Treatment with the vascular disruptive agent OXi4503 induces an immediate and widespread epithelial to mesenchymal transition in the surviving tumor

Cancer Medicine

Volumn 2, Issue 5, 2013, Pages 595-610

  Fifis, Theodora ^a   Nguyen, Linh ^a   Malcontenti Wilson, Cathy ^a   Chan, Lie Sam ^a   Nunes Costa, Patricia Luiza ^a   Daruwalla, Jurstine ^a   Nikfarjam, Mehrdad ^a   Muralidharan, Vijayaragavan ^a   Waltham, Mark ^b   Thompson, Erik W ^a,b   Christophi, Christopher ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

EMT; Growth factor; Hypoxia; OXi4503; Vascular disruptive agent; ZEB1

Indexed keywords

BETA CATENIN; COMBRETASTATIN A1 PHOSPHATE; DOXORUBICIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PIRARUBICIN; SCATTER FACTOR; SUNITINIB; TRANSCRIPTION FACTOR ZEB1; TRANSFORMING GROWTH FACTOR BETA; UVOMORULIN; VASCULOTROPIN; VIMENTIN;

ABLATION THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC THERAPY; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CHEMOTHERAPY; CELL SURVIVAL; COLORECTAL LIVER METASTASIS; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; HYPOXIA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SINGLE DRUG DOSE; TUMOR CELL; TUMOR NECROSIS; TUMOR RESISTANCE; UPREGULATION;

EMT; GROWTH FACTOR; HYPOXIA; OXI4503; VASCULAR DISRUPTIVE AGENT; ZEB1;

ANGIOGENIC PROTEINS; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BETA CATENIN; CADHERINS; CELL HYPOXIA; COLORECTAL NEOPLASMS; DIPHOSPHATES; DOWN-REGULATION; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LIVER NEOPLASMS; MALE; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, INBRED CBA; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; NEOPLASM, RESIDUAL; STILBENES; UP-REGULATION;

EID: 84902149320     PISSN: None     EISSN: 20457634     Source Type: Journal    
DOI: 10.1002/cam4.109     Document Type: Article

References (46)

1. Solyanik, G. I. 2010. Multifactorial nature of tumor drug resistance. Exp. Oncol. 32:181-185.
2. Bergers, G., and D. Hanahan. 2008. Modes of resistance to anti-angiogenic therapy. Nat. Rev. Cancer 8:592-603.
3. Rice, L., C. Pampo, S. Lepler, A. M. Rojiani, and D. W. Siemann. 2011. Support of a free radical mechanism for enhanced antitumor efficacy of the microtubule disruptor OXi4503. Microvasc. Res. 81:44-51.
4. Tozer, G. M., C. Kanthou, and B. C. Baguley. 2005. Disrupting tumour blood vessels. Nat. Rev. Cancer 5:423-435.
5. Nguyen, L., T. Fifis, C. Malcontenti-Wilson, L. S. Chan, P. L. Costa, M. Nikfarjam, et al. 2012. Spatial morphological and molecular differences within solid tumors may contribute to the failure of vascular disruptive agent treatments. BMC Cancer 12:522.
6. Shaked, Y., A. Ciarrocchi, M. Franco, C. R. Lee, S. Man, A. M. Cheung, et al. 2006. Therapy-induced acute recruitment of circulating endothelial progenitor cells to tumors. Science 313:1785-1787.
7. Allavena, P., A. Sica, C. Garlanda, and A. Mantovani. 2008. The Yin-Yang of tumor-associated macrophages in neoplastic progression and immune surveillance. Immunol. Rev. 222:155-161.
8. DeNardo, D. G., J. B. Barreto, P. Andreu, L. Vasquez, D. Tawfik, N. Kolhatkar, et al. 2009. CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell 16:91-102.
9. Arumugam, T., V. Ramachandran, K. F. Fournier, H. Wang, L. Marquis, J. L. Abbruzzese, et al. 2009. Epithelial to mesenchymal transition contributes to drug resistance in pancreatic cancer. Cancer Res. 69:5820-5828.
10. Creighton, C. J., X. Li, M. Landis, J. M. Dixon, V. M. Neumeister, A. Sjolund, et al. 2009. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc. Natl. Acad. Sci. USA 106:13820-13825.
11. Kuruppu, D., C. Christophi, J. F. Bertram, and P. E. O'Brien. 1996. Characterization of an animal model of hepatic metastasis. J. Gastroenterol. Hepatol. 11:26-32.
12. Eckhardt, B. L., B. S. Parker, R. K. van Laar, C. M. Restall, A. L. Natoli, M. D. Tavaria, et al. 2005. Genomic analysis of a spontaneous model of breast cancer metastasis to bone reveals a role for the extracellular matrix. Mol. Cancer Res. 3:1-13.
13. Chan, L. S., C. Malcontenti-Wilson, V. Muralidharan, and C. Christophi. 2007. Effect of vascular targeting agent Oxi4503 on tumor cell kinetics in a mouse model of colorectal liver metastasis. Anticancer Res. 27:2317-2323.
14. Daruwalla, J., M. Nikfarjam, K. Greish, C. Malcontenti-Wilson, V. Muralidharan, C. Christophi, et al. 2010. In vitro and in vivo evaluation of tumor targeting styrene-maleic acid copolymer-pirarubicin micelles: survival improvement and inhibition of liver metastases. Cancer Sci. 101:1866-1874.
15. Fifis, T., C. Malcontenti-Wilson, J. Amijoyo, B. Anggono, V. Muralidharan, M. Nikfarjam, et al. 2011. Changes in growth factor levels after thermal ablation in a murine model of colorectal liver metastases. HPB (Oxford) 13:246-255.
16. Rofstad, E. K., and K. Maseide. 1999. Radiobiological and immunohistochemical assessment of hypoxia in human melanoma xenografts: acute and chronic hypoxia in individual tumours. Int. J. Radiat. Biol. 75:1377-1393.
17. Brabletz, T., F. Hlubek, S. Spaderna, O. Schmalhofer, E. Hiendlmeyer, A. Jung, et al. 2005. Invasion and metastasis in colorectal cancer: epithelial-mesenchymal transition, mesenchymal-epithelial transition, stem cells and beta-catenin. Cells Tissues Organs 179:56-65.
18. Spaderna, S., O. Schmalhofer, F. Hlubek, G. Berx, A. Eger, S. Merkel, et al. 2006. A transient, EMT-linked loss of basement membranes indicates metastasis and poor survival in colorectal cancer. Gastroenterology 131:830-840.
19. Neo, J. H., C. Malcontenti-Wilson, V. Muralidharan, and C. Christophi. 2007. Effect of ACE inhibitors and angiotensin II receptor antagonists in a mouse model of colorectal cancer liver metastases. J. Gastroenterol. Hepatol. 22:577-584.
20. Buchler, P., H. A. Reber, M. Buchler, S. Shrinkante, M. W. Buchler, H. Friess, et al. 2003. Hypoxia-inducible factor 1 regulates vascular endothelial growth factor expression in human pancreatic cancer. Pancreas 26:56-64.
21. Gregory, P. A., C. P. Bracken, E. Smith, A. G. Bert, J. A. Wright, S. Roslan, et al. 2011. An autocrine TGF-beta/ZEB/miR-200 signaling network regulates establishment and maintenance of epithelial-mesenchymal transition. Mol. Biol. Cell 22:1686-1698.
22. Scarpino, S., E. Duranti, A. Stoppacciaro, E. Pilozzi, G. Natoli, S. Sciacchitano, et al. 2009. COX-2 is induced by HGF stimulation in Met-positive thyroid papillary carcinoma cells and is involved in tumour invasiveness. J. Pathol. 218:487-494.
23. Semenza, G. L. 2003. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3:721-732.
24. Christophi, C., N. Harun, and T. Fifis. 2008. Liver regeneration and tumor stimulation-a review of cytokine and angiogenic factors. J. Gastrointest. Surg. 12:966-980.
25. Epstein, R. J. 2007. VEGF signaling inhibitors: more pro-apoptotic than anti-angiogenic. Cancer Metastasis Rev. 26:443-452.
26. Shaked, Y., T. Tang, J. Woloszynek, L. G. Daenen, S. Man, P. Xu, et al. 2009. Contribution of granulocyte colony-stimulating factor to the acute mobilization of endothelial precursor cells by vascular disrupting agents. Cancer Res. 69:7524-7528.
27. Yang, A. D., E. R. Camp, F. Fan, L. Shen, M. J. Gray, W. Liu, et al. 2006. Vascular endothelial growth factor receptor-1 activation mediates epithelial to mesenchymal transition in human pancreatic carcinoma cells. Cancer Res. 66:46-51.
28. Peinado, H., and A. Cano. 2006. New potential therapeutic targets to combat epithelial tumor invasion. Clin. Transl. Oncol. 8:851-857.
29. Siegel, P. M., W. Shu, R. D. Cardiff, W. J. Muller, and J. Massague. 2003. Transforming growth factor beta signaling impairs Neu-induced mammary tumorigenesis while promoting pulmonary metastasis. Proc. Natl. Acad. Sci. USA 100:8430-8435.
30. Gregory, P. A., A. G. Bert, E. L. Paterson, S. C. Barry, A. Tsykin, G. Farshid, et al. 2008. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol. 10:593-601.
31. Xiong, W., Z. G. Ren, S. J. Qiu, H. C. Sun, L. Wang, B. B. Liu, et al. 2010. Residual hepatocellular carcinoma after oxaliplatin treatment has increased metastatic potential in a nude mouse model and is attenuated by Songyou Yin. BMC cancer 10:219.
32. Vincan, E., and N. Barker. 2008. The upstream components of the Wnt signalling pathway in the dynamic EMT and MET associated with colorectal cancer progression. Clin. Exp. Metastasis 25:657-663.
33. Aigner, K., B. Dampier, L. Descovich, M. Mikula, A. Sultan, M. Schreiber, et al. 2007. The transcription factor ZEB1 (deltaEF1) promotes tumour cell dedifferentiation by repressing master regulators of epithelial polarity. Oncogene 26:6979-6988.
34. Clarhaut, J., R. M. Gemmill, V. A. Potiron, S. Ait-Si-Ali, J. Imbert, H. A. Drabkin, et al. 2009. ZEB-1, a repressor of the semaphorin 3F tumor suppressor gene in lung cancer cells. Neoplasia 11:157-166.
35. Witta, S. E., R. M. Gemmill, F. R. Hirsch, C. D. Coldren, K. Hedman, L. Ravdel, et al. 2006. Restoring E-cadherin expression increases sensitivity to epidermal growth factor receptor inhibitors in lung cancer cell lines. Cancer Res. 66:944-950.
36. Nieto, M. A. 2011. The ins and outs of the epithelial to mesenchymal transition in health and disease. Annu. Rev. Cell Dev. Biol. 27:347-376.
37. Ansieau, S., S. Courtois-Cox, A. P. Morel, and A. Puisieux. 2011. Failsafe program escape and EMT: a deleterious partnership. Semin. Cancer Biol. 21:392-396.
38. Bui, T., J. Sequeira, T. C. Wen, A. Sola, Y. Higashi, H. Kondoh, et al. 2009. ZEB1 links p63 and p73 in a novel neuronal survival pathway rapidly induced in response to cortical ischemia. PLoS One 4:e4373.
39. Schofield, C. J., and P. J. Ratcliffe. 2004. Oxygen sensing by HIF hydroxylases. Nat. Rev. Mol. Cell Biol. 5:343-354.
40. Evdokimova, V., C. Tognon, T. Ng, P. Ruzanov, N. Melnyk, D. Fink, et al. 2009. Translational activation of snail1 and other developmentally regulated transcription factors by YB-1 promotes an epithelial-mesenchymal transition. Cancer Cell 15:402-415.
41. Brabletz, S., and T. Brabletz. 2010. The ZEB/miR-200 feedback loop-a motor of cellular plasticity in development and cancer? EMBO Rep. 11:670-677.
42. Kokkinos, M. I., R. Wafai, M. K. Wong, D. F. Newgreen, E. W. Thompson, and M. Waltham. 2007. Vimentin and epithelial-mesenchymal transition in human breast cancer-observations in vitro and in vivo. Cells Tissues Organs 185:191-203.
43. Hugo, H., M. L. Ackland, T. Blick, M. G. Lawrence, J. A. Clements, E. D. Williams, et al. 2007. Epithelial-mesenchymal and mesenchymal-epithelial transitions in carcinoma progression. J. Cell. Physiol. 213:374-383.
44. Ocana, O. H., R. Corcoles, A. Fabra, G. Moreno-Bueno, H. Acloque, S. Vega, et al. 2012. Metastatic colonization requires the repression of the epithelial-mesenchymal transition inducer prrx1. Cancer Cell 22:709-724.
45. Tsai, J. H., J. L. Donaher, D. A. Murphy, S. Chau, and J. Yang. 2012. Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell 22:725-736.
46. Wang, F., L. He, W. Q. Dai, Y. P. Xu, D. Wu, C. L. Lin, et al. 2012. Salinomycin inhibits proliferation and induces apoptosis of human hepatocellular carcinoma cells in vitro and in vivo. PLoS One 7:e50638.