Identification of two functionally distinct endosomal recycling pathways for dopamine D 2 receptor

Journal of Neuroscience

Volumn 32, Issue 21, 2012, Pages 7178-7190

  Li, Yun ^a   Roy, Brittany D ^a   Wang, Wei ^a   Zhang, Li ^b   Zhang, Lifeng ^a   Sampson, Stephen B ^a   Yang, Yupeng ^b   Lin, Da Ting ^a  

^a JACKSON LABORATORY   (United States)

^b University of Science and Technology of China   (China)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; CYCLIC AMP; DOPAMINE 2 RECEPTOR; RAB PROTEIN; RAB11 PROTEIN;

ANIMAL CELL; ARTICLE; BLEACHING; CELL MEMBRANE; CONTROLLED STUDY; DENDRITIC CELL; EMBRYO; ENDOSOME; FLUORESCENCE MICROSCOPY; GENE INSERTION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOMATIC CELL; STIMULATION;

ANIMALS; BICUCULLINE; CELLS, CULTURED; CEREBRAL CORTEX; COCULTURE TECHNIQUES; CORPUS STRIATUM; CYCLIC AMP; DOPAMINE; ENDOCYTOSIS; ENDOSOMES; HEK293 CELLS; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR IMAGING; NEURONS; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RECEPTORS, DOPAMINE D2;

EID: 84861302949     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0008-12.2012     Document Type: Article

References (59)

1. Bartlett SE, Enquist J, Hopf FW, Lee JH, Gladher F, Kharazia V, Waldhoer M, Mailliard WS, Armstrong R, Bonci A, Whistler JL (2005) Dopamine responsiveness is regulated by targeted sorting of D2 receptors. Proc Natl Acad Sci U S A 102:11521-11526.
2. Binda AV, Kabbani N, Lin R, Levenson R (2002) D2 and D3 dopamine receptor cell surface localization mediated by interaction with protein 4.1N. Mol Pharmacol 62:507-513.
3. Blum K, Sheridan PJ, Wood RC, Braverman ER, Chen TJ, Cull JG, Comings DE (1996) The D2 dopamine receptor gene as a determinant of reward deficiency syndrome. J R Soc Med 89:396-400.
4. Bunzow JR, Van Tol HH, Grandy DK, Albert P, Salon J, Christie M, Machida CA, Neve KA, Civelli O (1988) Cloning and expression of a rat D2 dopamine receptor cDNA. Nature 336:783-787.
5. Carlsson A (1988) The current status of the dopamine hypothesis of schizophrenia. Neuropsychopharmacology 1:179-186.
6. Celver J, Sharma M, Kovoor A (2010) RGS9-2 mediates specific inhibition of agonist-induced internalization of D2-dopamine receptors. J Neurochem 114:739-749.
7. Edelstein A, Amodaj N, Hoover K, Vale R, Stuurman N (2010) Computer control of microscopes using microManager. Current protocols in molecular biology, pp 14.20.1-14.20.17. Wiley Online Library.
8. Fetsko LA, Xu R, Wang Y (2003) Alterations in D1/D2 synergism may account for enhanced stereotypy and reduced climbing in mice lacking dopamine D2L receptor. Brain Res 967:191-200.
9. Free RB, Hazelwood LA, Cabrera DM, Spalding HN, Namkung Y, Rankin ML, Sibley DR (2007) D1 and D2 dopamine receptor expression is regulated by direct interaction with the chaperone protein calnexin. J Biol Chem 282:21285-21300.
10. Genedani S, Guidolin D, Leo G, Filaferro M, Torvinen M, Woods AS, Fuxe K, Ferré S, Agnati LF (2005) Computer-assisted image analysis of caveolin-1 involvement in the internalization process of adenosine A2Adopamine D2 receptor heterodimers. J Mol Neurosci 26:177-184.
11. Genedani S, Carone C, Guidolin D, Filaferro M, Marcellino D, Fuxe K, Agnati LF (2010) Differential sensitivity of A2A and especially D2 receptor trafficking to cocaine compared with lipid rafts in cotransfected CHO cell lines. Novel actions of cocaine independent of the DA transporter. J Mol Neurosci 41:347-357.
12. Holmes A, Lachowicz JE, Sibley DR (2004) Phenotypic analysis of dopamine receptor knockout mice; recent insights into the functional specificity of dopamine receptor subtypes. Neuropharmacology 47:1117-1134.
13. Iizuka Y, Sei Y, Weinberger DR, Straub RE (2007) Evidence that the BLOC-1 protein dysbindin modulates dopamine D2 receptor internalization and signaling but not D1 internalization. J Neurosci 27:12390-12395.
14. Jeanneteau F, Diaz J, Sokoloff P, Griffon N (2004) Interactions of GIPC with dopamine D2, D3 but not D4 receptors define a novel mode of regulation of G protein-coupled receptors. Mol Biol Cell 15:696-705.
15. Ji Y, Yang F, Papaleo F, Wang HX, Gao WJ, Weinberger DR, Lu B (2009) Role of dysbindin in dopamine receptor trafficking and cortical GABA function. Proc Natl Acad Sci U S A 106:19593-19598.
16. Kabbani N, Jeromin A, Levenson R (2004) Dynamin-2 associates with the dopamine receptor signalplex and regulates internalization of activated D2 receptors. Cell Signal 16:497-503.
17. Karam CS, Ballon JS, Bivens NM, Freyberg Z, Girgis RR, Lizardi-Ortiz JE, Markx S, Lieberman JA, Javitch JA (2010) Signaling pathways in schizophrenia: emerging targets and therapeutic strategies. Trends Pharmacol Sci 31:381-390.
18. Kenny PJ (2011) Reward mechanisms in obesity: new insights and future directions. Neuron 69:664-679.
19. Khan ZU, Mrzljak L, Gutierrez A, de la Calle A, Goldman-Rakic PS (1998) Prominence of the dopamine D2 short isoform in dopaminergic pathways. Proc Natl Acad Sci U S A 95:7731-7736.
20. Kim JH, Cho EY, Min C, Park JH, Kim KM (2008a) Characterization of functional roles of DRY motif in the 2nd intracellular loop of dopamine D2 and D3 receptors. Arch Pharm Res 31:474-481.
21. Kim KM, Valenzano KJ, Robinson SR, Yao WD, Barak LS, Caron MG (2001) Differential regulation of the dopamine D2 and D3 receptors by G protein-coupled receptor kinases and beta-arrestins. J Biol Chem 276:37409-37414.
22. Kim OJ (2008) Asingle mutation at lysine 241 alters expression and trafficking of the D2 dopamine receptor. J Recept Signal Transduct Res 28:453-464.
23. Kim OJ, Ariano MA, Namkung Y, Marinec P, Kim E, Han J, Sibley DR (2008b) D2 dopamine receptor expression and trafficking is regulated through direct interactions with ZIP. J Neurochem 106:83-95.
24. Lan H, Liu Y, Bell MI, Gurevich VV, Neve KA (2009) A dopamine D2 receptor mutant capable of G protein-mediated signaling but deficient in arrestin binding. Mol Pharmacol 75:113-123.
25. Lawford BR, Young R, Noble EP, Kann B, Ritchie T (2006) The D2 dopamine receptor (DRD2) gene is associated with co-morbid depression, anxiety and social dysfunction in untreated veterans with post-traumatic stress disorder. Eur Psychiatry 21:180-185.
26. Lin DT, Huganir RL (2007) PICK1 and phosphorylation of the glutamate receptor 2 (GluR2) AMPA receptor subunit regulates GluR2 recycling after NMDA receptor-induced internalization. J Neurosci 27:13903-13908.
27. Lin DT, Makino Y, Sharma K, Hayashi T, Neve R, Takamiya K, Huganir RL (2009) Regulation of AMPA receptor extrasynaptic insertion by 4.1N, phosphorylation and palmitoylation. Nat Neurosci 12:879-887.
28. Lin R, Karpa K, Kabbani N, Goldman-Rakic P, Levenson R (2001) Dopamine D2 and D3 receptors are linked to the actin cytoskeleton via interaction with filamin A. Proc Natl Acad Sci U S A 98:5258-5263.
29. Lin R, Canfield V, Levenson R (2002) Dominant negative mutants of filamin A block cell surface expression of the D2 dopamine receptor. Pharmacology 66:173-181.
30. Lindgren N, Usiello A, Goiny M, Haycock J, Erbs E, Greengard P, Hokfelt T, Borrelli E, Fisone G (2003) Distinct roles of dopamine D2L and D2S receptor isoforms in the regulation of protein phosphorylation at presynaptic and postsynaptic sites. Proc Natl Acad Sci U S A 100:4305-4309.
31. Luscher B, Fuchs T, Kilpatrick CL (2011) GABAA receptor traffickingmediated plasticity of inhibitory synapses. Neuron 70:385-409.
32. Macey TA, Gurevich VV, Neve KA (2004) Preferential Interaction between the dopamine D2 receptor and Arrestin2 in neostriatal neurons. Mol Pharmacol 66:1635-1642.
33. Mack KJ, O'Malley KL, Todd RD (1991) Differential expression of dopaminergic D2 receptor messenger RNAs during development. Brain Res Dev Brain Res 59:249-251.
34. Marley A, von Zastrow M (2010) Dysbindin promotes the post-endocytic sorting of G protein-coupled receptors to lysosomes. PLoS One 5:e9325.
35. Matsuda T, Cepko CL (2007) Controlled expression of transgenes introduced by in vivo electroporation. Proc Natl Acad Sci U S A 104:1027-1032.
36. Miesenböck G, De Angelis DA, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394:192-195.
37. Missale C, Nash SR, Robinson SW, Jaber M, Caron MG (1998) Dopamine receptors: from structure to function. Physiol Rev 78:189-225.
38. Namkung Y, Sibley DR (2004) Protein kinase C mediates phosphorylation, desensitization, and trafficking of the D2 dopamine receptor. J Biol Chem 279:49533-49541.
39. Namkung Y, Dipace C, Javitch JA, Sibley DR (2009) G protein-coupled receptor kinase-mediated phosphorylation regulates post-endocytic trafficking of the D2 dopamine receptor. J Biol Chem 284:15038-15051.
40. Neve KA, Neve RL, Fidel S, Janowsky A, Higgins GA (1991) Increased abundance of alternatively spliced forms of D2 dopamine receptormRNAafter denervation. Proc Natl Acad Sci U S A 88:2802-2806.
41. Park M, Penick EC, Edwards JG, Kauer JA, Ehlers MD (2004) Recycling endosomes supply AMPA receptors for LTP. Science 305:1972-1975.
42. Park SK, Nguyen MD, Fischer A, Luke MP, Affarel B, Dieffenbach PB, Tseng HC, Shi Y, Tsai LH (2005) Par-4 links dopamine signaling and depression. Cell 122:275-287.
43. Paspalas CD, Rakic P, Goldman-Rakic PS (2006) Internalization of D2 dopamine receptors is clathrin-dependent and select to dendro-axonic appositions in primate prefrontal cortex. Eur J Neurosci 24:1395-1403.
44. Rouge-Pont F, Usiello A, Benoit-Marand M, Gonon F, Piazza PV, Borrelli E (2002) Changes in extracellular dopamine induced by morphine and cocaine: crucial control by D2 receptors. J Neurosci 22:3293-3301.
45. Shepherd JD, Huganir RL (2007) The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu Rev Cell Dev Biol 23:613-643.
46. Shimokawa N, Haglund K, Hölter SM, Grabbe C, Kirkin V, Koibuchi N, Schultz C, Rozman J, Hoeller D, Qiu CH, Londoño MB, Ikezawa J, Jedlicka P, Stein B, Schwarzacher SW, Wolfer DP, Ehrhardt N, Heuchel R, Nezis I, Brech A, et al. (2010) CIN85 regulates dopamine receptor endocytosis and governs behaviour in mice. EMBO J 29:2421-2432.
47. Stenmark H (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10:513-525.
48. Sugiura H, Iwata K, Matsuoka M, Hayashi H, Takemiya T, Yasuda S, Ichikawa M, Yamauchi T, Mehlen P, Haga T, Yamagata K (2004) Inhibitory role of endophilin 3 in receptor-mediated endocytosis. J Biol Chem 279:23343-23348.
49. Sun X, Milovanovic M, Zhao Y, Wolf ME (2008) Acute and chronic dopamine receptor stimulation modulates AMPA receptor trafficking in nucleus accumbens neurons cocultured with prefrontal cortex neurons. J Neurosci 28:4216-4230.
50. Tirotta E, Fontaine V, Picetti R, Lombardi M, Samad TA, Oulad-Abdelghani M, Edwards R, Borrelli E (2008) Signaling by dopamine regulates D2 receptors trafficking at the membrane. Cell Cycle 7:2241-2248.
51. Torvinen M, Torri C, Tombesi A, Marcellino D, Watson S, Lluis C, Franco R, Fuxe K, Agnati LF (2005) Trafficking of adenosine A2A and dopamine D2 receptors. J Mol Neurosci 25:191-200.
52. Usiello A, Baik JH, Rougé-Pont F, Picetti R, Dierich A, LeMeur M, Piazza PV, Borrelli E (2000) Distinct functions of the two isoforms of dopamine D2 receptors. Nature 408:199-203.
53. Vickery RG, von Zastrow M (1999) Distinct dynamin-dependent and -independent mechanisms target structurally homologous dopamine receptors to different endocytic membranes. J Cell Biol 144:31-43.
54. Volkow ND, Fowler JS, Wang GJ, Baler R, Telang F (2009) Imaging dopamine's role in drug abuse and addiction. Neuropharmacology 56 [Suppl 1]:3-8.
55. Wang GJ, Volkow ND, Fowler JS (2002) The role of dopamine in motivation for food in humans: implications for obesity. Expert Opin Ther Targets 6:601-609.
56. Wise RA (2008) Dopamine and reward: the anhedonia hypothesis 30 years on. Neurotoxicity research 14:169-183.
57. Xiao MF, Xu JC, Tereshchenko Y, Novak D, Schachner M, Kleene R (2009) Neural cell adhesion molecule modulates dopaminergic signaling and behavior by regulating dopamine D2 receptor internalization. J Neurosci 29:14752-14763.
58. Xu R, Hranilovic D, Fetsko LA, Bucan M, Wang Y (2002) Dopamine D2S and D2L receptors may differentially contribute to the actions of antipsychotic and psychotic agents in mice. Mol Psychiatry 7:1075-1082.
59. Yudowski GA, Puthenveedu MA, von Zastrow M (2006) Distinct modes of regulated receptor insertion to the somatodendritic plasma membrane. Nat Neurosci 9:622-627.