Ral and phospholipase D2-dependent pathway for constitutive metabotropic glutamate receptor endocytosis

Journal of Neuroscience

Volumn 24, Issue 40, 2004, Pages 8752-8761

  Bhattacharya, Moshmi ^a   Babwah, Andy V ^a   Godin, Christina ^a   Anborgh, Pieter H ^a   Dale, Lianne B ^a   Poulter, Michael O ^c   Ferguson, Stephen S G ^a,b  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c CARLETON UNIVERSITY   (Canada)

Author keywords

Endocytosis; G protein coupled receptor; Glutamate; Metabotropic glutamate receptor; Phospholipase D; Ral GTP binding protein

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; ANTIPORTER; BETA 2 ADRENERGIC RECEPTOR; BETA ARRESTIN; BUTANOL; G PROTEIN COUPLED RECEPTOR; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR 1A; GLUTAMATE RECEPTOR 5A; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; METABOTROPIC RECEPTOR; PHOSPHATIDIC ACID; PHOSPHATIDYLINOSITIDE; PHOSPHOLIPASE D2; RAL PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; CELL COMMUNICATION AND CELL CONTACT; DOWNSTREAM PROCESSING; EFFECTOR CELL; ENDOCYTOSIS; HUMAN; HUMAN CELL; HYDROLYSIS; INTERNALIZATION; NERVE CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; RECEPTOR BINDING; REGULATORY MECHANISM;

ANIMALS; CELL LINE; CELLS, CULTURED; ENDOCYTOSIS; HUMANS; NEURONS; PHOSPHOLIPASE D; RAL GTP-BINDING PROTEINS; RATS; RECEPTORS, METABOTROPIC GLUTAMATE; SIGNAL TRANSDUCTION;

EID: 5444265165     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3155-04.2004     Document Type: Article

References (46)

1. Arneson LS, Kunz J, Anderson RA, Traub LM (1999) Coupled inositide phosphorylation and phospholipase D activation initiates clathrin-coat assembly on lysosomes. J Biol Chem 274:17794-17805.
2. Bhattacharya M, Anborgh PH, Babwah AV, Dale LB, Dobransky T, Benovic JL, Feldman RD, Verdi JM, Rylett RJ, Ferguson SSG (2002) β-Arrestins regulate a Ral-GDS Ral effector pathway that mediates cytoskeletal reorganization. Nat Cell Biol 4:547-555.
3. Bhowmick N, Narayan P, Puett D (1998) The endothelin subtype A receptor undergoes agonist- and antagonist-mediated internalization in the absence of signaling. Endocrinology 139:3185-3192.
4. Cao TT, Mays RW, von Zastrow M (1998) Regulated endocytosis of G-protein-coupled receptors by a biochemically and functionally distinct subpopulation of clathrin-coated pits. J Biol Chem 273:24592-24602.
5. Carroll RC, Zukin RS (2002) NMDA-receptor trafficking and targeting: implications for synaptic transmission and plasticity. Trends Neurosci 25:571-577.
6. Chavrier P, Goud B (1999) The role of ARF and Rab GTPases in membrane transport. Curr Opin Cell Biol 11:466-475.
7. 2-adrenergic receptor endocytosis. J Biol Chem 276:42509-42513.
8. Craven SE, El-Husseini AE, Bredt DS (1999) Synaptic targeting of the postsynaptic density protein PSD-95 mediated by lipid and protein motifs. Neuron 22:497-509.
9. Dale LB, Bhattacharya M, Anborgh PH, Murdoch B, Bhatia M, Nakanishi S, Ferguson SSG (2000) G protein-coupled receptor kinase mediated desensitization of metabotropic glutamate receptor 1α protects against cell death. J Biol Chem 275:38213-38220.
10. Dale LB, Bhattacharya M, Seachrist JL, Anborgh PH, Ferguson SSG (2001) Agonist-stimulated and tonic internalization of metabotropic glutamate receptor 1α in human embryonic kidney 293 cells: agonist-stimulated endocytosis is β-arrestin 1 isoform-specific. Mol Pharmacol 60:1243-1253.
11. Dale LB, Babwah AV, Ferguson SSG (2002) Mechanisms of metabotropic glutamate receptor desensitization: role in the patterning of effector enzyme activation. Neurochem Int 41:319-326.
12. Dale LB, Seachrist JL, Babwah AV, Ferguson SSG (2004) Regulation of angiotensin II 1A receptor intracellular retention, degradation and recycling by Rab5, Rab7 and Rab11 GTPases. J Biol Chem 279:13110-13118.
13. De Camilli P, Emr SD, McPherson PS, Novick P (1996) Phosphoinositides as regulators in membrane traffic. Science 271:1533-1539.
14. Du G, Huang P, Liang BT, Frohman MA (2004) Phospholipase D2 localizes to the plasma membrane and regulates angiotensin II receptor endocytosis. Mol Biol Cell 15:1024-1030.
15. Feig LA (2003) Ral-GTPases: approaching their 15 minutes of fame. Trends Cell Biol 13:419-425.
16. Ferguson SSG (2001) Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling. Pharmacol Rev 53:1-24.
17. Ferguson SSG, Downey 3rd WE, Colapietro AM, Barak LS, Menard L, Caron MG (1996) Role of β-arrestin in mediating agonist-promoted G protein-coupled receptor internalization. Science 271:363-366.
18. Fourgeaud L, Bessis AS, Rossignol F, Pin JP, Olivo-Marin JC, Hemar A (2003) The metabotropic glutamate receptor mGluR5 is endocytosed by a clathrin-independent pathway. J Biol Chem 278:12222-12230.
19. 2-adrenergic receptor. Nature 383:447-450.
20. Hanson JE, Smith Y (1999) Class I metabotropic glutamate receptors at GABAergic synapses in monkeys. J Neurosci 19:6488-6496.
21. Jullien-Flores V, Mahe Y, Mirey G, Leprince C, Meunier-Bisceuil B, Sorkin A, Camonis JH (2000) RLIP76, an effector of the GTPase Ral, interacts with the AP2 complex: involvement of the Ral pathway in receptor endocytosis. J Cell Sci 113:2837-2844.
22. Kim JH, Lee SD, Han JM, Lee TG, Kim Y, Park JB, Lambeth JD, Suh PG, Ryu SH (1998) Activation of phospholipase D1 by direct interaction with ADP-ribosylation factor 1 and RalA. FEBS Lett 430:231-235.
23. Koch T, Brandenburg LO, Schulz S, Liang Y, Klein J, Hollt V (2003) ADP-ribosylation factor-dependent phospholipase D2 activation is required for agonist-induced μ-opioid receptor endocytosis. J Biol Chem 278:9979-9985.
24. Koch T, Brandenburg LO, Liang Y, Schulz S, Beyer A, Schroder H, Hollt V (2004) Phospholipase D2 modulates agonist-induced μ-opioid receptor desensitization and resensitization. J Neurochem 88:680-688.
25. 2-adrenergic receptor/βarrestin complex recruits the clathrin adaptor AP-2 during endocytosis. Proc Natl Acad Sci USA 96:3712-3717.
26. Liscovitch M, Cantley LC (1995) Signal transduction and membrane traffic: the PITP/phosphoinositide connection. Cell 81:659-662.
27. Luo JQ, Liu X, Frankel P, Rotunda T, Ramos M, Flom J, Jiang H, Feig LA, Morris AJ, Kahn RA, Foster DA (1998) Functional association between Arf and RalA in active phospholipase D complex. Proc Natl Acad Sci USA 95:3632-3637.
28. Man HY, Lin JW, Ju WH, Ahmadian G, Liu L, Becker LE, Sheng M, Wang YT (2000) Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization. Neuron 25:649-662.
29. Matsuzaki T, Hanai S, Kishi H, Liu Z, Bao Y, Kikuchi A, Tsuchida K, Sugino H (2002) Regulation of endocytosis of activin type II receptors by a novel PDZ protein through Ral/Ral-binding protein 1-dependent pathway. J Biol Chem 277:19008-19018.
30. Minami I, Kengaku M, Smitt PS, Shigemoto R, Hirano T (2003) Long-term potentiation of mGluR1 activity by depolarization-induced Homerla in mouse cerebellar Purkinje neurons. Eur J Neurosci 17:1023-1032.
31. Morris AJ, Frohman MA, Engebrecht J (1997) Measurement of phospholipase D activity. Anal Biochem 252:1-9.
32. Nakanishi S (1994) Metabotropic glutamate receptors: synaptic transmission, modulation, and plasticity. Neuron 13:1031-1037.
33. Nakashima S, Morinaka K, Koyama S, Ikeda M, Kishida M, Okawa K, Iwamatsu A, Kishida S, Kikuchi A (1999) Small G protein Ral and its downstream molecules regulate endocytosis of EGF and insulin receptors. EMBO J 18:3629-3642.
34. Paing MM, Stutts AB, Kohout TA, Lefkowitz RJ, Trejo J (2002) β-Arrestins regulate protease-activated receptor-1 desensitization but not internalization or down-regulation. J Biol Chem 277:1292-1300.
35. Pellegrini-Giampietro DE, Torregrossa SA, Moroni F (1996) Pharmacological characterization of metabotropic glutamate receptors coupled to phospholipase D in the rat hippocampus. Br J Pharmacol 118:1035-1043.
36. Premont RT, Inglese J, Lefkowitz RJ (1995) Protein kinases that phosphorylate activated G protein-coupled receptors. FASEB J 9:175-182.
37. Pula G, Mundell SJ, Roberts PJ, Kelly E (2004) Agonist-independent internalization of metabotropic glutamate receptor 1a is arrestin- and clathrin-dependent and suppressed by receptor inverse agonists. J Neurochem 89:1009-1020.
38. Roettger BF, Ghanekar D, Rao R, Toledo C, Yingling J, Pinon D, Miller LJ (1997) Antagonist-stimulated internalization of the G protein-coupled cholecystokinin receptor. Mol Pharmacol 51:357-362.
39. Roseberry AG, Hosey MM (1999) Trafficking of M(2) muscarinic acetylcholine receptors. J Biol Chem 274:33671-33676.
40. Sallese M, Salvatore L, D'Urbano E, Sala G, Storto M, Launey T, Nicoletti F, Knopfel T, De Blasi A (2000) The G-protein-coupled receptor kinase GRK4 mediates homologous desensitization of metabotropic glutamate receptor 1. FASEB J 14:2569-2580.
41. Servitja JM, Masgrau R, Pardo R, Sarri E, von Eichel-Streiber C, Gutkind JS, Picatoste F (2003) Metabotropic glutamate receptors activate phospholipase D in astrocytes through a protein kinase C-dependent and Rho-independent pathway. Neuropharmacology 44:171-180.
42. Shapiro MJ, Trejo J, Zeng D, Coughlin SR (1996) Role of the thrombin receptor's cytoplasmic tail in intracellular trafficking. Distinct determinants for agonist-triggered versus tonic internalization and intracellular localization. J Biol Chem 271:32874-32880.
43. Shen Y, Xu L, Foster DA (2001) Role for phospholipase D in receptor-mediated endocytosis. Mol Cell Biol 21:595-602.
44. Shinomura T, del Rio E, Breen KC, Downes CP, McLaughlin M (2000) Activation of phospholipase D by metabotropic glutamate receptor agonists in rat cerebrocortical synaptosomes. Br J Pharmacol 131:1011-1018.
45. Slaaby R, Jensen T, Hansen HS, Frohman MA, Seedorf K (1998) PLD2 complexes with the EGF receptor and undergoes tyrosine phosphorylation at a single site upon agonist stimulation. J Biol Chem 273:33722-33727.
46. Tarasova NI, Stauber RH, Choi JK, Hudson EA, Czerwinski G, Miller JL, Pavlakis GN, Michejda CJ, Wank SA (1997) Visualization of G protein-coupled receptor trafficking with the aid of the green fluorescent protein. Endocytosis and recycling of cholecystokinin receptor type A. J Biol Chem 272:14817-14824.