Deciphering the GPER/GPR30-agonist and antagonists interactions using molecular modeling studies, molecular dynamics, and docking simulations

References

• Arnatt, C. K. , & Zhang, Y. (2013, July). G protein-coupled estrogen receptor (GPER) agonist dual binding mode analyses toward understanding of its activation mechanism: A comparative homology modeling approach. Molecular Informatics , 32 , 647–658.10.1002/minf.v32.7
   PubMed Web of Science ®Google Scholar
• Bai, L. Y. , Weng, J. R. , Hu, J. L. , Wang, D. , Sargeant, A. M. , & Chiu, C. F. (2013). G15, a GPR30 antagonist, induces apoptosis and autophagy in human oral squamous carcinoma cells. Chemico-Biological Interactions , 206 , 375–384. doi:10.1016/j.cbi.2013.10.014 10.1016/j.cbi.2013.10.014
   PubMed Web of Science ®Google Scholar
• Baquedano, M. S. , Saraco, N. , Berensztein, E. , Pepe, C. , Bianchini, M. , Levy, E. , … Belgorosky, A. (2007). Identification and developmental changes of aromatase and estrogen receptor expression in prepubertal and pubertal human adrenal tissues. Journal of Clinical Endocrinology and Metabolism , 92 , 2215–2222.10.1210/jc.2006-2329
   PubMed Web of Science ®Google Scholar
• Batcho, P. F. , Case, D. A. , & Schlick, T. (2001). Optimized particle-mesh Ewald/multiple-time step integration for molecular dynamics simulations. The Journal of Chemical Physics , 115 , 4003–4018.10.1063/1.1389854
   Web of Science ®Google Scholar
• Bermúdez-Lugo, J. A. , Perez-Gonzalez, O. , Rosales-Hernández, M. C. , Ilizaliturri-Flores, I. , Trujillo-Ferrara, J. , & Correa-Basurto, J. (2012). Exploration of the valproic acid binding site on histone deacetylase 8 using docking and molecular dynamic simulations. Journal of Molecular Modeling , 18 , 2301–2310. doi:10.1007/s00894-011-1240-z 10.1007/s00894-011-1240-z
   PubMed Web of Science ®Google Scholar
• Bhattacharya, S. , Hall, S. E. , Li, H. , & Vaidehi, N. (2008). Ligand-stabilized conformational states of human β2 adrenergic receptor: Insight into G-protein-coupled receptor activation. Biophysical Journal , 94 , 2027–2042.10.1529/biophysj.107.117648
   PubMed Web of Science ®Google Scholar
• Bjarnadóttir, T. K. , Gloriam, D. E. , Hellstrand, S. H. , Kristiansson, H. , Fredriksson, R. , & Schiöth, H. B. (2006). Comprehensive repertoire and phylogenetic analysis of the G protein coupled receptors in human and mouse. Genomics , 88 , 263–273.10.1016/j.ygeno.2006.04.001
   PubMed Web of Science ®Google Scholar
• Bologa, C. G. , Revankar, C. M. , Young, S. M. , Edwards, B. S. , Arterburn, J. B. , Kiselyov, A. S. , … Prossnitz, E. R. (2006). Virtual and biomolecular screening converge on a selective agonist for GPR30. Nature Chemical Biology , 2 , 207–212.10.1038/nchembio775
   PubMed Web of Science ®Google Scholar
• Burgoyne, N. J. , & Jackson, R. M. (2006). Predicting protein interaction sites: Binding hot-spots in protein–protein and protein–ligand interfaces. Bioinformatics , 22 , 1335–1342.10.1093/bioinformatics/btl079
   PubMed Web of Science ®Google Scholar
• Carmeci, C. , Thompson, D. A. , Ring, H. Z. , Francke, U. , & Weigel, R. J. (1997). Identification of a gene (GPR30) with homology to the G-protein-coupled receptor superfamily associated with estrogen receptor expression in breast cancer. Genomics , 45 , 607–617.10.1006/geno.1997.4972
   PubMed Web of Science ®Google Scholar
• Chen, Y. , Li, Z. , He, Y. , Shang, D. , Pan, J. , Wang, H. , … Wang, X. (2014). Estrogen and pure antiestrogen fulvestrant (ICI 182 780) augment cell- matrigel adhesion of MCF-7 breast cancer cells through a novel G protein coupled estrogen receptor (GPR30)-to-calpain signaling axis. Toxicology and Applied Pharmacology , 275, 176–181. doi:10.1016/j.taap.2014.01.005
   PubMed Web of Science ®Google Scholar
• Contreras-Romo, M. C. , Martínez-Archundia, M. , Deeb, O. , Slusarz, M. J. , Ramírez-Salinas, G. , Garduño-Juárez, R. , … Correa-Basurto, J. (2014). Exploring the ligand recognition properties of the human vasopressin v1a receptor using QSAR and molecular modeling studies. Chemical Biology & Drug Design , 83 , 207–223. doi:10.1111/cbdd.12229
   PubMed Web of Science ®Google Scholar
• Correa-Basurto, J. , Bello, M. , Rosales-Hernández, M. C. , Hernández-Rodríguez, M. , Nicolás-Vázquez, I. , Rojo-Domínguez, A. , … Flores-Sandoval, C. A. (2013). QSAR, docking, dynamic simulation and quantum mechanics studies to explore the recognition properties of cholinesterase binding sites. Chemico-biological Interactions , 209C , 1–13.
   Google Scholar
• Costanzi, Stefano (2012). Homology modeling of class A G protein-coupled receptors. Methods in Molecular Biology , 857 , 259–279. doi:10.1007/978-1-61779-588-6_11
   PubMedGoogle Scholar
• Dennis, M. K. , Burai, R. , Ramesh, C. , Petrie, W. K. , Alcon, S. N. , Nayak, T. K. , … Prossnitz, E. R. (2009). In vivo effects of a GPR30 antagonist. Nature Chemical Biology , 5 , 421–427.10.1038/nchembio.168
   PubMed Web of Science ®Google Scholar
• Dennis, M. K. , Field, A. S. , Burai, R. , Ramesh, C. , Petrie, W. K. , Bologa, C. G. , … Prossnitz, E. R. (2011). Identification of a GPER/GPR30 antagonist with improved estrogen receptor counterselectivity. Journal of Steroid Biochemistry & Molecular Biology. , 127 , 358–366.
   PubMed Web of Science ®Google Scholar
• Deroo, B. J. , & Korach, K. S. (2006). Estrogen receptors and human disease. Journal of Clinical Investigation , 116 , 561–570.10.1172/JCI27987
   PubMed Web of Science ®Google Scholar
• Fatakia, S. N. , Constanzi, S. , & Chow, C. C. (2011). Molecular evolution of the transmembrane domains of G protein coupled receptors. PLos ONE , 6 , e27813. doi:10.1371/journal.pone.0027813
   PubMed Web of Science ®Google Scholar
• Filardo, E. J. , Quinn, J. A. , Bland, K. I. , & Frackelton, A. R., Jr (2000). Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Molecular Endocrinology , 14 , 1649–1660.10.1210/mend.14.10.0532
   PubMed Web of Science ®Google Scholar
• Frisch, M. J. , Trucks, G. W. , Schlegel, H. B. , Scuseria, G. E. , Robb, M. A. , Cheeseman, J. R. , … Pople, J. A. (1998). Gaussian 98, revision A.9 . Pittsburgh, PA : Gaussian.
   Google Scholar
• Glykos, N. M. (2006). Software news and updates carma: A molecular dynamics analysis program. Journal of Computational Chemistry , 27 , 1765–1768.10.1002/(ISSN)1096-987X
   PubMed Web of Science ®Google Scholar
• Hamza, A. , Sarma, M. H. , & Sarma, R. H. (2003, June). Plausible interaction of an alpha-fetoprotein cyclopeptide with the G-protein-coupled receptor model GPR30: Docking study by molecular dynamics simulated annealing. Journal of Biomolecular Structure & Dynamics , 20 , 751–758.
   PubMed Web of Science ®Google Scholar
• Harris, G. L. , Creason, M. B. , Brulte, G. B. , & Herr, D. R. (2012). In vitro and in vivo antagonism of a g protein-coupled receptor (S1P3) with a novel blocking monoclonal antibody. PLoS ONE , 7 , e35129. doi:10.1371/journal.pone.0035129 10.1371/journal.pone.0035129
   PubMed Web of Science ®Google Scholar
• Humphrey, W. , Dalke, A. , & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics , 14 , 33–38.10.1016/0263-7855(96)00018-5
   PubMed Web of Science ®Google Scholar
• Kurt, A. H. , Tiftik, R. N. , Un, I. , Ulker, S. , & Buyukafsar, K. (2013). G protein-coupled estrogen receptor1 (GPER1) may mediate Rho-kinase (ROCK-2) up-regulation in coronary endothelial cells. Endocrine Regulations , 47 , 75–84.10.4149/endo_2013_02_75
   PubMedGoogle Scholar
• Lappano, R. , Rosano, C. , Santolla, M. F. , Pupo, M. , De Francesco, E. M. , De Marco, P. , … Maggiolini, M. (2012, June). Two novel GPER agonists induce gene expression changes and growth effects in cancer cells. Current Cancer Drug Targets , 12 , 531–542.10.2174/156800912800673284
   PubMed Web of Science ®Google Scholar
• Lappano, R. , Santolla, M. F. , Pupo, M. , Sinicropi, M. S. , Caruso, A. , Rosano, C. , & Maggiolini, M. (2012, January 17). MIBE acts as antagonist ligand of both estrogen receptor α and GPER in breast cancer cells. Breast Cancer Research , 14 , R12.10.1186/bcr3096
   PubMed Web of Science ®Google Scholar
• Laurie, A. T. , & Jackson, R. M. (2005). Q-SiteFinder: An energy-based method for the prediction of protein–ligand binding sites. Bioinformatics , 21 , 1908–1916.10.1093/bioinformatics/bti315
   PubMed Web of Science ®Google Scholar
• Lin, B. C. , Suzawa, M. , Blind, R. D. , Tobias, S. C. , Bulun, S. E. , Scalan, T. S. , & Ingraham, H. A. (2009). Stimulating the GPR30 estrogen receptor with a novel tamoxifen analogue activates SF-1 and promotes endometrial cell proliferation. Cancer Research , 69 , 5415–5423.10.1158/0008-5472.CAN-08-1622
   PubMed Web of Science ®Google Scholar
• Lundstrom, K. (2009). An overview on GPCRs and drug discovery: Structure-based drug design and structural biology on GPCRs. Methods in Molecular Biology , 552 , 51–66.10.1007/978-1-60327-317-6
   PubMedGoogle Scholar
• MacKerell, A. D. , Bashford, D. , Dunbrack, R. L. , Evanseck, J. D. , Field, M. J. , Fischer, S. , … Karplus, M. (1998). All-atom empirical potential for molecular modeling and dynamics studies of proteins. Journal of Physical Chemistry , 102 , 3586–3616.10.1021/jp973084f
   PubMed Web of Science ®Google Scholar
• Martínez-Archundia, M. , & José, Correa-Basurto (2013). Molecular dynamics simulations reveal initial structural and dynamic features for the A2AR as a result of ligand binding. Molecular Simulation , 40 . doi:10.1080/08927022.2013.835485
   Web of Science ®Google Scholar
• Martyna, G. J. , Tobias, D. J. , & Klein, M. L. (1994). Constant pressure molecular dynamics algorithms. The Journal of Chemical Physics , 101 , 4177–4189.10.1063/1.467468
   Web of Science ®Google Scholar
• Morris, G. M. , Huey, R. , Lindstrom, W. , Sanner, M. F. , Belew, R. K. , Goodsell, D. S. , & Olson, A. J. (2009, December). AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexiblity. Journal of Computational Chemistry , 30 , 2785–2791.10.1002/jcc.v30:16
   PubMed Web of Science ®Google Scholar
• O’Dowd, B. F. , Nguyen, T. , Marchese, A. , Cheng, R. , Lynch, K. R. , Heng, H. H. , … George, S. R. (1998). Discovery of three novel g-protein-coupled receptor genes. Genomics , 47 , 310–313.10.1006/geno.1998.5095
   PubMed Web of Science ®Google Scholar
• Owman, C. , Blay, P. , Nilsson, C. , & Lolait, S. J. (1996). Cloning of human cDNA encoding a novel heptahelix receptor expressed in Burkitt’s lymphoma and Widely distributed in brain and peripheral tissues. Biochemical and Biophysical Research Communications , 228 , 285–292.10.1006/bbrc.1996.1654
   PubMed Web of Science ®Google Scholar
• Paterni, I. , Bertini, S. , Granchi, C. , Macchia, M. , & Minutolo, F. (2013). Estrogen receptor ligands: A patent review update. Expert Opinion on Therapeutic Patents , 23 , 1247–1271.10.1517/13543776.2013.805206
   PubMed Web of Science ®Google Scholar
• Petrie, W. K. , Dennis, M. K. , Hu, C. , Dai, D. , Arterburn, J. B. , Smith, H. O. , … Prossnitz, E. R. (2013). G protein-coupled estrogen receptor-selective ligands modulate endometrial tumor growth. Obstetrics and Gynecology International , 2013 , 472720. doi:10.1155/2013/472720
   PubMedGoogle Scholar
• Phillips, J. C. , Braun, R. , Wang, W. , Gumbart, J. , Tajkhorshid, E. , Villa, E. , … Schulten, K. (2005). Scalable molecular dynamics with NAMD. Journal of Computational Chemistry , 26 , 1781–1802.10.1002/(ISSN)1096-987X
   PubMed Web of Science ®Google Scholar
• Prossnitz, E. R. , Arterburn, J. B. , Smith, H. O. , Oprea, T. I. , Sklar, L. A. , & Hathaway, H. J. (2008). Estrogen signaling through the transmembrane G protein-coupled receptor GPR30. Annual Review of Physiology , 70 , 165–190.10.1146/annurev.physiol.70.113006.100518
   PubMed Web of Science ®Google Scholar
• Revankar, C. M. , Cimino, D. F. , Sklar, L. A. , Arterburn, J. B. , & Prossnitz, E. R. (2005). A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science , 307 , 1625–1630.10.1126/science.1106943
   PubMed Web of Science ®Google Scholar
• Rodríguez, D. , Piñeiro, Á. , & Gutiérrez-de-Terán, H. (2011). Molecular dynamics simulations reveal insights into key structural elements of adenosine receptors. Biochemistry , 50 , 4194–4208.10.1021/bi200100t
   PubMed Web of Science ®Google Scholar
• Rosano, C. , Lappano, R. , Santolla, M. F. , Ponassi, M. , Donadini, A. , & Maggiolini, M. (2012). Recent advances in the rationale design of GPER ligands. Current Medicinal Chemistry , 19 , 6199–6206.10.2174/092986712804485755
   PubMed Web of Science ®Google Scholar
• Ryckaert, J. P. , Ciccotti, G. , & Berendsen, H. J. C. (1977). Numerical integration of the Cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes. Journal of Computational Physics , 23 , 321–341.
   Web of Science ®Google Scholar
• Soriano-Ursúa, M. A. , Trujillo-Ferrara, J. G. , Correa-Basurto, J. , & Vilar, S. (2013). Recent structural advances of β1 and β2 adrenoceptors yield keys for ligand recognition and drug design. Journal of Medicinal Chemistry , 56 , 8207–8223.10.1021/jm400471z
   PubMed Web of Science ®Google Scholar
• Takada, Y. , Kato, C. , Kondo, S. , Korenaga, R. , & Ando, J. (1997). Cloning of cDNAs encoding G protein-coupled receptor expressed in human endothelial cells exposed to fluid shear stress. Biochemical and Biophysical Research Communications , 240 , 737–741.10.1006/bbrc.1997.7734
   PubMed Web of Science ®Google Scholar
• Teuten, A. J. , Broadhurst, R. W. , Smith, R. A. , & Dobson, C. M. (1993). Characterization of structural and folding properties of streptokinase by N.M.R. spectroscopy. Biochemical Journal , 290 , 313–319.
   PubMed Web of Science ®Google Scholar
• Thomas, P. , Pang, Y. , Filardo, E. J. , & Dong, J. (2005). Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology , 146 , 624–632.10.1210/en.2004-1064
   PubMed Web of Science ®Google Scholar
• Trzaskowski, B. , Latek, D. , Yuan, S. , Ghoshdastider, U. , Debinski, A. , & Filipek, S. (2012). Action of molecular switches in GPCRs – Theoretical and experimental studies. Current Medicinal Chemistry , 19 , 1090–1109.10.2174/092986712799320556
   PubMed Web of Science ®Google Scholar
• Tsai, C. L. , Wu, H. M. , Lin, C. Y. , Lin, Y. J. , Chao, A. , Wang, T. H. , … Wang, H. S. (2013). Estradiol and tamoxifen induce cell migration through GPR30 and activation of focal adhesion kinase (FAK) in endometrial cancers with low or without nuclear estrogen receptor α (ERα). PLos ONE , 8 , e72999. doi:10.1371/journal.pone.0072999 10.1371/journal.pone.0072999
   PubMed Web of Science ®Google Scholar
• Vivacqua, A. , Bonofiglio, D. , Recchia, A. G. , Musti, A. M. , Picard, D. , Ando, S. , & Maggiolini, M. (2006). The G protein-coupled receptor GPR30 mediates the proliferative effects induced by 17β-estradiol and hydroxytamoxifen in endometrial cancer cells. Molecular Endocrinology , 20 , 631–646.10.1210/me.2005-0280
   PubMed Web of Science ®Google Scholar
• Wahlgren, W. Y. , Omran, H. , von Stetten, D. , Royant, A. , van der Post, S. , & Katona, G. (2012). Structural characterization of bacterioferritin from Blastochloris viridis. PLoS ONE , 7 , e46992. doi:10.1371/journal.pone.0046992 10.1371/journal.pone.0046992
   PubMed Web of Science ®Google Scholar
• Zhang, J. , & Zhang, Y. (2010). GPCRRD: G protein-coupled receptor spatial restraint database for 3D structure modeling and function annotation. Bioinformatics , 26 , 3004–3005.10.1093/bioinformatics/btq563
   PubMed Web of Science ®Google Scholar