The brain cytoplasmic RNA BC1 regulates dopamine D2 receptor-mediated transmission in the striatum

Journal of Neuroscience

Volumn 27, Issue 33, 2007, Pages 8885-8892

  Centonze, Diego ^a,c   Rossi, Silvia ^a,c   Napoli, Ilaria ^b,c   Mercaldo, Valentina ^b,c   Lacoux, Caroline ^b,c   Ferrari, Francesca ^b,c   Ciotti, Maria Teresa ^b,d   De Chiara, Valentina ^a,c   Prosperetti, Chiara ^a,c   Maccarrone, Mauro ^c,e   Fezza, Filomena ^b,c   Calabresi, Paolo ^c,f   Bernardi, Giorgio ^a,c   Bagni, Claudia ^b,c  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

^c IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^d CNR   (Italy)

^e UNIVERSITY OF TERAMO   (Italy)

^f UNIVERSITY OF PERUGIA   (Italy)

Author keywords

Electrophysiology; GABA transmission; IPSC; mRNA localization; Noncoding RNA; Plasticity

Indexed keywords

4 AMINOBUTYRIC ACID; BC1 RNA; BRAIN PROTEIN; BRAIN RECEPTOR; CANNABINOID 1 RECEPTOR; CYTOPLASM PROTEIN; DOPAMINE 2 RECEPTOR; FRAGILE X MENTAL RETARDATION PROTEIN; MESSENGER RNA; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DENDRITE; DOPAMINERGIC TRANSMISSION; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN STABILITY; RECEPTOR SENSITIVITY; RNA ANALYSIS; RNA TRANSLATION; SYNAPSE; TRANSLATION REGULATION;

ANIMALS; ANIMALS, NEWBORN; BIPHENYL COMPOUNDS; CELLS, CULTURED; CORPUS STRIATUM; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); INHIBITORY POSTSYNAPTIC POTENTIALS; ISOENZYMES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; OLIGONUCLEOTIDES; PATCH-CLAMP TECHNIQUES; PIPERAZINES; RECEPTORS, DOPAMINE D2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBONUCLEOPROTEINS, SMALL CYTOPLASMIC; RNA, MESSENGER; SYNAPTIC TRANSMISSION;

EID: 34548084302     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0548-07.2007     Document Type: Article

References (41)

1. Aronov S, Aranda G, Behar L, Ginzburg I (2002) Visualization of translated tau protein in the axons of neuronal P19 cells and characterization of tau RNP granules. J Cell Sci 115:3817-3827.
2. Bakker CE, Verheij C, Willemsen R, Vanderhelm R, Oerlemans F, Vermey M, Bygrave A, Hoogeveen AT, Oostra BA, Reyniers E (1994) Fmr1 knockout mice: a model to study fragile X mental retardation. Cell 78:23-33.
3. Berke JD, Hyman SE (2000) Addiction, dopamine, and the molecular mechanisms of memory. Neuron 25:515-532.
4. Binder LI, Frankfurter A, Rebhun LI (1985) The distribution of tau in the mammalian central nervous system. J Cell Biol 101:1371-1378.
5. Centonze D, Gubellini P, Usiello A, Rossi S, Tscherter A, Bracci E, Erbs E, Tognazzi N, Bernardi G, Pisani A, Calabresi P, Borrelli E (2004) Differential contribution of dopamine D2S and D2L receptors in the modulation of glutamate and GABA transmission in the striatum. Neuroscience 129:157-166.
6. Centonze D, Rossi S, Prosperetti C, Tscherter A, Bernardi G, Maccarrone M, Calabresi P (2005) Abnormal sensitivity to cannabinoid receptor stimulation might contribute to altered gamma-aminobutyric acid transmission in the striatum of R6/2 Huntington's disease mice. Biol Psychiatry 57:1583-1589.
7. Charvin D, Vanhoutte P, Pages C, Borrelli E, Caboche J (2005) Unraveling a role for dopamine in Huntington's disease: the dual role of reactive oxygen species and D2 receptor stimulation. Proc Natl Acad Sci USA 102:12218-12223.
8. Ferrari F, Mercaldo V, Piccoli G, Sala C, Cannata S, Achsel T, Bagni C (2007) The fragile X mental retardation protein-RNP granules show an mGluR-dependent localization in the post-synaptic spines. Mol Cell Neurosci 34:343-354.
9. 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.
10. 35S]GTP gamma S binding. Life Sci 65:1633-1645.
11. Goldberg MS, Pisani A, Haburcak M, Vortherms TA, Kitada T, Costa C, Tong Y, Martella G, Tscherter A, Martins A, Bernardi G, Roth BL, Pothos EN, Calabresi P, Shen J (2005) Nigrostriatal dopaminergic deficits and hypokinesia caused by inactivation of the familial Parkinsonism-linked gene DJ-1. Neuron 45:489-496.
12. Gustafson N, Gireesh-Dharmaraj E, Czubayko U, Blackwell KT, Plenz D (2006) A comparative voltage and current-clamp analysis of feedback and feedforward synaptic transmission in the striatal microcircuit in vitro. J Neurophysiol 95:737-752.
13. Guzman JN, Hernandez A, Galarraga E, Tapia D, Laville A, Vergara R, Aceves J, Bargas J (2003) Dopaminergic modulation of axon collaterals inter-connecting spiny neurons of the rat striatum. J Neurosci 23:8931-8940.
14. Hunt MJ, Kessal K, Garcia R (2005) Ketamine induces dopaminedependent depression of evoked hippocampal activity in the nucleus accumbens in freely moving rats. J Neurosci 25:524-531.
15. Johnson EM, Kinoshita Y, Weinreb DB, Wortman MJ, Simon R, Khalili K, Winckler B, Gordon J (2006) Role of Pur alpha in targeting mRNA to sites of translation in hippocampal neuronal dendrites. J Neurosci Res 83:929-943.
16. Kash SF, Tecott LH, Hodge C, Baekkeskov S (1999) Increased anxiety and altered responses to anxiolytics in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase. Proc Natl Acad Sci USA 96:1698-1703.
17. Kaufman DL, Houser CR, Tobin AJ (1991) Two forms of the gammaaminobutyric acid synthetic enzyme glutamate decarboxylase have distinct intraneuronal distributions and cofactor interactions. J Neurochem 56:720-723.
18. Kobayashi S, Agui K, Kamo S, Li Y, Anzai K (2000) Neural BC1 RNA associates with pur alpha, a single-stranded DNA and RNA binding protein, which is involved in the transcription of the BC1 RNA gene. Biochem Biophys Res Commun 277:341-347.
19. Koos T, Tepper JM, Wilson CJ (2004) Comparison of IPSCs evoked by spiny and fast-spiking neurons in the neostriatum. J Neurosci 24:7916-7922.
20. Lewejohann L, Skryabin BV, Sachser N, Prehn C, Heiduschka P, Thanos S, Jordan U, Dell'Omo G, Vyssotski AL, Pleskacheva MG, Lipp HP, Tiedge H, Brosius J, Prior H (2004) Role of a neuronal small non-messenger RNA: behavioural alterations in BC1 RNA-deleted mice. Behav Brain Res 154:273-289.
21. Mallardo M, Deitinghoff A, Muller J, Goetze B, Macchi P, Peters C, Kiebler MA (2003) Isolation and characterization of Staufen-containing ribonucleoprotein particles from rat brain. Proc Natl Acad Sci USA 100:2100-2105.
22. Muddashetty R, Khanam T, Kondrashov A, Bundman M, Iacoangeli A, Kremerskothen J, Duning K, Barnekow A, Huttenhofer A, Tiedge H, Brosius J (2002) Poly(A)-binding protein is associated with neuronal BC1 and BC200 ribonucleoprotein particles. J Mol Biol 321:433-445.
23. Muramatsu T, Ohmae A, Anzai K (1998) BC1 RNA protein particles in mouse brain contain two y-,h-element-binding proteins, translin and a 37 kDa protein. Biochem Biophys Res Commun 247:7-11.
24. Muslimov IA, Santi E, Homel P, Perini S, Higgins D, Tiedge H (1997) RNA transport in dendrites: a cis-acting targeting element is contained within neuronal BC1 RNA. J Neurosci 17:4722-4733.
25. Muslimov IA, Lin Y, Heller M, Brosius J, Zakeri Z, Tiedge H (2002) A small RNA in testis and brain: implications for male germ cell development. J Cell Sci 115:1243-1250.
26. Nader MA, Morgan D, Gage HD, Nader SH, Calhoun TL, Buchheimer N, Ehrenkaufer R, Mach RH (2006) PET imaging of dopamine D2 receptors during chronic cocaine self-administration in monkeys. Nat Neurosci 9:1050-1056.
27. Nimmrich V, Hargreaves EL, Muslimov IA, Bianchi R, Tiedge H (2005) Dendritic BC1 RNA: modulation by kindling-induced afterdischarges. Brain Res Mol Brain Res 133:110-118.
28. Obeso JA, Rodriguez-Oroz MC, Rodriguez M, Lanciego JL, Artieda J, Gonzalo N, Olanow CW (2000) Pathophysiology of the basal ganglia in Parkinson's disease. Trends Neurosci 23:S8-S19.
29. Plenz D (2003) When inhibition goes incognito: feedback interaction between spiny projection neurons in striatal function. Trends Neurosci 26:436-443.
30. Ponnusamy R, Nissim HA, Barad M (2005) Systemic blockade of D2-like dopamine receptors facilitates extinction of conditioned fear in mice. Learn Mem 12:399-406.
31. Rozhdestvensky TS, Kopylov AM, Brosius J, Huttenhofer A (2001) Neuronal BC1 RNA structure: evolutionary conversion of a tRNA(Ala) domain into an extended stem-loop structure. RNA 7:722-730.
32. Sareen J, Campbell DW, Leslie WD, Malisza KL, Stein MB, Paulus MP, Kravetsky LB, Kjernisted KD, Walker JR, Reiss JP (2007) Striatal function in generalized social phobia: a functional magnetic resonance imaging study. Biol Psychiatry 61:396-404.
33. Skryabin BV, Sukonina V, Jordan U, Lewejohann L, Sachser N, Muslimov I, Tiedge H, Brosius J (2003) Neuronal untranslated BC1 RNA: targeted gene elimination in mice. Mol Cell Biol 23:6435-6441.
34. Steward O, Schuman EM (2003) Compartmentalized synthesis and degradation of proteins in neurons. Neuron 40:347-359.
35. Tepper JM, Abercrombie ED, Bolam JP (2007) Basal ganglia macrocircuits. Prog Brain Res 160:3-7.
36. Tunstall MJ, Oorschot DE, Kean A, Wickens JR (2002) Inhibitory interactions between spiny projection neurons in the rat striatum. J Neurophysiol 88:1263-1269.
37. Usiello A, Baik JH, Rouge-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.
38. Wang H, Iacoangeli A, Popp S, Muslimov IA, Imataka H, Sonenberg N, Lomakin IB, Tiedge H (2002) Dendritic BC1 RNA: functional role in regulation of translation initiation. J Neurosci 22:10232-10241.
39. West N, Roy-Engel AM, Imataka H, Sonenberg N, Deininger P (2002) Shared protein components of SINE RNPs. J Mol Biol 321:423-432.
40. Zalfa F, Giorgi M, Primerano B, Moro A, Di Penta A, Reis S, Oostra B, Bagni C (2003) The fragile X syndrome protein FMRP associates with BC1 RNA and regulates the translation of specific mRNAs at synapses. Cell 112:317-327.
41. Zalfa F, Achsel T, Bagni C (2006) mRNPs, polysomes or granules: FMRP in neuronal protein synthesis. Curr Opin Neurobiol 16:265-269.