2,157
Views
12
CrossRef citations to date
0
Altmetric
Mini-Review

New insights into mechanisms of nuclear translocation of G-protein coupled receptors

, MBBS, MSc, PhD, & , MD, PhD
Pages 254-263 | Received 31 Oct 2016, Accepted 11 Jan 2017, Published online: 10 Feb 2017

References

  • Harris JR. The biochemistry and ultrastructure of the nuclear envelope. Biochim Biophys Acta 1978; 515:55-104; PMID:346065; http://dx.doi.org/10.1016/0304-4157(78)90008-4
  • Alber F, Dokudovskaya S, Veenhoff LM, Zhang W, Kipper J, Devos D, Suprapto A, Karni-Schmidt O, Williams R, Chait BT, et al. The molecular architecture of the nuclear pore complex. Nature 2007; 450:695-701; PMID:18046406; http://dx.doi.org/10.1038/nature06405
  • Devos D, Dokudovskaya S, Alber F, Williams R, Chait BT, Sali A, Rout MP. Components of coated vesicles and nuclear pore complexes share a common molecular architecture. PLoS Biol 2004; 2:e380; PMID:15523559; http://dx.doi.org/10.1371/journal.pbio.0020380
  • Schirmer EC, Gerace L. The nuclear membrane proteome: extending the envelope. Trends Biochem Sci 2005; 30:551-8; PMID:16125387; http://dx.doi.org/10.1016/j.tibs.2005.08.003
  • Arib G, Akhtar A. Multiple facets of nuclear periphery in gene expression control. Curr Opin Cell Biol 2011; 23:346-53; PMID:21242077; http://dx.doi.org/10.1016/j.ceb.2010.12.005
  • Korfali N, Wilkie GS, Swanson SK, Srsen V, de Las Heras J, Batrakou DG, Malik P, Zuleger N, Kerr AR, Florens L, et al. The nuclear envelope proteome differs notably between tissues. Nucleus 2012; 3:552-64; PMID:22990521; http://dx.doi.org/10.4161/nucl.22257
  • Fredriksson R, Lagerstrom MC, Lundin LG, Schioth HB. The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol Pharmacol 2003; 63:1256-72; PMID:12761335; http://dx.doi.org/10.1124/mol.63.6.1256
  • Hamm HE. The many faces of G protein signaling. J Biol Chem 1998; 273:669-72; PMID:9422713; http://dx.doi.org/10.1074/jbc.273.2.669
  • Hur EM, Kim KT. G protein-coupled receptor signalling and cross-talk: achieving rapidity and specificity. Cell Signal 2002; 14:397-405; PMID:11882384; http://dx.doi.org/10.1016/S0898-6568(01)00258-3
  • Zhu T, Gobeil F, Vazquez-Tello A, Leduc M, Rihakova L, Bossolasco M, Bkaily G, Peri K, Varma DR, Orvoine R, et al. Intracrine signaling through lipid mediators and their cognate nuclear G-protein-coupled receptors: a paradigm based on PGE2, PAF, and LPA1 receptors. Can J Physiol Pharmacol 2006; 84:377-91; PMID:16902584; http://dx.doi.org/10.1139/y05-147
  • Joyal JS, Bhosle VK, Chemtob S. Subcellular G-protein coupled receptor signaling hints at greater therapeutic selectivity. Expert Opin Ther Targets 2015; 19:717-21; PMID:25976229; http://dx.doi.org/10.1517/14728222.2015.1042365
  • Song S, Rosen KM, Corfas G. Biological function of nuclear receptor tyrosine kinase action. Cold Spring Harb Perspect Biol 2013; 5(7) pii: a009001; PMID:23818495; http://dx.doi.org/10.1101/cshperspect.a009001
  • Maraldi NM, Mazzotti G, Capitani S, Rizzoli R, Zini N, Squarzoni S, Manzoli FA. Morphological evidence of function-related localization of phospholipids in the cell nucleus. Adv Enzyme Regul 1992; 32:73-90; PMID:1496925; http://dx.doi.org/10.1016/0065-2571(92)90009-O
  • Fricker M, Hollinshead M, White N, Vaux D. Interphase nuclei of many mammalian cell types contain deep, dynamic, tubular membrane-bound invaginations of the nuclear envelope. J Cell Biol 1997; 136:531-44; PMID:9024685; http://dx.doi.org/10.1083/jcb.136.3.531
  • Duvernay MT, Filipeanu CM, Wu G. The regulatory mechanisms of export trafficking of G protein-coupled receptors. Cell Signal 2005; 17:1457-65; PMID:16014327; http://dx.doi.org/10.1016/j.cellsig.2005.05.020
  • Saraste J. Spatial and functional aspects of ER-Golgi Rabs and tethers. Front Cell Dev Biol 2016; 4:28; PMID:27148530; http://dx.doi.org/10.3389/fcell.2016.00028
  • Schindler M, Holland JF, Hogan M. Lateral diffusion in nuclear membranes. J Cell Biol 1985; 100:1408-14; PMID:3988794; http://dx.doi.org/10.1083/jcb.100.5.1408
  • Ungricht R, Klann M, Horvath P, Kutay U. Diffusion and retention are major determinants of protein targeting to the inner nuclear membrane. J Cell Biol 2015; 209:687-703; PMID:26056139; http://dx.doi.org/10.1083/jcb.201409127
  • Wang G, Wu G. Small GTPase regulation of GPCR anterograde trafficking. Trends Pharmacol Sci 2012; 33:28-34; PMID:22015208; http://dx.doi.org/10.1016/j.tips.2011.09.002
  • Iborra FJ, Jackson DA, Cook PR. Coupled transcription and translation within nuclei of mammalian cells. Science 2001; 293:1139-42; PMID:11423616; http://dx.doi.org/10.1126/science.1061216
  • Joyal JS, Nim S, Zhu T, Sitaras N, Rivera JC, Shao Z, Sapieha P, Hamel D, Sanchez M, Zaniolo K, et al. Subcellular localization of coagulation factor II receptor-like 1 in neurons governs angiogenesis. Nat Med 2014; 20:1165-73; PMID:25216639; http://dx.doi.org/10.1038/nm.3669
  • Di Benedetto A, Sun L, Zambonin CG, Tamma R, Nico B, Calvano CD, et al. Osteoblast regulation via ligand-activated nuclear trafficking of the oxytocin receptor. Proc Natl Acad Sci U S A 2014; 111:16502-7; PMID:25378700; http://dx.doi.org/10.1073/pnas.1419349111
  • Zhang C, Clarke PR. Chromatin-independent nuclear envelope assembly induced by Ran GTPase in Xenopus egg extracts. Science 2000; 288:1429-32; PMID:10827954; http://dx.doi.org/10.1126/science.288.5470.1429
  • Askjaer P, Galy V, Hannak E, Mattaj IW. Ran GTPase cycle and importins alpha and beta are essential for spindle formation and nuclear envelope assembly in living Caenorhabditis elegans embryos. Mol Biol Cell 2002; 13:4355-70; PMID:12475958; http://dx.doi.org/10.1091/mbc.E02-06-0346
  • Gorlich D, Kutay U. Transport between the cell nucleus and the cytoplasm. Annu Rev Cell Dev Biol 1999; 15:607-60; PMID:10611974; http://dx.doi.org/10.1146/annurev.cellbio.15.1.607
  • Kalab P, Weis K, Heald R. Visualization of a Ran-GTP gradient in interphase and mitotic Xenopus egg extracts. Science 2002; 295:2452-6; PMID:11923538; http://dx.doi.org/10.1126/science.1068798
  • King MC, Lusk CP, Blobel G. Karyopherin-mediated import of integral inner nuclear membrane proteins. Nature 2006; 442:1003-7; PMID:16929305; http://dx.doi.org/10.1038/nature05075
  • Kalderon D, Richardson WD, Markham AF, Smith AE. Sequence requirements for nuclear location of simian virus 40 large-T antigen. Nature 1984; 311:33-8; PMID:6088992; http://dx.doi.org/10.1038/311033a0
  • Robbins J, Dilworth SM, Laskey RA, Dingwall C. Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell 1991; 64:615-23; PMID:1991323; http://dx.doi.org/10.1016/0092-8674(91)90245-T
  • Kosugi S, Hasebe M, Matsumura N, Takashima H, Miyamoto-Sato E, Tomita M, Yanagawa H. Six classes of nuclear localization signals specific to different binding grooves of importin alpha. J Biol Chem 2009; 284:478-85; PMID:19001369; http://dx.doi.org/10.1074/jbc.M807017200
  • Lu D, Yang H, Shaw G, Raizada MK. Angiotensin II-induced nuclear targeting of the angiotensin type 1 (AT1) receptor in brain neurons. Endocrinology 1998; 139:365-75; PMID:9421435
  • Lee DK, Lanca AJ, Cheng R, Nguyen T, Ji XD, Gobeil F, Jr, Chemtob S, George SR, O'Dowd BF. Agonist-independent nuclear localization of the Apelin, angiotensin AT1, and bradykinin B2 receptors. J Biol Chem 2004; 279:7901-8; PMID:14645236; http://dx.doi.org/10.1074/jbc.M306377200
  • Cattaneo F, Parisi M, Fioretti T, Sarnataro D, Esposito G, Ammendola R. Nuclear localization of Formyl-Peptide Receptor 2 in human cancer cells. Arch Biochem Biophys 2016; 603:10-9; PMID:27177968; http://dx.doi.org/10.1016/j.abb.2016.05.006
  • Nielsen CK, Campbell JI, Ohd JF, Morgelin M, Riesbeck K, Landberg G, Sjölander A. A novel localization of the G-protein-coupled CysLT1 receptor in the nucleus of colorectal adenocarcinoma cells. Cancer Res 2005; 65:732-42; PMID:15705869
  • Marrache AM, Gobeil F, Jr, Bernier SG, Stankova J, Rola-Pleszczynski M, Choufani S, Bkaily G, Bourdeau A, Sirois MG, Vazquez-Tello A, et al. Proinflammatory gene induction by platelet-activating factor mediated via its cognate nuclear receptor. J Immunol 2002; 169:6474-81; PMID:12444157; http://dx.doi.org/10.4049/jimmunol.169.11.6474
  • Bhosle VK, Rivera JC, Zhou TE, Omri S, Sanchez M, Hamel D, Zhu T, Rouget R, Rabea AA, Hou X, et al. Nuclear localization of platelet-activating factor receptor controls retinal neovascularization. Cell Discov 2016; 2:16017; PMID:27462464; http://dx.doi.org/10.1038/celldisc.2016.17
  • Lam MH, Briggs LJ, Hu W, Martin TJ, Gillespie MT, Jans DA. Importin beta recognizes parathyroid hormone-related protein with high affinity and mediates its nuclear import in the absence of importin alpha. J Biol Chem 1999; 274:7391-8; PMID:10066803; http://dx.doi.org/10.1074/jbc.274.11.7391
  • Beguelin W, Diaz Flaque MC, Proietti CJ, Cayrol F, Rivas MA, Tkach M, Rosemblit C, Tocci JM, Charreau EH, Schillaci R, et al. Progesterone receptor induces ErbB-2 nuclear translocation to promote breast cancer growth via a novel transcriptional effect: ErbB-2 function as a coactivator of Stat3. Mol Cell Biol 2010; 30:5456-72; PMID:20876300; http://dx.doi.org/10.1128/MCB.00012-10
  • Chook YM, Suel KE. Nuclear import by karyopherin-betas: recognition and inhibition. Biochim Biophys Acta 2011; 1813:1593-606; PMID:21029754; http://dx.doi.org/10.1016/j.bbamcr.2010.10.014
  • Lee BJ, Cansizoglu AE, Suel KE, Louis TH, Zhang Z, Chook YM. Rules for nuclear localization sequence recognition by karyopherin beta 2. Cell 2006; 126:543-58; PMID:16901787; http://dx.doi.org/10.1016/j.cell.2006.05.049
  • Pickard BW, Hodsman AB, Fraher LJ, Watson PH. Type 1 parathyroid hormone receptor (PTH1R) nuclear trafficking: association of PTH1R with importin alpha1 and beta. Endocrinology 2006; 147:3326-32; PMID:16574786; http://dx.doi.org/10.1210/en.2005-1408
  • Favre N, Camps M, Arod C, Chabert C, Rommel C, Pasquali C. Chemokine receptor CCR2 undergoes transportin1-dependent nuclear translocation. Proteomics 2008; 8:4560-76; PMID:18846510; http://dx.doi.org/10.1002/pmic.200800211
  • Don-Salu-Hewage AS, Chan SY, McAndrews KM, Chetram MA, Dawson MR, Bethea DA, Hinton CV. Cysteine (C)-x-C receptor 4 undergoes transportin 1-dependent nuclear localization and remains functional at the nucleus of metastatic prostate cancer cells. PLoS One 2013; 8:e57194; PMID:23468933; http://dx.doi.org/10.1371/journal.pone.0057194
  • Mizuno-Yamasaki E, Rivera-Molina F, Novick P. GTPase networks in membrane traffic. Annu Rev Biochem 2012; 81:637-59; PMID:22463690; http://dx.doi.org/10.1146/annurev-biochem-052810-093700
  • Johnson DC, Baines JD. Herpesviruses remodel host membranes for virus egress. Nat Rev Microbiol 2011; 9:382-94; PMID:21494278; http://dx.doi.org/10.1038/nrmicro2559
  • Burns LT, Wente SR. Trafficking to uncharted territory of the nuclear envelope. Curr Opin Cell Biol 2012; 24:341-9; PMID:22326668; http://dx.doi.org/10.1016/j.ceb.2012.01.009
  • Miaczynska M, Christoforidis S, Giner A, Shevchenko A, Uttenweiler-Joseph S, Habermann B, et al. APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 2004; 116:445-56; PMID:15016378; http://dx.doi.org/10.1016/S0092-8674(04)00117-5
  • Maltese WA, Soule G, Gunning W, Calomeni E, Alexander B. Mutant Rab24 GTPase is targeted to nuclear inclusions. BMC Cell Biol 2002; 3:25; PMID:12323076; http://dx.doi.org/10.1186/1471-2121-3-25
  • Horgan CP, McCaffrey MW. The dynamic Rab11-FIPs. Biochem Soc Trans 2009; 37:1032-6; PMID:19754446; http://dx.doi.org/10.1042/BST0371032
  • Fielding AB, Schonteich E, Matheson J, Wilson G, Yu X, Hickson GR, Srivastava S, Baldwin SA, Prekeris R, Gould GW. Rab11-FIP3 and FIP4 interact with Arf6 and the exocyst to control membrane traffic in cytokinesis. EMBO J 2005; 24:3389-99; PMID:16148947; http://dx.doi.org/10.1038/sj.emboj.7600803
  • Campa CC, Hirsch E. Rab11 and phosphoinositides: A synergy of signal transducers in the control of vesicular trafficking. Adv Biol Regul 2016; pii: S2212–4926(16)30043-4; PMID:27658318; http://dx.doi.org/10.1016/j.jbior.2016.09.002
  • Lim YS, Tang BL. A role for Rab23 in the trafficking of Kif17 to the primary cilium. J Cell Sci 2015; 128:2996-3008; PMID:26136363; http://dx.doi.org/10.1242/jcs.163964
  • Williams CL. The polybasic region of Ras and Rho family small GTPases: a regulator of protein interactions and membrane association and a site of nuclear localization signal sequences. Cell Signal 2003; 15:1071-80; PMID:14575862; http://dx.doi.org/10.1016/S0898-6568(03)00098-6
  • Mahalakshmi RN, Ng MY, Guo K, Qi Z, Hunziker W, Beguin P. Nuclear localization of endogenous RGK proteins and modulation of cell shape remodeling by regulated nuclear transport. Traffic 2007; 8:1164-78; PMID:17605760; http://dx.doi.org/10.1111/j.1600-0854.2007.00599.x
  • Cullen PJ. Endosomal sorting and signalling: an emerging role for sorting nexins. Nat Rev Mol Cell Biol 2008; 9:574-82; PMID:18523436; http://dx.doi.org/10.1038/nrm2427
  • Simunovic M, Voth GA, Callan-Jones A, Bassereau P. When physics takes over: BAR proteins and membrane curvature. Trends Cell Biol 2015; 25:780-92; PMID:26519988; http://dx.doi.org/10.1016/j.tcb.2015.09.005
  • Heydorn A, Sondergaard BP, Ersboll B, Holst B, Nielsen FC, Haft CR, Whistler J, Schwartz TW. A library of 7TM receptor C-terminal tails. Interactions with the proposed post-endocytic sorting proteins ERM-binding phosphoprotein 50 (EBP50), N-ethylmaleimide-sensitive factor (NSF), sorting nexin 1 (SNX1), and G protein-coupled receptor-associated sorting protein (GASP). J Biol Chem 2004; 279:54291-303; PMID:15452121; http://dx.doi.org/10.1074/jbc.M406169200
  • Nisar S, Kelly E, Cullen PJ, Mundell SJ. Regulation of P2Y1 receptor traffic by sorting Nexin 1 is retromer independent. Traffic 2010; 11:508-19; PMID:20070609; http://dx.doi.org/10.1111/j.1600-0854.2010.01035.x
  • Gonzalez-Granado JM, Navarro-Puche A, Molina-Sanchez P, Blanco-Berrocal M, Viana R, Font de Mora J, et al. Sorting nexin 6 enhances lamin a synthesis and incorporation into the nuclear envelope. PLoS One 2014; 9:e115571; PMID:25535984; http://dx.doi.org/10.1371/journal.pone.0115571
  • Zhu CH, Morse LR, Battaglino RA. SNX10 is required for osteoclast formation and resorption activity. J Cell Biochem 2012; 113:1608-15; PMID:22174188
  • Xu J, Xu T, Wu B, Ye Y, You X, Shu X, Pei D, Liu J. Structure of sorting nexin 11 (SNX11) reveals a novel extended phox homology (PX) domain critical for inhibition of SNX10-induced vacuolation. J Biol Chem 2013; 288:16598-605; PMID:23615901; http://dx.doi.org/10.1074/jbc.M112.449306
  • Kang DS, Tian X, Benovic JL. Role of beta-arrestins and arrestin domain-containing proteins in G protein-coupled receptor trafficking. Curr Opin Cell Biol 2014; 27:63-71; PMID:24680432; http://dx.doi.org/10.1016/j.ceb.2013.11.005
  • Vilardaga JP, Gardella TJ, Wehbi VL, Feinstein TN. Non-canonical signaling of the PTH receptor. Trends Pharmacol Sci 2012; 33:423-31; PMID:22709554; http://dx.doi.org/10.1016/j.tips.2012.05.004
  • Claing A, Chen W, Miller WE, Vitale N, Moss J, Premont RT, Lefkowitz RJ. beta-Arrestin-mediated ADP-ribosylation factor 6 activation and beta 2-adrenergic receptor endocytosis. J Biol Chem 2001; 276:42509-13; PMID:11533043; http://dx.doi.org/10.1074/jbc.M108399200
  • Macia E, Partisani M, Paleotti O, Luton F, Franco M. Arf6 negatively controls the rapid recycling of the beta2 adrenergic receptor. J Cell Sci 2012; 125:4026-35; PMID:22611259; http://dx.doi.org/10.1242/jcs.102343
  • Kang J, Shi Y, Xiang B, Qu B, Su W, Zhu M, Zhang M, Bao G, Wang F, Zhang X, et al. A nuclear function of beta-arrestin1 in GPCR signaling: regulation of histone acetylation and gene transcription. Cell 2005; 123:833-47; PMID:16325578; http://dx.doi.org/10.1016/j.cell.2005.09.011
  • Scott MG, Le Rouzic E, Perianin A, Pierotti V, Enslen H, Benichou S, Marullo S, Benmerah A. Differential nucleocytoplasmic shuttling of beta-arrestins. Characterization of a leucine-rich nuclear export signal in beta-arrestin2. J Biol Chem 2002; 277:37693-701; PMID:12167659; http://dx.doi.org/10.1074/jbc.M207552200
  • DeFea KA, Zalevsky J, Thoma MS, Dery O, Mullins RD, Bunnett NW. beta-arrestin-dependent endocytosis of proteinase-activated receptor 2 is required for intracellular targeting of activated ERK1/2. J Cell Biol 2000; 148:1267-81; PMID:10725339; http://dx.doi.org/10.1083/jcb.148.6.1267
  • Mosca TJ, Schwarz TL. The nuclear import of Frizzled2-C by Importins-beta11 and alpha2 promotes postsynaptic development. Nat Neurosci 2010; 13:935-43; PMID:20601947; http://dx.doi.org/10.1038/nn.2593
  • Valdehita A, Bajo AM, Fernandez-Martinez AB, Arenas MI, Vacas E, Valenzuela P, Ruíz-Villaespesa A, Prieto JC, Carmena MJ. Nuclear localization of vasoactive intestinal peptide (VIP) receptors in human breast cancer. Peptides 2010; 31:2035-45; PMID:20691743; http://dx.doi.org/10.1016/j.peptides.2010.07.024
  • Savard M, Barbaz D, Belanger S, Muller-Esterl W, Bkaily G, D'Orleans-Juste P, Coté J, Bovenzi V, Gobeil F Jr. Expression of endogenous nuclear bradykinin B2 receptors mediating signaling in immediate early gene activation. J Cell Physiol 2008; 216:234-44; PMID:18264983; http://dx.doi.org/10.1002/jcp.21398
  • Charo DN, Ho M, Fajardo G, Kawana M, Kundu RK, Sheikh AY, Finsterbach TP, Leeper NJ, Ernst KV, Chen MM, et al. Endogenous regulation of cardiovascular function by apelin-APJ. Am J Physiol Heart Circ Physiol 2009; 297:H1904-13; PMID:19767528; http://dx.doi.org/10.1152/ajpheart.00686.2009
  • Gobeil F, Jr., Bernier SG, Vazquez-Tello A, Brault S, Beauchamp MH, Quiniou C, Marrache AM, Checchin D, Sennlaub F, Hou X, et al. Modulation of pro-inflammatory gene expression by nuclear lysophosphatidic acid receptor type-1. J Biol Chem 2003; 278:38875-83; PMID:12847111; http://dx.doi.org/10.1074/jbc.M212481200
  • Waters CM, Saatian B, Moughal NA, Zhao Y, Tigyi G, Natarajan V, Pyne S, Pyne NJ. Integrin signalling regulates the nuclear localization and function of the lysophosphatidic acid receptor-1 (LPA1) in mammalian cells. Biochem J 2006; 398:55-62; PMID:16716145; http://dx.doi.org/10.1042/BJ20060155
  • Estrada R, Wang L, Jala VR, Lee JF, Lin CY, Gray RD, Haribabu B, Lee MJ. Ligand-induced nuclear translocation of S1P(1) receptors mediates Cyr61 and CTGF transcription in endothelial cells. Histochem Cell Biol 2009; 131:239-49; PMID:18936953; http://dx.doi.org/10.1007/s00418-008-0521-9
  • Lynch JM, Henson PM. The intracellular retention of newly synthesized platelet-activating factor. J Immunol 1986; 137:2653-61; PMID:3093579
  • Wright CD, Wu SC, Dahl EF, Sazama AJ, O'Connell TD. Nuclear localization drives alpha1-adrenergic receptor oligomerization and signaling in cardiac myocytes. Cell Signal 2012; 24:794-802; PMID:22120526; http://dx.doi.org/10.1016/j.cellsig.2011.11.014
  • Bkaily G, Sleiman S, Stephan J, Asselin C, Choufani S, Kamal M, Jacques D, Gobeil F Jr, D'Orléans-Juste P. Angiotensin II AT1 receptor internalization, translocation and de novo synthesis modulate cytosolic and nuclear calcium in human vascular smooth muscle cells. Can J Physiol Pharmacol 2003; 81:274-87; PMID:12733826; http://dx.doi.org/10.1139/y03-007
  • Wang L, Wang Z, Yang B, Yang Q, Wang L, Sun Y. CXCR4 nuclear localization follows binding of its ligand SDF-1 and occurs in metastatic but not primary renal cell carcinoma. Oncol Rep 2009; 22:1333-9; PMID:19885584
  • Bkaily G, Choufani S, Hassan G, El-Bizri N, Jacques D, D'Orleans-Juste P. Presence of functional endothelin-1 receptors in nuclear membranes of human aortic vascular smooth muscle cells. J Cardiovasc Pharmacol 2000; 36:S414-7; PMID:11078437; http://dx.doi.org/10.1097/00005344-200036051-00121
  • Boivin B, Chevalier D, Villeneuve LR, Rousseau E, Allen BG. Functional endothelin receptors are present on nuclei in cardiac ventricular myocytes. J Biol Chem 2003; 278:29153-63; PMID:12756260; http://dx.doi.org/10.1074/jbc.M301738200
  • Jacques D, Descorbeth M, Abdel-Samad D, Provost C, Perreault C, Jules F. The distribution and density of ET-1 and its receptors are different in human right and left ventricular endocardial endothelial cells. Peptides 2005; 26:1427-35; PMID:16042982; http://dx.doi.org/10.1016/j.peptides.2005.03.048
  • Mathew D, Ataman B, Chen J, Zhang Y, Cumberledge S, Budnik V. Wingless signaling at synapses is through cleavage and nuclear import of receptor DFrizzled2. Science 2005; 310:1344-7; PMID:16311339; http://dx.doi.org/10.1126/science.1117051
  • Doufexis M, Storr HL, King PJ, Clark AJ. Interaction of the melanocortin 2 receptor with nucleoporin 50: evidence for a novel pathway between a G-protein-coupled receptor and the nucleus. FASEB J 2007; 21:4095-100; PMID:17625072; http://dx.doi.org/10.1096/fj.06-7927com
  • Ferrandon S, Feinstein TN, Castro M, Wang B, Bouley R, Potts JT, Gardella TJ, Vilardaga JP. Sustained cyclic AMP production by parathyroid hormone receptor endocytosis. Nat Chem Biol 2009; 5:734-42; PMID:19701185; http://dx.doi.org/10.1038/nchembio.206
  • Benard G, Massa F, Puente N, Lourenco J, Bellocchio L, Soria-Gomez E, Matias I, Delamarre A, Metna-Laurent M, Cannich A, et al. Mitochondrial CB(1) receptors regulate neuronal energy metabolism. Nat Neurosci 2012; 15:558-64; PMID:22388959; http://dx.doi.org/10.1038/nn.3053
  • Sergin I, Jong Y-JI, Harmon SK, Kumar V, O'Malley KL. Sequences within the C-terminus of the metabotropic glutamate receptor, mGluR5, are responsible for inner nuclear membrane localization. J Biol Chem 2017; pii: jbc.M116.757724; PMID:28096465; http://dx.doi.org/10.1074/jbc.M116.757724

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.