Suppression of EGF-induced tumor cell migration and matrix metalloproteinase-9 expression by capsaicin via the inhibition of EGFR-mediated FAK/Akt, PKC/Raf/ERK, p38 MAPK, and AP-1 signaling

Molecular Nutrition and Food Research

Volumn 55, Issue 4, 2011, Pages 594-605

  Hwang, Yong Pil ^a   Yun, Hyo Jeong ^a   Choi, Jae Ho ^a   Han, Eun Hee ^a   Kim, Hyung Gyun ^a   Song, Gye Yong ^a   Kwon, Kwang il ^a   Jeong, Tae Cheon ^b   Jeong, Hye Gwang ^a  

^a Chungnam National University   (South Korea)

^b Yeungnam University   (South Korea)

Author keywords

Anti metastatic; AP 1; Capsaicin; EGF; MMP 9

Indexed keywords

ANTINEOPLASTIC AGENT; CAPSAICIN; EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GELATINASE A; GELATINASE B; HORMONE ANTAGONIST; MATRIX METALLOPROTEINASE 14; MESSENGER RNA; MMP14 PROTEIN, HUMAN; MMP2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR AP 1;

ARTICLE; CANCER INVASION; CELL MOTION; CELL NUCLEUS; DOWN REGULATION; DRUG ANTAGONISM; DRUG EFFECT; FIBROSARCOMA; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; CAPSAICIN; CELL LINE, TUMOR; CELL MOVEMENT; CELL NUCLEUS; DOWN-REGULATION; EPIDERMAL GROWTH FACTOR; FIBROSARCOMA; GENE EXPRESSION REGULATION, NEOPLASTIC; HORMONE ANTAGONISTS; HUMANS; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; NEOPLASM INVASIVENESS; PHOSPHORYLATION; PROTEIN TRANSPORT; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-1;

EID: 79953301141     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201000292     Document Type: Article

References (40)

1. Liotta, L. A., Steeg, P. S., Stetler-Stevenson, W. G., Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell 1991, 64, 327-336.
2. Deryugina, E. I., Luo, G. X., Reisfeld, R. A., Bourdon, M. A. et al., Tumor cell invasion through matrigel is regulated by activated matrix metalloproteinase-2. Anticancer Res. 1997, 17, 3201-3210.
3. Westermarck, J., Kahari, V. M., Regulation of matrix metalloproteinase expression in tumor invasion. FASEB J. 1999, 13, 781-792.
4. Van den Steen, P., Dubois, B., Nelissen, I., Rudd, P. et al, Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9). Crit. Rev. Biochem. Mol. Biol. 2002, 37, 375-536.
5. Sato, H., Takino, T., Okada, Y., Cao, J. et al., A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 1994, 370, 61-65.
6. Yan, C., Boyd, D. D., Regulation of matrix metalloproteinase gene expression. J. Cell. Physiol. 2007, 211, 19-26.
7. Cho, H. J., Kang, J. H., Kwak, J. Y., Lee, T. S. et al., Ascofuranone suppresses PMA-mediated matrix metalloproteinase-9 gene activation through the Ras/Raf/MEK/ERK- and Ap1-dependent mechanisms. Carcinogenesis 2007, 28, 1104-1110.
8. Kajanne, R., Miettinen, P., Mehlem, A., Leivonen, S. K. et al., EGF-R regulates MMP function in fibroblasts through MAPK and AP-1 pathways. J. Cell. Physiol. 2007, 212, 489-497.
9. Liu, Z., Klominek, J., Regulation of matrix metalloproteaseactivity in malignant mesothelioma cell lines by growth factors. Thorax 2003, 58, 198-203.
10. Nutt, J., Durkan, G., Mellon, J., Lunec, J., Matrix metalloproteinases (MMPs) in bladder cancer: the induction of MMP9 by epidermal growth factor and its detection in urine. BJU Int. 2003, 91, 99-104.
11. Marmor, M. D., Skaria, K. B., Yarden, Y., Signal transduction and oncogenesis by ErbB/HER receptors. Int. J. Radiat. Oncol. Biol. Phys. 2004, 58, 903-913.
12. Yatabe, Y., Takahashi, T., Mitsudomi, T., Epidermal growth factor receptor gene amplification is acquired in association with tumor progression of EGFR-mutated lung cancer. Cancer Res. 2008, 68, 2106-2111.
13. Prenzel, N., Fischer, O. M., Streit, S., Hart, S. et al., The epidermal growth factor receptor family as a central element for cellular signal transduction and diversification. Endocr. Relat. Cancer 2001, 8, 11-31.
14. Yarden, Y., Sliwkowski, M. X., Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2001, 2, 127-137.
15. Cheresh, D. A., Leng, J., Klemke, R. L., Regulation of cell contraction and membrane ruffling by distinct signals in migratory cells. J. Cell Biol. 1999, 146, 1107-1116.
16. Glading, A., Chang, P., Lauffenburger, D. A., Wells, A., Epidermal growth factor receptor activation of calpain is required for fibroblast motility and occurs via an ERK/MAP kinase signaling pathway. J. Biol. Chem. 2000, 275, 2390-2398.
17. Carlomagno, F., Santoro, M., Receptor tyrosine kinases as targets for anticancer therapeutics. Curr. Med. Chem. 2005, 12, 1773-1781.
18. Surh, Y. J., Cancer chemoprevention with dietary phytochemicals. Nat. Rev. Cancer 2003, 3, 768-780.
19. Sporn, M. B., Suh, N., Chemoprevention of cancer. Carcinogenesis 2000, 21, 525-530.
20. Lippman, S. M., Hong, W. K., Cancer prevention science and practice. Cancer Res. 2002, 62, 5119-5125.
21. Cordell, G. A., Araujo, O. E., Capsaicin: Identification, nomenclature, and pharmacotherapy. Ann. Pharmacother. 1993, 27, 330-336.
22. Matucci Cerinic, M., McCarthy, G., Lombardi, A., Pignone, A. et al., Neurogenic influences in arthritis: potential modification by capsaicin. J. Rheumatol. 1995, 22, 1447-1449.
23. Sindrup, S. H., Jensen, T. S., Efficacy of pharmacological treatments of neuropathic pain: an update and effect related to mechanism of drug action. Pain 1999, 83, 389-400.
24. Aggarwal, B. B., Shishodia, S., Molecular targets of dietary agents for prevention and therapy of cancer. Biochem. Pharmacol. 2006, 71, 1397-1421.
25. Amantini, C., Mosca, M., Nabissi, M., Lucciarini, R. et al., Capsaicin-induced apoptosis of glioma cells is mediated by TRPV1 vanilloid receptor and requires p38 MAPK activation. J. Neurochem. 2007, 102. 977-990.
26. Huang, S. P., Chen, J. C., Wu, C. C., Chen, C. T. et al., Capsaicin-induced apoptosis in human hepatoma HepG2 cells. Anticancer Res. 2009, 29, 165-174.
27. Shin, D. H., Kim, O. H., Jun, H. S., Kang, M. K., Inhibitory effect of capsaicin on B16-F10 melanoma cell migration via the phosphatidylinositol 3-kinase/Akt/Rac1 signal pathway. Exp. Mol. Med. 2008, 40, 486-494.
28. Eberhardt, W., Schulze, M., Engels, C., Klasmeier, E. et al., Glucocorticoid-mediated suppression of cytokine-induced matrix metalloproteinase-9 expression in rat mesangial cells: involvement of nuclear factor-kappaB and Ets transcription factors. Mol. Endocrinol. 2002, 16, 1752-1766.
29. Lee, K. J., Hwang, S. J., Choi, J. H., Jeong, H. G., Saponins derived from the roots of Platycodon grandiflorum inhibit HT-1080 cell invasion and MMPs activities: regulation of NF-kappaB activation via ROS signal pathway. Cancer Lett. 2008, 268, 233-243.
30. Johnson, M. R., Wang, K., Smith, J. B., Heslin, M. J. et al., Quantitation of dihydropyrimidine dehydrogenase expression by real-time reverse transcription polymerase chain reaction. Anal. Biochem. 2000, 278, 175-184.
31. Hwang, Y. P., Yun, H. J., Kim, H. G., Han, E. H. et al., Suppression of PMA-induced tumor cell invasion by dihydroartemisinin via inhibition of PKCalpha/Raf/MAPKs and NF-kappaB/AP-1-dependent mechanisms. Biochem. Pharmacol. 2010, 79, 1714-1726.
32. Han, E. H., Kim, J. Y., Kim, H. K., Hwang, Y. P. et al., o, p'-DDT induces cyclooxygenase-2 gene expression in murine macrophages: Role of AP-1 and CRE promoter elements and PI3-kinase/Akt/MAPK signaling pathways. Toxicol. Appl. Pharmacol. 2008, 233, 333-342.
33. Kazes, I., Elalamy, I., Sraer, J. D., Hatmi, M. et al, Platelet release of trimolecular complex components MT1-MMP/TIMP2/MMP2: involvement in MMP2 activation and platelet aggregation. Blood 2000, 96, 3064-3069.
34. Dickinson, D. A., Iles, K. E., Zhang, H., Blank, V. et al., Curcumin alters EpRE and AP-1 binding complexes and elevates glutamate-cysteine ligase gene expression. FASEB J. 2003, 17, 473-475.
35. Hahm, E. R., Gho, Y. S., Park, S., Park, C. et al., Synthetic curcumin analogs inhibit activator protein-1 transcription and tumor-induced angiogenesis. Biochem. Biophys. Res. Commun. 2004, 321, 337-344.
36. Wang, H. H., Hsieh, H. L., Wu, C. Y., Sun, C. C. et al., Oxidized low-density lipoprotein induces matrix metalloproteinase-9 expression via a p42/p44 and JNK-dependent AP-1 pathway in brain astrocytes. Glia 2009, 57, 24-38.
37. Jun, H. S., Park, T., Lee, C. K., Kang, M. K. et al., Capsaicin induced apoptosis of B16-F10 melanoma cells through down-regulation of Bcl-2. Food Chem. Toxicol. 2007, 45, 708-715.
38. Egeblad, M., Werb, Z., New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2002, 2, 161-174.
39. Surh, Y. J., Han, S. S., Keum, Y. S., Seo, H. J. et al., Inhibitory effects of curcumin and capsaicin on phorbol ester-induced activation of eukaryotic transcription factors, NF-kappaB and AP-1. Biofactors 2000, 12, 107-112.
40. Oyagbemi, A. A., Saba, A. B., Azeez, O. I., Capsaicin: a novel chemopreventive molecule and its underlying molecular mechanisms of action. Indian J. Cancer 2010, 47, 53-58.