Dopamine Receptor Interacting Proteins (DRIPs) of Dopamine D1-like Receptors in the Central Nervous System

  • Wang, Min (Department of Neuroscience, Centre for Addiction and Mental Health) ;
  • Lee, Frank J.S. (Department of Neuroscience, Centre for Addiction and Mental Health) ;
  • Liu, Fang (Department of Neuroscience, Centre for Addiction and Mental Health)
  • Received : 2008.03.25
  • Accepted : 2008.03.27
  • Published : 2008.04.30

Abstract

Dopamine is a major neurotransmitter in the mammalian central nervous system (CNS) that regulates neuroendocrine functions, locomotor activity, cognition and emotion. The dopamine system has been extensively studied because dysfunction of this system is linked to various pathological conditions including Parkinson's disease, schizophrenia, Tourette's syndrome, and drug addiction. Accordingly, intense efforts to delineate the full complement of signaling pathways mediated by individual receptor subtypes have been pursued. Dopamine D1-like receptors are of particular interest because they are the most abundant dopamine receptors in CNS. Recent work suggests that dopamine signaling could be regulated via dopamine receptor interacting proteins (DRIPs). Unraveling these DRIPs involved in the dopamine system may provide a better understanding of the mechanisms underlying CNS disorders related to dopamine system dysfunction and may help identify novel therapeutic targets.

Keywords

References

  1. Aebersold, R., and Mann, M. (2003). Mass spectrometry-based proteomics. Nature 422, 198-207 https://doi.org/10.1038/nature01511
  2. Agnati, L.F., Fuxe, K., Benfenati, F., Celani, M.F., Battistini, N., Mutt, V., Cavicchioli, L., Galli, G., and Hokfelt, T. (1983). Differential modulation by CCK-8 and CCK-4 of 3H spiperone binding sites linked to dopamine and 5-hydroxytryptamine receptors in the brain of the rat. Neurosci. Lett 35, 179-183 https://doi.org/10.1016/0304-3940(83)90547-5
  3. Bai, M. (2004). Dimerization of G-protein-coupled receptors: roles in signal transduction. Cell Signal 16, 175-186 https://doi.org/10.1016/S0898-6568(03)00128-1
  4. Barnard, E.A., Skolnick, P., Olsen, R.W., Mohler, H., Sieghart, W., Biggio, G., Braestrup, C., Bateson, A.N., and Langer, S.Z. (1998). International union of pharmacology. XV. Subtypes of gamma-aminobutyric acidA receptors: classification on the basis of subunit structure and receptor function. Pharmacol. Rev. 50, 291-313
  5. Bergson, C., Levenson, R., Goldman-Rakic, P.S., and Lidow, M.S. (2003). Dopamine receptor-interacting proteins: the Ca(2+) connection in dopamine signaling. Trends Pharmacol. Sci. 24, 486-492 https://doi.org/10.1016/S0165-6147(03)00232-3
  6. Bermak, J.C., Li, M., Bullock, C., Weingarten, P., and Zhou, Q.Y. (2002). Interaction of gamma-COP with a transport motif in the D1 receptor C-terminus. Eur. J. Cell Biol. 81, 77-85 https://doi.org/10.1078/0171-9335-00222
  7. Bermak, J.C., Li, M., Bullock, C., and Zhou, Q.Y. (2001). Regulation of transport of the dopamine D1 receptor by a new membrane-associated ER protein. Nat. Cell Biol. 3, 492-498 https://doi.org/10.1038/35074561
  8. Bouvier, M. (2001). Oligomerization of G-protein-coupled transmitter receptors. Nat. Rev. Neurosci. 2, 274-286 https://doi.org/10.1038/35067575
  9. Bozzi, Y., and Borrelli, E. (2006). Dopamine in neurotoxicity and neuroprotection: what do D2 receptors have to do with it? Trends Neurosci. 29, 167-174 https://doi.org/10.1016/j.tins.2006.01.002
  10. Breitwieser, G.E. (2004). G protein-coupled receptor oligomerization: implications for G protein activation and cell signaling. Circ. Res. 94, 17-27 https://doi.org/10.1161/01.RES.0000110420.68526.19
  11. Chini, B., and Parenti, M. (2004) G-protein coupled receptors in lipid rafts and caveolae: how, when and why do they go there? J. Mol. Endocrinol. 32, 325-338 https://doi.org/10.1677/jme.0.0320325
  12. Choi, D.W. (1988). Glutamate neurotoxicity and diseases of the nervous system. Neuron 1, 623-634 https://doi.org/10.1016/0896-6273(88)90162-6
  13. Conn, P.M., Ulloa-Aguirre, A., Ito, J., and Janovick, J.A. (2007). G protein-coupled receptor trafficking in health and disease: lessons learned to prepare for therapeutic mutant rescue in vivo. Pharmacol. Rev. 59, 225-250 https://doi.org/10.1124/pr.59.3.2
  14. Dziedzicka-Wasylewska, M., Faron-Gorecka, A., Andrecka, J., Polit, A., Kusmider, M., and Wasylewski, Z. (2006). Fluorescence studies reveal heterodimerization of dopamine D1 and D2 receptors in the plasma membrane. Biochemistry 45, 8751-8759 https://doi.org/10.1021/bi060702m
  15. Elmhurst, J.L., Xie, Z., O'Dowd, B.F., and George, S.R. (2000). The splice variant D3nf reduces ligand binding to the D3 dopamine receptor: evidence for heterooligomerization. Brain Res. Mol. Brain Res. 80, 63-74 https://doi.org/10.1016/S0169-328X(00)00120-0
  16. Ferre, S., Fredholm, B.B., Morelli, M., Popoli, P., and Fuxe, K. (1997). Adenosine-dopamine receptor-receptor interactions as an integrative mechanism in the basal ganglia. Trends Neurosci. 20, 482-487 https://doi.org/10.1016/S0166-2236(97)01096-5
  17. Fiorentini, C., Gardoni, F., Spano, P., Di Luca, M., and Missale, C. (2003). Regulation of dopamine D1 receptor trafficking and desensitization by oligomerization with glutamate Nmethyl-D-aspartate receptors. J. Biol. Chem. 278, 20196-20202 https://doi.org/10.1074/jbc.M213140200
  18. Gines, S., Hillion, J., Torvinen, M., Le Crom, S., Casado, V., Canela, E.I., Rondin, S., Lew, J.Y., Watson, S., Zoli, M., et al. (2000). Dopamine D1 and adenosine A1 receptors form functionally interacting heteromeric complexes. Proc. Natl. Acad. Sci. USA 97, 8606-8611
  19. Goldman-Rakic, P.S. (1998). The cortical dopamine system: role in memory and cognition. Adv. Pharmacol. 42, 707-711
  20. Goldman-Rakic, P.S., Muly, E.C. 3rd., and Williams, G.V. (2000). D(1) receptors in prefrontal cells and circuits. Brain Res. Brain Res. Rev. 31, 295-301 https://doi.org/10.1016/S0165-0173(99)00045-4
  21. Greengard, P. (2001). The neurobiology of slow synaptic transmission. Science 294, 1024-1030 https://doi.org/10.1126/science.294.5544.1024
  22. Gu, W.H., Yang, S., Shi, W.X., Jin, G.Z., and Zhen, X.C. (2007). Requirement of PSD-95 for dopamine D1 receptor modulating glutamate NR1a/NR2B receptor function. Acta Pharmacol. Sin. 28, 756-762 https://doi.org/10.1111/j.1745-7254.2007.00557.x
  23. Hammond, C., Braakman, I., and Helenius, A. (1994). Role of N-linked oligosaccharide recognition, glucose trimming, and calnexin in glycoprotein folding and quality control. Proc. Natl. Acad. Sci. USA 91, 913-917
  24. Heydorn, A., Sondergaard, B.P., Hadrup, N., Holst, B., Haft, C.R., and Schwartz, T.W. (2004). Distinct in vitro interaction pattern of dopamine receptor subtypes with adaptor proteins involved in post-endocytotic receptor targeting. FEBS Lett. 556, 276-280 https://doi.org/10.1016/S0014-5793(03)01431-5
  25. Hillion, J., Canals, M., Torvinen, M., Casado, V., Scott, R., Terasmaa, A., Hansson, A., Watson, S., Olah, M.E., Mallol, J., et al. (2002). Coaggregation, cointernalization, and codesensitization of adenosine A2A receptors and dopamine D2 receptors. J. Biol. Chem. 277, 18091-18097 https://doi.org/10.1074/jbc.M107731200
  26. Kanda, T., Jackson, M.J., Smith, L.A., Pearce, R.K., Nakamura, J., Kase, H., Kuwana, Y., and Jenner, P. (1998). Adenosine A2A antagonist: a novel antiparkinsonian agent that does not provoke dyskinesia in parkinsonian monkeys. Ann. Neurol. 43, 507-513 https://doi.org/10.1002/ana.410430415
  27. Karpa, K.D., Lin, R., Kabbani, N., and Levenson, R. (2000). The dopamine D3 receptor interacts with itself and the truncated D3 splice variant d3nf: D3-D3nf interaction causes mislocalization of D3 receptors. Mol. Pharmacol. 58, 677-683 https://doi.org/10.1124/mol.58.4.677
  28. Kim, E., and Sheng, M. (2004). PDZ domain proteins of synapses. Nat. Rev. Neurosci. 5, 771-781 https://doi.org/10.1038/nrn1517
  29. Kim, O.J., Ariano, M.A., Lazzarini, R.A., Levine, M.S., and Sibley, D.R. (2002). Neurofilament-M interacts with the D1 dopamine receptor to regulate cell surface expression and desensitization. J. Neurosci. 22, 5920-5930 https://doi.org/10.1523/JNEUROSCI.22-14-05920.2002
  30. Kim, O.J., Gardner, B.R., Williams, D.B., Marinec, P.S., Cabrera, D.M., Peters, J.D., Mak, C.C., Kim, K.M., and Sibley, D.R. (2004). The role of phosphorylation in D1 dopamine receptor desensitization: evidence for a novel mechanism of arrestin association. J. Biol. Chem. 279, 7999-8010 https://doi.org/10.1074/jbc.M308281200
  31. Kong, M.M., Fan, T., Varghese, G., O'Dowd, B.F., and George, S.R. (2006). Agonist-induced cell surface trafficking of an intracellularly sequestered D1 dopamine receptor homooligomer. Mol. Pharmacol. 70, 78-89
  32. Kong, M.M., Hasbi, A., Mattocks, M., Fan, T., O'Dowd, B.F., and George, S.R. (2007). Regulation of D1 dopamine receptor trafficking and signaling by caveolin-1. Mol. Pharmacol. 72, 1157-1170 https://doi.org/10.1124/mol.107.034769
  33. Kornau, H.C., Schenker, L.T., Kennedy, M.B., and Seeburg, P.H. (1995). Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269, 1737-1740 https://doi.org/10.1126/science.7569905
  34. Kroeger, K.M., Pfleger, K.D., and Eidne, K.A. (2003). G-protein coupled receptor oligomerization in neuroendocrine pathways. Front. Neuroendocrinol. 24, 254-278 https://doi.org/10.1016/j.yfrne.2003.10.002
  35. Lavine, N., Ethier, N., Oak, J.N., Pei, L., Liu, F., Trieu, P., Rebois, R.V., Bouvier, M., Hebert, T.E., and Van Tol, H.H. (2002). G protein-coupled receptors form stable complexes with inwardly rectifying potassium channels and adenylyl cyclase. J. Biol. Chem. 277, 46010-46019 https://doi.org/10.1074/jbc.M205035200
  36. Lee, F.J., and Liu, F. (2004). Direct interactions between NMDA and D1 receptors: a tale of tails. Biochem. Soc. Trans. 32(Pt 6), 1032-1036 https://doi.org/10.1042/BST0321032
  37. Lee, F.J., Xue, S., Pei, L., Vukusic, B., Chery, N., Wang, Y., Wang, Y.T., Niznik, H.B., Yu, X.M., and Liu, F. (2002). Dual regulation of NMDA receptor functions by direct proteinprotein interactions with the dopamine D1 receptor. Cell 111, 219-230 https://doi.org/10.1016/S0092-8674(02)00962-5
  38. Lee, S.P., O'Dowd, B.F., Ng, G.Y., Varghese, G., Akil, H., Mansour, A., Nguyen, T., and George, S.R. (2000). Inhibition of cell surface expression by mutant receptors demonstrates that D2 dopamine receptors exist as oligomers in the cell. Mol. Pharmacol. 58, 120-128 https://doi.org/10.1124/mol.58.1.120
  39. Lee, S.P., So, C.H., Rashid, A.J., Varghese, G., Cheng, R., Lanca, A.J., O'Dowd, B.F., and George, S.R. (2004). Dopamine D1 and D2 receptor co-activation generates a novel phospholipase C-mediated calcium signal. J. Biol. Chem. 279, 35671-35678 https://doi.org/10.1074/jbc.M401923200
  40. Li, Z., Benard, O., and Margolskee, R.F. (2006). Ggamma13 interacts with PDZ domain-containing proteins. J. Biol. Chem. 281, 11066-11073 https://doi.org/10.1074/jbc.M600113200
  41. Liu, F., Wan, Q., Pristupa, Z.B., Yu, X.M., Wang, Y.T., and Niznik, H.B. (2000). Direct protein-protein coupling enables cross-talk between dopamine D5 and gamma-aminobutyric acid A receptors. Nature 403, 274-280 https://doi.org/10.1038/35002014
  42. Luttrell, L.M., Roudabush, F.L., Choy, E.W., Miller, W.E., Field, M.E., Pierce, K.L., and Lefkowitz, R.J. (2001). Activation and targeting of extracellular signal-regulated kinases by beta-arrestin scaffolds. Proc. Natl. Acad. Sci. USA 98, 2449-2454
  43. Macdonald, R.L., and Olsen, R.W. (1994). GABAA receptor channels. Annu. Rev. Neurosci. 17, 569-602 https://doi.org/10.1146/annurev.ne.17.030194.003033
  44. Macey, T.A., Liu, Y., Gurevich, V.V., and Neve, K.A. (2005). Dopamine D1 receptor interaction with arrestin3 in neostriatal neurons. J. Neurochem. 93, 128-134 https://doi.org/10.1111/j.1471-4159.2004.02998.x
  45. Mason, J.N., Kozell L.B., and Neve K.A. (2002). Regulation of dopamine D(1) receptor trafficking by protein kinase Adependent phosphorylation. Mol. Pharmacol. 61, 806-816 https://doi.org/10.1124/mol.61.4.806
  46. Molinari, M., Eriksson, K.K., Calanca, V., Galli, C., Cresswell P., Michalak M., and Helenius, A. (2004). Contrasting functions of calreticulin and calnexin in glycoprotein folding and ER quality control. Mol. Cell 13, 125-135 https://doi.org/10.1016/S1097-2765(03)00494-5
  47. Neve, K.A., Seamans, J.K., and Trantham-Davidson, H. (2004). Dopamine receptor signaling. J. Recept. Signal Transduct. Res. 24, 165-205 https://doi.org/10.1081/RRS-200029981
  48. Ng, G.Y., George, S.R., Zastawny, R.L., Caron, M., Bouvier, M., Dennis, M., and O'Dowd, B.F. (1993). Human serotonin1B receptor expression in Sf9 cells: phosphorylation, palmitoylation, and adenylyl cyclase inhibition. Biochemistry 32, 11727-11733 https://doi.org/10.1021/bi00094a032
  49. Ng, G.Y., O'Dowd, B.F., Caron, M., Dennis, M., Brann, M.R., and George, S.R. (1994). Phosphorylation and palmitoylation of the human D2L dopamine receptor in Sf9 cells. J. Neurochem. 63, 1589-1595 https://doi.org/10.1046/j.1471-4159.1994.63051589.x
  50. Niethammer, M., Kim, E., and Sheng, M. (1996). Interaction between the C terminus of NMDA receptor subunits and multiple members of the PSD-95 family of membraneassociated guanylate kinases. J. Neurosci. 16, 2157-2163 https://doi.org/10.1523/JNEUROSCI.16-07-02157.1996
  51. Nimchinsky, E.A., Hof, P.R., Janssen, W.G., Morrison, J.H., and Schmauss, C. (1997). Expression of dopamine D3 receptor dimers and tetramers in brain and in transfected cells. J. Biol. Chem. 272, 29229-29237 https://doi.org/10.1074/jbc.272.46.29229
  52. O'Dowd, B.F., Ji, X., Alijaniaram, M., Rajaram, R.D., Kong, M.M., Rashid, A., Nguyen, T., and George, S.R. (2005). Dopamine receptor oligomerization visualized in living cells. J. Biol. Chem. 280, 37225-37235 https://doi.org/10.1074/jbc.M504562200
  53. Pei, L., Lee, F.J., Moszczynska, A., Vukusic, B., and Liu, F. (2004). Regulation of dopamine D1 receptor function by physical interaction with the NMDA receptors. J. Neurosci. 24, 1149-1158 https://doi.org/10.1523/JNEUROSCI.3922-03.2004
  54. Pippig, S., Andexinger, S., and Lohse, M.J. (1995). Sequestration and recycling of beta 2-adrenergic receptors permit receptor resensitization. Mol. Pharmacol. 47, 666-676
  55. Poisbeau, P., Cheney, M.C., Browning, M.D., and Mody, I. (1999). Modulation of synaptic GABAA receptor function by PKA and PKC in adult hippocampal neurons. J. Neurosci. 19, 674-683 https://doi.org/10.1523/JNEUROSCI.19-02-00674.1999
  56. Radnikow, G., and Misgeld, U. (1998). Dopamine D1 receptors facilitate GABAA synaptic currents in the rat substantia nigra pars reticulata. J. Neurosci. 18, 2009-2016 https://doi.org/10.1523/JNEUROSCI.18-06-02009.1998
  57. Rapacciuolo, A., Suvarna, S., Barki-Harrington, L., Luttrell, L.M., Cong, M., Lefkowitz, R.J., and Rockman, H.A. (2003). Protein kinase A and G protein-coupled receptor kinase phosphorylation mediates beta-1 adrenergic receptor endocytosis through different pathways. J. Biol. Chem. 278, 35403-35411 https://doi.org/10.1074/jbc.M305675200
  58. Rashid, A.J., So, C.H., Kong, M.M., Furtak, T., El-Ghundi, M., Cheng, R., O'Dowd, B.F., and George, S.R. (2007) D1-D2 dopamine receptor heterooligomers with unique pharmacology are coupled to rapid activation of Gq/11 in the striatum. Proc. Natl. Acad. Sci. USA 104, 654-659
  59. Rimondini, R., Ferre, S., Ogren, S.O., and Fuxe, K. (1997). Adenosine A2A agonists: a potential new type of atypical antipsychotic. Neuropsychopharmacology 17, 82-91 https://doi.org/10.1016/S0893-133X(97)00033-X
  60. Rocheville, M., Lange, D.C., Kumar, U., Patel, S.C., Patel, R.C., and Patel, Y.C. (2000). Receptors for dopamine and somatostatin: formation of hetero-oligomers with enhanced functional activity. Science 288, 154-157 https://doi.org/10.1126/science.288.5463.154
  61. Roseberry, A.G., and Hosey, M.M. (2001). Internalization of the M2 muscarinic acetylcholine receptor proceeds through an atypical pathway in HEK293 cells that is independent of clathrin and caveolae. J. Cell Sci. 114(Pt 4), 739-746
  62. Scarselli, M., Novi, F., Schallmach, E., Lin, R., Baragli, A., Colzi, A., Griffon, N., Corsini, G.U., Sokoloff, P., Levenson, R., et al. (2001). D2/D3 dopamine receptor heterodimers exhibit unique functional properties. J. Biol. Chem. 276, 30308-30314 https://doi.org/10.1074/jbc.M102297200
  63. Schultz, W. (2002). Getting formal with dopamine and reward. Neuron 36, 241-263 https://doi.org/10.1016/S0896-6273(02)00967-4
  64. Scott, L., Kruse, M.S., Forssberg, H., Brismar, H., Greengard, P., and Aperia, A. (2002). Selective up-regulation of dopamine D1 receptors in dendritic spines by NMDA receptor activation. Proc. Natl. Acad. Sci. USA 99, 1661-1664
  65. Scott, L., Zelenin, S., Malmersjo, S., Kowalewski, J.M., Markus, E.Z., Nairn, A.C., Greengard, P., Brismar, H., and Aperia, A. (2006). Allosteric changes of the NMDA receptor trap diffusible dopamine 1 receptors in spines. Proc. Natl. Acad. Sci. USA 103, 762-767
  66. Smart, T.G. (1997). Regulation of excitatory and inhibitory neurotransmitter- gated ion channels by protein phosphorylation. Curr. Opin. Neurobiol. 7, 358-367 https://doi.org/10.1016/S0959-4388(97)80063-3
  67. So, C.H., Varghese, G., Curley, K.J., Kong, M.M., Alijaniaram, M., Ji, X., Nguyen, T., O'Dowd, B.F., and George, S.R. (2005). D1 and D2 dopamine receptors form heterooligomers and cointernalize after selective activation of either receptor. Mol. Pharmacol. 68, 568-578
  68. So, C.H., Verma, V., O'Dowd, B.F., and George, S.R. (2007). Desensitization of the dopamine D1 and D2 receptor heterooligomer mediated calcium signal by agonist occupancy of either receptor. Mol. Pharmacol. 72, 450-462 https://doi.org/10.1124/mol.107.034884
  69. Solanto, M.V. (2002). Dopamine dysfunction in AD/HD: integrating clinical and basic neuroscience research. Behav. Brain Res. 130, 65-71 https://doi.org/10.1016/S0166-4328(01)00431-4
  70. Swanton, E., High, S., and Woodman, P. (2003). Role of calnexin in the glycan-independent quality control of proteolipid protein. EMBO J. 22, 2948-2958 https://doi.org/10.1093/emboj/cdg300
  71. Tsao, P., Cao, T., and von Zastrow, M. (2001). Role of endocytosis in mediating downregulation of G-protein-coupled receptors. Trends Pharmacol. Sci. 22, 91-96
  72. Undie, A.S., Weinstock, J., Sarau, H.M., and Friedman, E. (1994). Evidence for a distinct D1-like dopamine receptor that couples to activation of phosphoinositide metabolism in brain. J. Neurochem. 62, 2045-2048 https://doi.org/10.1046/j.1471-4159.1994.62052045.x
  73. Volkow, N.D., Fowler, J.S., and Wang, G.J. (2002). Role of dopamine in drug reinforcement and addiction in humans: results from imaging studies. Behav. Pharmacol. 13, 355-366 https://doi.org/10.1097/00008877-200209000-00008
  74. Yan, Z., and Surmeier, D.J. (1997). D5 dopamine receptors enhance Zn2+-sensitive GABA(A) currents in striatal cholinergic interneurons through a PKA/PP1 cascade. Neuron 19, 1115-1126 https://doi.org/10.1016/S0896-6273(00)80402-X
  75. Zeng, C., Wang, Z., Li, H., Yu, P., Zheng, S., Wu, L., Asico, L.D., Hopfer, U., Eisner, G.M., Felder, R.A., et al. (2006). D3 dopamine receptor directly interacts with D1 dopamine receptor in immortalized renal proximal tubule cells. Hypertension 47, 573-579 https://doi.org/10.1161/01.HYP.0000199983.24674.83
  76. Zhang, J., Vinuela, A., Neely, M.H., Hallett, P.J., Grant, S.G., Miller, G.M., Isacson, O., Caron, M.G., and Yao, W.D. (2007). Inhibition of the dopamine D1 receptor signaling by PSD-95. J. Biol. Chem. 282, 15778-15789 https://doi.org/10.1074/jbc.M611485200
  77. Zoli, M., Agnati, L.F., Hedlund, P.B., Li, X.M., Ferre, S., and Fuxe, K. (1993). Receptor-receptor interactions as an integrative mechanism in nerve cells. Mol. Neurobiol. 7, 293-334 https://doi.org/10.1007/BF02769180