Changes in the expression of genes encoding for mGlu4 and mGlu5 receptors and other regulators of the indirect pathway in acute mouse models of drug-induced parkinsonism

Neuropharmacology

Volumn 95, Issue , 2015, Pages 50-58

  Cannella, Milena ^a   Motolese, Marta ^a   Bucci, Domenico ^a   Molinaro, Gemma ^a   Gradini, Roberto ^b   Bruno, Valeria ^a,c   Nicoletti, Ferdinando ^a,c   Battaglia, Giuseppe ^a  

^a IRCCS NEUROMED   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Haloperidol; Indirect pathway; Metabotropic glutamate receptors; MPTP; Parkinsonism

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; ADENOSINE A2A RECEPTOR; CANNABINOID 1 RECEPTOR; HALOPERIDOL; METABOTROPIC RECEPTOR 4; METABOTROPIC RECEPTOR 5; PREPROENKEPHALIN; PREPROENKEPHALIN A; UNCLASSIFIED DRUG; ADENOSINE A2 RECEPTOR; ENKEPHALIN; GRM5 PROTEIN, MOUSE; METABOTROPIC RECEPTOR; PROTEIN C FOS; PROTEIN PRECURSOR;

ADAPTIVE BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CATALEPSY; CONTROLLED STUDY; CORPUS STRIATUM; DISEASE MODEL; DOWN REGULATION; GENE DELETION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GLOBUS PALLIDUS; MOUSE; NONHUMAN; PARKINSONISM; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; THALAMUS NUCLEUS; UPREGULATION; VENTROMEDIAL THALAMIC NUCLEUS; ACUTE DISEASE; ANIMAL; C57BL MOUSE; COMPARATIVE STUDY; GENETICS; KNOCKOUT MOUSE; METABOLISM; NERVE CELL; PATHOLOGY; THALAMUS VENTRAL NUCLEUS; TIME;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; ACUTE DISEASE; ANIMALS; CATALEPSY; CORPUS STRIATUM; ENKEPHALINS; HALOPERIDOL; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; PARKINSONIAN DISORDERS; PROTEIN PRECURSORS; PROTO-ONCOGENE PROTEINS C-FOS; RECEPTOR, CANNABINOID, CB1; RECEPTOR, METABOTROPIC GLUTAMATE 5; RECEPTORS, ADENOSINE A2; RECEPTORS, METABOTROPIC GLUTAMATE; TIME FACTORS; VENTRAL THALAMIC NUCLEI;

EID: 84924952805     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2015.02.024     Document Type: Article

References (61)

1. M. Amalric, S. Lopez, C. Goudet, G. Fisone, G. Battaglia, F. Nicoletti, J.P. Pin, and F.C. Acher Group III and subtype 4 metabotropic glutamate receptor agonists: discovery and pathophysiological applications in Parkinson's disease Neuropharmacology 66 2013 53 64
2. M.C. Asselin, J.J. Soghomonian, P.Y. Côté, and A. Parent Striatal changes in preproenkephalin mRNA levels in parkinsonian monkeys Neuroreport 5 1994 2137 2140
3. G. Battaglia, C.L. Busceti, G. Molinaro, F. Biagioni, M. Storto, F. Fornai, F. Nicoletti, and V. Bruno Endogenous activation of mGlu5 metabotropic glutamate receptors contributes to the development of nigrostriatal damage induced by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in mice J. Neurosci. 24 2004 828 835
4. G. Battaglia, C.L. Busceti, G. Molinaro, F. Biagioni, A. Traficante, F. Nicoletti, and V. Bruno Pharmacological activation of mGlu4 metabotropic glutamate receptors reduces nigrostriatal degeneration in mice treated with 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine J. Neurosci. 26 2006 7222 7229
5. G. Battaglia, M.G. Farrace, P.G. Mastroberardino, I. Viti, G.M. Fimia, J. Van Beeumen, B. Devreese, G. Melino, G. Molinaro, C.L. Busceti, F. Biagioni, F. Nicoletti, and M. Piacentini Transglutaminase 2 ablation leads to defective function of mitochondrial respiratory complex I affecting neuronal vulnerability in experimental models of extrapyramidal disorders J. Neurochem. 100 2007 36 49
6. E. Bezard, C.E. Gross, and J.M. Brotchie Presymptomatic compensation in Parkinson's disease is not dopamine-mediated Trends Neurosci. 26 2003 215 221
7. L.M. Billings, and J.F. Marshall Glutamic acid decarboxylase 67 mRNA regulation in two globus pallidus neuron populations by dopamine and the subthalamic nucleus J. Neurosci. 24 2004 3094 3103
8. L.C. Blume, C.E. Bass, S.R. Childers, G.D. Dalton, D.C. Roberts, J.M. Richardson, R. Xiao, D.E. Selley, and A.C. Howlett Striatal CB1 and D2 receptors regulate expression of each other, CRIP1A and δ opioid systems J. Neurochem. 124 2013 808 820
9. J. Brotchie, and C. Fitzer-Attas Mechanisms compensating for dopamine loss in early Parkinson disease Neurology 72 2009 S32 S38
10. P. Calabresi, A. Saiardi, A. Pisani, J.H. Baik, D. Centonze, N.B. Mercuri, G. Bernardi, and E. Borrelli Abnormal synaptic plasticity in the striatum of mice lacking dopamine D2 receptors J. Neurosci. 17 1997 4536 4544
11. P.J. Conn, G. Battaglia, M.J. Marino, and F. Nicoletti Metabotropic glutamate receptors in the basal ganglia motor circuit Nat. Rev. Neurosci. 6 2005 787 798
12. C. Corti, L. Aldegheri, P. Somogyi, and F. Ferraguti Distribution and synaptic localisation of the metabotropic glutamate receptor 4(mGluR4) in the rodent CNS Neuroscience 110 3 2002 403 420
13. I. Crespo, H. de Gomez, F.F.R. Rodriguez de, and M. Navarro Pretreatment with subeffective doses of Rimonabant attenuates orexigenic actions of orexin A-hypocretin 1 Neuropharmacology 54 2008 219 225
14. P. DeBoer, M.J. Heeringa, and E.D. Abercrombie Spontaneous release of acetylcholine in striatum is preferentially regulated by inhibitory dopamine D2 receptors Eur. J. Pharmacol. 317 1996 257 262
15. M. Dragunow, and R. Faull The use of c-fos as a metabolic marker in neuronal pathway tracing J. Neurosci. Methods 29 3 1989 261 265
16. F. Fallarino, C. Volpi, F. Fazio, S. Notartomaso, C. Vacca, C. Busceti, S. Bicciato, G. Battaglia, V. Bruno, P. Puccetti, M.C. Fioretti, F. Nicoletti, U. Grohmann, and R. Di Marco Metabotropic glutamate receptor-4 modulates adaptive immunity and restrains neuroinflammation Nat. Med. 16 2010 897 902
17. K. Fuxe, L.F. Agnati, K. Jacobsen, J. Hillion, M. Canals, M. Torvinen, B. Tinner-Staines, W. Staines, D. Rosin, A. Terasmaa, P. Popoli, G. Leo, V. Vergoni, C. Lluis, F. Ciruela, R. Franco, and S. Ferré Receptor heteromerization in adenosine A2A receptor signaling: relevance for striatal function and Parkinson's disease Neurology 2003 S19 S23
18. F. Gasparini, T. Di Paolo, and B. Gomez-Mancilla Metabotropic glutamate receptors for Parkinson's disease therapy Park. Dis. 2013 2013 196028
19. C.R. Gerfen, T.M. Engber, L.C. Mahan, Z. Susel, T.N. Chase, F.J. Monsma Jr., and D.R. Sibley D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons Science 250 1990 1429 1432
20. K.P. Gudehithlu, A.M. Duchemin, G.A. Tejwani, N.H. Neff, and M. Hadjiconstantinou Preproenkephalin mRNA and methionine-enkephalin increase in mouse striatum after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine treatment J. Neurochem. 56 1991 1043 1048
21. P.J. Hallett, A.W. Dunah, P. Ravenscroft, S. Zhou, E. Bezard, A.R. Crossman, J.M. Brotchie, and D.G. Standaert Alterations of striatal NMDA receptor subunits associated with the development of dyskinesia in the MPTP-lesioned primate model of Parkinson's disease Neuropharmacology 48 2005 503 516
22. R.E. Hekkila, A. Hess, and R.C. Duvoisin Dopaminergic neurotoxicity of 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine in mice Science 224 1984 1451 1453
23. H. Hermann, G. Marsicano, and B. Lutz Coexpression of the cannabinoid receptor type 1 with dopamine and serotonin receptors in distinct neuronal subpopulations of the adult mouse forebrain Neuroscience 109 2002 451 460
24. M.T. Herrero, S.J. Augood, E.C. Hirsch, F. Javoy-Agid, M.R. Luquin, Y. Agid, J.A. Obeso, and P.C. Emson Effects of L-DOPA on preproenkephalin and preprotachykinin gene expression in the MPTP-treated monkey striatum Neuroscience 68 1995 1189 1198
25. N. Ismayilova, A. Verkhratsky, and M.J. Dascombe Changes in mGlu5 receptor expression in the basal ganglia of reserpinised rats Eur. J. Pharmacol. 545 2006 134 141
26. K.A. Johnson, P.J. Conn, and C.M. Niswender Glutamate receptors as therapeutic targets for Parkinson's disease CNS Neurol. Disord. Drug Targets 8 2009 475 491
27. N. Jones, C. Bleickardt, D. Mullins, E. Parker, and R. Hodgson A2A receptor antagonists do not induce dyskinesias in drug-naive or L-dopa sensitized rats Brain Res. Bull. 98 2013 163 169
28. M.A. King, N. Scotty, R.L. Klein, and E.M. Meyer Particle detection, number estimation, and feature measurement in gene transfer studies: optical fractionators stereology integrated with digital image processing and analysis Methods 28 2002 293 299
29. A.C. Kreitzer, and R.C. Malenka Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson's disease models Nature 445 2007 643 647
30. K.J. Kovács c-Fos as a transcription factor: a stressful (re)view from a functional map Neurochem. Int. 33 1998 287 297
31. C.S. Lee, A. Samii, V. Sossi, T.J. Ruth, M. Schulzer, J.E. Holden, J. Wudel, P.K. Pal, R. de la Fuente-Fernandez, D.B. Calne, and A.J. Stoessl In vivo positron emission tomographic evidence for compensatory changes in presynaptic dopaminergic nerve terminals in Parkinson's disease Ann. Neurol. 47 2000 493 503
32. B.K. Lipska, and D.R. Weinberger Delayed effects of neonatal hippocampal damage on haloperidol-induced catalepsy and apomorphine-induced stereotypic behaviors in the rat Brain Res. Dev. Brain Res. 75 1993 213 222
33. S. Lopez, N. Turle-Lorenzo, F. Acher, E. De Leonibus, A. Mele, and M. Amalric Targeting group III metabotropic glutamate receptors produces complex behavioral effects in rodent models of Parkinson's disease J. Neurosci. 27 2007 6701 6711
34. P. Mailleux, and J.J. Vanderhaeghen Age-related loss of cannabinoid receptor binding sites and mRNA in the rat striatum Neurosci. Lett. 147 1992 179 181
35. N. Mallet, B.R. Micklem, P. Henny, M.T. Brown, C. Williams, J.P. Bolam, K.C. Nakamura, and P.J. Magill Dichotomous organization of the external globus pallidus Neuron 74 2012 1075 1086
36. M.J. Marino, O. Valenti, J.A. O'Brien, D.L. Williams Jr., and P.J. Conn Modulation of inhibitory transmission in the rat globus pallidus by activation of mGluR4 Ann. N. Y. Acad. Sci. 1003 2003 435 437
37. J. Marrocco, J. Mairesse, D. Bucci, L. Lionetto, G. Battaglia, M. Consolazione, L. Ravasi, M. Simmaco, S. Morley-Fletcher, S. Maccari, and F. Nicoletti Early life stress causes refractoriness to haloperidol-induced catalepsy Mol. Pharmacol. 84 2 2013 244 251
38. A.B. Martín, E. Fernandez-Espejo, B. Ferrer, M.A. Gorriti, A. Bilbao, M. Navarro, F. Rodriguez de Fonseca, and R. Moratalla Expression and function of CB1 receptor in the rat striatum: localization and effects on D1 and D2 dopamine receptor-mediated motor behaviors Neuropsychopharmacology 33 2008 1667 1679
39. F. Mátyás, Y. Yanovsky, K. Mackie, W. Kelsch, U. Misgeld, and T.F. Freund Subcellular localization of type 1 cannabinoid receptors in the rat basal ganglia Neuroscience 137 2006 337 361
40. G. Maura, A. Giardi, and M. Raiteri Release-regulating D-2 dopamine receptors are located on striatal glutamatergic nerve terminals J. Pharmacol. Exp. Ther. 247 2 1988 680 684
41. M.J. Messenger, L.G. Dawson, and S. Duty Changes in metabotropic glutamate receptor 1-8 gene expression in the rodent basal ganglia motor loop following lesion of the nigrostriatal tract Neuropharmacology 43 2002 261 271
42. B.H. Meurers, G. Dziewczapolski, T. Shi, A. Bittner, F. Kamme, and C.W. Shults Dopamine depletion induces distinct compensatory gene expression changes in DARPP-32 signal transduction cascades of striatonigral and striatopallidal neurons J. Neurosci. 29 2009 6828 6839
43. H.H. Nickols, and P.J. Conn Development of allosteric modulators of GPCRs for treatment of CNS disorders Neurobiol. Dis. 61 2014 55 71
44. F. Nicoletti, J. Bockaert, G.L. Collingridge, P.J. Conn, F. Ferraguti, D.D. Schoepp, J.T. Wroblewski, and J.P. Pin Metabotropic glutamate receptors: from the workbench to the bedside Neuropharmacology 60 2011 1017 1041
45. A.P. Nisbet, O.J. Foster, A. Kingsbury, D.J. Eve, S.E. Daniel, C.D. Marsden, and A.J. Lees Preproenkephalin and preprotachykinin messenger RNA expression in normal human basal ganglia and in Parkinson's disease Neuroscience 66 1995 361 376
46. B. Ouattara, F. Gasparini, M. Morissette, L. Grégoire, P. Samadi, B. Gomez-Mancilla, and T. Di Paolo Effect of L-Dopa on metabotropic glutamate receptor 5 in the brain of parkinsonian monkeys J. Neurochem. 113 2010 715 724
47. R. Pekhletski, R. Gerlai, L.S. Overstreet, X.P. Huang, N. Agopyan, N.T. Slater, W. Abramow-Newerly, J.C. Roder, and D.R. Hampson Impaired cerebellar synaptic plasticity and motor performance in mice lacking the mGluR4 subtype of metabotropic glutamate receptor J. Neurosci. 16 1996 6364 6373
48. A. Pisani, G. Martella, A. Tscherter, P. Bonsi, N. Sharma, G. Bernardi, and D.G. Standaert 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. 24 2006 318 325
49. R. Rodríguez-Puertas, M. Herrera-Marschitz, J. Koistinaho, and T. Hökfelt Dopamine D1 receptor modulation of glutamate receptor messenger RNA levels in the neocortex and neostriatum of unilaterally 6-hydroxydopamine-lesioned rats Neuroscience 89 1999 781 797
50. R. Sanchez-Pernaute, J.Q. Wang, D. Kuruppu, L. Cao, W. Tueckmantel, A. Kozikowski, O. Isacson, and A.L. Brownell Enhanced binding of metabotropic glutamate receptor type 5 (mGluR5) PET tracers in the brain of parkinsonian primates Neuroimage 42 2008 248 251
51. S.F. Sawyer, M.E. Martone, and P.M. Groves A GABA immunocytochemical study of rat motor thalamus: light and electron microscopic observations Neuroscience 42 1991 103 124
52. V. Sossi, R. de la Fuente-Fernández, M. Schulzer, A.R. Troiano, T.J. Ruth, and A.J. Stoessl Dopamine transporter relation to dopamine turnover in Parkinson's disease: a positron emission tomography study Ann. Neurol. 62 2007 468 474
53. B. Szabo, L. Dörner, C. Pfreundtner, W. Nörenberg, and K. Starke Inhibition of GABAergic inhibitory postsynaptic currents by cannabinoids in rat corpus striatum Neuroscience 85 1998 395 403
54. G.R. Uhl, D. Walther, D. Mash, B. Faucheux, and F. Javoy-Agid Dopamine transporter messenger RNA in Parkinson's disease and control substantia nigra neurons Ann. Neurol. 35 1994 494 498
55. O. Valenti, M.J. Marino, M. Wittmann, E. Lis, A.G. DiLella, G.G. Kinney, and P.J. Conn Group III metabotropic glutamate receptor-mediated modulation of the striatopallidal synapse J. Neurosci. 23 2003 7218 7226
56. O. Valenti, G. Mannaioni, G.R. Seabrook, P.J. Conn, and M.J. Marino Group III metabotropic glutamate-receptor-mediated modulation of excitatory transmission in rodent substantia nigra pars compacta dopamine neurons J. Pharmacol. Exp. Ther. 313 2005 1296 1304
57. V. Van Waes, J.A. Beverley, H. Siman, K.Y. Tseng, and H. Steiner CB1 Cannabinoid receptor expression in the striatum: association with corticostriatal circuits and developmental regulation Front. Pharmacol. 3 2012 21
58. Z. Yan, W.J. Song, and J. Surmeier D2 dopamine receptors reduce N-type Ca2+ currents in rat neostriatal cholinergic interneurons through a membrane-delimited, protein-kinase-C-insensitive pathway J. Neurophysiol. 77 1997 1003 1015
59. S. Yin, M.J. Noetzel, K.A. Johnson, R. Zamorano, N. Jalan-Sakrikar, K.J. Gregory, P.J. Conn, and C.M. Niswender Selective actions of novel allosteric modulators reveal functional heteromers of metabotropic glutamate receptors in the CNS J. Neurosci. 34 2014 79 94
60. G. Zetler, and G.H. Baumann Pharmacokinetics and effects of haloperidol in the isolated mouse Pharmacology 31 1985 318 327
61. M.J. Zigmond, A.L. Acheson, M.K. Stachowiak, and E.M. Stricker Neurochemical compensation after nigrostriatal bundle injury in an animal model of preclinical parkinsonism Arch. Neurol. 41 1984 856 861