Rab11a and myosin Vb regulate recycling of the M4 muscarinic acetylcholine receptor

Journal of Neuroscience

Volumn 22, Issue 22, 2002, Pages 9776-9784

  Volpicelli, Laura A ^a   Lah, James J ^a   Fang, Guofu ^a   Goldenring, James R ^b   Levey, Allan I ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Endocytosis; Endosomes; G protein coupled receptor; Internalization; Muscarinic acetylcholine receptors; Myosin Vb; PC12 cells; Rab11a; Recycling; Transferrin receptor; Unconventional myosins

Indexed keywords

G PROTEIN COUPLED RECEPTOR; LIGAND; MUSCARINIC M4 RECEPTOR; MYOSIN V; MYOSIN VB; RAB PROTEIN; RAB11A PROTEIN; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; BRAIN; CELL CULTURE; CELL STRAIN; CELL SURFACE; CENTRAL NERVOUS SYSTEM; CHOLINERGIC STIMULATION; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; INTRACELLULAR TRANSPORT; LOCOMOTION; MENTAL DISEASE; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RAT;

EID: 0037112197     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-22-09776.2002     Document Type: Article

References (56)

1. Anborgh PH, Seachrist JL, Dale LB, Ferguson SS (2000) Receptor/beta-arrestin complex formation and the differential trafficking and resensitization of beta2-adrenergic and angiotensin II type 1A receptors. Mol Endocrinol 14:2040-2053.
2. Berkeley JL, Levey AI (2000) Muscarinic activation of mitogen-activated protein kinase in PC12 cells. J Neurochem 75:487-493.
3. Bernard V, Levey AI, Bloch B (1999) Regulation of the subcellular distribution of m4 muscarinic acetylcholine receptors in striatal neurons in vivo by the cholinergic environment: Evidence for regulation of cell surface receptors by endogenous and exogenous stimulation. J Neurosci 19:10237-10249.
4. Bloch B, Dumartin B, Bernard V (1999) In vivo regulation of intraneuronal trafficking of G protein-coupled receptors for neurotransmitters. Trends Pharmacol Sci 20:315-319.
5. Bodick NC, Offen WW, Levey AI, Cutler NR, Gauthier SG, Satlin A, Shannon HE, Tollefson GD, Rasmussen K, Bymaster FP, Hurley DJ, Potter WZ, Paul SM (1997) Effects of xanomeline, a selective muscarinic receptor agonist, on cognitive function and behavioral symptoms in Alzheimer disease. Arch Neurol 54:465-473.
6. Bogatkewitsch GS, Lenz W, Jakobs KH, Van Koppen CJ (1996) Receptor internalization delays m4 muscarinic acetylcholine receptor resensitization at the plasma membrane. Mol Pharmacol 50:424-429.
7. Cao TT, Deacon HW, Reczek D, Bretscher A, von Zastrow M (1999) A kinase-regulated PDZ-domain interaction controls endocytic sorting of the beta2-adrenergic receptor. Nature 401:286-290.
8. Carroll RC, Beattie EC, von Zastrow M, Malenka RC (2001) Role of AMPA receptor endocytosis in synaptic plasticity. Nat Rev Neurosci 2:315-324.
9. Casanova JE, Wang X, Kumar R, Bhartur SG, Navarre J, Woodrum JE, Altschuler Y, Ray GS, Goldenring JR (1999) Association of Rab25 and Rab11a with the apical recycling system of polarized Madin-Darby canine kidney cells. Mol Biol Cell 10:47-61.
10. Chavrier P, Parton RG, Hauri HP, Simons K, Zerial M (1990) Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 62:317-329.
11. Felder CC, Porter AC, Skillman TL, Zhang L, Bymaster FP, Nathanson NM, Hamilton SE, Gomeza J, Wess J, McKinzie DL (2001) Elucidating the role of muscarinic receptors in psychosis. Life Sci 68:2605-2613.
12. Feng Y, Press B, Wandinger-Ness A (1995) Rab 7: An important regulator of late endocytic membrane traffic. J Cell Biol 131:1435-1452.
13. Finn AK, Whistler JL (2001) Endocytosis of the mu opioid receptor reduces tolerance and a cellular hallmark of opiate withdrawal. Neuron 32:829-839.
14. Ghosh RN, Gelman DL, Maxfield FR (1994) Quantification of low density lipoprotein and transferrin endocytic sorting HEp2 cells using confocal microscopy. J Cell Sci 107:2177-2189.
15. Gomeza J, Zhang L, Kostenis E, Felder C, Bymaster F, Brodkin J, Shannon H, Xia B, Deng C, Wess J (1999) Enhancement of D1 dopamine receptor-mediated locomotor stimulation in M(4) muscarinic acetylcholine receptor knockout mice. Proc Natl Acad Sci USA 96:10483-10488.
16. Green EG, Ramm E, Riley NM, Spiro DJ, Goldenring JR, Wessling-Resnick M (1997) Rab11 is associated with transferrin-containing recycling compartments in K562 cells. Biochem Biophys Res Commun 239:612-616.
17. Hales CM, Griner R, Hobdy-Henderson KC, Dorn MC, Hardy D, Kumar R, Navarre J, Chan EK, Lapierre LA, Goldenring JR (2001) Identification and characterization of a family of Rab11-interacting proteins. J Biol Chem 276:39067-39075.
18. He L, Fong J, von Zastrow M, Whistler JL (2002) Regulation of opioid receptor trafficking and morphine tolerance by receptor oligomerization. Cell 108:271-282.
19. 4 muscarinic receptor proteins in the rat striatum: Light and electron microscopic immunocytochemistry using subtype-specific antibodies. J Neurosci 14:3351-3363.
20. Hopkins CR, Trowbridge IS (1983) Internalization and processing of transferrin and the transferrin receptor in human carcinoma A431 cells. J Cell Biol 97:508-521.
21. Hopkins CR, Gibson A, Shipman M, Miller K (1990) Movement of internalized ligand-receptor complexes along a continuous endosomal reticulum. Nature 346:335-339.
22. Hopkins CR, Gibson A, Shipman M, Strickland DK, Trowbridge IS (1994) In migrating fibroblasts, recycling receptors are concentrated in narrow tubules in the pericentriolar area, and then routed to the plasma membrane of the leading lamella. J Cell Biol 125:1265-1274.
23. Hunyady L, Baukal AJ, Gaborik Z, Olivares-Reyes JA, Bor M, Szaszak M, Lodge R, Catt KJ, Balla T (2002) Differential PI 3-kinase dependence of early and late phases of recycling of the internalized AT1 angiotensin receptor. J Cell Biol 157:1211-1222.
24. Innamorati G, Le Gouill C, Balamotis M, Birnbaumer M (2001) The long and the short cycle. Alternative intracellular routes for trafficking of G-protein-coupled receptors. J Biol Chem 276:13096-13103.
25. Koenig JA, Edwardson JM (1997) Endocytosis and recycling of G protein-coupled receptors. Trends Pharmacol Sci 18:276-287.
26. Kreuzer OJ, Krisch B, Dery O, Bunnett NW, Meyerhof W (2001) Agonist-mediated endocytosis of rat somatostatin receptor subtype 3 involves beta-arrestin and clathrin coated vesicles. J Neuroendocrinol 13:279-287.
27. Krudewig R, Langer B, Vogler O, Markschies N, Erl M, Jakobs KH, van Koppen CJ (2000) Distinct internalization of M2 muscarinic acetylcholine receptors confers selective and long-lasting desensitization of signaling to phospholipase C. J Neurochem 74:1721-1730.
28. Lapierre LA, Kumar R, Hales CM, Navarre J, Bhartur SG, Burnette JO, Provance Jr DW, Mercer JA, Bahler M, Goldenring JR (2001) Myosin vb is associated with plasma membrane recycling systems. Mol Biol Cell 12:1843-1857.
29. Lefkowitz RJ (1998) G protein-coupled receptors. III. New roles for receptor kinases and beta-arrestins in receptor signaling and desensitization. J Biol Chem 273:18677-18680.
30. Levey AI, Kitt CA, Simonds WF, Price DL, Brann MR (1991) Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies. J Neurosci 11:3218-3226.
31. Mellman I (1996) Endocytosis and molecular sorting. Annu Rev Cell Dev Biol 12:575-625.
32. Moore RH, Tuffaha A, Millman EE, Dai W, Hall HS, Dickey BF, Knoll BJ (1999) Agonist-induced sorting of human beta2-adrenergic receptors to lysosomes during downregulation. J Cell Sci 112:329-338.
33. Muriel MP, Bernard V, Levey AI, Laribi O, Abrous DN, Agid Y, Bloch B, Hirsch EC (1999) Levodopa induces a cytoplasmic localization of D1 dopamine receptors in striatal neurons in Parkinson's disease. Ann Neurol 46:103-111.
34. Prekeris R, Klumperman J, Scheller RH (2000) A Rab11/Rip11 protein complex regulates apical membrane trafficking via recycling endo: Somes. Mol Cell 6:1437-1448.
35. Prekeris R, Davies JM, Scheller RH (2001) Identification of a novel Rab11/25 binding domain present in Eferin and Rip proteins. J Biol Chem 276:38966-38970.
36. Ren M, Xu G, Zeng J, De Lemos-Chiarandini C, Adesnik M, Sabatini DD (1998) Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. Proc Natl Acad Sci USA 95:6187-6192.
37. Roche KW, Standley S, McCallum J, Dune Ly C, Ehlers MD, Wenthold RJ (2001) Molecular determinants of NMDA receptor internalization. Nat Neurosci 4:794-802.
38. Rubino M, Miaczynska M, Lippe R, Zerial M (2000) Selective membrane recruitment of EEA1 suggests a role in directional transport of clathrin-coated vesicles to early endosomes. J Biol Chem 275:3745-3748.
39. Seachrist JL, Anborgh PH, Ferguson SS (2000) beta 2-adrenergic receptor internalization, endosomal sorting, and plasma membrane recycling are regulated by rab GTPases. J Biol Chem 275:27221-27228.
40. Sheehan D, Ray GS, Calhoun BC, Goldenring JR (1996) A somatodendritic distribution of Rab11 in rabbit brain neurons. Neuro Report 7:1297-1300.
41. Sonnichsen B, De Renzis S, Nielsen E, Rietdorf J, Zerial M (2000) Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J Cell Biol 149:901-914.
42. St. John PA, Gordon H (2001) Agonists cause endocytosis of nicotinic acetylcholine receptors on cultured myotubes. J Neurobiol 49:212-223.
43. Szekeres PG, Koenig JA, Edwardson JM (1998) Involvement of receptor cycling and receptor reserve in resensitization of muscarinic responses in SH-SY5Y human neuroblastoma cells. J Neurochem 70:1694-1703.
44. Tolbert LM, Lameh J (1996) Human muscarinic cholinergic receptor Hm1 internalizes via clathrin-coated vesicles. J Biol Chem 271:17335-17342.
45. Trejo J, Coughlin SR (1999) The cytoplasmic tails of protease-activated receptor-1 and substance P receptor specify sorting to lysosomes versus recycling. J Biol Chem 274:2216-2224.
46. Tsao PI, von Zastrow M (2000) Type-specific sorting of G protein-coupled receptors after endocytosis. J Biol Chem 275:11130-11140.
47. Ullrich O, Horiuchi H, Bucci C, Zerial M (1994) Membrane association of Rab5 mediated by GDP-dissociation inhibitor and accompanied by GDP/GTP exchange. Nature 368:157-160.
48. Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG (1996) Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol 135:913-924.
49. van der Sluijs P, Hull M, Webster P, Male P, Goud B, Mellman I (1992) The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway. Cell 70:729-740.
50. Volpicelli LA, Lah JJ, Levey AI (2001) Rab5-dependent trafficking of the m4 muscarinic acetylcholine receptor to the plasma membrane, early endosomes, and multivesicular bodies. J Biol Chem 276:47590-47598.
51. von Zastrow M, Kobilka BK (1992) Ligand-regulated internalization and recycling of human beta 2-adrenergic receptors between the plasma membrane and endosomes containing transferrin receptors. J Biol Chem 267:3530-3538.
52. Wang H, Han H, Zhang L, Shi H, Schram G, Nattel S, Wang Z (2001) Expression of multiple subtypes of muscarinic receptors and cellular distribution in the human heart. Mol Pharmacol 59:1029-1036.
53. Whistler JL, Chuang HH, Chu P, Jan LY, von Zastrow M (1999) Functional dissociation of mu opioid receptor signaling and endocytosis: Implications for the biology of opiate tolerance and addiction. Neuron 23:737-746.
54. Yamashiro DJ, Tycko B, Fluss SR, Maxfield FR (1984) Segregation of transferrin to a mildly acidic (pH 6.5) para-Golgi compartment in the recycling pathway. Cell 37:789-800.
55. Zhang W, Basile AS, Gomeza J, Volpicelli LA, Levey AI, Wess J (2002) Characterization of central inhibitory muscarinic autoreceptors by the use of muscarinic acetylcholine receptor knock-out mice. J Neurosci 22:1709-1717.
56. Zhao LP, Koslovsky JS, Reinhard J, Bahler M, Witt AE, Provance Jr DW, Mercer JA (1996) Cloning and characterization of myr 6, an unconventional myosin of the dilute/myosin-V family. Proc Natl Acad Sci USA 93:10826-10831.