Targeting endothelin-1 receptor/β-arrestin1 network for the treatment of ovarian cancer

References

• Rosanò L, Spinella F, Bagnato A. Endothelin 1 in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer. 2013;13:637–651.
   PubMed Web of Science ®Google Scholar
• Davenport AP, Hyndman KA, Dhaun N, et al. Endothelin. Pharmacol Rev. 2016;68:357–418.
   PubMed Web of Science ®Google Scholar
• Yanagisawa M, Kurihara H, Kimura S, et al. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature. 1988;332:411–415.
   PubMed Web of Science ®Google Scholar
• Arai H, Hori S, Aramori I, et al. Cloning and expression of a cDNA encoding an endothelin receptor. Nature. 1990;348:730–732.
   PubMed Web of Science ®Google Scholar
• Nelson JB, Hedican SP, George DJ, et al. Identification of endothelin-1 in the pathophysiology of metastatic adenocarcinoma of the prostate. Nature Med. 1995;1:944–949.
   PubMed Web of Science ®Google Scholar
• Bagnato A, Tecce R, Moretti C, et al. Autocrine actions of endothelin-1 as a growth factor in human ovarian carcinoma cells. Clin Cancer Res. 1995;1:1059–1066.
   PubMed Web of Science ®Google Scholar
• Nelson J, Bagnato A, Battistini B, et al. The endothelin axis: emerging role in cancer. Nat Rev Cancer. 2003;3:110–116.
   PubMed Web of Science ®Google Scholar
• Peng J, Zhang G, Wang Q, et al. ROCK cooperated with ET-1 to induce epithelial to mesenchymal transition through SLUG in human ovarian cancer cells. Biosci Biotechnol Biochem. 2012;76:42–47.
   PubMed Web of Science ®Google Scholar
• Rosanò L, Varmi M, Salani D, et al. Endothelin-1 induces tumor proteinase activation and invasiveness of ovarian carcinoma cells. Cancer Res. 2001;61:8340–8346.
   PubMed Web of Science ®Google Scholar
• Spinella F, Rosanò L, Di Castro V, et al. Endothelin-1 decreases gap junctional intercellular communication by inducing phosphorylation of connexin 43 in human ovarian carcinoma cells. J Biol Chem. 2003;278:41294–41301.
   PubMed Web of Science ®Google Scholar
• Spinella F, Rosanò L, Di Castro V, et al. Endothelin-1-induced prostaglandin E2-EP2, EP4 signaling regulates vascular endothelial growth factor production and ovarian carcinoma cell invasion. J Biol Chem. 2004;279:46700–46705.
   PubMed Web of Science ®Google Scholar
• Spinella F, Rosanò L, Di Castro V, et al. Inhibition of cyclooxygenase-1 and -2 expression by targeting the endothelin a receptor in human ovarian carcinoma cells. Clin Cancer Res. 2004;10:4670–4679.
   PubMed Web of Science ®Google Scholar
• Rosanò L, Spinella F, Di Castro V, et al. Integrin-linked kinase functions as a downstream mediator of endothelin-1 to promote invasive behavior in ovarian carcinoma. Mol Cancer Ther. 2006;5:833–842.
   PubMed Web of Science ®Google Scholar
• Spinella F, Garrafa E, Di Castro V, et al. Endothelin-1 stimulates lymphatic endothelial cells and lymphatic vessels to grow and invade. Cancer Res. 2009;69:2669–2676.
   PubMed Web of Science ®Google Scholar
• Wu MH, Huang CY, Lin J, et al. Endothelin-1 promotes vascular endothelial growth factor-dependent angiogenesis in human chondrosarcoma cells. Oncogene. 2014;33:1725–1735.
   PubMed Web of Science ®Google Scholar
• Wülfing P, Kersting C, Buerger H, et al. Expression patterns of angiogenic and lymphangiogenic factors in ductal breast carcinoma in situ. Br J Cancer. 2005;92:1720–1728.
   PubMed Web of Science ®Google Scholar
• Buckanovich RJ, Facciabene A, Kim S, et al. Endothelin B receptor mediates the endothelial barrier to T cell homing to tumors and disables immune therapy. Nature Med. 2008;14:28–36.
   PubMed Web of Science ®Google Scholar
• Knowles JP, Shi-Wen X, Haque SU, et al. Endothelin-1 stimulates colon cancer adjacent fibroblasts. Int J Cancer. 2012;130:1264–1272.
   PubMed Web of Science ®Google Scholar
• Huang WH, Chang MC, Tsai KS, et al. Mesenchymal stem cells promote growth and angiogenesis of tumors in mice. Oncogene. 2013;32:4343–4354.
   PubMed Web of Science ®Google Scholar
• Russignan A, Spina C, Tamassia N, et al. Endothelin-1 receptor blockade as new possible therapeutic approach in multiple myeloma. Br J Haematol. 2017 Jun 9. DOI:10.1111/bjh.14771
   Web of Science ®Google Scholar
• Siegel RL, Miller KD, Jemal A. Cancer statistics. Cancer J Clin. 2015;65:5–29.
   PubMed Web of Science ®Google Scholar
• Bagnato A, Salani D, Di Castro V, et al. Expression of endothelin 1 and endothelin A receptor in ovarian carcinoma: evidence for an autocrine role in tumor growth. Cancer Res. 1999;59:720–727.
   PubMed Web of Science ®Google Scholar
• Moraitis S, Miller WR, Smyth JF, et al. Paracrine regulation of ovarian cancer by endothelin. Eur J Cancer. 1999;35:1381–1387.
   PubMed Web of Science ®Google Scholar
• Bagnato A, Tecce R, Di Castro V, et al. Activation of mitogenic signaling by endothelin 1 in ovarian carcinoma cells. Cancer Res. 1997;57:1306–1311.
   PubMed Web of Science ®Google Scholar
• Moraitis S, Langdon SP, Miller WR. Endothelin expression and responsiveness in human ovarian carcinoma cell lines. Eur J Cancer. 1997;33:661–668.
   PubMed Web of Science ®Google Scholar
• Salani D, Di Castro V, Nicotra MR, et al. Role of endothelin-1 in neovascularization of ovarian carcinoma. Am J Pathol. 2000;157:1537–1547.
   PubMed Web of Science ®Google Scholar
• Sestito R, Cianfrocca R, Rosanò L, et al. miR-30a inhibits endothelin A receptor and chemoresistance in ovarian carcinoma. Oncotarget. 2016;7:4009–4023.
   PubMed Web of Science ®Google Scholar
• Kandalaft LE, Motz GT, Busch J, et al. Angiogenesis and the tumor vasculature as antitumor immune modulators: the role of vascular endothelial growth factor and endothelin. Curr Top Microbiol Immunol. 2011;344:129–148.
   PubMed Web of Science ®Google Scholar
• Bremnes T, Paasche JD, Mehlum A, et al. Regulation and intracellular trafficking pathways of the endothelin receptors. J Biol Chem. 2000;275:17596–17604.
   PubMed Web of Science ®Google Scholar
• Lefkowitz RJ. G protein-coupled receptors. III. New roles for receptor kinases and beta-arrestins in receptor signaling and desensitization. J Biol Chem. 1998;273:18677–18680.
   PubMed Web of Science ®Google Scholar
• Peterson YK, Luttrell LM. The diverse roles of arrestin scaffolds in G protein-coupled receptor signaling. Pharmacol Rev. 2017;69:256–297.
   PubMed Web of Science ®Google Scholar
• Min J, Defea K. β-Arrestin-dependent actin reorganization: bringing the right players together at the leading edge. Mol Pharmacol. 2011;80:760–768.
   PubMed Web of Science ®Google Scholar
• Rosanò L, Bagnato A. β-Arrestin1 at the cross-road of endothelin-1 signaling in cancer. J Exp Clin Cancer Res. 2016;35:121–132.
   PubMed Web of Science ®Google Scholar
• Maguire JJ, Kuc RE, Pell VR, et al. Comparison of human ETA and ETB receptor signalling via G-protein and β-arrestin pathways. Life Sci. 2012;91:544–549.
   PubMed Web of Science ®Google Scholar
• Miller WE, Lefkowitz RJ. Expanding roles for beta-arrestins as scaffolds and adapters in GPCR signaling and trafficking. Curr Opin Cell Biol. 2001;13:139–145.
   PubMed Web of Science ®Google Scholar
• Shukla AK, Xiao K, Lefkowitz RJ. Emerging paradigms of β-arrestin-dependent seven transmembrane receptor signaling. Trends Biochem Sci. 2011;36:457–469.
   PubMed Web of Science ®Google Scholar
• Ranjan R, Dwivedi H, Baidya M, et al. Novel structural insights into GPCR-β-arrestin interaction and signaling. Trends Cell Biol. 2017 Jun 23. pii: S0962-8924(17)30087-9. DOI:10.1016/j.tcb.2017.05.008
   PubMedGoogle Scholar
• Rosanò L, Cianfrocca R, Masi S, et al. Beta-arrestin links endothelin A receptor to beta-catenin signaling to induce ovarian cancer cell invasion and metastasis. Proc Natl Acad Sci USA. 2009;106:2806–2811.
   PubMed Web of Science ®Google Scholar
• Teoh JP, Park KM, Wang Y, et al. Endothelin-1/endothelin A receptor-mediated biased signaling is a new player in modulating human ovarian cancer cell tumorigenesis. Cell Signal. 2014;26:2885–2895.
   PubMed Web of Science ®Google Scholar
• Cianfrocca R, Rosanò L, Spinella F, et al. Beta-arrestin-1 mediates the endothelin-1-induced activation of Akt and integrin-linked kinase. Can J Physiol Pharmacol. 2010;8:796–801.
   Web of Science ®Google Scholar
• Tocci P, Caprara V, Cianfrocca R, et al. Endothelin-1/endothelin A receptor axis activates RhoA GTPase in epithelial ovarian cancer. Life Sci. 2016;159:49–54.
   PubMed Web of Science ®Google Scholar
• Cianfrocca R, Tocci P, Rosanò L, et al. Nuclear β-arrestin1 is a critical cofactor of hypoxia-inducible factor-1α signaling in endothelin-1-induced ovarian tumor progression. Oncotarget. 2016;7:17790–17804.
   PubMed Web of Science ®Google Scholar
• Rosanò L, Cianfrocca R, Tocci P, et al. Endothelin A receptor/β-arrestin signaling to the Wnt pathway renders ovarian cancer cells resistant to chemotherapy. Cancer Res. 2014;74:7453–7464.
   PubMed Web of Science ®Google Scholar
• Cianfrocca R, Tocci P, Semprucci E, et al. β-Arrestin 1 is required for endothelin-1-induced NF-κB activation in ovarian cancer cells. Life Sci. 2014;118:179–184.
   PubMed Web of Science ®Google Scholar
• Spinella F, Caprara V, Di Castro V, et al. Endothelin-1 induces the transactivation of vascular endothelial growth factor receptor-3 and modulates cell migration and vasculogenic mimicry in melanoma cells. J Mol Med (Berl). 2013;91:395–405.
   PubMed Web of Science ®Google Scholar
• Rosanò L, Cianfrocca R, Tocci P, et al. β-arrestin-1 is a nuclear transcriptional regulator of endothelin-1-induced β-catenin signaling. Oncogene. 2013;32:5066–5077.
   PubMed Web of Science ®Google Scholar
• Semprucci E, Tocci P, Cianfrocca R, et al. Endothelin A receptor drives invadopodia function and cell motility through the β-arrestin/PDZ-RhoGEF pathway in ovarian carcinoma. Oncogene. 2016;35:3432–3442.
   PubMed Web of Science ®Google Scholar
• Thomsen AR, Plouffe B, Cahill TJ 3rd, et al. GPCR-G protein-β-arrestin super-complex mediates sustained G protein signaling. Cell. 2016;166:907–919.
   PubMed Web of Science ®Google Scholar
• Saykali BA, El-Sibai M. Invadopodia, regulation, and assembly in cancer cell invasion. Cell Commun Adhes. 2014;21:207–212.
   PubMed Web of Science ®Google Scholar
• Hastie EL, Sherwood DR. A new front in cell invasion: the invadopodial membrane. Eur J Cell Biol. 2016;95:441–448.
   PubMed Web of Science ®Google Scholar
• Kang J, Shi Y, Xiang B, et al. A nuclear function of beta-arrestin1 in GPCR signalling: regulation of histone acetylation and gene transcription. Cell. 2005;123:833–847.
   PubMed Web of Science ®Google Scholar
• Pillai S, Trevino J, Rawal B, et al. β-arrestin-1 mediates nicotine-induced metastasis through E2F1 target genes that modulate epithelial-mesenchymal transition. Cancer Res. 2015;75:1009–1020.
   PubMed Web of Science ®Google Scholar
• Perumal D, Pillai S, Nguyen J, et al. Nicotinic acetylcholine receptors induce c-Kit ligand/stem cell factor and promote stemness in an ARRB1/β-arrestin-1 dependent manner in NSCLC. Oncotarget. 2014;5:10486–10502.
   PubMed Web of Science ®Google Scholar
• Hoeppner CZ, Cheng N, Ye RD. Identification of a nuclear localization sequence in β-arrestin-1 and its functional implications. J Biol Chem. 2012;287:8932–8943.
   PubMed Web of Science ®Google Scholar
• Shenoy SK, Han S, Zhao YL, et al. β-arrestin1 mediates metastatic growth of breast cancer cells by facilitating HIF-1-dependent VEGF expression. Oncogene. 2012;31:282–292.
   PubMed Web of Science ®Google Scholar
• Zecchini V, Madhu B, Russell R, et al. Nuclear ARRB1 induces pseudohypoxia and cellular metabolism reprogramming in prostate cancer. Embo J. 2014;33:1365–1382.
   PubMed Web of Science ®Google Scholar
• Purayil HT, Zhang Y, Dey A, et al. Arrestin2 modulates androgen receptor activation. Oncogene. 2015;34:3144–3151.
   PubMed Web of Science ®Google Scholar
• Jazaeri AA, Awtrey CS, Chandramouli GV, et al. Gene expression profiles associated with response to chemotherapy in epithelial ovarian cancers. Clin Cancer Res. 2005;11:6300–6310.
   PubMed Web of Science ®Google Scholar
• Rosanò L, Cianfrocca R, Spinella F, et al. Acquisition of chemoresistance and EMT phenotype is linked with activation of the endothelin A receptor pathway in ovarian carcinoma cells. Clin Cancer Res. 2011;17:2350–2360.
   PubMed Web of Science ®Google Scholar
• Sestito R, Cianfrocca R, Rosanò L, et al. Macitentan blocks endothelin-1 receptor activation required for chemoresistant ovarian cancer cell plasticity and metastasis. Life Sci. 2016;159:43–48.
   PubMed Web of Science ®Google Scholar
• Bell D, Berchuck A, Birrer M, et al. Integrated genomic analyses of ovarian carcinoma. Cancer Genome Atlas Research Network. Nature. 2011;474:609–615.
   PubMed Web of Science ®Google Scholar
• Cerami E, Gao J, Dogrusoz U, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012;2:401–404.
   PubMed Web of Science ®Google Scholar
• Cognetti F, Bagnato A, Colombo N, et al. A phase II, randomized, double-blind study of zibotentan (ZD4054) in combination with carboplatin/paclitaxel versus placebo in combination with carboplatin/paclitaxel in patients with advanced ovarian cancer sensitive to platinum-based chemotherapy (AGO-OVAR 2.14). Gynecol Oncol. 2013;130:31–37.
   PubMed Web of Science ®Google Scholar
• Kim SJ, Kim JS, Kim SW, et al. Macitentan (ACT-064992), a tissue-targeting endothelin receptor antagonist, enhances therapeutic efficacy of paclitaxel by modulating survival pathways in orthotopic models of metastatic human ovarian cancer. Neoplasia. 2011;3:167–179.
   Web of Science ®Google Scholar
• Kim SJ, Kim JS, Kim SW, et al. Antivascular therapy for multidrug-resistant ovarian tumors by macitentan, a dual endothelin receptor antagonist. Transl Oncol. 2012;5:39–47.
   PubMed Web of Science ®Google Scholar
• Coffman L, Mooney C, Lim J, et al. Endothelin receptor-A is required for the recruitment of antitumor T cells and modulates chemotherapy induction of cancer stem cells. Cancer Biol Ther. 2013;14:184–192.
   PubMed Web of Science ®Google Scholar
• Kim SJ, Lee HJ, Kim MS, et al. Macitentan, a dual endothelin receptor antagonist, in combination with temozolomide leads to glioblastoma regression and long-term survival in mice. Clin Cancer Res. 2015;21:4630–4641.
   PubMed Web of Science ®Google Scholar
• Lee HJ, Hanibuchi M, Kim SJ, et al. Treatment of experimental human breast cancer and lung cancer brain metastases in mice by macitentan, a dual antagonist of endothelin receptors, combined with paclitaxel. Neuro Oncol. 2016;18(4):86–96.
   Web of Science ®Google Scholar
• Kim SW, Choi HJ, Lee HJ, et al. Role of the endothelin axis in astrocyte- and endothelial cell-mediated chemoprotection of cancer cells. Neuro Oncol. 2014;12:1585–1598.
   Web of Science ®Google Scholar
• Rosanò L, Bagnato A. Endothelin therapeutics in cancer: where are we? Am J Physiol Regul Integr Comp Physiol. 2016;310:R469–75.
   PubMed Web of Science ®Google Scholar
• Preston CC, Goode EL, Hartmann LC, et al. Immunity and immune suppression in human ovarian cancer. Immunotherapy. 2011;3:539–556.
   PubMed Web of Science ®Google Scholar
• Matulonis UA, Sood AK, Fallowfield L, et al. Ovarian cancer. Nat Rev Dis Primers. 2016;2:16061.
   PubMed Web of Science ®Google Scholar
• Spinella F, Rosanò L, Di Castro V, et al. Endothelin-1 induces vascular endothelial growth factor by increasing hypoxia-inducible factor-1alpha in ovarian carcinoma cells. J Biol Chem. 2002;277:27850–27855.
   PubMed Web of Science ®Google Scholar
• Rosanò L, Spinella F, Castro Di V, et al. Endothelin-1 promotes epithelial-to-mesenchymal transition in human ovarian cancer cells. Cancer Res. 2005;65:11649–11657.
   PubMed Web of Science ®Google Scholar
• Cianfrocca R, Rosanò L, Tocci P, et al. Blocking endothelin-1-receptor/β-catenin circuit sensitizes to chemotherapy in colorectal cancer. Cell Death Differ. 2017. DOI:10.1038/cdd.2017.121
   PubMed Web of Science ®Google Scholar