Dual-action combination therapy enhances angiogenesis while reducing tumor growth and spread

Cancer Cell

Volumn 27, Issue 1, 2015, Pages 123-137

  Wong, Ping Pui ^a   Demircioglu, Fevzi ^a   Ghazaly, Essam ^a   Alrawashdeh, Wasfi ^a   Stratford, Michael R L ^b   Scudamore, Cheryl L ^c   Cereser, Biancastella ^a   Crnogorac Jurcevic, Tatjana ^a   McDonald, Stuart ^a   Elia, George ^a   Hagemann, Thorsten ^a,d   Kocher, Hemant M ^a,d   Hodivala Dilke, Kairbaan M ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c MRC MAMMALIAN GENETICS UNIT   (United Kingdom)

^d ROYAL LONDON HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; ANTINEOPLASTIC ANTIMETABOLITE; CILENGITIDE; DEOXYCYTIDINE; DRUG ADMINISTRATION; DRUG THERAPY; GEMCITABINE; SNAKE VENOM; VERAPAMIL;

ANALOGS AND DERIVATIVES; ANGIOGENESIS; ANIMAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD FLOW; C57BL MOUSE; CANCER COMBINATION CHEMOTHERAPY; CANCER TRANSPLANTATION; CARCINOMA, LEWIS LUNG; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; DRUG THERAPY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LOW DRUG DOSE; LUNG; MALE; METASTASIS; MONOTHERAPY; MOUSE; NEOVASCULARIZATION, PATHOLOGIC; NONHUMAN; PANCREAS; PANCREATIC NEOPLASMS; PATHOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR CELL; TUMOR CELL LINE; TUMOR GROWTH; VASCULARIZATION;

ADMINISTRATION AND DOSAGE; ANALOGS AND DERIVATIVES; ANIMALS; ANTIMETABOLITES, ANTINEOPLASTIC; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BLOOD SUPPLY; CARCINOMA, LEWIS LUNG; CELL LINE, TUMOR; DEOXYCYTIDINE; DRUG SYNERGISM; DRUG THERAPY; HUMANS; LUNG; MICE; MICE, INBRED C57BL; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC; PANCREAS; PANCREATIC NEOPLASMS; PATHOLOGY; SNAKE VENOMS; THERAPEUTIC USE; VERAPAMIL;

EID: 84922180322     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2014.10.015     Document Type: Article

References (44)

1. Ahmed, J.H., Elliott, H.L., Meredith, P.A., and Reid, J.L. (1992).). Low-dose verapamil in middle-aged and elderly patients with angina pectoris: no evidence of increased susceptibility to the cardiac effects. Cardiovasc. Drugs Ther. 6, 153-158.
2. Batchelor, T.T., Sorensen, A.G., di Tomaso, E., Zhang, W.T., Duda, D.G., Cohen, K.S., Kozak, K.R., Cahill, D.P., Chen, P.J., Zhu, M., et al. (2007). AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 11, 83-95.
3. Bergman, A.M., Pinedo, H.M., Talianidis, I., Veerman, G., Loves, W.J., van der Wilt, C.L., and Peters, G.J. (2003). Increased sensitivity to gemcitabine of P-glycoprotein and multidrug resistance-associated protein-overexpressing human cancer cell lines. Br. J. Cancer 88, 1963-1970.
4. Candussio, L., Decorti, G., Crivellato, E., Granzotto, M., Rosati, A., Giraldi, T., and Bartoli, F. (2002). Toxicologic and pharmacokinetic study of low doses of verapamil combined with doxorubicin. Life Sci. 71, 3109-3119.
5. Carmeliet, P., and Jain, R.K. (2011). Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nat. Rev. Drug Discov. 10, 417-427.
6. Coate, L.E., John, T., Tsao, M.S., and Shepherd, F.A. (2009). Molecular predictive and prognostic markers in non-small-cell lung cancer. Lancet Oncol. 10, 1001-1010.
7. Ebos, J.M., Lee, C.R., Cruz-Munoz, W., Bjarnason, G.A., Christensen, J.G., and Kerbel, R.S. (2009). Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 15, 232-239.
8. Eisinger-Mathason, T.S., Zhang, M., Qiu, Q., Skuli, N., Nakazawa, M.S., Karakasheva, T., Mucaj, V., Shay, J.E., Stangenberg, L., Sadri, N., et al. (2013). Hypoxia-dependent modification of collagen networks promotes sarcoma metastasis. Cancer Dis. 3, 1190-1205.
9. Eltzschig, H.K., Abdulla, P., Hoffman, E., Hamilton, K.E., Daniels, D., Schönfeld, C., Löffler, M., Reyes, G., Duszenko, M., Karhausen, J., et al. (2005). HIF-1-dependent repression of equilibrative nucleoside transporter (ENT) in hypoxia. J. Exp. Med. 202, 1493-1505.
10. Erkan, M., Reiser-Erkan, C., Michalski, C.W., Kong, B., Esposito, I., Friess, H., and Kleeff, J. (2012). The impact of the activated stroma on pancreatic ductal adenocarcinoma biology and therapy resistance. Curr. Mol. Med. 12, 288-303.
11. Errasti-Murugarren, E., Pastor-Anglada, M., and Casado, F.J. (2007). Role of CNT3 in the transepithelial flux of nucleosides and nucleoside-derived drugs. J. Physiol. 582, 1249-1260.
12. Errasti-Murugarren, E., Ferná ndez-Calotti, P., Veyhl-Wichmann, M., Diepold, M., Pinilla-Macua, I., Pérez-Torras, S., Kipp, H., Koepsell, H., and Pastor- Anglada, M. (2012). Role of the transporter regulator protein (RS1) in the modulation of concentrative nucleoside transporters (CNTs) in epithelia. Mol. Pharmacol. 82, 59-67.
13. Farrell, J.J., Elsaleh, H., Garcia, M., Lai, R., Ammar, A., Regine, W.F., Abrams, R., Benson, A.B., Macdonald, J., Cass, C.E., et al. (2009). Human equilibrative nucleoside transporter 1 levels predict response to gemcitabine in patients with pancreatic cancer. Gastroenterology 136, 187-195.
14. Feng, L., Fitzsimmons, B.F., Young, W.L., Berman, M.F., Lin, E., Aagaard, B.D., Duong, H., and Pile-Spellman, J. (2002). Intraarterially administered verapamil as adjunct therapy for cerebral vasospasm: safety and 2-year experience. AJNR Am. J. Neuroradiol. 23, 1284-1290.
15. Gusella, M., Pasini, F., Bolzonella, C., Meneghetti, S., Barile, C., Bononi, A., Toso, S., Menon, D., Crepaldi, G., Modena, Y., et al. (2011). Equilibrative nucleoside transporter 1 genotype, cytidine deaminase activity and age predict gemcitabine plasma clearance in patients with solid tumours. Br. J. Clin. Pharmacol. 71, 437-444.
16. Hidalgo, M. (2010). Pancreatic cancer. N. Engl. J. Med. 362, 1605-1617.
17. Hingorani, S.R., Wang, L., Multani, A.S., Combs, C., Deramaudt, T.B., Hruban, R.H., Rustgi, A.K., Chang, S., and Tuveson, D.A. (2005). Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell 7, 469-483.
18. Huang, Y., Yuan, J., Righi, E., Kamoun, W.S., Ancukiewicz, M., Nezivar, J., Santosuosso, M., Martin, J.D., Martin, M.R., Vianello, F., et al. (2012). Vascular normalizing doses of antiangiogenic treatment reprogram the immunosuppressive tumor microenvironment and enhance immunotherapy. Proc. Natl. Acad. Sci. USA 109, 17561-17566.
19. Hwang, R.F., Moore, T., Arumugam, T., Ramachandran, V., Amos, K.D., Rivera, A., Ji, B., Evans, D.B., and Logsdon, C.D. (2008). Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Res. 68, 918-926.
20. Kaelin, W.G., Jr., Shrivastav, S., Shand, D.G., and Jirtle, R.L. (1982). Effect of verapamil on malignant tissue blood flow in SMT-2A tumor-bearing rats. Cancer Res. 42, 3944-3949.
21. Mas-Moruno, C., Rechenmacher, F., and Kessler, H. (2010). Cilengitide: the first anti-angiogenic small molecule drug candidate design, synthesis and clinical evaluation. Anticancer. Agents Med. Chem. 10, 753-768.
22. Miller, T.P., Grogan, T.M., Dalton, W.S., Spier, C.M., Scheper, R.J., and Salmon, S.E. (1991). P-glycoprotein expression in malignant lymphoma and reversal of clinical drug resistance with chemotherapy plus high-dose verapamil. J. Clin. Oncol. 9, 17-24.
23. Morote-Garcia, J.C., Rosenberger, P., Nivillac, N.M., Coe, I.R., and Eltzschig, H.K. (2009). Hypoxia-inducible factor-dependent repression of equilibrative nucleoside transporter 2 attenuates mucosal inflammation during intestinal hypoxia. Gastroenterology 136, 607-618.
24. Nisato, R.E., Tille, J.C., Jonczyk, A., Goodman, S.L., and Pepper, M.S. (2003). alphav beta 3 and alphav beta 5 integrin antagonists inhibit angiogenesis in vitro. Angiogenesis 6, 105-119.
25. Okines, A., and Cunningham, D. (2009). Current perspective: bevacizumab in colorectal cancer-a time for reappraisal? Eur. J. Cancer 45, 2452-2461.
26. Olive, K.P., Jacobetz, M.A., Davidson, C.J., Gopinathan, A., McIntyre, D., Honess, D., Madhu, B., Goldgraben, M.A., Caldwell, M.E., Allard, D., et al. (2009). Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 324, 1457-1461.
27. Oliveira-Ferrer, L., Hauschild, J., Fiedler, W., Bokemeyer, C., Nippgen, J., Celik, I., and Schuch, G. (2008). Cilengitide induces cellular detachment and apoptosis in endothelial and glioma cells mediated by inhibition of FAK/src/ AKT pathway. J. Exp. Clin. Cancer Res. 27, 86.
28. Özdemir, B.C., Pentcheva-Hoang, T., Carstens, J.L., Zheng, X., Wu, C.C., Simpson, T.R., Laklai, H., Sugimoto, H., Kahlert, C., Novitskiy, S.V., et al. (2014). Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival. Cancer Cell 25, 719-734.
29. Pàez-Ribes, M., Allen, E., Hudock, J., Takeda, T., Okuyama, H., Viñals, F., Inoue, M., Bergers, G., Hanahan, D., and Casanovas, O. (2009). Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 15, 220-231.
30. Plunkett, W., Huang, P., Xu, Y.Z., Heinemann, V., Grunewald, R., and Gandhi, V. (1995). Gemcitabine: metabolism, mechanisms of action, and self-potentiation. Semin. Oncol. 22 (4, Suppl 11), 3-10.
31. Provenzano, P.P., Cuevas, C., Chang, A.E., Goel, V.K., Von Hoff, D.D., and Hingorani, S.R. (2012). Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma. Cancer Cell 21, 418-429.
32. Reynolds, A.R., Hart, I.R., Watson, A.R., Welti, J.C., Silva, R.G., Robinson, S.D., Da Violante, G., Gourlaouen, M., Salih, M., Jones, M.C., et al. (2009). Stimulation of tumor growth and angiogenesis by low concentrations of RGD-mimetic integrin inhibitors. Nat. Med. 15, 392-400.
33. Rhim, A.D., Oberstein, P.E., Thomas, D.H., Mirek, E.T., Palermo, C.F., Sastra, S.A., Dekleva, E.N., Saunders, T., Becerra, C.P., Tattersall, I.W., et al. (2014). Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma. Cancer Cell 25, 735-747.
34. Seigneuric, R., Starmans, M.H., Fung, G., Krishnapuram, B., Nuyten, D.S., van Erk, A., Magagnin, M.G., Rouschop, K.M., Krishnan, S., Rao, R.B., et al. (2007). Impact of supervised gene signatures of early hypoxia on patient survival. Radiother. Oncol. 83, 374-382.
35. Shojaei, F. (2012). Anti-angiogenesis therapy in cancer: current challenges and future perspectives. Cancer Lett. 320, 130-137.
36. Spivak-Kroizman, T.R., Hostetter, G., Posner, R., Aziz, M., Hu, C., Demeure, M.J., Von Hoff, D., Hingorani, S.R., Palculict, T.B., Izzo, J., et al. (2013). Hypoxia triggers hedgehog-mediated tumor-stromal interactions in pancreatic cancer. Cancer Res. 73, 3235-3247.
37. Van der Veldt, A.A., Lubberink, M., Bahce, I., Walraven, M., de Boer, M.P., Greuter, H.N., Hendrikse, N.H., Eriksson, J., Windhorst, A.D., Postmus, P.E., et al. (2012). Rapid decrease in delivery of chemotherapy to tumors after anti-VEGF therapy: implications for scheduling of anti-angiogenic drugs. Cancer Cell 21, 82-91.
38. Webb, T. (2005). Vascular normalization: study examines how antiangiogenesis therapies work. J. Natl. Cancer Inst. 97, 336-337.
39. Weidner, N., Semple, J.P., Welch, W.R., and Folkman, J. (1991). Tumor angiogenesis and metastasis-correlation in invasive breast carcinoma. N. Engl. J. Med. 324, 1-8.
40. Wood, P.J., and Hirst, D.G. (1989). Modification of tumour response by calcium antagonists in the SCVII/St tumour implanted at two different sites. Int. J. Radiat. Biol. 56, 355-367.
41. Yamada, S., Bu, X.Y., Khankaldyyan, V., Gonzales-Gomez, I., McComb, J.G., and Laug, W.E. (2006). Effect of the angiogenesis inhibitor Cilengitide (EMD 121974) on glioblastoma growth in nude mice. Neurosurgery 59, 1304-1312, discussion 1312.
42. Yang, M.H., Wu, M.Z., Chiou, S.H., Chen, P.M., Chang, S.Y., Liu, C.J., Teng, S.C., and Wu, K.J. (2008). Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat. Cell Biol. 10, 295-305.
43. Yokoi, K., and Fidler, I.J. (2004). Hypoxia increases resistance of human pancreatic cancer cells to apoptosis induced by gemcitabine. Clin. Cancer Res. 10, 2299-2306.
44. Young, J.D., Yao, S.Y., Baldwin, J.M., Cass, C.E., and Baldwin, S.A. (2013). The human concentrative and equilibrative nucleoside transporter families, SLC28 and SLC29. Mol. Aspects Med. 34, 529-547.