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G Protein-Coupled Receptor Kinases pp 237–269Cite as

Regulation of Dopamine-Dependent Behaviors by G Protein-Coupled Receptor Kinases

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Part of the book series: Methods in Pharmacology and Toxicology ((MIPT))

Abstract

Neurotransmitter dopamine exerts its effects via five subtypes of dopamine receptors, D1 through D5, all of which belong to the superfamily of G protein-coupled receptors (GPCRs). Agonist-activated GPCRs are selectively phosphorylated by GRKs, whereupon arrestin proteins bind active phosphoreceptors, blocking further G protein activation, facilitating GPCR internalization via coated pits, and initiating G protein-independent round of signaling. GRKs are rate limiting in this process. Four non-visual GRK subtypes are ubiquitously expressed and present in virtually every neuron expressing dopamine receptors. Here we describe the effects of individual GRKs on the dopamine receptor signaling and trafficking in cultured cells, as well as in in vivo models of dopamine-mediated signaling: response to psychostimulants and l-DOPA-induced dyskinesia, a debilitating side effect of l-DOPA replacement therapy in Parkinson’s disease. The in vivo findings demonstrate differential effects of GRK subtypes on signaling of individual dopamine receptors in the brain. Effect of GRK isoform on psychostimulant-induced behavior is not only dependent on the dopamine receptor but also on the neuronal type in which the isoform operates, as evidenced by the cell-selective GRK deletions. In addition, certain behavioral effects of GRK3 do not require its kinase activity, and are apparently mediated by the ability of its RGS-like domain to bind α-subunits of Gq/11 and suppress their signaling. Thus, in vivo dopamine signaling in the brain serves as a powerful model for unraveling biological actions of different GRK subtypes.

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References

  1. Carman CV, Benovic JL (1998) G-protein-coupled receptors: turn-ons and turn-offs. Curr Opin Neurobiol 8:335–344

    Article  CAS  PubMed  Google Scholar 

  2. Gurevich VV, Gurevich EV (2004) The molecular acrobatics of arrestin activation. Trends Pharmacol Sci 25(2):105–111

    Article  CAS  PubMed  Google Scholar 

  3. Gurevich VV, Gurevich EV (2006) The structural basis of arrestin-mediated regulation of G-protein-coupled receptors. Pharmacol Ther 110(3):465–502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Gurevich EV, Gurevich VV (2006) Arrestins: ubiquitous regulators of cellular signaling pathways. Genome Biol 7(9):236

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Gurevich VV, Gurevich EV (2014) Overview of different mechanisms of arrestin-mediated signaling. Curr Protoc Pharmacol 67(2.10):1–9

    Google Scholar 

  6. Willets JM, Parent JL, Benovic JL, Kelly E (1999) Selective reduction in A2 adenosine receptor desensitization following antisense-induced suppression of G protein-coupled receptor kinase 2 expression. J Neurochem 73:1781–1789

    CAS  PubMed  Google Scholar 

  7. Bohn LM, Gainetdinov RR, Sotnikova TD, Medvedev IO, Lefkowitz RJ, Dykstra LA, Caron MG (2003) Enhanced rewarding properties of morphine, but not cocaine, in beta(arrestin)-2 knock-out mice. J Neurosci 23(32):10265–10273

    CAS  PubMed  Google Scholar 

  8. Bohn LM, Lefkowitz RJ, Gainetdinov RR, Peppel K, Caron MG, Lin FT (1999) Enhanced morphine analgesia in mice lacking beta-arrestin2. Science 286:2495–2498

    Article  CAS  PubMed  Google Scholar 

  9. Pan L, Gurevich EV, Gurevich VV (2003) The nature of the arrestin x receptor complex determines the ultimate fate of the internalized receptor. J Biol Chem 278:11623–11632

    Article  CAS  PubMed  Google Scholar 

  10. 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

    Article  CAS  PubMed  Google Scholar 

  11. Xu J, Dodd RL, Makino CL, Simon MI, Baylor DA, Chen J (1997) Prolonged photoresponses in transgenic mouse rods lacking arrestin. Nature 389(6650):505–509

    Article  CAS  PubMed  Google Scholar 

  12. Menard L, Ferguson SS, Zhang J, Lin FT, Lefkowitz RJ, Caron MG, Barak LS (1997) Synergistic regulation of beta2-adrenergic receptor sequestration: intracellular complement of beta-adrenergic receptor kinase and beta-arrestin determine kinetics of internalization. Mol Pharmacol 51:800–808

    CAS  PubMed  Google Scholar 

  13. Iaccarino G, Rockman HA, Shotwell KF, Tomhave ED, Koch WJ (1998) Myocardial overexpression of GRK3 in transgenic mice: evidence for in vivo selectivity of GRKs. Am J Physiol 275:1298–1306

    Google Scholar 

  14. Gainetdinov RR, Bohn LM, Sotnikova TD, Cyr M, Laakso A, Macrae AD, Torres GE, Kim KM, Lefkowitz RJ, Caron MG, Premont RT (2003) Dopaminergic supersensitivity in G protein-coupled receptor kinase 6-deficient mice. Neuron 38:291–303

    Article  CAS  PubMed  Google Scholar 

  15. Willets JM, Nash MS, Challiss RA, Nahorski SR (2004) Imaging of muscarinic acetylcholine receptor signaling in hippocampal neurons: evidence for phosphorylation-dependent and -independent regulation by G-protein-coupled receptor kinases. J Neurosci 24(17):4157–4162

    Article  CAS  PubMed  Google Scholar 

  16. Gainetdinov RR, Bohn LM, Walker JK, Laporte SA, Macrae AD, Caron MG, Lefkowitz RJ, Premont RT (1999) Muscarinic supersensitivity and impaired receptor desensitization in G protein-coupled receptor kinase 5-deficient mice. Neuron 24(4):1029–1036

    Article  CAS  PubMed  Google Scholar 

  17. Kim J, Ahn S, Ren XR, Whalen EJ, Reiter E, Wei H, Lefkowitz RJ (2005) Functional antagonism of different G protein-coupled receptor kinases for beta-arrestin-mediated angiotensin II receptor signaling. Proc Natl Acad Sci U S A 102:142–1447

    Google Scholar 

  18. Ren XR, Reiter E, Ahn S, Kim J, Chen W, Lefkowitz RJ (2005) Different G protein-coupled receptor kinases govern G protein and beta-arrestin-mediated signaling of V2 vasopressin receptor. Proc Natl Acad Sci U S A 102:1448–1453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Gurevich EV, Tesmer JJ, Mushegian A, Gurevich VV (2012) G protein-coupled receptor kinases: more than just kinases and not only for GPCRs. Pharmacol Ther 133:40–69

    Article  CAS  PubMed  Google Scholar 

  20. Dixon RA, Kobilka BK, Strader DJ, Benovic JL, Dohlman HG, Frielle T, Bolanowski MA, Bennett CD, Rands E, Diehl RE, Mumford RA, Slater EE, Sigal IS, Caron MG, Lefkowitz RJ, Strader CD (1986) Cloning of the gene and cDNA for mammalian beta-adrenergic receptor and homology with rhodopsin. Nature 321:75–79

    Article  CAS  PubMed  Google Scholar 

  21. 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(6201):783–787

    Article  CAS  PubMed  Google Scholar 

  22. Dal Toso R, Sommer B, Ewert M, Herb A, Pritchett DB, Bach A, Shivers BD, Seeburg PH (1989) The dopamine D2 receptor: two molecular forms generated by alternative splicing. EMBO J 8(13):4025–4034

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Monsma FJ Jr, McVittie LD, Gerfen CR, Mahan LC, Sibley DR (1989) Multiple D2 dopamine receptors produced by alternative RNA splicing. Nature 342(6252):926–929

    Article  CAS  PubMed  Google Scholar 

  24. Dearry A, Gingrich JA, Falardeau P, Fremeau RT Jr, Bates MD, Caron MG (1990) Molecular cloning and expression of the gene for a human D1 dopamine receptor. Nature 347(6288):72–76

    Article  CAS  PubMed  Google Scholar 

  25. Monsma FJ Jr, Mahan LC, McVittie LD, Gerfen CR, Sibley DR (1990) Molecular cloning and expression of a D1 dopamine receptor linked to adenylyl cyclase activation. Proc Natl Acad Sci U S A 87(17):6723–6727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Sunahara RK, Niznik HB, Weiner DM, Stormann TM, Brann MR, Kennedy JL, Gelernter JE, Rozmahel R, Yang YL, Israel Y, Seeman P, O'Dowd BF (1990) Human dopamine D1 receptor encoded by an intronless gene on chromosome 5. Nature 347(6288):80–83

    Article  CAS  PubMed  Google Scholar 

  27. Giros B, Martres MP, Sokoloff P, Schwartz JC (1990) Gene cloning of human dopaminergic D3 receptor and identification of its chromosome. C R Acad Sci III 311(13):501–508

    CAS  PubMed  Google Scholar 

  28. Van Tol HH, Bunzow JR, Guan HC, Sunahara RK, Seeman P, Niznik HB, Civelli O (1991) Cloning of the gene for a human dopamine D4 receptor with high affinity for the antipsychotic clozapine. Nature 350(6319):610–614

    Article  PubMed  Google Scholar 

  29. Sunahara RK, Guan HC, O'Dowd BF, Seeman P, Laurier LG, Ng G, George SR, Torchia J, Van Tol HH, Niznik HB (1991) Cloning of the gene for a human dopamine D5 receptor with higher affinity for dopamine than D1. Nature 350(6319):614–619

    Article  CAS  PubMed  Google Scholar 

  30. Tiberi M, Nash S, Bertrand L, Lefkowitz RJ, Caron MG (1996) Differential regulation of dopamine D1A receptor responsiveness by various G protein-coupled receptor kinases. J Biol Chem 271(7):3771–3778

    Article  CAS  PubMed  Google Scholar 

  31. Jiang D, Sibley DR (1999) Regulation of D(1) dopamine receptors with mutations of protein kinase phosphorylation sites: attenuation of the rate of agonist-induced desensitization. Mol Pharmacol 56(4):675–683

    CAS  PubMed  Google Scholar 

  32. Kim OJ, Gardner BR, Williams DB, Marinec PS, Cabrera DM, Peters JD, Mak CC, Kim KM, Sibley DR (2004) The role of phosphorylation in D1 dopamine receptor desensitization: evidence for a novel mechanism of arrestin association. J Biol Chem 279:7999–8010

    Article  CAS  PubMed  Google Scholar 

  33. Pals-Rylaarsdam R, Gurevich VV, Lee KB, Ptasienski J, Benovic JL, Hosey MM (1997) Internalization of the m2 muscarinic acetylcholine receptor: arrestin-independent and -dependent pathways. J Biol Chem 272:23682–23689

    Article  CAS  PubMed  Google Scholar 

  34. Whistler JL, Tsao P, von Zastrow M (2001) A phosphorylation-regulated brake mechanism controls the initial endocytosis of opioid receptors but is not required for post-endocytic sorting to lysosomes. J Biol Chem 276:34331–34338

    Article  CAS  PubMed  Google Scholar 

  35. Palczewski K, Buczylko J, Kaplan MW, Polans AS, Crabb JW (1991) Mechanism of rhodopsin kinase activation. J Biol Chem 266:12949–12955

    CAS  PubMed  Google Scholar 

  36. Rankin ML, Marinec PS, Cabrera DM, Wang Z, Jose PA, Sibley DR (2006) The D1 dopamine receptor is constitutively phosphorylated by G protein-coupled receptor kinase 4. Mol Pharmacol 69(3):759–769

    CAS  PubMed  Google Scholar 

  37. Villar VA, Jones JE, Armando I, Palmes-Saloma C, Yu P, Pascua AM, Keever L, Arnaldo FB, Wang Z, Luo Y, Felder RA, Jose PA (2009) G protein-coupled receptor kinase 4 (GRK4) regulates the phosphorylation and function of the dopamine D3 receptor. J Biol Chem 284(32):21425–21434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. 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(22):15038–15051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Cho D, Zheng M, Min C, Ma L, Kurose H, Park JH, Kim KM (2010) Agonist-induced endocytosis and receptor phosphorylation mediate resensitization of dopamine D(2) receptors. Mol Endocrinol 24(3):574–586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Li L, Homan KT, Vishnivetskiy SA, Manglik A, Tesmer JJ, Gurevich VV, Gurevich EV (2015) G Protein-coupled receptor kinases of the GRK4 protein subfamily phosphorylate inactive G Protein-coupled Receptors (GPCRs). J Biol Chem 290(17):10775–10790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Mushegian A, Gurevich VV, Gurevich EV (2012) The origin and evolution of G protein-coupled receptor kinases. PLoS One 7(3):e33806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. De Lean A, Stadel JM, Lefkowitz RJ (1980) A ternary complex model explains the agonist-specific binding properties of the adenylate cyclase-coupled beta-adrenergic receptor. J Biol Chem 255(15):7108–7117

    PubMed  Google Scholar 

  43. Samama P, Cotecchia S, Costa T, Lefkowitz RJ (1993) A mutation-induced activated state of the beta 2-adrenergic receptor. Extending the ternary complex model. J Biol Chem 268(7):4625–4636

    CAS  PubMed  Google Scholar 

  44. Benovic JL, Strasser RH, Caron MG, Lefkowitz RJ (1986) Beta-adrenergic receptor kinase: identification of a novel protein kinase that phosphorylates the agonist-occupied form of the receptor. Proc Natl Acad Sci U S A 83(9):2797–2801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Benovic JL, Mayor FJ, Somers RL, Caron MG, Lefkowitz RJ (1986) Light-dependent phosphorylation of rhodopsin by beta-adrenergic receptor kinase. Nature 321(6073):869–872

    Article  CAS  PubMed  Google Scholar 

  46. Gurevich VV, Benovic JL (1993) Visual arrestin interaction with rhodopsin: sequential multisite binding ensures strict selectivity towards light-activated phosphorylated rhodopsin. J Biol Chem 268:11628–11638

    CAS  PubMed  Google Scholar 

  47. Gurevich VV, Pals-Rylaarsdam R, Benovic JL, Hosey MM, Onorato JJ (1997) Agonist-receptor-arrestin, an alternative ternary complex with high agonist affinity. J Biol Chem 272:28849–28852

    Article  CAS  PubMed  Google Scholar 

  48. Farrens DL, Altenbach C, Yang K, Hubbell WL, Khorana HG (1996) Requirement of rigid-body motion of transmembrane helices for light activation of rhodopsin. Science 274:768–770

    Article  CAS  PubMed  Google Scholar 

  49. Rasmussen SG, DeVree BT, Zou Y, Kruse AC, Chung KY, Kobilka TS, Thian FS, Chae PS, Pardon E, Calinski D, Mathiesen JM, Shah ST, Lyons JA, Caffrey M, Gellman SH, Steyaert J, Skiniotis G, Weis WI, Sunahara RK, Kobilka BK (2011) Crystal structure of the β2 adrenergic receptor-Gs protein complex. Nature 477:549–555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Rasmussen SG, Choi HJ, Fung JJ, Pardon E, Casarosa P, Chae PS, Devree BT, Rosenbaum DM, Thian FS, Kobilka TS, Schnapp A, Konetzki I, Sunahara RK, Gellman SH, Pautsch A, Steyaert J, Weis WI, Kobilka BK (2011) Structure of a nanobody-stabilized active state of the β(2) adrenoceptor. Nature 469:175–180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Kang Y, Zhou XE, Gao X, He Y, Liu W, Ishchenko A, Barty A, White TA, Yefanov O, Han GW, Xu Q, de Waal PW, Ke J, Tan MHE, Zhang C, Moeller A, West GM, Van Eps N, Caro LN, Vishnivetskiy SA, Lee RJ, Suino-Powell KM, Gu X, Pal K, Ma J, Zhi X, Boutet S, Williams GJ, Messerschmidt M, Gati C, Zatsepin NA, Wang D, James D, Basu S, Roy-Chowdhuty S, Conrad S, Coe J, Liu H, Lisova S, Kupitz C, Grotjohann I, Fromme R, Jiang Y, Tan M, Yang H, Li J, Wang M, Zheng Z, Li D, Zhao Y, Standfuss J, Diederichs K, Dong Y, Potter CS, Carragher B, Caffrey M, Jiang H, Chapman HN, Spence JCH, Fromme P, Weierstall U, Ernst OP, Katritch V, Gurevich VV, Griffin PR, Hubbell WL, Stevens RC, Cherezov V, Melcher K, Xu HE (2015) Crystal structure of rhodopsin bound to arrestin determined by femtosecond X-ray laser. Nature 523:561–567.

    Google Scholar 

  52. Pao CS, Barker BL, Benovic JL (2009) Role of the amino terminus of G protein-coupled receptor kinase 2 in receptor phosphorylation. Biochemistry 48(30):7325–7333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Beautrait A, Michalski KR, Lopez TS, Mannix KM, McDonald DJ, Cutter AR, Medina CB, Hebert AM, Francis CJ, Bouvier M, Tesmer JJ, Sterne-Marr R (2014) Mapping the putative G protein-coupled receptor (GPCR) docking site on GPCR kinase 2: insights from intact cell phosphorylation and recruitment assays. J Biol Chem 289(36):25262–25275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Strachan RT, Sun JP, Rominger DH, Violin JD, Ahn S, Rojas Bie Thomsen A, Zhu X, Kleist A, Costa T, Lefkowitz RJ (2014) Divergent transducer-specific molecular efficacies generate biased agonism at a G protein-coupled receptor (GPCR). J Biol Chem 289(20):14211–14224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Nestler EJ (2005) The neurobiology of cocaine addiction. Sci Pract Perspect 3:4–10

    Article  PubMed  PubMed Central  Google Scholar 

  56. Thomas MJ, Kalivas PW, Shaham Y (2008) Neuroplasticity in the mesolimbic dopamine system and cocaine addiction. Br J Pharmacol 154:327–342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Feltenstein MW, See RE (2008) The neurocircuitry of addiction: an overview. Br J Pharmacol 154:261–274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Gerfen CR, Keefe KA, Gauda EB (1995) D1 and D2 dopamine receptor function in the striatum: coactivation of D1- and D2-dopamine receptors on separate populations of neurons results in potentiated immediate early gene response in D1-containing neurons. J Neurosci 15:8167–8176

    CAS  PubMed  Google Scholar 

  59. Gerfen CR, McGinty JF, Young WS (1991) Dopamine differentially regulates dynorphin, substance P, and enkephalin expression in striatal neurons: in situ hybridization histochemical analysis. J Neurosci 11:1016–1031

    CAS  PubMed  Google Scholar 

  60. Gerfen CR, Miyachi S, Paletzki R, Brown P (2002) D1 dopamine receptor supersensitivity in the dopamine-depleted striatum results from a switch in the regulation of ERK1/2 kinase. J Neurosci 22:5042–5054

    CAS  PubMed  Google Scholar 

  61. Le Moine C, Bloch B (1995) D1 and D2 dopamine receptor gene expression in the rat striatum: sensitive cRNA probes demonstrate prominent segregation of D1 and D2 mRNAs in distinct neuronal populations of the dorsal and ventral striatum. J Comp Neurol 355:418–426

    Article  PubMed  Google Scholar 

  62. Rashid AJ, O’Dowd BF, Verma V, George SR (2007) Neuronal Gq/11-coupled dopamine receptors: an uncharted role for dopamine. Trends Pharmacol Sci 28:551–555

    Article  CAS  PubMed  Google Scholar 

  63. Rashid AJ, So CH, Kong MM, Furtak T, El-Ghundi M, Cheng R, O'Dowd BF, George SR (2007) D1-D2 dopamine receptor heterooligomers with unique pharmacology are coupled to rapid activation of Gq/11 in the striatum. Proc Natl Acad Sci U S A 104:654–659

    Article  CAS  PubMed  Google Scholar 

  64. Bertran-Gonzalez J, Bosch C, Maroteaux M, Matamales M, Hervé D, Valjent E, Girault JA (2008) Opposing patterns of signaling activation in dopamine D1 and D2 receptor-expressing striatal neurons in response to cocaine and haloperidol. J Neurosci 28:5671–5685

    Article  CAS  PubMed  Google Scholar 

  65. Matamales M, Bertran-Gonzalez J, Salomon L, Degos B, Deniau JM, Valjent E, Hervé D, Girault JA (2009) Striatal medium-sized spiny neurons: identification by nuclear staining and study of neuronal subpopulations in BAC transgenic mice. PLoS One 4:e4770

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Lee SP, So CH, Rashid AJ, Varghese G, Cheng R, Lanca AJ, O'Dowd BF, George SR (2004) Dopamine D1 and D2 receptor co-activation generates a novel phospholipase C-mediated calcium signal. J Biol Chem 279:35671–35678

    Article  CAS  PubMed  Google Scholar 

  67. Bordet R, Ridray S, Carboni C, Diaz J, Sokoloff P, Schwartz JC (1997) Induction of dopamine D3 receptor expression as a mechanism of behavioral sensitization to levodopa. Proc Natl Acad Sci U S A 94:3363–3367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Bordet R, Ridray S, Schwartz JC, Sokoloff P (2000) Involvement of the direct striatonigral pathway in levodopa-induced sensitization in 6-hydroxydopamine-lesioned rats. Eur J Neurosci 12:2117–2123

    Article  CAS  PubMed  Google Scholar 

  69. Ding J, Guzman JN, Tkatch T, Chen S, Goldberg JA, Ebert PJ, Levitt P, Wilson CJ, Hamm HE, Surmeier DJ (2006) RGS4-dependent attenuation of M4 autoreceptor function in striatal cholinergic interneurons following dopamine depletion. Nat Neurosci 9:832–842

    Article  CAS  PubMed  Google Scholar 

  70. Ding Y, Won L, Britt JP, Lim SA, McGehee DS, Kang UJ (2011) Enhanced striatal cholinergic neuronal activity mediates L-DOPA-induced dyskinesia in parkinsonian mice. Proc Natl Acad Sci U S A 108:840–845

    Article  CAS  PubMed  Google Scholar 

  71. Wang Z, Kai L, Day M, Ronesi J, Yin HH, Ding J, Tkatch T, Lovinger DM, Surmeier DJ (2006) Dopaminergic control of corticostriatal long-term synaptic depression in medium spiny neurons is mediated by cholinergic interneurons. Neuron 50:443–452

    Article  CAS  PubMed  Google Scholar 

  72. Ciliax BJ, Nash N, Heilman C, Sunahara R, Hartney A, Tiberi M, Rye DB, Caron MG, Niznik HB, Levey AI (2000) Dopamine D5 receptor immunolocalization in rat and monkey brain. Synapse 37:125–145

    Article  CAS  PubMed  Google Scholar 

  73. Khan ZU, Gutiérrez A, Martín R, Peñafiel A, Rivera A, de la Calle A (2000) Dopamine D5 receptors of rat and human brain. Neuroscience 100:689–699

    Article  CAS  PubMed  Google Scholar 

  74. Berlanga ML, Simpson TK, Alcantara AA (2005) Dopamine D5 receptor localization on cholinergic neurons of the rat forebrain and diencephalon: a potential neuroanatomical substrate involved in mediating dopaminergic influences on acetylcholine release. J Comp Neurol 492:34–49

    Article  CAS  PubMed  Google Scholar 

  75. Laakso A, Mohn AR, Gainetdinov RR, Caron MG (2002) Experimental genetic approaches to addiction. Neuron 36:213–228

    Article  CAS  PubMed  Google Scholar 

  76. Koob GF (1992) Drugs of abuse: anatomy, pharmacology and function of reward pathways. Trends Pharmacol Sci 13:177–184

    Article  CAS  PubMed  Google Scholar 

  77. Gainetdinov RR, Premont RT, Bohn LM, Lefkowitz RJ, Caron MG (2004) Desensitization of G protein-coupled receptors and neuronal functions. Annu Rev Neurosci 27:107–144

    Article  CAS  PubMed  Google Scholar 

  78. Premont RT, Gainetdinov RR (2007) Physiological roles of G protein-coupled receptor kinases and arrestins. Annu Rev Physiol 69:511–534

    Article  CAS  PubMed  Google Scholar 

  79. Arriza JL, Dawson TM, Simerly RB, Martin LJ, Caron MG, Snyder SH, Lefkowitz RJ (1992) The G-protein-coupled receptor kinases bARK1 and bARK2 are widely distributed at synapses in rat brain. J Neurosci 12:4045–4055

    CAS  PubMed  Google Scholar 

  80. Iwata K, Ito K, Fukuzaki A, Inaki K, Haga T (1999) Dynamin and rab5 regulate GRK2-dependent internalization of dopamine D2 receptors. Eur J Biochem 263(2):596–602

    Article  CAS  PubMed  Google Scholar 

  81. Kabbani N, Negyessy L, Lin R, Goldman-Rakic P, Levenson R (2002) Interaction with neuronal calcium sensor NCS-1 mediates desensitization of the D2 dopamine receptor. J Neurosci 22(19):8476–8486

    CAS  PubMed  Google Scholar 

  82. Banday AA, Fazili FR, Lokhandwala MF (2007) Insulin causes renal dopamine D1 receptor desensitization via GRK2-mediated receptor phosphorylation involving phosphatidylinositol 3-kinase and protein kinase C. Am J Physiol Renal Physiol 293(3):F877–F884

    Article  CAS  PubMed  Google Scholar 

  83. Sedaghat K, Nantel MF, Ginsberg S, Lalonde V, Tiberi M (2006) Molecular characterization of dopamine D2 receptor isoforms tagged with green fluorescent protein. Mol Biotechnol 34(1):1–14

    Article  CAS  PubMed  Google Scholar 

  84. Schroeder JA, McCafferty MR, Unterwald EM (2009) Regulation of dynamin 2 and G protein-coupled receptor kinase 2 in rat nucleus accumbens during acute and repeated cocaine administration. Synapse 63(10):863–870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Jaber M, Koch WJ, Rockman H, Smith B, Bond RA, Sulik KK, Ross J Jr, Lefkowitz RJ, Caron MG, Giros B (1996) Essential role of beta-adrenergic receptor kinase 1 in cardiac development and function. Proc Natl Acad Sci U S A 93(23):12974–12979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Daigle TL, Caron MG (2012) Elimination of GRK2 from cholinergic neurons reduces behavioral sensitivity to muscarinic receptor activation. J Neurosci 32:11461–11466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Daigle TL, Ferris MJ, Gainetdinov RR, Sotnikova TD, Urs NM, Jones SR, Caron MG (2014) Selective deletion of GRK2 alters psychostimulant-induced behaviors and dopamine neurotransmission. Neuropsychopharmacology 10:2450–2462

    Article  CAS  Google Scholar 

  88. Beyer CE, Steketee JD (2002) Cocaine sensitization: modulation by dopamine D2 receptors. Cereb Cortex 12:526–535

    Article  PubMed  Google Scholar 

  89. Bychkov E, Zurkovsky L, Garret M, Ahmed MR, Gurevich EV (2013) Distinct cellular and subcellular distribution of G protein-coupled receptor kinase and arrestin isoforms in the striatum. PLoS One 7:e48912

    Article  CAS  Google Scholar 

  90. Erdtmann-Vourliotis M, Mayer P, Ammon S, Riechert U, Hollt V (2001) Distribution of G-protein-coupled receptor kinase (GRK) isoforms 2, 3, 5 and 6 mRNA in the rat brain. Brain Res Mol Brain Res 95(1-2):129–137

    Article  CAS  PubMed  Google Scholar 

  91. Raehal KM, Schmid CL, Medvedev IO, Gainetdinov RR, Premont RT, Bohn LM (2009) Morphine-induced physiological and behavioral responses in mice lacking G protein-coupled receptor kinase 6. Drug Alcohol Depend 104(3):187–196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Seeman P, Weinshenker D, Quirion R, Srivastava LK, Bhardwaj SK, Grandy DK, Premont RT, Sotnikova TD, Boksa P, El-Ghundi M, O'Dowd BF, George SR, Perreault ML, Mannisto PT, Robinson S, Palmiter RD, Tallerico T (2005) Dopamine supersensitivity correlates with D2High states, implying many paths to psychosis. Proc Natl Acad Sci U S A 102(9):3513–3518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Bychkov E, Ahmed MR, Dalby KN, Gurevich EV (2007) Dopamine depletion and subsequent treatment with L-DOPA, but not the long-lived dopamine agonist pergolide, enhances activity of the Akt pathway in the rat striatum. J Neurochem 102:699–711

    Article  CAS  PubMed  Google Scholar 

  94. Santini E, Valjent E, Usiello A, Carta M, Borgkvist A, Girault J-A, Herve D, Greengard P, Fisone G (2007) Critical Involvement of cAMP/DARPP-32 and extracellular signal-regulated protein kinase signaling in L-DOPA-induced dyskinesia. J Neurosci 27:6995–7005

    Article  CAS  PubMed  Google Scholar 

  95. Ahmed MR, Bychkov E, Kook S, Zurkovsky L, Dalby KN, Gurevich EV (2015) Overexpression of GRK6 rescues L-DOPA-induced signaling abnormalities in the dopamine-depleted striatum of hemiparkinsonian rats. Exp Neurol 266:42–54

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Aubert I, Guigoni HK, Li Q, Dovero S, Barthe N, Bioulac BH, Gross CE, Fisone G, Bloch B, Bezard E (2005) Increased D1 dopamine receptor signaling in levodopa-induced dyskinesia. Ann Neurol 57:17–26

    Article  CAS  PubMed  Google Scholar 

  97. Guigoni C, Aubert I, Li Q, Gurevich VV, Benovic JL, Ferry S, Mach U, Stark H, Leriche L, Hakansson K, Bioulac BH, Gross CE, Sokoloff P, Fisone G, Gurevich EV, Bloch B, Bezard E (2005) Pathogenesis of levodopa-induced dyskinesia: focus on D1 and D3 dopamine receptors. Parkinsonism Relat Disord 11(Suppl 1):S25–S29

    Article  PubMed  Google Scholar 

  98. Kovoor A, Seyffarth P, Ebert J, Barghshoon S, Chen C-K, Schwarz S, Axelrod JD, Cheyette BNR, Simon MI, Lester HA, Schwarz J (2005) D2 dopamine receptors colocalize regulator of G-protein signaling 9-2 (RGS9-2) via the RGS9 DEP domain, and RGS9 knock-out mice develop dyskinesias associated with dopamine pathways. J Neurosci 25:2157–2165

    Article  CAS  PubMed  Google Scholar 

  99. Gold SJ, Hoang CV, Potts BW, Porras G, Pioli E, Kim KW, Nadjar A, Qin C, LaHoste GJ, Li Q, Bioulac BH, Waugh JL, Gurevich E, Neve RL, Bezard E (2007) RGS9 2 negatively modulates l-3,4-dihydroxyphenylalanine-Induced dyskinesia in experimental Parkinson’s disease. J Neurosci 27:14338–14348

    Article  CAS  PubMed  Google Scholar 

  100. Fahn S (2008) How do you treat motor complications in Parkinson’s disease: medicine, surgery, or both? Ann Neurol 64(Suppl 2):S56–S64

    PubMed  Google Scholar 

  101. Stocchi F, Nordera G, Marsden CD (1997) Strategies for treating patients with advanced Parkinson's disease with disastrous fluctuations and dyskinesias. Clin Neuropharmacol 20:95–115

    Article  CAS  PubMed  Google Scholar 

  102. Cotzias GC, Papavasiliou PS, Gellene R (1969) Modification of Parkinsonism by chronic treatment with L-dopa. N Engl J Med 280(7):337–345

    Article  CAS  PubMed  Google Scholar 

  103. Bezard E, Gross CE, Qin L, Gurevich VV, Benovic JL, Gurevich EV (2005) L-DOPA reverses the MPTP-induced elevation of the arrestin2 and GRK6 expression and enhanced ERK activation in monkey brain. Neurobiol Dis 18:323–335

    Article  CAS  PubMed  Google Scholar 

  104. Brown A, Deutch AY, Colbran RJ (2005) Dopamine depletion alters phosphorylation of striatal proteins in a model of Parkinsonism. Eur J Neurosci 22:247–256

    Article  PubMed  PubMed Central  Google Scholar 

  105. Kim DS, Palmiter RD, Cummins A, Gerfen CR (2006) Reversal of supersensitive striatal dopamine D1 receptor signaling and extracellular signal-regulated kinase activity in dopamine-deficient mice. Neuroscience 137:1381–1388

    Article  CAS  PubMed  Google Scholar 

  106. Santini E, Sgambato-Faure V, Li Q, Savasta M, Dovero S, Fisone G, Bezard E (2010) Distinct changes in cAMP and extracellular signal-regulated protein kinase signalling in L-DOPA-induced dyskinesia. PLoS One 5:e12322

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  107. Sgambato-Faure V, Buggia V, Gilbert F, Levesque D, Benabid AL, Berger F (2005) Coordinated and spatial upregulation of arc in striatonigral neurons correlates with L-dopa-induced behavioral sensitization in dyskinetic rats. J Neuropathol Exp Neurol 64:936–947

    Article  CAS  PubMed  Google Scholar 

  108. Ahmed MR, Berthet A, Bychkov E, Porras G, Li Q, Bioulac BH, Carl YT, Bloch B, Kook S, Aubert I, Dovero S, Doudnikoff E, Gurevich VV, Gurevich EV, Bezard E (2010) Lentiviral overexpression of GRK6 alleviates L-dopa-induced dyskinesia in experimental Parkinson's disease. Sci Transl Med 2:28ra28

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  109. Ahmed MR, Bychkov E, Gurevich VV, Benovic JL, Gurevich EV (2007) Altered expression and subcellular distribution of GRK subtypes in the dopamine-depleted rat basal ganglia is not normalized by l-DOPA treatment. J Neurochem 104:1622–1636

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  110. Cenci MA, Lundblad M (2007) Ratings of L-DOPA-induced dyskinesia in the unilateral 6-OHDA lesion model of Parkinson's disease in rats and mice. Curr Protoc Neurosci 9 (Unit 9.25)

    Google Scholar 

  111. Cenci MA, Konradi C (2010) Maladaptive striatal plasticity in L-DOPA-induced dyskinesia. Prog Brain Res 183:209–233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Cenci MA, Lee CS, Björklund A (1998) L-DOPA-induced dyskinesia in the rat is associated with striatal overexpression of prodynorphin- and glutamic acid decarboxylase mRNA. Eur J Neurosci 10:2694–2706

    Article  CAS  PubMed  Google Scholar 

  113. Cenci MA (2007) Dopamine dysregulation of movement control in L-DOPA-induced dyskinesia. Trends Neurosci 30:236–243

    Article  CAS  PubMed  Google Scholar 

  114. Bezard E, Ferry S, Mach U, Stark H, Leriche L, Boraud T, Gross CE, Sokoloff P (2003) Attenuation of levodopa-induced dyskinesia by normalizing dopamine D3 receptor function. Nat Med 9(6):762–767

    Article  CAS  PubMed  Google Scholar 

  115. Gurevich EV, Benovic JL, Gurevich VV (2004) Arrestin2 expression selectively increases during neural differentiation. J Neurochem 91(6):1404–1416

    Article  CAS  PubMed  Google Scholar 

  116. Bychkov E, Gurevich VV, Joyce JN, Benovic JL, Gurevich EV (2008) Arrestins and two receptor kinases are upregulated in Parkinson’s disease with dementia. Neurobiol Aging 29:379–396

    Article  CAS  PubMed  Google Scholar 

  117. Ahmed MR, Bychkov E, Li L, Gurevich VV, Gurevich EV (2015) GRK3 suppresses L-DOPA-induced dyskinesia in the rat model of Parkinson’s disease via its RGS homology domain. Sci Rep 5:10920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Guigoni C, Doudnikoff E, Li Q, Bloch B, Bezard E (2007) Altered D1 dopamine receptor trafficking in Parkinsonian and dyskinetic non-human primates. Neurobiol Dis 26(2):452

    Article  CAS  PubMed  Google Scholar 

  119. Siderovski DP, Hessel A, Chung S, Mak TW, Tyers M (1996) A new family of regulators of G-protein-coupled receptors? Curr Biol 6:211–212

    Article  CAS  PubMed  Google Scholar 

  120. Hollinger S, Hepler JR (2002) Cellular regulation of RGS proteins: modulators and integrators of G protein signaling. Pharmacol Rev 54:527–559

    Article  CAS  PubMed  Google Scholar 

  121. Lodowski DT, Tesmer VM, Benovic JL, Tesmer JJ (2006) The structure of G protein-coupled receptor kinase (GRK)-6 defines a second lineage of GRKs. J Biol Chem 281:16785–16793

    Article  CAS  PubMed  Google Scholar 

  122. Day PW, Wedegaertner PB, Benovic JL (2004) Analysis of G-protein-coupled receptor kinase RGS homology domains. Methods Enzymol 390:295–310

    Article  CAS  PubMed  Google Scholar 

  123. Carman CV, Parent JL, Day PW, Pronin AN, Sternweis PM, Wedegaertner PB, Gilman AG, Benovic JL, Kozasa T (1999) Selective regulation of Galpha(q/11) by an RGS domain in the G protein-coupled receptor kinase, GRK2. J Biol Chem 274:34483–34492

    Article  CAS  PubMed  Google Scholar 

  124. Day PW, Carman CV, Sterne-Marr R, Benovic JL, Wedegaertner PB (2003) Differential interaction of GRK2 with members of the Gaq family. Biochemistry 42:9176–9184

    Article  CAS  PubMed  Google Scholar 

  125. Sterne-Marr R, Dhami GK, Tesmer JJ, Ferguson SS (2004) Characterization of GRK2 RH domain-dependent regulation of GPCR coupling to heterotrimeric G proteins. Methods Enzymol 390:310–336

    Article  CAS  PubMed  Google Scholar 

  126. Sterne-Marr R, Tesmer JJ, Day PW, Stracquatanio RP, Cilente JA, O'Connor KE, Pronin AN, Benovic JL, Wedegaertner PB (2003) G protein-coupled receptor Kinase 2/G alpha q/11 interaction. A novel surface on a regulator of G protein signaling homology domain for binding G alpha subunits. J Biol Chem 278:6050–6058

    Article  CAS  PubMed  Google Scholar 

  127. Usui I, Imamura T, Satoh H, Huang J, Babendure JL, Hupfeld CJ, Olefsky JM (2004) GRK2 is an endogenous protein inhibitor of the insulin signaling pathway for glucose transport stimulation. EMBO J 23:2821–2829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Dhami GK, Dale LB, Anborgh PH, O'Connor-Halligan KE, Sterne-Marr R, Ferguson SS (2004) G Protein-coupled receptor kinase 2 regulator of G protein signaling homology domain binds to both metabotropic glutamate receptor 1a and Galphaq to attenuate signaling. J Biol Chem 279:16614–16620

    Article  CAS  PubMed  Google Scholar 

  129. Dhami GK, Anborgh PH, Dale LB, Sterne-Marr R, Ferguson SSG (2002) Phosphorylation-independent regulation of metabotropic glutamate receptor signaling by G protein-coupled receptor kinase 2. J Biol Chem 277(28):25266–25272

    Article  CAS  PubMed  Google Scholar 

  130. Bezard E, Brotchie JM, Gross CE (2001) Pathophysiology of levodopa-induced dyskinesia: potential for new therapies. Nat Rev Neurosci 2:577–588

    Article  CAS  PubMed  Google Scholar 

  131. Berthet A, Porras G, Doudnikoff E, Stark H, Cador M, Bezard E, Bloch B (2009) Pharmacological analysis demonstrates dramatic alteration of D1 dopamine receptor neuronal distribution in the rat analog of L-DOPA-induced dyskinesia. J Neurosci 29:4829–4835

    Article  CAS  PubMed  Google Scholar 

  132. Darmopil S, Martín AB, De Diego IR, Ares S, Moratalla R (2009) Genetic inactivation of dopamine D1 but not D2 receptors inhibits L-DOPA-induced dyskinesia and histone activation. Biol Psychiatry 66:603–613

    Article  CAS  PubMed  Google Scholar 

  133. Morissette M, Grondin R, Goulet M, Bédard PJ, Di Paolo T (1999) Differential regulation of striatal preproenkephalin and preprotachykinin mRNA levels in MPTP-lesioned monkeys chronically treated with dopamine D1 or D2 agonists. J Neurochem 72:682–692

    Article  CAS  PubMed  Google Scholar 

  134. Gurevich EV, Gurevich VV (2008) Dopamine receptors and the treatment of Parkinson’s disease. In: Neve KA (ed) Dopamine receptors, 2nd edn. Humana, Portland, OR, pp 525–584

    Google Scholar 

  135. Bastide MF, Meissner WG, Picconi B, Fasano S, Fernagut PO, Feyder M, Francardo V, Alcacer C, Ding Y, Brambilla R, Fisone G, Joe Stoessl A, Bourdenx M, Engeln M, Navailles S, De Deurwaerdère P, Ko WK, Simola N, Morelli M, Groc L, Rodriguez MC, Gurevich EV, Quik Morari M, Mellone M, Gardoni F, Tronci E, Guehl D, Tison F, Crossman AR, Kang UJ, Steece-Collier K, Fox S, Carta M, Angela-Cenci M, Bézard E (2015) Pathophysiology of L-dopa-induced motor and non-motor complications in Parkinson’s disease. Prog Neurobiol 132:96–168

    Article  CAS  PubMed  Google Scholar 

  136. Paul ML, Currie RW, Robertson HA (1995) Priming of a D1 dopamine receptor behavioural response is dissociated from striatal immediate-early gene activity. Neuroscience 66:347–359

    Article  CAS  PubMed  Google Scholar 

  137. Paul ML, Graybiel AM, David JC, Robertson HA (1992) D1-like and D2-like dopamine receptors synergistically activate rotation and c-fos expression in the dopamine-depleted striatum in a rat model of Parkinson's disease. J Neurosci 12:3729–3742

    CAS  PubMed  Google Scholar 

  138. Pollack AE, Strauss JB (1999) Time dependence and role of N-methyl-D-aspartate glutamate receptors in the priming of D2-mediated rotational behavior and striatal Fos expression in 6-hydroxydopamine lesioned rats. Brain Res 827:160–168

    Article  CAS  PubMed  Google Scholar 

  139. Moore CA, Milano SK, Benovic JL (2007) Regulation of receptor trafficking by GRKs and arrestins. Annu Rev Physiol 69:451–482

    Article  CAS  PubMed  Google Scholar 

  140. Banday AA, Lokhandwala MF (2007) Oxidative stress reduces renal dopamine D1 receptor-Gq/11alpha G protein-phospholipase C signaling involving G protein-coupled receptor kinase 2. Am J Physiol Ren Physiol 293:F306–F315

    Article  CAS  Google Scholar 

  141. Felder CC, Blecher M, Jose PA (1989) Dopamine-1-mediated stimulation of phospholipase C activity in rat renal cortical membranes. J Biol Chem 264:8739–8745

    CAS  PubMed  Google Scholar 

  142. Felder CC, Jose PA, Axelrod J (1989) The dopamine-1 agonist, SKF 82526, stimulates phospholipase-C activity independent of adenylate cyclase. J Pharmacol Exp Ther 248:171–175

    CAS  PubMed  Google Scholar 

  143. Liu J, Wang F, Huang C, Long LH, Wu WN, Cai F, Wang JH, Ma LQ, Chen JG (2009) Activation of phosphatidylinositol-linked novel D1 dopamine receptor contributes to the calcium mobilization in cultured rat prefrontal cortical astrocytes. Cell Mol Neurobiol 29:317–328

    Article  CAS  PubMed  Google Scholar 

  144. Liu J, Wang W, Wang F, Cai F, Hu ZL, Yang YJ, Chen J, Chen JG (2009) Phosphatidylinositol-linked novel D(1) dopamine receptor facilitates long-term depression in rat hippocampal CA1 synapses. Neuropharmacology 57:164–171

    Article  CAS  PubMed  Google Scholar 

  145. Mizuno K, Kurokawa K, Ohkuma S (2012) Dopamine D1 receptors regulate type 1 inositol 1,4,5-trisphosphate receptor expression via both AP-1- and NFATc4-mediated transcriptional processes. J Neurochem 122:702–713

    Article  CAS  PubMed  Google Scholar 

  146. Pacheco MA, Jope RS (1997) Comparison of [3H]phosphatidylinositol and [3H]phosphatidylinositol 4,5- bisphosphate hydrolysis in postmortem human brain membranes and characterization of stimulation by dopamine D1 receptors. J Neurochem 69:639–644

    Article  CAS  PubMed  Google Scholar 

  147. Perreault ML, Hasbi A, O'Dowd BF, George SR (2014) Heteromeric dopamine receptor signaling complexes: emerging neurobiology and disease relevance. Neuropsychopharmacology 39:156–168

    Article  CAS  PubMed  Google Scholar 

  148. Undie AS, Friedman E (1990) Stimulation of a dopamine D1 receptor enhances inositol phosphates formation in rat brain. J Pharmacol Exp Ther 253:987–992

    CAS  PubMed  Google Scholar 

  149. Undie AS, Friedman E (1992) Selective dopaminergic mechanism of dopamine and SKF38393 stimulation of inositol phosphate formation in rat brain. Eur J Pharmacol 226:297–302

    Article  CAS  PubMed  Google Scholar 

  150. Undie AS, Friedman E (1994) Inhibition of dopamine agonist-induced phosphoinositide hydrolysis by concomitant stimulation of cyclic AMP formation in brain slices. J Neurochem 63:222–230

    Article  CAS  PubMed  Google Scholar 

  151. Yu Y, Wang JR, Sun PH, Guo Y, Zhang ZJ, Jin GZ, Zhen X (2008) Neuroprotective effects of atypical D1 receptor agonist SKF83959 are mediated via D1 receptor-dependent inhibition of glycogen synthase kinase-3 beta and a receptor-independent anti-oxidative action. J Neurochem 104:946–956

    Article  CAS  PubMed  Google Scholar 

  152. Zhang X, Zhou Z, Wang D, Li A, Yin Y, Gu X, Ding F, Zhen X, Zhou J (2009) Activation of phosphatidylinositol-linked D1-like receptor modulates FGF-2 expression in astrocytes via IP3-dependent Ca2+ signaling. J Neurosci 29:7766–7775

    Article  CAS  PubMed  Google Scholar 

  153. Frederick AL, Yano H, Trifilieff P, Vishwasrao HD, Biezonski D, Mészáros J, Urizar E, Sibley DR, Kellendonk C, Sonntag KC, Graham DL, Colbran RJ, Stanwood GD, Javitch JA (2015) Evidence against dopamine D1/D2 receptor heteromers. Mol Psychiatry 20(11):1373–85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Lee SM, Kant A, Blake D, Murthy V, Boyd K, Wyrick SJ, Mailman RB (2014) SKF-83959 is not a highly-biased functionally selective D1 dopamine receptor ligand with activity at phospholipase C. Neuropharmacology 86:145–154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Lee SM, Yang Y, Mailman RB (2014) Dopamine D1 receptor signaling: does GαQ-phospholipase C actually play a role? J Pharmacol Exp Ther 351:9–17

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  156. Medvedev IO, Ramsey AJ, Masoud ST, Bermejo MK, Urs N, Sotnikova TD, Beaulieu JM, Gainetdinov RR, Salahpour A (2013) D1 dopamine receptor coupling to PLCβ regulates forward locomotion in mice. J Neurosci 33:18125–18133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Sahu A, Tyeryar KR, Vongtau HO, Sibley DR, Undieh AS (2009) D5 dopamine receptors are required for dopaminergic activation of phospholipase C. Mol Pharmacol 75:447–453

    Article  CAS  PubMed  Google Scholar 

  158. Aubert I, Ghorayeb I, Normand E, Bloch B (2000) Phenotypical characterization of the neurons expressing the D1 and D2 dopamine receptors in the monkey striatum. J Comp Neurol 418:22–32

    Article  CAS  PubMed  Google Scholar 

  159. Perreault ML, Hasbi A, Alijaniaram M, Fan T, Varghese G, Fletcher PJ, Seeman P, O'Dowd BF, George SR (2010) The dopamine D1-D2 receptor heteromer localizes in dynorphin/enkephalin neurons: increased high affinity state following amphetamine and in schizophrenia. J Biol Chem 285:36625–36634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Surmeier DJ, Song WJ, Yan Z (1996) Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. J Neurosci 16:6579–6591

    CAS  PubMed  Google Scholar 

  161. Testa CM, Standaert DG, Landwehrmeyer GB, Penney JBJ, Young AB (1995) Differential expression of mGluR5 metabotropic glutamate receptor mRNA by rat striatal neurons. J Comp Neurol 354:241–252

    Article  CAS  PubMed  Google Scholar 

  162. Testa CM, Friberg IK, Weiss SW, Standaert DG (1998) Immunohistochemical localization of metabotropic glutamate receptors mGluR1a and mGluR2/3 in the rat basal ganglia. J Comp Neurol 390:5–19

    Article  CAS  PubMed  Google Scholar 

  163. Paquet M, Smith Y (2003) Group I metabotropic glutamate receptors in the monkey striatum: subsynaptic association with glutamatergic and dopaminergic afferents. J Neurosci 23:7659–7669

    CAS  PubMed  Google Scholar 

  164. Smith Y, Charara A, Hanson JE, Paquet M, Levey AI (2000) GABA(B) and group I metabotropic glutamate receptors in the striatopallidal complex in primates. J Anat 196:555–576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Mela F, Marti M, Dekundy A, Danysz W, Morari M, Cenci MA (2007) Antagonism of metabotropic glutamate receptor type 5 attenuates l-DOPA-induced dyskinesia and its molecular and neurochemical correlates in a rat model of Parkinson's disease. J Neurochem 101:483–497

    Article  CAS  PubMed  Google Scholar 

  166. Rylander D, Recchia A, Mela F, Dekundy A, Danysz W, Cenci MA (2009) Pharmacological modulation of glutamate transmission in a rat model of L-DOPA-induced dyskinesia: effects on motor behavior and striatal nuclear signaling. J Pharmacol Exp Ther 330:227–235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Bubser M, Backstrom JR, Sanders-Bush E, Roth BL, Deutch AY (2001) Distribution of serotonin 5-HT2A receptors in afferents of the rat striatum. Synapse 39:297–304

    Article  CAS  PubMed  Google Scholar 

  168. Huot P, Fox SH, Newman-Tancredi A, Brotchie JM (2011) Anatomically selective serotonergic type 1A and serotonergic type 2A therapies for Parkinson’s disease: an approach to reducing dyskinesia without exacerbating parkinsonism? J Pharmacol Exp Ther 339:2–8

    Article  CAS  PubMed  Google Scholar 

  169. Calabresi P, Centonze D, Gubellini P, Pisani A, Bernardi G (2000) Acetylcholine-mediated modulation of striatal function. Trends Neurosci 23:120–126

    Article  CAS  PubMed  Google Scholar 

  170. Pisani A, Bernardi G, Ding J, Surmeier DJ (2007) Re-emergence of striatal cholinergic interneurons in movement disorders. Trends Neurosci 30:545–553

    Article  CAS  PubMed  Google Scholar 

  171. Santini E, Feyder M, Gangarossa G, Bateup HS, Greengard P, Fisone G (2012) Dopamine- and cAMP-regulated phosphoprotein of 32-kDa (DARPP-32)-dependent activation of extracellular signal-regulated kinase (ERK) and mammalian target of rapamycin complex 1 (mTORC1) signaling in experimental parkinsonism. J Biol Chem 287:27806–27812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Alcacer C, Santini E, Valjent E, Gaven F, Girault JA, Hervé D (2012) Gα(olf) mutation allows parsing the role of cAMP-dependent and extracellular signal-regulated kinase-dependent signaling in L-3,4-dihydroxyphenylalanine-induced dyskinesia. J Neurosci 32:5900–5910

    Article  CAS  PubMed  Google Scholar 

  173. Fasano S, Bezard E, D'Antoni A, Francardo V, Indrigo M, Qin L, Doveró S, Cerovic M, Cenci MA, Brambilla R (2010) Inhibition of Ras-guanine nucleotide-releasing factor 1 (Ras-GRF1) signaling in the striatum reverts motor symptoms associated with L-dopa-induced dyskinesia. Proc Natl Acad Sci U S A 107:21824–21829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Akerboom J, Chen TW, Wardill TJ, Tian L, Marvin JS, Mutlu S, Calderón NC, Esposti F, Borghuis BG, Sun XR, Gordus A, Orger MB, Portugues R, Engert F, Macklin JJ, Filosa A, Aggarwal A, Kerr RA, Takagi R, Kracun S, Shigetomi E, Khakh BS, Baier H, Lagnado L, Wang SS, Bargmann CI, Kimmel BE, Jayaraman V, Svoboda K, Kim DS, Schreiter ER, Looger LL (2012) Optimization of a GCaMP calcium indicator for neural activity imaging. J Neurosci 32:13819–13840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Santini E, Alcacer C, Cacciatore S, Heiman M, Hervé D, Greengard P, Girault JA, Valjent E, Fisone G (2009) L-DOPA activates ERK signaling and phosphorylates histone H3 in the striatonigral medium spiny neurons of hemiparkinsonian mice. J Neurochem 108:621–633

    Article  CAS  PubMed  Google Scholar 

  176. Westin JE, Vercammen L, Strome EM, Konradi C, Cenci MA (2007) Spatiotemporal pattern of striatal ERK1/2 phosphorylation in a rat model of L-DOPA-induced dyskinesia and the role of dopamine D1 receptors. Biol Psychiatry 62:800–810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Xiao K, McClatchy DB, Shukla AK, Zhao Y, Chen M, Shenoy SK, Yates JR 3rd, Lefkowitz RJ (2007) Functional specialization of beta-arrestin interactions revealed by proteomic analysis. Proc Natl Acad Sci U S A 104(29):12011–12016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Armentero MT, Pinna A, Ferré S, Lanciego JL, Müller CE, Franco R (2011) Past, present and future of A(2A) adenosine receptor antagonists in the therapy of Parkinson’s disease. Pharmacol Ther 132:280–299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Fredduzzi S, Moratalla R, Monopoli A, Cuellar B, Xu K, Ongini E, Impagnatiello F, Schwarzschild MA, Chen JF (2002) Persistent behavioral sensitization to chronic L-DOPA requires A2A adenosine receptors. J Neurosci 22:1054–1062

    CAS  PubMed  Google Scholar 

  180. Bibbiani F, Oh JD, Chase TN (2001) Serotonin 5-HT1A agonist improves motor complications in rodent and primate Parkinsonian models. Neurology 57:1829–1834

    Article  CAS  PubMed  Google Scholar 

  181. Dupre KB, Eskow KL, Barnum CJ, Bishop C (2008) Striatal 5-HT1A receptor stimulation reduces D1 receptor-induced dyskinesia and improves movement in the hemiparkinsonian rat. Neuropharmacology 55:1321–1328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  182. Dupre KB, Ostock CY, Eskow Jaunarajs KL, Button T, Savage LM, Wolf W, Bishop C (2011) Local modulation of striatal glutamate efflux by serotonin 1A receptor stimulation in dyskinetic, hemiparkinsonian rat. Exp Neurol 229:288–299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  183. Dupre KB, Ostock CY, George JA, Eskow Jaunarajs KL, Hueston CM, Bishop C (2013) Effects of 5-HT receptor stimulation on D1 receptor agonist-induced striatonigral activity and dyskinesia in hemiparkinsonian rats. ACS Chem Neurosci 4:747–760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Iderberg H, Rylander D, Bimpisidis Z, Cenci MA (2013) Modulating mGluR5 and 5-HT1A/1B receptors to treat l-DOPA-induced dyskinesia: effects of combined treatment and possible mechanisms of action. Exp Neurol 250:116–124

    Article  CAS  PubMed  Google Scholar 

  185. Zhang X, Andren PE, Greengard P, Svenningsson P (2008) Evidence for a role of the 5-HT1B receptor and its adaptor protein, p11, in l-DOPA treatment of an animal model of Parkinsonism. Proc Natl Acad Sci U S A 105:2163–2168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Chen L, Togasaki DM, Langston JW, Di Monte DA, Quik M (2005) Enhanced striatal opioid receptor-mediated G-protein activation in L-DOPA-treated dyskinetic monkeys. Neuroscience 132:409–420

    Article  CAS  PubMed  Google Scholar 

  187. Cox H, Togasaki DM, Chen L, Langston JW, Di Monte DA, Quik M (2007) The selective kappa-opioid receptor agonist U50,488 reduces L-dopa-induced dyskinesias but worsens Parkinsonism in MPTP-treated primates. Exp Neurol 205:101–107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  188. Henrya B, Foxb SH, Crossmanb AR, Brotchieb JM (2001) μ- and δ-opioid receptor antagonists reduce levodopa-induced dyskinesia in the MPTP-lesioned primate model of Parkinson’s disease. Exp Neurol 171:139–146

    Article  CAS  Google Scholar 

  189. Cao X, Yasuda T, Uthayathas S, Watts RL, Mouradian MM, Mochizuki H, Papa SM (2010) Striatal overexpression of DeltaFosB reproduces chronic levodopa-induced involuntary movements. J Neurosci 30:7335–7343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  190. Berton O, Guigoni C, Li Q, Bioulac BH, Aubert I, Gross CE, Dileone RJ, Nestler EJ, Bezard E (2009) Striatal overexpression of DeltaJunD resets L-DOPA-induced dyskinesia in a primate model of Parkinson disease. Biol Psychiatry 66:554–561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  191. Engeln M, Bastide MF, Toulmé E, Dehay B, Bourdenx M, Doudnikoff E, Li Q, Gross CE, Boué-Grabot E, Pisani A, Bezard E, Fernagut PO (2016) Selective inactivation of striatal FosB/ΔFosB-expressing neurons alleviates l-dopa-induced dyskinesia. Biol Psychiatry 79(5):354–61

    Article  CAS  PubMed  Google Scholar 

  192. Cenci MA (2002) Transcription factors involved in the pathogenesis of L-DOPA-induced dyskinesia in a rat model of Parkinson’s disease. Amino Acids 23:105–109

    Article  CAS  PubMed  Google Scholar 

  193. Ding WQ, Larsson C, Alling C (1998) Stimulation of muscarinic receptors induces expression of individual Fos and Jun genes through different transduction pathways. J Neurochem 70:1722–1729

    Article  CAS  PubMed  Google Scholar 

  194. Robison AJ, Vialou V, Mazei-Robison M, Feng J, Kourrich S, Collins M, Wee S, Koob G, Turecki G, Neve R, Thomas M, Nestler EJ (2013) Behavioral and structural responses to chronic cocaine require a feedforward loop involving ΔFosB and calcium/calmodulin-dependent protein kinase II in the nucleus accumbens shell. J Neurosci 33:4295–4307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  195. Beaulieu JM, Espinoza S, Gainetdinov RR (2015) Dopamine receptors – IUPHAR Review 13. Br J Pharmacol 172:1–23

    Article  CAS  PubMed  Google Scholar 

  196. United Nations Office on Drugs and Crime (2014) World drug report 2014. United Nations Office on Drugs and Crime, Vienna

    Google Scholar 

  197. Robison AJ, Nestler EJ (2011) Transcriptional and epigenetic mechanisms of addiction. Nat Rev Neurosci 12:623–637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  198. Beaulieu J-M, Tirotta E, Sotnikova TD, Masri B, Salahpour A, Gainetdinov RR, Borrelli E, Caron MG (2007) Regulation of Akt signaling by D2 and D3 dopamine receptors in vivo. J Neurosci 27(4):881–885

    Article  CAS  PubMed  Google Scholar 

  199. Beaulieu JM, Gainetdinov RR, Caron MG (2007) The Akt-GSK-3 signaling cascade in the actions of dopamine. Trends Pharmacol Sci 28:166–172

    Article  CAS  PubMed  Google Scholar 

  200. Beaulieu JM, Sotnikova TD, Marion S, Lefkowitz RJ, Gainetdinov RR, Caron MG (2005) An Akt/beta-arrestin 2/PP2A signaling complex mediates dopaminergic neurotransmission and behavior. Cell 122:261–273

    Article  CAS  PubMed  Google Scholar 

  201. Kordower JH, Olanow CW, Dodiya HB, Chu Y, Beach TG, Adler CH, Halliday GM, Bartus RT (2013) Disease duration and the integrity of the nigrostriatal system in Parkinson’s disease. Brain 136:2419–2431

    Article  PubMed  PubMed Central  Google Scholar 

  202. Murer MG, Moratalla R (2011) Striatal signaling in l-DOPA-induced dyskinesia: common mechanisms with drug abuse and long term memory involving D1 dopamine receptor stimulation. Front Neuroanat 5:51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Pharmacology, Vanderbilt University, Preston Research Building, Room 417C, 2200 Pierce Avenue, Nashville, TN, 37221, USA

    Eugenia V. Gurevich & Vsevolod V. Gurevich

  2. Institute of Translational Biomedicine, St. Petersburg State University, St. Petersburg, 199034, Russia

    Raul R. Gainetdinov

  3. Skolkovo Institute of Science and Technology, Skolkovo, 143025, Moscow Region, Russia

    Raul R. Gainetdinov

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  1. Eugenia V. Gurevich
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  2. Raul R. Gainetdinov
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  3. Vsevolod V. Gurevich
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Correspondence to Eugenia V. Gurevich .

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Editors and Affiliations

  1. Department of Pharmacology, Vanderbilt University , NASHVILLE, Tennessee, USA

    Vsevolod V. Gurevich

  2. Department of Pharmacology, Vanderbilt University, Nashville, Tennessee, USA

    Eugenia V. Gurevich

  3. Life Sciences Institute, University of Michigan, Ann Arbor, Michigan, USA

    John J.G. Tesmer

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Gurevich, E.V., Gainetdinov, R.R., Gurevich, V.V. (2016). Regulation of Dopamine-Dependent Behaviors by G Protein-Coupled Receptor Kinases. In: Gurevich, V., Gurevich, E., Tesmer, J. (eds) G Protein-Coupled Receptor Kinases. Methods in Pharmacology and Toxicology. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-3798-1_11

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  • DOI: https://doi.org/10.1007/978-1-4939-3798-1_11

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