Endocytosis and recycling of G protein-coupled receptors.

Agonist stimulation of G protein-coupled receptors causes a dramatic reorganization of their intracellular distribution. Activation of receptors triggers receptor endocytosis and, since receptors recycle back to the surface continuously, a new steady state is reached where a significant proportion of receptors is located internally. Although this movement of receptors is remarkable, its role has been enigmatic. Recent developments have provided insight into the compartments through which the receptors move, the nature of the signals that trigger receptor translocation, and the significance of receptor cycling for cell function. In this article, Jennifer Koenig and Michael Edwardson review recent progress in this field and place receptor cycling into a mathematical framework that reveals the extent and rate of intracellular receptor movement.

[1]  G. Holman,et al.  Comparison of GLUT4 and GLUT1 subcellular trafficking in basal and insulin-stimulated 3T3-L1 cells. , 1993, The Journal of biological chemistry.

[2]  A. Sleight,et al.  Identification of 5-hydroxytryptamine7 receptor binding sites in rat hypothalamus: sensitivity to chronic antidepressant treatment. , 1995, Molecular pharmacology.

[3]  C. Burd,et al.  Receptor signalling and the regulation of endocytic membrane transport. , 1996, Current opinion in cell biology.

[4]  M. Castel,et al.  Retrograde axonal transport of neurotensin in the dopaminergic nigrostriatal pathway in the rat , 1990, Neuroscience.

[5]  K. Jakobs,et al.  Deletion analysis of the m4 muscarinic acetylcholine receptor. Molecular determinants for activation of but not coupling to the Gi guanine-nucleotide-binding regulatory protein regulate receptor internalization. , 1994, European journal of biochemistry.

[6]  J. Edwardson,et al.  Intracellular trafficking of the muscarinic acetylcholine receptor: importance of subtype and cell type. , 1996, Molecular pharmacology.

[7]  R. Jensen,et al.  Chronic Desensitization and Down-regulation of the Gastrin-releasing Peptide Receptor Are Mediated by a Protein Kinase C-dependent Mechanism (*) , 1995, The Journal of Biological Chemistry.

[8]  S. Kanba,et al.  Desensitization of muscarinic M1 receptors of murine neuroblastoma cells (clone N1E-115) without receptor down-regulation and protein kinase C activity. , 1990, Biochemical pharmacology.

[9]  K A Overholser,et al.  Rate constants for binding, dissociation, and internalization of EGF: effect of receptor occupancy and ligand concentration. , 1990, Biochemistry.

[10]  M. Caron,et al.  Role of Phosphorylation in Agonist-promoted β2-Adrenergic Receptor Sequestration , 1995, The Journal of Biological Chemistry.

[11]  M. Lohse,et al.  Sequestration and recycling of beta 2-adrenergic receptors permit receptor resensitization. , 1995, Molecular pharmacology.

[12]  O. Bakke,et al.  Targeting of membrane proteins to endosomes and lysosomes. , 1994, Trends in cell biology.

[13]  J. Edwardson,et al.  Kinetic analysis of the trafficking of muscarinic acetylcholine receptors between the plasma membrane and intracellular compartments. , 1994, The Journal of biological chemistry.

[14]  J. Tooze,et al.  Tubular early endosomal networks in AtT20 and other cells , 1991, The Journal of cell biology.

[15]  A. Beaudet,et al.  Thr-422 and Tyr-424 Residues in the Carboxyl Terminus Are Critical for the Internalization of the Rat Neurotensin Receptor (*) , 1995, The Journal of Biological Chemistry.

[16]  B. Aggarwal,et al.  The p60 Tumor Necrosis Factor (TNF) Receptor-associated Kinase (TRAK) Binds Residues 344–397 within the Cytoplasmic Domain Involved in TNF Signaling (*) , 1995, The Journal of Biological Chemistry.

[17]  J. Baumgold,et al.  Relationship between desensitization and sequestration of muscarinic cholinergic receptors in two neuronal cell lines , 1989, Neuropharmacology.

[18]  R. Leduc,et al.  The tyrosine within the NPXnY motif of the human angiotensin II type 1 receptor is involved in mediating signal transduction but is not essential for internalization. , 1996, Molecular pharmacology.

[19]  R. Solari,et al.  Receptor mediated endocytosis and intracellular fate of interleukin 1. , 1994, Biochemical pharmacology.

[20]  M. Caron,et al.  Role of β-Arrestin in Mediating Agonist-Promoted G Protein-Coupled Receptor Internalization , 1996, Science.

[21]  K. Baker,et al.  Stable expression of a truncated AT1A receptor in CHO-K1 cells. The carboxyl-terminal region directs agonist-induced internalization but not receptor signaling or desensitization. , 1995, The Journal of biological chemistry.

[22]  K. Kameyama,et al.  Sequestration of muscarinic acetylcholine receptor m2 subtypes. Facilitation by G protein-coupled receptor kinase (GRK2) and attenuation by a dominant-negative mutant of GRK2. , 1994, The Journal of biological chemistry.

[23]  H. Wiley,et al.  Anomalous binding of epidermal growth factor to A431 cells is due to the effect of high receptor densities and a saturable endocytic system , 1988, The Journal of cell biology.

[24]  T. Haga,et al.  Promoter Region of the Rat m4 Muscarinic Acetylcholine Receptor Gene Contains a Cell Type-specific Silencer Element (*) , 1996, The Journal of Biological Chemistry.

[25]  M. Caron,et al.  Multiple pathways of rapid beta 2-adrenergic receptor desensitization. Delineation with specific inhibitors. , 1990, The Journal of biological chemistry.

[26]  R. Nissenson,et al.  The Cytoplasmic Tail of the G-protein-coupled Receptor for Parathyroid Hormone and Parathyroid Hormone-related Protein Contains Positive and Negative Signals for Endocytosis (*) , 1995, The Journal of Biological Chemistry.

[27]  K. Angelides,et al.  Ligand-stimulated beta 2-adrenergic receptor internalization via the constitutive endocytic pathway into rab5-containing endosomes. , 1995, Journal of cell science.

[28]  J. Benovic,et al.  Desensitization and Internalization of the m2 Muscarinic Acetylcholine Receptor Are Directed by Independent Mechanisms * , 1995, The Journal of Biological Chemistry.

[29]  K. Kameyama,et al.  Phosphorylation of Human m1 Muscarinic Acetylcholine Receptors by G Protein-coupled Receptor Kinase 2 and Protein Kinase C (*) , 1996, The Journal of Biological Chemistry.

[30]  C. Logsdon,et al.  Mutation of carboxyl-terminal threonine residues in human m3 muscarinic acetylcholine receptor modulates the extent of sequestration and desensitization. , 1995, Molecular pharmacology.

[31]  M. Roth,et al.  Phosphatidic acid formation by phospholipase D is required for transport from the endoplasmic reticulum to the Golgi complex , 1997, Current Biology.

[32]  B. Kobilka,et al.  Intracellular targeting and trafficking of thrombin receptors. A novel mechanism for resensitization of a G protein-coupled receptor. , 1994, The Journal of biological chemistry.

[33]  B. Aggarwal,et al.  Protein-tyrosine Phosphatase Inhibitors Block Tumor Necrosis Factor-dependent Activation of the Nuclear Transcription Factor NF-B (*) , 1995, The Journal of Biological Chemistry.

[34]  Hong Yang,et al.  Involvement of MAP Kinase in Angiotensin II-Induced Phosphorylation and Intracellular Targeting of Neuronal AT1 Receptors , 1997, The Journal of Neuroscience.

[35]  D. Linseman,et al.  Agonist‐Induced Endocytosis of Muscarinic Cholinergic Receptors: Relationship to Stimulated Phosphoinositide Turnover , 1997, Journal of neurochemistry.

[36]  R Barber,et al.  Repetitive endocytosis and recycling of the beta 2-adrenergic receptor during agonist-induced steady state redistribution. , 1996, Molecular pharmacology.

[37]  M. Caron,et al.  A highly conserved tyrosine residue in G protein-coupled receptors is required for agonist-mediated beta 2-adrenergic receptor sequestration. , 1994, The Journal of biological chemistry.

[38]  J. Edwardson,et al.  Somatostatin receptors in Neuro2A neuroblastoma cells: ligand internalization , 1997, British journal of pharmacology.

[39]  L. Miller,et al.  Dual pathways of internalization of the cholecystokinin receptor , 1995, The Journal of cell biology.

[40]  A. Tobin,et al.  Identification of a Novel Receptor Kinase That Phosphorylates a Phospholipase C-linked Muscarinic Receptor (*) , 1996, The Journal of Biological Chemistry.

[41]  Howard Riezman,et al.  Ubiquitination of a Yeast Plasma Membrane Receptor Signals Its Ligand-Stimulated Endocytosis , 1996, Cell.

[42]  B. Kobilka,et al.  Antagonist-dependent and -independent steps in the mechanism of adrenergic receptor internalization. , 1994, The Journal of biological chemistry.

[43]  M. Caron,et al.  Phosphorylation sites on two domains of the beta 2-adrenergic receptor are involved in distinct pathways of receptor desensitization. , 1989, The Journal of biological chemistry.

[44]  A. Tobin,et al.  Rapid agonist-mediated phosphorylation of m3-muscarinic receptors revealed by immunoprecipitation. , 1993, The Journal of biological chemistry.

[45]  J. Benovic,et al.  β-Arrestin acts as a clathrin adaptor in endocytosis of the β2-adrenergic receptor , 1996, Nature.

[46]  H. Mori,et al.  Stepwise Movement of Preproteins in the Process of Translocation across the Cytoplasmic Membrane of Escherichia coli(*) , 1995, The Journal of Biological Chemistry.

[47]  M. Caron,et al.  beta-Arrestin: a protein that regulates beta-adrenergic receptor function. , 1990, Science.

[48]  K. Jakobs,et al.  Receptor internalization delays m4 muscarinic acetylcholine receptor resensitization at the plasma membrane. , 1996, Molecular pharmacology.

[49]  S. Ōmura,et al.  Degradation Process of Ligand-stimulated Platelet-derived Growth Factor β -Receptor Involves Ubiquitin-Proteasome Proteolytic Pathway * , 1995, The Journal of Biological Chemistry.

[50]  E. Ikonen,et al.  Functional rafts in cell membranes , 1997, Nature.

[51]  S. A. Ernst,et al.  Muscarinic Receptor Sequestration in SH‐SY5Y Neuroblastoma Cells Is Inhibited when Clathrin Distribution Is Perturbed , 1996, Journal of neurochemistry.

[52]  M. Caron,et al.  The conserved seven-transmembrane sequence NP(X)2,3Y of the G-protein-coupled receptor superfamily regulates multiple properties of the beta 2-adrenergic receptor. , 1995, Biochemistry.

[53]  J. Edwardson,et al.  Routes of delivery of muscarinic acetylcholine receptors to the plasma membrane in NG108‐15 cells , 1994, British journal of pharmacology.

[54]  J. Perkins,et al.  A comparison of catecholamine-induced internalization of beta-adrenergic receptors and receptor-mediated endocytosis of epidermal growth factor in human astrocytoma cells. Inhibition by phenylarsine oxide. , 1985, The Journal of biological chemistry.

[55]  D. Lauffenburger,et al.  Receptors: Models for Binding, Trafficking, and Signaling , 1993 .

[56]  L. Hunyady,et al.  Agonist-induced endocytosis and signal generation in adrenal glomerulosa cells. A potential mechanism for receptor-operated calcium entry. , 1991, The Journal of biological chemistry.

[57]  K. Catt,et al.  Effects of Second Intracellular Loop Mutations on Signal Transduction and Internalization of the Gonadotropin-releasing Hormone Receptor (*) , 1995, The Journal of Biological Chemistry.

[58]  L. Slice,et al.  The conserved NPXnY motif present in the gastrin-releasing peptide receptor is not a general sequestration sequence. , 1994, The Journal of biological chemistry.