Rhes regulates dopamine D2 receptor transmission in striatal cholinergic interneurons

Neurobiology of Disease

Volumn 78, Issue , 2015, Pages 146-161

  Sciamanna, Giuseppe ^a,b   Napolitano, Francesco ^c,d   Pelosi, Barbara ^e   Bonsi, Paola ^b   Vitucci, Daniela ^d,f   Nuzzo, Tommaso ^d   Punzo, Daniela ^d   Ghiglieri, Veronica ^g   Ponterio, Giulia ^a,b   Pasqualetti, Massimo ^e,h   Pisani, Antonio ^a,b   Usiello, Alessandro ^d,i  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^d CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^e UNIVERSITY OF PISA   (Italy)

^f UNIVERSITY OF NAPLES PARTHENOPE   (Italy)

^g UNIVERSITY OF PERUGIA   (Italy)

^h ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

ⁱ SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

Calcium; Cholinergic interneurons; D2 dopamine receptors; Dystonia; Rhes; Striatum

Indexed keywords

CALCIUM ION; CAV2.2 CALCIUM CHANNEL; DOPAMINE 2 RECEPTOR; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; GUANINE NUCLEOTIDE BINDING PROTEIN; NEUROPEPTIDE Y; PARVALBUMIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN RHES; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; MESSENGER RNA; PROTEIN KINASE B; RASD2 PROTEIN, HUMAN; RASD2 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL SPECIFICITY; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC TRANSMISSION; ENZYME INHIBITION; FEMALE; GABAERGIC SYSTEM; GENE; GENE EXPRESSION; GENE FUNCTION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN SITU HYBRIDIZATION; INTERNEURON; INTRACELLULAR SIGNALING; MALE; MOUSE; NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; RES GENE; ACTION POTENTIAL; ADOLESCENT; ADULT; ANIMAL; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ADOLESCENT; ADULT; ANIMALS; CHOLINERGIC NEURONS; CORPUS STRIATUM; FEMALE; GTP-BINDING PROTEINS; HUMANS; INTERNEURONS; MALE; MICE; MICE, KNOCKOUT; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, DOPAMINE D2; RNA, MESSENGER; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY; SYNAPTIC TRANSMISSION;

EID: 84927730062     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2015.03.021     Document Type: Article

References (60)

1. Agretti P., De Marco G., Pinchera A., Vitti P., Bernal J., Tonacchera M. Ras homolog enriched in striatum inhibits the functional activity of wild type thyrotropin, follicle-stimulating hormone, luteinizing hormone receptors and activating thyrotropin receptor mutations by altering their expression in COS-7 cells. J. Endocrinol. Investig. 2007, 30:279-284.
2. Alessi D.R., Deak M., Casamayor A., Caudwell F.B., Morrice N., Norman D.G., Gaffney P., Reese C.B., MacDougall C.N., Harbison D., Ashworth A., Bownes M. 3-Phosphoinositide-dependent protein kinase-1 (PDK1): structural and functional homology with the Drosophila DSTPK61 kinase. Curr. Biol. 1997, 7:776-789.
3. Aosaki T., Kiuchi K., Kawaguchi Y. Dopamine D1-like receptor activation excites rat striatal large aspiny neurons in vitro. J. Neurosci. Off. J. Soc. Neurosci. 1998, 18:5180-5190.
4. Baiamonte B.A., Lee F.A., Brewer S.T., Spano D., LaHoste G.J. Attenuation of Rhes activity significantly delays the appearance of behavioral symptoms in a mouse model of Huntington's disease. PLoS One 2013, 8:e53606. 10.1371/journal.pone.0053606.
5. Bang S., Steenstra C., Kim S.F. Striatum specific protein, Rhes regulates AKT pathway. Neurosci. Lett. 2012, 521:142-147.
6. Beaulieu J.M., Sotnikova T.D., Marion S., Lefkowitz R.J., Gainetdinov R.R., Caron M.G. An Akt/beta-arrestin 2/PP2A signaling complex mediates dopaminergic neurotransmission and behavior. Cell 2005, 122:261-273.
7. Bergson C., Mrzljak L., Smiley J.F., Pappy M., Levenson R., Goldman-Rakic P.S. Regional, cellular, and subcellular variations in the distribution of D1 and D5 dopamine receptors in primate brain. J. Neurosci. 1995, 15:7821-7836.
8. Calabresi P., Centonze D., Pisani A., Sancesario G., North R.A., Bernardi G. Muscarinic IPSPs in rat striatal cholinergic interneurones. J. Physiol. 1998, 510(Pt 2):421-427.
9. Chen H.-T., Ruan N.-Y., Chen J.-C., Lin T.-Y. Dopamine D2 receptor-mediated Akt/PKB signalling: initiation by the D2S receptor and role in quinpirole-induced behavioural activation. ASN Neuro 2012, 4:371-382.
10. DeBoer P., Heeringa M.J., Abercrombie E.D. Spontaneous release of acetylcholine in striatum is preferentially regulated by inhibitory dopamine D2 receptors. Eur. J. Pharmacol. 1996, 317:257-262.
11. Dhar V., Nandi A., Schildkraut C.L., Skoultchi A.I. Erythroid-specific nuclease-hypersensitive sites flanking the human beta-globin domain. Mol. Cell. Biol. 1990, 10:4324-4333.
12. Errico F., Santini E., Migliarini S., Borgkvist A., Centonze D., Nasti V., Carta M., De Chiara V., Prosperetti C., Spano D., Herve D., Pasqualetti M., Di Lauro R., Fisone G., Usiello A. The GTP-binding protein Rhes modulates dopamine signalling in striatal medium spiny neurons. Mol. Cell. Neurosci. 2008, 37:335-345.
13. Falk J.D., Vargiu P., Foye P.E., Usui H., Perez J., Danielson P.E., Lerner D.L., Bernal J., Sutcliffe J.G. Rhes: a striatal-specific Ras homolog related to Dexras1. J. Neurosci. Res. 1999, 57:782-788.
14. Goodchild R.E., Kim C.E., Dauer W.T. Loss of the dystonia-associated protein torsinA selectively disrupts the neuronal nuclear envelope. Neuron 2005, 48:923-932.
15. Graybiel A.M. Neurotransmitters and neuromodulators in the basal ganglia. Trends Neurosci. 1990, 13:244-254.
16. Harrison L.M., He Y. Rhes and AGS1/Dexras1 affect signaling by dopamine D1 receptors through adenylyl cyclase. J. Neurosci. Res. 2011, 89:874-882.
17. Harrison L.M., LaHoste G.J. Rhes, the Ras homolog enriched in striatum, is reduced under conditions of dopamine supersensitivity. Neuroscience 2006, 137:483-492.
18. Harrison L.M., Lahoste G.J., Ruskin D.N. Ontogeny and dopaminergic regulation in brain of Ras homolog enriched in striatum (Rhes). Brain Res. 2008, 1245:16-25.
19. Harrison L.M., Muller S.H., Spano D. Effects of the Ras homolog Rhes on Akt/protein kinase B and glycogen synthase kinase 3 phosphorylation in striatum. Neuroscience 2013, 236:21-30.
20. Johansson P.A., Irmler M., Acampora D., Beckers J., Simeone A., Götz M. The transcription factor Otx2 regulates choroid plexus development and function. Development 2013, 140:1055-1066.
21. Laurberg P. Thyroid function: thyroid hormones, iodine and the brain-an important concern. Nat. Rev. Endocrinol. 2009, 5:475-476.
22. Lhuillier L., Dryer S.E. Developmental regulation of neuronal K(Ca) channels by TGFbeta1: an essential role for PI3 kinase signaling and membrane insertion. J. Neurophysiol. 2002, 88:954-964.
23. Louis E.D., Lee P., Quinn L., Marder K. Dystonia in Huntington's disease: prevalence and clinical characteristics. Mov. Disord. 1999, 14:95-101.
24. 2+ channel currents in cultured sensory neurones is dependent on culture conditions and channel subunit expression. Neuropharmacology 2002, 42:353-366.
25. + channels reduces autonomous activity in striatal cholinergic interneurons. J. Neurosci. 2004, 24:10289-10301.
26. Mealer R.G., Subramaniam S., Snyder S.H. Rhes deletion is neuroprotective in the 3-nitropropionic acid model of Huntington's disease. J. Neurosci. 2013, 33:4206-4210.
27. Mealer R.G., Murray A.J., Shahani N., Subramaniam S., Snyder S.H. Rhes, a striatal-selective protein implicated in Huntington disease, binds beclin-1 and activates autophagy. J. Biol. Chem. 2014, 289:3547-3554.
28. Migliarini S., Pacini G., Pelosi B., Lunardi G., Pasqualetti M. Lack of brain serotonin affects postnatal development and serotonergic neuronal circuitry formation. Mol. Psychiatry 2013, 18:1106-1118.
29. Missale C., Nash S.R., Robinson S.W., Jaber M., Caron M.G. Dopamine receptors: from structure to function. Physiol. Rev. 1998, 78:189-225.
30. Napolitano F., Pasqualetti M., Usiello A., Santini E., Pacini G., Sciamanna G., Errico F., Tassone A., Di Dato V., Martella G., Cuomo D., Fisone G., Bernardi G., Mandolesi G., Mercuri N.B., Standaert D.G., Pisani A. Dopamine D2 receptor dysfunction is rescued by adenosine A2A receptor antagonism in a model of DYT1 dystonia. Neurobiol. Dis. 2010, 38:434-445.
31. Pan W.X., Mao T., Dudman J.T. Inputs to the dorsal striatum of the mouse reflect the parallel circuit architecture of the forebrain. Front. Neuroanat. 2010, 4:147. (27).
32. Pasqualetti M., Ori M., Castagna M., Marazziti D., Cassano G.B., Nardi I. Distribution and cellular localization of the serotonin type 2C receptor messenger RNA in human brain. Neuroscience 1999, 92:601-611.
33. Pasqualetti M., Ren S.-Y., Poulet M., LeMeur M., Dierich A., Rijli F.M. A Hoxa2 knockin allele that expresses EGFP upon conditional Cre-mediated recombination. Genesis 2002, 32:109-111.
34. 210-Cre transgenic mouse line reveals non-serotonergic expression domains of Pet1 both in CNS and periphery. PLoS One 2014, 9(8):e104318. (6).
35. Pham C.T., MacIvor D.M., Hug B.A., Heusel J.W., Ley T.J. Long-range disruption of gene expression by a selectable marker cassette. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:13090-13095.
36. Pisani A., Bonsi P., Centonze D., Calabresi P., Bernardi G. Activation of D2-like dopamine receptors reduces synaptic inputs to striatal cholinergic interneurons. J. Neurosci. 2000, 20:RC69.
37. Pisani A., Martella G., Tscherter A., Bonsi P., Sharma N., Bernardi G., Standaert D.G. Altered responses to dopaminergic D2 receptor activation and N-type calcium currents in striatal cholinergic interneurons in a mouse model of DYT1 dystonia. Neurobiol. Dis. 2006, 24:318-325.
38. Pisani A., Bernardi G., Ding J., Surmeier D.J. Re-emergence of striatal cholinergic interneurons in movement disorders. Trends Neurosci. 2007, 30:545-553.
39. Rivera A., Alberti I., Martín A.B., Narváez J.A., de la Calle A., Moratalla R. Molecular phenotype of rat striatal neurons expressing the dopamine D5 receptor subtype. Eur. J. Neurosci. 2002, 16:2049-2058.
40. Santini E., Valjent E., Fisone G. mTORC1 signaling in Parkinson's disease and L-DOPA-induced dyskinesia: a sensitized matter. Cell Cycle 2010, 9:2713-2718.
41. Sciamanna G., Tassone A., Martella G., Mandolesi G., Puglisi F., Cuomo D., Madeo G., Ponterio G., Standaert D.G., Bonsi P., Pisani A. Developmental profile of the aberrant dopamine D2 receptor response in striatal cholinergic interneurons in DYT1 dystonia. PLoS One 2011, 6:e24261.
42. Sciamanna G., Hollis R., Ball C., Martella G., Tassone A., Marshall A., Parsons D., Li X., Yokoi F., Zhang L., Li Y., Pisani A., Standaert D.G. Cholinergic dysregulation produced by selective inactivation of the dystonia-associated protein torsinA. Neurobiol. Dis. 2012, 47:416-427.
43. Sciamanna G., Tassone A., Mandolesi G., Puglisi F., Ponterio G., Martella G., Madeo G., Bernardi G., Standaert D.G., Bonsi P., Pisani A. Cholinergic dysfunction alters synaptic integration between thalamostriatal and corticostriatal inputs in DYT1 dystonia. J. Neurosci. 2012, 32:11991-12004.
44. Sciamanna G., Ponterio G., Tassone A., Maltese M., Madeo G., Martella G., Poli S., Schirinzi T., Bonsi P., Pisani A. Negative allosteric modulation of mGlu5 receptor rescues striatal D2 dopamine receptor dysfunction in rodent models of DYT1 dystonia. Neuropharmacology 2014, 85:440-450.
45. Spano D., Branchi I., Rosica A., Pirro M.T., Riccio A., Mithbaokar P., Affuso A., Arra C., Campolongo P., Terracciano D., Macchia V., Bernal J., Alleva E., Di Lauro R. Rhes is involved in striatal function. Mol. Cell. Biol. 2004, 24:5788-5796.
46. Subramaniam S., Snyder S.H. Huntington's disease is a disorder of the corpus striatum: focus on Rhes (Ras homologue enriched in the striatum). Neuropharmacology 2011, 60:1187-1192.
47. Subramaniam S., Sixt K.M., Barrow R., Snyder S.H. Rhes, a striatal specific protein, mediates mutant-huntingtin cytotoxicity. Science 2009, 324:1327-1330.
48. Subramaniam S., Mealer R.G., Sixt K.M., Barrow R.K., Usiello A., Snyder S.H. Rhes, a physiologic regulator of sumoylation, enhances cross-sumoylation between the basic sumoylation enzymes E1 and Ubc9. J. Biol. Chem. 2010, 285:20428-20432.
49. Subramaniam S., Napolitano F., Mealer R.G., Kim S., Errico F., Barrow R., Shahani N., Tyagi R., Snyder S.H., Usiello A. Rhes, a striatal-enriched small G protein, mediates mTOR signaling and l-DOPA-induced dyskinesia. Nat. Neurosci. 2012, 15:191-193.
50. Thapliyal A., Bannister R.A., Hanks C., Adams B.A. The monomeric G proteins AGS1 and Rhes selectively influence Galphai-dependent signaling to modulate N-type (CaV2.2) calcium channels. Am. J. Physiol. Cell Physiol. 2008, 295:C1417-C1426.
51. Tuan D., Solomon W., Li Q., London I.M. The beta-like-globin gene domain in human erythroid cells. Proc. Natl. Acad. Sci. U. S. A. 1985, 82:6384-6388.
52. Vallortigara J., Alfos S., Micheau J., Higueret P., Enderlin V. T3 administration in adult hypothyroid mice modulates expression of proteins involved in striatal synaptic plasticity and improves motor behavior. Neurobiol. Dis. 2008, 31:378-385.
53. Vallortigara J., Chassande O., Higueret P., Enderlin V. Thyroid hormone receptor alpha plays an essential role in the normalisation of adult-onset hypothyroidism-related hypoexpression of synaptic plasticity target genes in striatum. J. Neuroendocrinol. 2009, 21:49-56.
54. Vargiu P., Morte B., Manzano J., Perez J., de Abajo R., Gregor Sutcliffe J., Bernal J. Thyroid hormone regulation of Rhes, a novel Ras homolog gene expressed in the striatum. Mol. Brain Res. 2001, 94:1-8.
55. Vargiu P., Abajo R.D., Garcia-Ranea J.A., Valencia A., Santisteban P., Crespo P., Bernal J. The small GTP-binding protein, Rhes, regulates signal transduction from G protein-coupled receptors. Oncogene 2004, 23:559-568.
56. Viard P., Butcher A.J., Halet G., Davies A., Nürnberg B., Heblich F., Dolphin A.C. PI3K promotes voltage-dependent calcium channel trafficking to the plasma membrane. Nat. Neurosci. 2004, 7:939-946.
57. Wullschleger S., Loewith R., Hall M.N. TOR signaling in growth and metabolism. Cell 2006, 124:471-484.
58. 2+-sensitive GABA(A) currents in striatal cholinergic interneurons through a PKA/PP1 cascade. Neuron 1997, 19:1115-1126.
59. 2+ currents in rat neostriatal cholinergic interneurons through a membrane-delimited, protein-kinase-C-insensitive pathway. J. Neurophysiol. 1997, 77:1003-1015.
60. Zhou F.-M., Wilson C.J., Dani J.A. Cholinergic interneuron characteristics and nicotinic properties in the striatum. J. Neurobiol. 2002, 53:590-605.