Apelin binding to human APJ receptor leads to biased signaling

O'Dowd, 1993, A human gene that shows identity with the gene encoding the angiotensin receptor is located on chromosome 11, Gene, 136, 355, 10.1016/0378-1119(93)90495-O Tatemoto, 1998, Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor, Biochem. Biophys. Res. Commun., 251, 471, 10.1006/bbrc.1998.9489 Chen, 2003, Novel role for the potent endogenous inotrope apelin in human cardiac dysfunction, Circulation, 108, 1432, 10.1161/01.CIR.0000091235.94914.75 Sorli, 2007, Apelin is a potent activator of tumour neoangiogenesis, Oncogene, 26, 7692, 10.1038/sj.onc.1210573 Zhou, 2003, The N-terminal domain of APJ, a CNS-based coreceptor for HIV-1, is essential for its receptor function and coreceptor activity, Virology, 317, 84, 10.1016/j.virol.2003.08.026 Gerbier, 2015, New structural insights into the apelin receptor: identification of key residues for apelin binding, FASEB J., 29, 314, 10.1096/fj.14-256339 Ferguson, 2001, Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling, Pharmacol. Rev., 53, 1 Lee, 2010, The fate of the internalized apelin receptor is determined by different isoforms of apelin mediating differential interaction with beta-arrestin, Biochem. Biophys. Res. Commun., 395, 185, 10.1016/j.bbrc.2010.03.151 Iturrioz, 2010, By interacting with the C-terminal Phe of apelin, Phe255 and Trp259 in helix VI of the apelin receptor are critical for internalization, J. Biol. Chem., 285, 32627, 10.1074/jbc.M110.127167 Katoh, 2002, MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform, Nucleic Acids Res., 30, 3059, 10.1093/nar/gkf436 Katoh, 2005, MAFFT version 5: improvement in accuracy of multiple sequence alignment, Nucleic Acids Res., 33, 511, 10.1093/nar/gki198 Klock, 2009, The polymerase incomplete primer extension (PIPE) method applied to high-throughput cloning and site-directed mutagenesis, Methods Mol. Biol., 498, 91, 10.1007/978-1-59745-196-3_6 Sali, 1993, Comparative protein modelling by satisfaction of spatial restraints, J. Mol. Biol., 234, 779, 10.1006/jmbi.1993.1626 Dolinsky, 2004, PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations, Nucleic Acids Res., 32, W665, 10.1093/nar/gkh381 Bradford, 1976, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 72, 248, 10.1016/0003-2697(76)90527-3 Laemmli, 1970, Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature, 227, 680, 10.1038/227680a0 Kumar, 2014, Easy and efficient protocol for purification of recombinant peptides, Protein Expr. Purif., 95, 129, 10.1016/j.pep.2013.12.004 Kaur, 2009, A modified Western blot protocol for enhanced sensitivity in the detection of a membrane protein, Anal. Biochem., 384, 348, 10.1016/j.ab.2008.10.005 Kenakin, 2012, A simple method for quantifying functional selectivity and agonist bias, ACS Chem. Neurosci., 3, 193, 10.1021/cn200111m Clark, 2010, Importance of extracellular loop one of the neuropeptide S receptor for biogenesis and function, Peptides, 31, 130, 10.1016/j.peptides.2009.10.015 Correa, 2006, Role of the Cys18-Cys274 disulfide bond and of the third extracellular loop in the constitutive activation and internalization of angiotensin II type 1 receptor, Regul. Pept., 134, 132, 10.1016/j.regpep.2006.02.008 Tan, 2013, Structure of the CCR5 chemokine receptor-HIV entry inhibitor maraviroc complex, Science, 341, 1387, 10.1126/science.1241475 Wu, 2010, Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists, Science, 330, 1066, 10.1126/science.1194396 Falcao-Pires, 2010, The apelinergic system: a promising therapeutic target, Expert Opin. Ther. Targets, 14, 633, 10.1517/14728221003752743 Kleinz, 2005, Emerging roles of apelin in biology and medicine, Pharmacol. Ther., 107, 198, 10.1016/j.pharmthera.2005.04.001 Chng, 2013, ELABELA: a hormone essential for heart development signals via the apelin receptor, Dev. Cell, 27, 672, 10.1016/j.devcel.2013.11.002 Venkatakrishnan, 2013, Molecular signatures ofG-protein-coupled receptors, Nature, 494, 185, 10.1038/nature11896 Keov, 2014, Molecular mechanisms of bitopic ligand engagement with the M1 muscarinic acetylcholine receptor, J. Biol. Chem., 289, 23817, 10.1074/jbc.M114.582874 Lin, 1996, Ligand stabilization of the β2 adrenergic receptor: effect of DTT on receptor conformation monitored by circular dichroism and fluorescence spectroscopy, Biochemistry, 35, 14445, 10.1021/bi961619+ Pierce, 2002, Seven-transmembrane receptors, Nat. Rev. Mol. Cell Biol., 3, 639, 10.1038/nrm908 Caunt, 2006, Seven-transmembrane receptor signalling and ERK compartmentalization, Trends Endocrinol. Metab., 17, 276, 10.1016/j.tem.2006.07.008 Ahn, 2004, Differential kinetic and spatial patterns of beta-arrestin and G protein-mediated ERK activation by the angiotensin II receptor, J. Biol. Chem., 279, 35518, 10.1074/jbc.M405878200 Shenoy, 2006, Beta-arrestin-dependent, G protein-independent ERK1/2 activation by the beta2 adrenergic receptor, J. Biol. Chem., 281, 1261, 10.1074/jbc.M506576200 Yue, 2011, Apelin decreases lipolysis via G(q), G(i), and AMPK-dependent mechanisms, Endocrinology, 152, 59, 10.1210/en.2010-0576 Masri, 2002, Apelin (65-77) activates extracellular signal-regulated kinases via a PTX-sensitive G protein, Biochem. Biophys. Res. Commun., 290, 539, 10.1006/bbrc.2001.6230 Lane, 2013, Bridging the gap: bitopic ligands of G-protein-coupled receptors, Trends Pharmacol. Sci., 34, 59, 10.1016/j.tips.2012.10.003 Sbai, 2014, Biased signaling through G-protein-coupled PROKR2 receptors harboring missense mutations, FASEB J., 28, 3734, 10.1096/fj.13-243402 Kobilka, 2007, Conformational complexity of G-protein- coupled receptors, Trends Pharmacol. Sci., 28, 397, 10.1016/j.tips.2007.06.003 Nakajima, 2012, Design and functional characterization of a novel, arrestin-biased designer G protein-coupled receptor, Mol. Pharmacol., 82, 575, 10.1124/mol.112.080358 Evans, 2010, Ligand-directed signalling at beta-adrenoceptors, Br. J. Pharmacol., 159, 1022, 10.1111/j.1476-5381.2009.00602.x Vardy, 2013, Conformational ensembles in GPCR activation, Cell, 152, 385, 10.1016/j.cell.2013.01.025 Barwell, 2011, Extracellular loops 1 and 3 and their associated transmembrane regions of the calcitonin receptor-like receptor are needed for CGRP receptor function, Biochim. Biophys. Acta, 1813, 1906, 10.1016/j.bbamcr.2011.06.005 Massotte, 2005, The second extracellular loop: a damper for G protein-coupled receptors?, Nat. Struct. Mol. Biol., 12, 287, 10.1038/nsmb0405-287 Scarselli, 2007, Multiple residues in the second extracellular loop are critical for M3 muscarinic acetylcholine receptor activation, J. Biol. Chem., 282, 7385, 10.1074/jbc.M610394200