Src inhibition potentiates antitumoral effect of paclitaxel by blocking tumor-induced angiogenesis

Experimental Cell Research

Volumn 328, Issue 1, 2014, Pages 20-31

  Delle Monache, Simona ^a   Sanità, Patrizia ^a   Calgani, Alessia ^a   Schenone, Silvia ^b   Botta, Lorenzo ^c   Angelucci, Adriano ^a  

^a UNIVERSITY OF L'AQUILA   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c UNIVERSITY OF SIENA   (Italy)

Author keywords

Angiogenesis; Chemotherapy; Prostate cancer; Reactive oxygen species; Src; Taxanes

Indexed keywords

ANTINEOPLASTIC AGENT; DASATINIB; FOCAL ADHESION KINASE; HEAT SHOCK PROTEIN 90; HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MATRIGEL; PACLITAXEL; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; S13; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; FOCAL ADHESION KINASE 1; PROTEIN KINASE INHIBITOR; PTK2 PROTEIN, HUMAN; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2, HUMAN;

ANGIOGENESIS ASSAY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; BONE METASTASIS; CANCER CELL; CANCER GROWTH; CANCER INHIBITION; CANCER SIZE; CELL MIGRATION; DRUG POTENTIATION; DRUG SPECIFICITY; ENDOTHELIUM CELL; ENZYME INHIBITION; HUMAN; HUMAN CELL; IC50; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PROSTATE CANCER; PROSTATE CANCER CELL LINE; PROTEIN EXPRESSION; TUMOR XENOGRAFT; UMBILICAL VEIN ENDOTHELIAL CELL; ANIMAL; ANTAGONISTS AND INHIBITORS; APOPTOSIS; CELL MOTION; CELL PROLIFERATION; DRUG EFFECTS; ENZYME IMMUNOASSAY; FLUORESCENT ANTIBODY TECHNIQUE; METABOLISM; NEOVASCULARIZATION, PATHOLOGIC; PATHOLOGY; PROSTATIC NEOPLASMS; TUMOR CELL CULTURE; VASCULARIZATION; WESTERN BLOTTING;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; BLOTTING, WESTERN; CELL MOVEMENT; CELL PROLIFERATION; FLUORESCENT ANTIBODY TECHNIQUE; FOCAL ADHESION KINASE 1; HUMANS; IMMUNOENZYME TECHNIQUES; MALE; MICE; NEOVASCULARIZATION, PATHOLOGIC; PACLITAXEL; PROSTATIC NEOPLASMS; PROTEIN KINASE INHIBITORS; SRC-FAMILY KINASES; TUMOR CELLS, CULTURED; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84907973716     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2014.08.002     Document Type: Article

References (36)

1. Petrylak D.P., Tangen C.M., Hussain M.H., Lara P.N., Jones J.A., Taplin M.E., Burch P.A., Berry D., Moinpour C., Kohli M., et al. Docetaxel and estramustine compared with mitoxantrone and prednisone for advanced refractory prostate cancer. N. Engl. J. Med. 2004, 351:1513-1520.
2. Tannock I.F., Osoba D., Stockler M.R., Ernst D.S., Neville A.J., Moore M.J., Armitage G.R., Wilson J.J., Venner P.M., Coppin C.M., et al. Chemotherapy with mitoxantrone plus prednisone or prednisone alone for symptomatic hormone-resistant prostate cancer: a Canadian randomized trial with palliative end points. J. Clin. Oncol. 1996, 14:1756-1764.
3. Sternberg C.N., Petrylak D.P., Sartor O., Witjes J.A., Demkow T., Ferrero J.M., Eymard J.C., Falcon S., Calabro F., James N., et al. Multinational, double-blind, phase III study of prednisone and either satraplatin or placebo in patients with castrate-refractory prostate cancer progressing after prior chemotherapy: the SPARC trial. J. Clin. Oncol. 2009, 27:5431-5438.
4. de Bono J.S., Oudard S., Ozguroglu M., Hansen S., Machiels J.P., Kocak I., Gravis G., Bodrogi I., Mackenzie M.J., Shen L., et al. Prednisone plus cabazitaxel or mitoxantrone for metastatic castration-resistant prostate cancer progressing after docetaxel treatment: a randomised open-label trial. Lancet 2010, 376:1147-1154.
5. Beltran H., Beer T.M., Carducci M.A., de Bono J., Gleave M., Hussain M., Kelly W.K., Saad F., Sternberg C., Tagawa S.T., et al. New therapies for castration-resistant prostate cancer: efficacy and safety. Eur. Urol. 2011, 60:279-290.
6. Tatarov O., Mitchell T.J., Seywright M., Leung H.Y., Brunton V.G., Edwards J. SRC family kinase activity is up-regulated in hormone-refractory prostate cancer. Clin. Cancer Res. 2009, 15:3540-3549.
7. Mayer E.L., Krop I.E. Advances in targeting SRC in the treatment of breast cancer and other solid malignancies. Clin. Cancer Res. 2010, 16:3526-3532.
8. Cai H., Babic I., Wei X., Huang J., Witte O.N. Invasive prostate carcinoma driven by c-Src and androgen receptor synergy. Cancer Res. 2011, 71:862-872.
9. Angelucci A., Schenone S., Gravina G.L., Muzi P., Festuccia C., Vicentini C., Botta M., Bologna M. Pyrazolo[3,4-d]pyrimidines c-Src inhibitors reduce epidermal growth factor-induced migration in prostate cancer cells. Eur. J. Cancer 2006, 42:2838-2845.
10. Ishizawar R.C., Miyake T., Parsons S.J. c-Src modulates ErbB2 and ErbB3 heterocomplex formation and function. Oncogene 2007, 26:3503-3510.
11. Yu E.Y., Massard C., Gross M.E., Carducci M.A., Culine S., Hudes G., Posadas E.M., Sternberg C.N., Wilding G., Trudel G.C., et al. Once-daily dasatinib: expansion of phase II study evaluating safety and efficacy of dasatinib in patients with metastatic castration-resistant prostate cancer. Urology 2011, 77:1166-1171.
12. Araujo J.C., Mathew P., Armstrong A.J., Braud E.L., Posadas E., Lonberg M., Gallick G.E., Trudel G.C., Paliwal P., Agrawal S., et al. Dasatinib combined with docetaxel for castration-resistant prostate cancer: results from a phase 1-2 study. Cancer 2012, 118:63-71.
13. Hockel M., Vaupel P. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J. Natl. Cancer Inst. 2001, 93:266-276.
14. Semenza G.L., Agani F., Feldser D., Iyer N., Kotch L., Laughner E., Yu A. Hypoxia, HIF-1, and the pathophysiology of common human diseases. Adv. Exp. Med. Biol. 2000, 475:123-130.
15. Ivan M., Kondo K., Yang H., Kim W., Valiando J., Ohh M., Salic A., Asara J.M., Lane W.S., Kaelin W.G. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 2001, 292:464-468.
16. Jiang B.H., Agani F., Passaniti A., Semenza G.L. V-SRC induces expression of hypoxia-inducible factor 1 (HIF-1) and transcription of genes encoding vascular endothelial growth factor and enolase 1: involvement of HIF-1 in tumor progression. Cancer Res. 1997, 57:5328-5335.
17. Schenone S., Bruno O., Bondavalli F., Ranise A., Mosti L., Menozzi G., Fossa P., Donnini S., Santoro A., Ziche M., et al. Antiproliferative activity of new 1-aryl-4-amino-1H-pyrazolo[3,4-d]pyrimidine derivatives toward the human epidermoid carcinoma A431 cell line. Eur. J. Med. Chem. 2004, 39:939-946.
18. Radi M., Evensen L., Dreassi E., Zamperini C., Caporicci M., Falchi F., Musumeci F., Schenone S., Lorens J.B., Botta M. A combined targeted/phenotypic approach for the identification of new antiangiogenics agents active on a zebrafish model: from in silico screening to cyclodextrin formulation. Bioorg. Med. Chem. Lett. 2012, 22:5579-5583.
19. Passaniti A., Taylor R.M., Pili R., Guo Y., Long P.V., Haney J.A., Pauly R.R., Grant D.S., Martin G.R. A simple, quantitative method for assessing angiogenesis and antiangiogenic agents using reconstituted basement membrane, heparin, and fibroblast growth factor. Lab. Investig. 1992, 67:519-528.
20. Zudaire E., Gambardella L., Kurcz C., Vermeren S. A computational tool for quantitative analysis of vascular networks. PLoS One 2011, 6:e27385.
21. Berthold D.R., Pond G.R., Soban F., de Wit R., Eisenberger M., Tannock I.F. Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer: updated survival in the TAX 327 study. J. Clin. Oncol. 2008, 26:242-245.
22. Aggarwal R., Ryan C.J. Castration-resistant prostate cancer: targeted therapies and individualized treatment. Oncologist 2011, 16:264-275.
23. Han L.Y., Landen C.N., Trevino J.G., Halder J., Lin Y.G., Kamat A.A., Kim T.J., Merritt W.M., Coleman R.L., Gershenson D.M., et al. Antiangiogenic and antitumor effects of SRC inhibition in ovarian carcinoma. Cancer Res. 2006, 66:8633-8639.
24. Anbalagan M., Ali A., Jones R.K., Marsden C.G., Sheng M., Carrier L., Bu Y., Hangauer D., Rowan B.G. Peptidomimetic Src/pretubulin inhibitor KX-01 alone and in combination with paclitaxel suppresses growth, metastasis in human ER/PR/HER2-negative tumor xenografts. Mol. Cancer Ther. 2012, 11:1936-1947.
25. Lee Y.C., Huang C.F., Murshed M., Chu K., Araujo J.C., Ye X., deCrombrugghe B., Yu-Lee L.Y., Gallick G.E., Lin S.H. Src family kinase/abl inhibitor dasatinib suppresses proliferation and enhances differentiation of osteoblasts. Oncogene 2010, 29:3196-3207.
26. de Vries T.J., Mullender M.G., van Duin M.A., Semeins C.M., James N., Green T.P., Everts V., Klein-Nulend J. The Src inhibitor AZD0530 reversibly inhibits the formation and activity of human osteoclasts. Mol. Cancer Res. 2009, 7:476-488.
27. Araujo J.C., Trudel G.C., Saad F., Armstrong A.J., Yu E.Y., Bellmunt J., Wilding G., McCaffrey J., Serrano S.V., Matveev V.B., et al. Docetaxel and dasatinib or placebo in men with metastatic castration-resistant prostate cancer (READY): a randomised, double-blind phase 3 trial. Lancet Oncol. 2013, 14:1307-1316.
28. Bruns A.F., Yuldasheva N., Latham A.M., Bao L., Pellet-Many C., Frankel P., Stephen S.L., Howell G.J., Wheatcroft S.B., Kearney M.T., et al. A heat-shock protein axis regulates VEGFR2 proteolysis, blood vessel development and repair. PLoS One 2012, 7:e48539.
29. Koshiji M., Huang L.E. Dynamic balancing of the dual nature of HIF-1alpha for cell survival. Cell Cycle 2004, 3:853-854.
30. Pan Y., Mansfield K.D., Bertozzi C.C., Rudenko V., Chan D.A., Giaccia A.J., Simon M.C. Multiple factors affecting cellular redox status and energy metabolism modulate hypoxia-inducible factor prolyl hydroxylase activity in vivo and in vitro. Mol. Cell. Biol. 2007, 27:912-925.
31. Zhou Q., Liu L.Z., Fu B., Hu X., Shi X., Fang J., Jiang B.H. Reactive oxygen species regulate insulin-induced VEGF and HIF-1alpha expression through the activation of p70S6K1 in human prostate cancer cells. Carcinogenesis 2007, 28:28-37.
32. Migliaccio A., Di Domenico M., Castoria G., Nanayakkara M., Lombardi M., de Falco A., Bilancio A., Varricchio L., Ciociola A., Auricchio F. Steroid receptor regulation of epidermal growth factor signaling through Src in breast and prostate cancer cells: steroid antagonist action. Cancer Res. 2005, 65:10585-10593.
33. Lee L.F., Guan J., Qiu Y., Kung H.J. Neuropeptide-induced androgen independence in prostate cancer cells: roles of nonreceptor tyrosine kinases Etk/Bmx, Src, and focal adhesion kinase. Mol. Cell. Biol. 2001, 21:8385-8397.
34. Santucci M.A., Corradi V., Mancini M., Manetti F., Radi M., Schenone S., Botta M. C6-unsubstituted pyrazolo[3,4-d]pyrimidines are dual Src/Abl inhibitors effective against imatinib mesylate resistant chronic myeloid leukemia cell lines. ChemMedChem 2009, 4:118-126.
35. Chang Y.M., Bai L., Liu S., Yang J.C., Kung H.J., Evans C.P. Src family kinase oncogenic potential and pathways in prostate cancer as revealed by AZD0530. Oncogene 2008, 27:6365-6375.
36. Khromova N.V., Kopnin P.B., Stepanova E.V., Agapova L.S., Kopnin B.P. p53 hot-spot mutants increase tumor vascularization via ROS-mediated activation of the HIF1/VEGF-A pathway. Cancer Lett. 2009, 276:143-151.