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Eco/Toxicology

Cardiotoxin III suppresses the invasiveness of MDA-MB-231 cells by targeting proto-oncogene tyrosine-protein kinase Src and reversing mesenchymal-to-epithelial transition

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Pages 942-958 | Received 14 Aug 2015, Accepted 23 Dec 2015, Published online: 22 Jan 2016

References

  • Avizienyte, E., and M.C. Frame. 2005. “Src and FAK Signalling Controls Adhesion Fate and The Epithelial-To-Mesenchymal Transition.” Current Opinion in Cell Biology 17 (5): 542–547.
  • Baranwal, S., and S.K. Alahari. 2009. “Molecular Mechanisms Controlling E-Cadherin Expression in Breast Cancer.” Biochemical and Biophysical Research Communications 384 (1): 6–11.
  • Barrallo-Gimeno, A., and M.A. Nieto. 2005. “The Snail Genes as Inducers of Cell Movement and Survival: Implications in Development and Cancer.” Development 132 (14): 3151–3161.
  • Batlle, E., E. Sancho, C. Franci, D. Dominguez, M. Monfar, J. Baulida, and A. Garcia De Herreros. 2000. “The Transcription Factor Snail is A Repressor of E-Cadherin Gene Expression in Epithelial Tumour Cells.” Nature Cell Biology 2 (2): 84–89.
  • Betapudi, V., L.S. Licate, and T.T. Egelhoff. 2006. “Distinct Roles of Nonmuscle Myosin II Isoforms in The Regulation of MDA-MB-231 Breast Cancer Cell Spreading and Migration.” Cancer Research 66 (9): 4725–4733.
  • Blick, T., E. Widodo, H. Hugo, M. Waltham, M.E. Lenburg, R.M. Neve, and E.W. Thompson. 2008. “Epithelial Mesenchymal Transition Traits in Human Breast Cancer Cell Lines.” Clinical & Experimental Metastasis 25 (6): 629–642.
  • Brown, M.C., and C.E. Turner. 2004. “Paxillin: Adapting to Change.” Physiological Reviews 84 (4): 1315–1339.
  • Cavallaro, U., and G. Christofori. 2004. “Multitasking in Tumor Progression: Signaling Functions of Cell Adhesion Molecules.” Annals of the New York Academy of Sciences 1014: 58–66.
  • Chien, C.M., S.H. Yang, L.S. Chang, and S.R. Lin. 2008. “Involvement of Both Endoplasmic Reticulum- and Mitochondria-Dependent Pathways in Cardiotoxin III-Induced Apoptosis in HL-60 cells.” Clinical and Experimental Pharmacology & Physiology 35 (9): 1059–1064.
  • Chiu, C.C., K.L. Lin, C.M. Chien, L.S. Chang, and S.R. Lin. 2009. “Effects of Cardiotoxin III on NF-kappaB Function, Proliferation, and Apoptosis in Human Breast MCF-7 Cancer Cells.” Oncology Research 17 (7): 311–321.
  • Chiu, H.Y., K.H. Sun, S.Y. Chen, H.H. Wang, M.Y. Lee, Y.C. Tsou, S.C. Jwo, G.H. Sun, and S.J. Tang. 2012. “Autocrine CCL2 Promotes Cell Migration and Invasion Via PKC Activation and Tyrosine Phosphorylation of Paxillin in Bladder Cancer Cells.” Cytokine 59 (2): 423–432.
  • de Herreros, A.G., S. Peiro, M. Nassour, and P. Savagner. 2010. “Snail Family Regulation and Epithelial Mesenchymal Transitions in Breast Cancer Progression.” Journal of Mammary Gland Biology and Neoplasia 15 (2): 135–147.
  • Deryugina, E.I., and J.P. Quigley. 2006. “Matrix Metalloproteinases and Tumor Metastasis.” Cancer and Metastasis Reviews 25 (1): 9–34.
  • DeSantis, C., R. Siegel, P. Bandi, and A. Jemal. 2011. “Breast Cancer Statistics, 2011.” CA: A Cancer Journal for Clinicians 61 (6): 409–418
  • Dhasarathy, A., D. Phadke, D. Mav, R.R. Shah, and P.A. Wade. 2011. “The Transcription Factors Snail and Slug Activate The Transforming Growth Factor-Beta Signaling Pathway in Breast Cancer.” PLoS One 6 (10): e26514.
  • Drasin, D.J., T.P. Robin, and H.L. Ford. 2011. “Breast Cancer Epithelial-To-Mesenchymal Transition: Examining The Functional Consequences of Plasticity.” Breast Cancer Research 13 (6): 226.
  • Dufton, M.J., and R.C. Hider. 1988. “Structure and Pharmacology of Elapid Cytotoxins.” Pharmacology & Therapeutics 36 (1): 1–40.
  • Foroni, C., M. Broggini, D. Generali, and G. Damia. 2012. “Epithelial-Mesenchymal Transition and Breast Cancer: Role, Molecular Mechanisms and Clinical Impact.” Cancer Treatment Reviews 38 (6): 689–697.
  • Grunert, S., M. Jechlinger, and H. Beug. 2003. “Diverse Cellular and Molecular Mechanisms Contribute to Epithelial Plasticity and Metastasis.” Nature Reviews Molecular Cell Biology 4 (8): 657–665.
  • Guo, W., and F.G. Giancotti. 2004. “Integrin Signalling During Tumour Progression.” Nature Reviews Molecular Cell Biology 5 (10): 816–826.
  • Hazan, R.B., R. Qiao, R. Keren, I. Badano, and K. Suyama. 2004. “Cadherin Switch in Tumor Progression.” Annals of the New York Academy of Sciences 1014: 155–163.
  • Huber, M.A., N. Azoitei, B. Baumann, S. Grunert, A. Sommer, H. Pehamberger, N. Kraut, H. Beug, and T. Wirth. 2004. “NF-kappaB is Essential for Epithelial–Mesenchymal Transition and Metastasis in A Model of Breast Cancer Progression.” Journal of Clinical Investigation 114 (4): 569–581.
  • Hugo, H., M.L. Ackland, T. Blick, M.G. Lawrence, J.A. Clements, E.D. Williams, and E.W. Thompson. 2007. “Epithelial–Mesenchymal and Mesenchymal–Epithelial Transitions in Carcinoma Progression.” Journal of Cellular Physiology 213 (2): 374–383.
  • Irby, R.B., and T.J. Yeatman. 2000. “Role of Src Expression and Activation in Human Cancer.” Oncogene 19 (49): 5636–4642.
  • Kalluri, R., and R.A. Weinberg. 2009. “The Basics of Epithelial-Mesenchymal Transition.” Journal of Clinical Investigation 119 (6): 1420–1428.
  • Karihtala, P., P. Auvinen, S. Kauppila, K.M. Haapasaari, A. Jukkola-Vuorinen, and Y. Soini. 2013. “Vimentin, Zeb1 and Sip1 are Up-Regulated in Triple-Negative and Basal-Like Breast Cancers: Association with an Aggressive Tumour Phenotype.” Breast Cancer Research and Treatment 138 (1): 81–90.
  • Kessenbrock, K., V. Plaks, and Z. Werb. 2010. “Matrix Metalloproteinases: Regulators of The Tumor Microenvironment.” Cell 141 (1): 52–67.
  • Li, C.W., W. Xia, L. Huo, S.O. Lim, Y. Wu, J.L. Hsu, C.H. Chao, et al. 2012. “Epithelial-Mesenchymal Transition Induced by TNF-Alpha Requires NF-kappa B-Mediated Transcriptional Upregulation of Twist1.” Cancer Research 72 (5): 1290–1300.
  • Libra, M., A. Scalisi, N. Vella, S. Clementi, R. Sorio, F. Stivala, D.A. Spandidos, and C. Mazzarino. 2009. “Uterine Cervical Carcinoma: Role of Matrix Metalloproteinases (Review).” International Journal of Oncology 34 (4): 897–903.
  • Lien, H.C., Y.H. Hsiao, Y.S. Lin, Y.T. Yao, H.F. Juan, W.H. Kuo, M.C. Hung, K.J. Chang, and F.J. Hsieh. 2007. “Molecular Signatures of Metaplastic Carcinoma of The Breast by Large-Scale Transcriptional Profiling: Identification of Genes Potentially Related to Epithelial–Mesenchymal Transition.” Oncogene 26 (57): 7859–7871.
  • Lilienbaum, A., and D. Paulin. 1993. “Activation of The Human Vimentin Gene by The Tax Human T-cell Leukemia Virus. I. Mechanisms of Regulation by the NF-kappa B Transcription Factor.” Journal of Biological Chemistry 268 (3): 2180–2188.
  • Lin, K.L., J.C. Su, C.M. Chien, P.W. Chuang, L.S. Chang, and S.R. Lin. 2010. “Down-Regulation of the JAK2/PI3K-Mediated Signaling Activation is Involved in Taiwan Cobra Cardiotoxin III-Induced Apoptosis of Human Breast MDA-MB-231 Cancer Cells.” Toxicon 55 (7): 1263–1273.
  • Lin, S.R., L.S. Chang, and K.L. Chang. 2002. “Separation and Structure–Function Studies of Taiwan Cobra Cardiotoxins.” Journal of Protein Chemistry 21 (2): 81–86.
  • Liu, X., and R. Feng. 2010. “Inhibition of Epithelial to Mesenchymal Transition in Metastatic Breast Carcinoma Cells by c-Src Suppression.” Acta Biochimica et Biophysica Sinica 42 (7): 496–501.
  • Ma, J.G., H. Huang, S.M. Chen, Y. Chen, X.L. Xin, L.P. Lin, J. Ding, H. Liu, and L.H. Meng. 2011. “PH006, A Novel and Selective Src Kinase Inhibitor, Suppresses Human Breast Cancer Growth and Metastasis in Vitro and in Vivo.” Breast Cancer Research and Treatment 130 (1): 85–96.
  • Mandal, M., J.N. Myers, S.M. Lippman, F.M. Johnson, M.D. Williams, S. Rayala, K. Ohshiro, et al. 2008. “Epithelial to Mesenchymal Transition in Head and Neck Squamous Carcinoma: Association of Src Activation with E-Cadherin Down-Regulation, Vimentin Expression, and Aggressive Tumor Features.” Cancer 112 (9): 2088–2100.
  • Martin, T.A., A. Goyal, G. Watkins, and W.G. Jiang. 2005. “Expression of The Transcription Factors Snail, Slug, and Twist and Their Clinical Significance in Human Breast Cancer.” Annals of Surgical Oncology 12 (6): 488–496.
  • McLean, G.W., N.O. Carragher, E. Avizienyte, J. Evans, V.G. Brunton, and M.C. Frame. 2005. “The Role of Focal-Adhesion Kinase in Cancer - A New Therapeutic Opportunity.” Nature Reviews Cancer 5 (7): 505–515.
  • Min, C., S.F. Eddy, D.H. Sherr, and G.E. Sonenshein. 2008. “NF-kappaB and Epithelial to Mesenchymal Transition of Cancer.” Journal of Cellular Biochemistry 104 (3): 733–744.
  • Montserrat, N., A. Gallardo, D. Escuin, L. Catasus, J. Prat, F.J. Gutierrez-Avigno, G. Peiro, A. Barnadas, and E. Lerma. 2011. “Repression of E-Cadherin by SNAIL, ZEB1, and TWIST in Invasive Ductal Carcinomas of The Breast: A Cooperative Effort?” Human Pathology 42 (1): 103–110.
  • Nagathihalli, N.S., and N.B. Merchant. 2012. “Src-Mediated Regulation of E-Cadherin and EMT in Pancreatic Cancer.” Frontiers in Bioscience 17: 2059–2069.
  • Nieto, M.A. 2002. “The Snail Superfamily of Zinc-Finger Transcription Factors.” Nature Reviews Molecular Cell Biology 3 (3): 155–166.
  • Radisky, E.S., and D.C. Radisky. 2010. “Matrix Metalloproteinase-Induced Epithelial–Mesenchymal Transition in Breast Cancer.” Journal of Mammary Gland Biology and Neoplasia 15 (2): 201–212.
  • Ranogajec, I., J. Jakic-Razumovic, V. Puzovic, and J. Gabrilovac. 2012. “Prognostic Value of Matrix Metalloproteinase-2 (MMP-2), Matrix Metalloproteinase-9 (MMP-9) and Aminopeptidase N/CD13 in Breast Cancer Patients.” Medical Oncology 29 (2): 561–569.
  • Sarrio, D., S.M. Rodriguez-Pinilla, D. Hardisson, A. Cano, G. Moreno-Bueno, and J. Palacios. 2008. “Epithelial–Mesenchymal Transition in Breast Cancer Relates to The Basal-Like Phenotype.” Cancer Research 68 (4): 989–997.
  • Scorilas, A., A. Karameris, N. Arnogiannaki, A. Ardavanis, P. Bassilopoulos, T. Trangas, and M. Talieri. 2001. “Overexpression of Matrix-Metalloproteinase-9 in Human Breast Cancer: A Potential Favourable Indicator in Node-Negative Patients.” British Journal of Cancer 84 (11): 1488–1496.
  • Shah, P.P., M.Y. Fong, and S.S. Kakar. 2012. “PTTG Induces EMT Through Integrin Alpha Vbeta3-focal Adhesion Kinase Signaling in Lung Cancer Cells.” Oncogene 31 (26): 3124–3135.
  • Sharma, A., and B.J. Mayer. 2008. “Phosphorylation of p130Cas Initiates Rac Activation and Membrane Ruffling.” BMC Cell Biology 9: 50–65.
  • Siegel, R., E. Ward, O. Brawley, and A. Jemal. 2011. “Cancer Statistics, 2011: The Impact of Eliminating Socioeconomic and Racial Disparities on Premature Cancer Deaths.” CA: A Cancer Journal for Clinicians 61 (4): 212–236.
  • Sivakumar, R., H. Koga, K. Selvendiran, M. Maeyama, T. Ueno, and M. Sata. 2009. “Autocrine Loop for IGF-I Receptor Signaling in SLUG-Mediated Epithelial-Mesenchymal Transition.” International Journal of Oncology 34 (2): 329–338.
  • Soini, Y., H. Tuhkanen, R. Sironen, I. Virtanen, V. Kataja, P. Auvinen, A. Mannermaa, and V.M. Kosma. 2011. “Transcription Factors zeb1, Twist and Snail in Breast Carcinoma.” BMC Cancer 11: 73–81.
  • Summy, J.M., and G.E. Gallick. 2003. “Src Family Kinases in Tumor Progression and Metastasis.” Cancer Metastasis Reviews 22 (4): 337–358.
  • Thiery, J.P. 2002. “Epithelial–Mesenchymal Transitions in Tumour Progression.” Nature Reviews Cancer 2 (6): 442–454.
  • Thiery, J.P. 2003. “Epithelial–Mesenchymal Transitions in Development and Pathologies.” Current Opinion in Cell Biology 15 (6): 740–746.
  • Thiery, J.P., H. Acloque, R.Y. Huang, and M.A. Nieto. 2009. “Epithelial–Mesenchymal Transitions in Development and Disease.” Cell 139 (5): 871–890.
  • Tomaskovic-Crook, E., E.W. Thompson, and J.P. Thiery. 2009. “Epithelial to Mesenchymal Transition and Breast Cancer.” Breast Cancer Research 11 (6): 213.
  • Tsai, P.C., C.L. Chu, C.C. Chiu, L.S. Chang, and S.R. Lin. 2013. “Inhibition of Src Activation with Cardiotoxin III Blocks Migration and Invasion of MDA-MB-231 Cells.” Toxicon 74: 56–67.
  • Tsai, P.C., C.L. Chu, C.C. Chiu, L.S. Chang, and S.R. Lin. 2014. “Cardiotoxin III Suppresses Hepatocyte Growth Factor-Stimulated Migration and Invasion of MDA-MB-231 Cells.” Cell Biochemistry and Function 32 (6): 485–495.
  • Tsai, P.C., C.Y. Hsieh, C.C. Chiu, C.K. Wang, L.S. Chang, and S.R. Lin. 2012. “Cardiotoxin III Suppresses MDA-MB-231 Cell Metastasis Through The Inhibition of EGF/EGFR-Mediated Signaling Pathway.” Toxicon 60 (5): 734–743.
  • van Roy, F., and G. Berx. 2008. “The Cell-Cell Adhesion Molecule E-Cadherin.” Cellular and Molecular Life Sciences 65 (23): 3756–3788.
  • Voulgari, A., and A. Pintzas. 2009. “Epithelial–Mesenchymal Transition in Cancer Metastasis: Mechanisms, Markers and Strategies to Overcome Drug Resistance in The Clinic.” Biochimica et Biophysica Acta 1796 (2): 75–90.
  • Vuoriluoto, K., H. Haugen, S. Kiviluoto, J.P. Mpindi, J. Nevo, C. Gjerdrum, C. Tiron, J.B. Lorens, and J. Ivaska. 2011. “Vimentin Regulates EMT Induction by Slug and Oncogenic H-Ras and Migration by Governing Axl Expression in Breast Cancer.” Oncogene 30 (12): 1436–1448.
  • Wang, Y., J. Shi, K. Chai, X. Ying, and B.P. Zhou. 2013. “The Role of Snail in EMT and Tumorigenesis.” Current Cancer Drug Targets 13 (9): 963–972.
  • Wei, J., G. Xu, M. Wu, Y. Zhang, Q. Li, P. Liu, T. Zhu, et al. 2008. “Overexpression of Vimentin Contributes to Prostate Cancer Invasion and Metastasis via src Regulation.” Anticancer Research 28 (1A): 327–334.
  • Willipinski-Stapelfeldt, B., S. Riethdorf, V. Assmann, U. Woelfle, T. Rau, G. Sauter, J. Heukeshoven, and K. Pantel. 2005. “Changes in Cytoskeletal Protein Composition Indicative of an Epithelial–Mesenchymal Transition in Human Micrometastatic and Primary Breast Carcinoma Cells.” Clinical Cancer Research 11 (22): 8006–8014.
  • Yang, J., J.A. Eddy, Y. Pan, A. Hategan, I. Tabus, Y. Wang, D. Cogdell, et al. 2010. “Integrated Proteomics and Genomics Analysis Reveals A Novel Mesenchymal to Epithelial Reverting Transition in Leiomyosarcoma Through Regulation of Slug.” Molecular & Cellular Proteomics 9 (11): 2405–2413.
  • Yang, S.H., C.M. Chien, L.S. Chang, and S.R. Lin. 2007. “Involvement of c-jun N-Terminal Kinase in G2/M Arrest and Caspase-Mediated Apoptosis Induced by Cardiotoxin III (Naja Naja Atra) in K562 Leukemia Cells.” Toxicon 49 (7): 966–974.

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