Identification of Two Benzopyrroloxazines Acting as Selective GPER Antagonists in Breast Cancer Cells and Cancer-Associated Fibroblasts

References

• Deroo BJ , KorachKS. Estrogen receptors and human disease. J. Clin. Invest.116, 561–570 (2006).
   PubMed Web of Science ®Google Scholar
• Maggiolini M , PicardD. The unfolding stories of GPR30, a new membrane bound estrogen receptor. J. Endocrinol.204, 105–114 (2010).
   PubMed Web of Science ®Google Scholar
• Filardo EJ , QuinnJA, BlandKI, FrackeltonJrAR. Estrogen-induced activation Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor throughout release of HB-EGF. Mol. Endocrinol.14, 1649–1660 (2000).
   PubMed Web of Science ®Google Scholar
• Prossnitz ER , MaggioliniM. Mechanisms of estrogen signaling and gene expression via GPR30. Mol. Cell. Endocrinol.308, 32–38 (2009).
   PubMed Web of Science ®Google Scholar
• Bologa CG , RevankarCM, YoungSMet al. Virtual and biomolecular screening converge on a selective agonist for GPR30. Nat. Chem. Biol.2, 207–212 (2006).
   PubMed Web of Science ®Google Scholar
• Prossnitz ER , OpreaTI, SklarLA, ArterburnJB. The ins and outs of GPR30: a transmembrane estrogen receptor. J. Steroid Biochem. Mol. Biol.109, 350–353 (2008).
   PubMed Web of Science ®Google Scholar
• Prossnitz ER , BartonM. The G-protein-coupled estrogen receptor GPER in health and disease. Nat. Rev. Endocrinol.7, 715–726 (2011).
   PubMed Web of Science ®Google Scholar
• Hammond R , MaukR, NinaciD, NelsonD, GibbsRB. Chronic treatment with estrogen receptor agonists restores acquisition of a spatial learning task in young ovariectomized rats. Horm. Behav.56, 309–314 (2009).
   PubMed Web of Science ®Google Scholar
• Blasko E , HaskellCA, LeungSet al. Beneficial role of the GPR30 agonist G-1 in an animal model of multiple sclerosis. J. Neuroimmunol.214, 67–77 (2009).
   PubMed Web of Science ®Google Scholar
• Arterburn JB , OpreaTI, ProssnitzER, EdwardsBS, SklarLA. Discovery of selective probes and antagonists for G protein-coupled receptors for FPR/FPRL1 and GPR30. Curr. Top. Med. Chem.9, 1227–1236 (2009).
   PubMed Web of Science ®Google Scholar
• Lindsey SH , CohenJA, BrosnihanKB, GallagherPE, ChappellMC. Chronic treatment with the G protein-coupled receptor 30 agonist G-1 decreases blood pressure in ovariectomized mRen2. Lewis rats. Endocrinology150, 3753–3758 (2009).
   PubMed Web of Science ®Google Scholar
• Lappano R , RosanoC, SantollaMFet al. Two novel GPER agonists induce gene expression changes and growth effects in cancer cells. Curr. Cancer Drug Targ.12, 531–542 (2012).
   PubMed Web of Science ®Google Scholar
• Santolla MF , De FrancescoEM, LappanoR, RosanoC, AbonanteS, Maggiolini, M. Niacin activates the G protein-coupled estrogen receptor (GPER)-mediated signaling. Cell. Signal.26 (7), 1466–1475 (2014).
   PubMed Web of Science ®Google Scholar
• Dennis MK , FieldAS, BuraiRet al. Identification of GPER/GPR30 antagonist with improved estrogen receptor counterselectivity. J. Steroid Biochem. Mol. Biol.127, 358–366 (2011).
   PubMed Web of Science ®Google Scholar
• Huryn DM , ResnickLO, WipfP. Contributions of academic laboratories to the discovery and development of chemical biology tools. J. Med. Chem.56, 7161–7176 (2013).
   PubMed Web of Science ®Google Scholar
• Burai R , RameshC, NayakTKet al. Synthesis and characterization of tricarbonyl-Re/Tc(I) chelate probes targeting the G protein-coupled estrogen receptor GPER/GPR30. PLoS ONE7, e46861 (2012).
   PubMed Web of Science ®Google Scholar
• Lappano R , SantollaMF, PupoMet al. MIBE acts as antagonist ligand of both estrogen receptor α and GPER in breast cancer cells. Breast Cancer Res.14, R12 (2012).
   PubMed Web of Science ®Google Scholar
• Lorusso G , RüeggC. The tumor microenvironment and its contribution to tumor evolution toward metastasis. Histochem. Cell Biol.130, 1091–1103 (2008).
   PubMed Web of Science ®Google Scholar
• Sali A , BlundellTL. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol.234, 779–815 (1993).
   PubMed Web of Science ®Google Scholar
• Rosano C , LappanoR, SantollaMF, PonassiM, DonadiniA, MaggiolinM. Recent advances in the rationale design of GPER ligands. Curr. Med. Chem.19, 6199–6206 (2012).
   PubMed Web of Science ®Google Scholar
• Murshudov GN , SkubákP, LebedevAAet al. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D67, 355–367 (2011).
   PubMed Web of Science ®Google Scholar
• Lappano R , RosanoC, De MarcoP, De FrancescoEM, PezziV, MaggioliniM. Estriol acts as a GPR30 antagonist in estrogen receptor-negative breast cancer cells. Mol. Cell Endocrinol.204, 105–114 (2010).
   Google Scholar
• Chimento A , CasaburiI, BartucciMet al. Selective GPER activation decreases proliferation and activates apoptosis in tumor Leydig cells. Cell Death Dis.4, e747 (2013).
   PubMed Web of Science ®Google Scholar
• Amaro AA , EspositoAI, MirisolaVet al. Endocrine disruptor agent nonyl phenol exerts an estrogen-like transcriptional activity on estrogen receptor positive breast cancer cells. Curr. Med. Chem.21, 630–640 (2014).
   PubMed Web of Science ®Google Scholar
• Pettersen EF , GoddardTD, HuangCCet al. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem.25, 1605–1612 (2004).
   PubMed Web of Science ®Google Scholar
• Lappano R , RecchiaAG, De FrancescoEMet al. The cholesterol metabolite 25-hydroxycholesterol activates estrogen receptor α-mediated signaling in cancer cells and in cardiomyocytes. PLoS ONE6, e16631 (2011).
   PubMed Web of Science ®Google Scholar
• Jirkovsky I , HumberLG, BaudyR. 4-Substituted-4H-pyrrolo[2,1-c][1,4]benzoxazines. J. Heterocyclic Chem.13, 311–316 (1976).
   Web of Science ®Google Scholar
• Lancelot J-C , RaultS, LadureeD, RobbaM. Pyrido[3,2-e]pyrrolo[1,2-a]pyrazines. Chem. Pharm. Bull.33, 2798–2802 (1985).
   Web of Science ®Google Scholar
• Ren P-D , PanS-F, DongT-W, WuS-H. The novel reduction systems: NaBH4-SbCl3 or NaBH4-BiCl3 for conversion of nitroarenes to primary amines. Synthetic Commun.25, 3799–3803 (1995).
   Web of Science ®Google Scholar
• Dennis MK , BuraiR, RameshCet al. In vivo effects of a GPR30 antagonist. Nat. Chem. Biol.5, 421–427 (2009).
   PubMed Web of Science ®Google Scholar
• Bhowmick NA , MosesHL. Tumor-stroma interactions. Curr. Opin. Genet. Dev.15, 97–101 (2005).
   PubMed Web of Science ®Google Scholar
• Bhowmick NA , NeilsonEG, MosesHL. Stromal fibroblasts in cancer initiation and progression. Nature432, 332–337 (2004).
   PubMed Web of Science ®Google Scholar
• Yamaguchi Y , HayashiS. Estrogen-related cancer microenvironment of breast carcinoma. Endocr. J.56, 1–7 (2009).
   PubMed Web of Science ®Google Scholar