lakins, J. N.; Egeblad, M.; Erler, J. T.; Fong, S. F.; Csiszar, K.; Giaccia, A.; Weninger, W.; Yamauchi, M.; Gasser, D. L.; Weaver, V. M. Matrix crosslinking forces tumor progression by enhancing integrin signaling Cell 2009, 139, 891-906
12. Kagan, H. M.; Li, W. Lysyl oxidase: properties, specificity, and biological roles inside and outside of the cell J. Cell. Biochem. 2003, 88, 660-672
13. Smith-Mungo, L. I.; Kagan, H. M. Lysyl oxidase: properties, regulation and multiple functions in biology Matrix Biol. 1998, 16, 387-398
14. Hamalainen, E. R.; Jones, T. A.; Sheer, D.; Taskinen, K.; Pihlajaniemi, T.; Kivirikko, K. I. Molecular cloning of human lysyl oxidase and assignment of the gene to chromosome 5q23.3-31.2 Genomics 1991, 11, 508-516
15. Park, H. J.; Gusarova, G.; Wang, Z.; Carr, J. R.; Li, J.; Kim, K. H.; Qiu, J.; Park, Y. D.; Williamson, P. R.; Hay, N.; Tyner, A. L.; Lau, L. F.; Costa, R. H.; Raychaudhuri, P. Deregulation of FoxM1b leads to tumour metastasis EMBO Mol. Med. 2011, 3, 21-34
16. Giampuzzi, M.; Botti, G.; Di Duca, M.; Arata, L.; Ghiggeri, G.; Gusmano, R.; Ravazzolo, R.; Di Donato, A. Lysyl oxidase activates the transcription activity of human collagene III promoter. Possible involvement of Ku antigen J. Biol. Chem. 2000, 275, 36341-36349
17. Payne, S. L.; Fogelgren, B.; Hess, A. R.; Seftor, E. A.; Wiley, E. L.; Fong, S. F.; Csiszar, K.; Hendrix, M. J.; Kirschmann, D. A. Lysyl oxidase regulates breast cancer cell migration and adhesion through a hydrogen peroxide-mediated mechanism Cancer Res. 2005, 65, 11429-11436
18. Barry-Hamilton, V.; Spangler, R.; Marshall, D.; McCauley, S.; Rodriguez, H. M.; Oyasu, M.; Mikels, A.; Vaysberg, M.; Ghermazien, H.; Wai, C.; Garcia, C. A.; Velayo, A. C.; Jorgensen, B.; Biermann, D.; Tsai, D.; Green, J.; Zaffryar-Eilot, S.; Holzer, A.; Ogg, S.; Thai, D.; Neufeld, G.; Van Vlasselaer, P.; Smith, V. Allosteric inhibition of lysyl oxidase-like-2 impedes the development of a pathologic microenvironment Nat. Med. 2010, 16, 1009-1017
19. Murawaki, Y.; Kusakabe, Y.; Hirayama, C. Serum lysyl oxidase activity in chronic liver disease in comparison with serum levels of prolyl hydroxylase and laminin Hepatology 1991, 14, 1167-1173
20. Reddy, S. K.; Steel, J. L.; Chen, H. W.; DeMateo, D. J.; Cardinal, J.; Behari, J.; Humar, A.; Marsh, J. W.; Geller, D. A.; Tsung, A. Outcomes of curative treatment for hepatocellular cancer in nonalcoholic steatohepatitis versus hepatitis C and alcoholic liver disease Hepatology 2012, 55, 1809-1819
21. Nischalke, H. D.; Berger, C.; Luda, C.; Berg, T.; Muller, T.; Grunhage, F.; Lammert, F.; Coenen, M.; Kramer, B.; Korner, C.; Vidovic, N.; Oldenburg, J.; Nattermann, J.; Sauerbruch, T.; Spengler, U. The PNPLA3 rs738409 148M/M genotype is a risk factor for liver cancer in alcoholic cirrhosis but shows no or weak association in hepatitis C cirrhosis PloS One 2011, 6, e27087
22. McKillop, I. H.; Schrum, L. W. Role of alcohol in liver carcinogenesis Semin. Liver Dis. 2009, 29, 222-232
23. Chen, C. S.; Wu, C. H.; Lai, Y. C.; Lee, W. S.; Chen, H. M.; Chen, R. J.; Chen, L. C.; Ho, Y. S.; Wang, Y. J. NF-κB-activated tissue transglutaminase is involved in ethanol-induced hepatic injury and the possible role of propolis in preventing fibrogenesis Toxicology 2008, 246, 148-157
24. Wu, C. H.; Ho, Y. S.; Tsai, C. Y.; Wang, Y. J.; Tseng, H.; Wei, P. L.; Lee, C. H.; Liu, R. S.; Lin, S. Y. In vitro and in vivo study of phloretin-induced apoptosis in human liver cancer cells involving inhibition of type II glucose transporter Int. J. Cancer 2009, 124, 2210-2219
25. Yang, K. C.; Tsai, C. Y.; Wang, Y. J.; Wei, P. L.; Lee, C. H.; Chen, J. H.; Wu, C. H.; Ho, Y. S. Apple polyphenol phloretin potentiates the anticancer actions of paclitaxel through induction of apoptosis in human hep G2 cells Mol. Carcinog. 2009, 48, 420-431
26. Huang, C. S.; Lee, Y. R.; Chen, C. S.; Tu, S. H.; Wang, Y. J.; Lee, C. H.; Chen, L. C.; Chang, H. W.; Chang, C. H.; Chih-Ming, S.; Wu, C. H.; Ho, Y. S. Long-term ethanol exposure causes human liver cancer cells to become resistant to mitomycin C treatment through the inactivation of bad-mediated apoptosis Mol. Carcinog. 2010, 49, 728-738
27. Monthakantirat, O.; De-Eknamkul, W.; Umehara, K.; Yoshinaga, Y.; Miyase, T.; Warashina, T.; Noguchi, H. Phenolic constituents of the rhizomes of the Thai medicinal plant Belamcanda chinensis with proliferative activity for two breast cancer cell lines J. Nat. Prod. 2005, 68, 361-364
28. Kuttan, R.; Sudheeran, P. C.; Josph, C. D. Turmeric and curcumin as topical agents in cancer therapy Tumori 1987, 73, 29-31
29. Pan, M. H.; Gao, J. H.; Lai, C. S.; Wang, Y. J.; Chen, W. M.; Lo, C. Y.; Wang, M.; Dushenkov, S.; Ho, C. T. Antitumor activity of 3,5,4′- trimethoxystilbene in COLO 205 cells and xenografts in SCID mice Mol. Carcinogen. 2008, 47, 184-196
30. Weng, C. J.; Yang, Y. T.; Ho, C. T.; Yen, G. C. Mechanisms of apoptotic effects induced by resveratrol, dibenzoylmethane, and their analogues on human lung carcinoma cells J. Agric. Food Chem. 2009, 57, 5235-5243
31. Knowles, B. B.; Howe, C. C.; Aden, D. P. Human hepatocellular carcinoma cell lines secrete the major plasma proteins and hepatitis B surface antigen Science 1980, 209, 497-499
32. Eysseric, H.; Gonthier, B.; Soubeyran, A.; Bessard, G.; Saxod, R.; Barret, L. There is not simple method to maintain a constant ethanol concentration in long-term cell culture: keys to a solution applied to the survey of astrocytic ethanol absorption Alcohol 1997, 14, 111-115
33. Pan, M. H.; Huang, M. C.; Wang, Y. J.; Lin, J. K.; Lin, C. H. Induction of apoptosis by hydroxydibenzoylmethane through coordinative modulation of cyclin D3, Bcl-X(L), and Bax, release of cytochrome c, and sequential activation of caspases in human colorectal carcinoma cells J. Agric. Food Chem. 2003, 51, 3977-3984
34. Chen, L. C.; Liu, Y. C.; Liang, Y. C.; Ho, Y. S.; Lee, W. S. Magnolol inhibits human glioblastoma cell proliferation through upregulation of p21/Cip1 J. Agric. Food Chem. 2009, 57, 7331-7337
35. Chen, R. J.; Tsai, S. J.; Ho, C. T.; Pan, M. H.; Ho, Y. S.; Wu, C. H.; Wang, Y. J. Chemopreventive effects of pterostilbene on urethane-induced lung carcinogenesis in mice via the inhibition of EGFR-mediated pathways and the induction of apoptosis and autophagy J. Agric. Food Chem. 2012, 60, 11533-11541
36. Chen, L. C.; Tu, S. H.; Huang, C. S.; Chen, C. S.; Ho, C. T.; Lin, H. W.; Lee, C. H.; Chang, H. W.; Chang, C. H.; Wu, C. H.; Lee, W. S.; Ho, Y. S. Human breast cancer cell metastasis is attenuated by lysyl oxidase inhibitors through down-regulation of focal adhesion kinase and the paxillin-signaling pathway Breast Cancer Res. Treat. 2012, 134, 989-1004
37. Tu, S. H.; Chang, C. C.; Chen, C. S.; Tam, K. W.; Wang, Y. J.; Lee, C. H.; Lin, H. W.; Cheng, T. C.; Huang, C. S.; Chu, J. S.; Shih, N. Y.; Chen, L. C.; Leu, S. J.; Ho, Y. S.; Wu, C. H. Increased expression of enolase alpha in human breast cancer confers tamoxifen resistance in human breast cancer cells Breast Cancer Res. Treat. 2010, 121, 539-553
38. Lee, C. H.; Huang, C. S.; Chen, C. S.; Tu, S. H.; Wang, Y. J.; Chang, Y. J.; Tam, K. W.; Wei, P. L.; Cheng, T. C.; Chu, J. S.; Chen, L. C.; Wu, C. H.; Ho, Y. S. Overexpression and activation of the α9-nicotinic receptor during tumorigenesis in human breast epithelial cells J. Natl. Cancer Inst. 2010, 102, 1322-1335
39. Raucy, J. L.; Lasker, J.; Ozaki, K.; Zoleta, V. Regulation of CYP2E1 by ethanol and palmitic acid and CYP4A11 by clofibrate in primary cultures of human hepatocytes Toxicol. Sci. 2004, 79, 233-241
40. Navasumrit, P.; Ward, T. H.; Dodd, N. J.; O'Connor, P. J. Ethanol-induced free radicals and hepatic DNA strand breaks are prevented in vivo by antioxidants: effects of acute and chronic ethanol exposure Carcinogenesis 2000, 21, 93-99
41. Suh, Y.; Yoon, C. H.; Kim, R. K.; Lim, E. J.; Oh, Y. S.; Hwang, S. G.; An, S.; Yoon, G.; Gye, M. C.; Yi, J. M.; Kim, M. J.; Lee, S. J. Claudin-1 induces epithelial-mesenchymal transition through activation of the c-Abl-ERK signaling pathway in human liver cells Oncogene 2012, 10.1038/onc.2012.505
42. Martin, T. A.; Mason, M. D.; Jiang, W. G. Tight junctions in cancer metastasis Front. Biosci. 2011, 16, 898-936
43. Sato, S.; Trackman, P. C.; Maki, J. M.; Myllyharju, J.; Kirsch, K. H.; Sonenshein, G. E. The Ras signaling inhibitor LOX-PP interacts with Hsp70 and c-Raf to reduce Erk activation and transformed phenotype of breast cancer cells Mol. Cell. Biol. 2011, 31, 2683-2695
44. Yang, P.; Li, Q. J.; Feng, Y.; Zhang, Y.; Markowitz, G. J.; Ning, S.; Deng, Y.; Zhao, J.; Jiang, S.; Yuan, Y.; Wang, H. Y.; Cheng, S. Q.; Xie, D.; Wang, X. F. TGF-β-miR-34a-CCL22 signaling-induced Treg cell recruitment promotes venous metastases of HBV-positive hepatocellular carcinoma Cancer Cell 2012, 22, 291-303
45. Jing, Y.; Han, Z.; Liu, Y.; Sun, K.; Zhang, S.; Jiang, G.; Li, R.; Gao, L.; Zhao, X.; Wu, D.; Cai, X.; Wu, M.; Wei, L. Mesenchymal stem cells in inflammation microenvironment accelerates hepatocellular carcinoma metastasis by inducing epithelial-mesenchymal transition PloS One 2012, 7, e43272
46. Siddikuzzaman; Grace, V. M.; Guruvayoorappan, C. Lysyl oxidase: a potential target for cancer therapy Inflammopharmacology 2011, 19, 117-129
47. Robles, E.; Gomez, T. M. Focal adhesion kinase signaling at sites of integrin-mediated adhesion controls axon pathfinding Nat. Neurosci. 2006, 9, 1274-1283
48. Petit, V.; Boyer, B.; Lentz, D.; Turner, C. E.; Thiery, J. P.; Valles, A. M. Phosphorylation of tyrosine residues 31 and 118 on paxillin regulates cell migration through an association with CRK in NBT-II cells J. Cell Biol. 2000, 148, 957-970
49. Natarajan, V.; Scribner, W. M.; al-Hassani, M.; Vepa, S. Reactive oxygen species signaling through regulation of protein tyrosine phosphorylation in endothelial cells Environ. Health Perspect. 1998, 106 (SUPPL. 5) 1205-1212
50. Taylor, M. A.; Amin, J. D.; Kirschmann, D. A.; Schiemann, W. P. Lysyl oxidase contributes to mechanotransduction-mediated regulation of transforming growth factor-beta signaling in breast cancer cells Neoplasia 2011, 13, 406-418
51. Nellaiappan, K.; Risitano, A.; Liu, G.; Nicklas, G.; Kagan, H. M. Fully processed lysyl oxidase catalyst translocates from the extracellular space into nuclei of aortic smooth-muscle cells J. Cell Biochem. 2000, 79, 576-582
52. Basuroy, S.; Dunagan, M.; Sheth, P.; Seth, A.; Rao, R. K. Hydrogen peroxide activates focal adhesion kinase and c-Src by a phosphatidylinositol 3 kinase-dependent mechanism and promotes cell migration in Caco-2 cell monolayers Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299, G186-G195
53. Takahashi, M.; Furihata, M.; Akimitsu, N.; Watanabe, M.; Kaul, S.; Yumoto, N.; Okada, T. A highly bone marrow metastatic murine breast cancer model established through in vivo selection exhibits enhanced anchorage-independent growth and cell migration mediated by ICAM-1 Clin. Exp. Metastasis 2008, 25, 517-529
54. Pan, M. H.; Sin, Y. H.; Lai, C. S.; Wang, Y. J.; Lin, J. K.; Wang, M.; Ho, C. T. Induction of apoptosis by 1-(2-hydroxy-5-methylphenyl)-3-phenyl-1,3- propanedione through reactive oxygen species production, GADD153 expression, and caspases activation in human epidermoid carcinoma cells J. Agric. Food Chem. 2005, 53, 9039-9049
55. Pan, Y. C.; Li, C. F.; Ko, C. Y.; Pan, M. H.; Chen, P. J.; Tseng, J. T.; Wu, W. C.; Chang, W. C.; Huang, A. M.; Sterneck, E.; Wang, J. M. CEBPD reverses RB/E2F1-mediated gene repression and participates in HMDB-induced apoptosis of cancer cells Clin. Cancer Res. 2010, 16, 5770-5780
56. Zhang, L.; Zhou, G.; Song, W.; Tan, X.; Guo, Y.; Zhou, B.; Jing, H.; Zhao, S.; Chen, L. Pterostilbene protects vascular endothelial cells against oxidized low-density lipoprotein-induced apoptosis in vitro and in vivo Apoptosis 2012, 17, 25-36
57. Pan, M. H.; Chiou, Y. S.; Chen, W. J.; Wang, J. M.; Badmaev, V.; Ho, C. T. Pterostilbene inhibited tumor invasion via suppressing multiple signal transduction pathways in human hepatocellular carcinoma cells Carcinogenesis 2009, 30, 1234-1242
58. Papachroni, K. K.; Piperi, C.; Levidou, G.; Korkolopoulou, P.; Pawelczyk, L.; Diamanti-Kandarakis, E.; Papavassiliou, A. G. Lysyl oxidase interacts with AGE signalling to modulate collagen synthesis in polycystic ovarian tissue J. Cell. Mol. Med. 2010, 14, 2460-2469