Enhanced sensitivity to group II mGlu receptor activation at corticostriatal synapses in mice lacking the familial parkinsonism-linked genes PINK1 or Parkin

Experimental Neurology

Volumn 215, Issue 2, 2009, Pages 388-396

  Martella, G ^a   Platania, P ^a   Vita, D ^b   Sciamanna, G ^b   Cuomo, D ^a   Tassone, A ^b   Tscherter, A ^a   Kitada, T ^c   Bonsi, P ^b   Shen, J ^c   Pisani, A ^a,b  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Electrophysiology; Metabotropic glutamate receptor; Monogenic parkinsonism; Striatum

Indexed keywords

2 AMINO 4 PHOSPHONOBUTYRIC ACID; 4 AMINO 2 OXABICYCLO[3.1.0]HEXANE 4,6 DICARBOXYLIC ACID; METABOTROPIC RECEPTOR; PARKIN;

ARTICLE; CHOLINERGIC SYSTEM; CORPUS STRIATUM; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; FACILITATION; INTERNEURON; MEMBRANE DEPOLARIZATION; MOUSE; NONHUMAN; PARKINSONISM; PRIORITY JOURNAL; RECEPTOR SENSITIVITY; RECEPTOR UPREGULATION; SYNAPSE;

AMINO ACIDS; ANIMALS; BICYCLO COMPOUNDS, HETEROCYCLIC; BIOPHYSICAL PROCESSES; CEREBRAL CORTEX; CORPUS STRIATUM; DOPAMINE AGENTS; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; LEVODOPA; MEMBRANE POTENTIALS; MICE; MICE, KNOCKOUT; NEURONS; PATCH-CLAMP TECHNIQUES; PROPIONIC ACIDS; PROTEIN KINASES; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPSES; UBIQUITIN-PROTEIN LIGASES;

EID: 58149527808     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2008.11.001     Document Type: Article

References (55)

1. Albanese A., Valente E.M., Romito L.M., Bellacchio E., Elia A.E., and Dallapiccola B. The PINK1 phenotype can be indistinguishable from idiopathic Parkinson disease. Neurology 64 11 (2005) 1958-1960
2. Battaglia G., Busceti C.L., Pontarelli F., Biagioni F., Fornai F., Paparelli A., Bruno V., Ruggieri S., and Nicoletti F. Protective role of group-II metabotropic glutamate receptors against nigro-striatal degeneration induced by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in mice. Neuropharmacology 45 2 (2003) 155-166
3. Bekkers J.M., Richerson G.B., and Stevens C.F. Origin of variability in quantal size in cultured hippocampal neurons and hippocampal slices. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 5359-5362
4. Bergman H., Wichmann T., and DeLong M.R. Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 249 (1990) 1436-1438
5. Bergman H., Wichmann T., Karmon B., and DeLong M.R. The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J. Neurophysiol. 72 (1994) 507-520
6. Bevan M.D., Magill P.J., Terman D., Bolam J.P., and Wilson C.J. Move to the rhythm: oscillations in the subthalamic nucleus-external globus pallidus network. Trends Neurosci. 25 (2002) 525-531
7. Binkofski F., Reetz K., Gaser C., Hilker R., Hagenah J., Hedrich K., van Eimeren T., Thiel A., Büchel C., Pramstaller P.P., Siebner H.R., and Klein C. Morphometric fingerprint of asymptomatic Parkin and PINK1 mutation carriers in the basal ganglia. Neurology 69 9 (2007) 842-850
8. Bonifati V., Rizzu P., van Baren M.J., Schaap O., Breedveld G.J., Krieger E., Dekker M.C., Squitieri F., Ibanez P., Joosse M., van Dongen J.W., Vanacore N., van Swieten J.C., Brice A., Meco G., van Duijn C.M., Oostra B.A., and Heutink P. Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science 299 5604 (2003) 256-259
9. Bonsi P., Cuomo D., De Persis C., Centonze D., Bernardi G., Calabresi P., and Pisani A. Modulatory action of metabotropic glutamate receptor (mGluR) 5 on mGluR1 function in striatal cholinergic interneurons. Neuropharmacology 49 Suppl. 1 (2005) 104-113
10. Bonsi P., Sciamanna G., Mitrano D.A., Cuomo D., Bernardi G., Platania P., Smith Y., and Pisani A. Functional and ultrastructural analysis of group I mGluR in striatal fast-spiking interneurons. Eur. J. Neurosci. 25 5 (2007) 1319-1331
11. Bonsi P., Platania P., Martella G., Madeo G., Vita D., Tassone A., Bernardi G., and Pisani A. Distinct roles of group I mGlu receptors in striatal function. Neuropharmacology 55 4 (2008) 392-395
12. Calabresi P., Mercuri N.B., De Murtas M., and Bernardi G. Involvement of GABA systems in feedback regulation of glutamate- and GABA-mediated synaptic potentials in rat neostriatum. J. Physiol. 440 (1991) 581-599
13. Calabresi P., Mercuri N.B., Sancesario G., and Bernardi G. Electrophysiology of dopamine-denervated striatal neurons. Implications for Parkinson's disease. Brain 116 Pt 2 (1993) 433-452
14. Clark I.E., Dodson M.W., Jiang C., Cao J.H., Huh J.R., Seol J.H., Yoo S.J., Hay B.A., and Guo M. Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature 441 (2006) 1162-1166
15. Conn P.J., and Pin J.P. Pharmacology and functions of metabotropic glutamate receptors. Annu. Rev. Pharmacol. Toxicol. 37 (1997) 205-237
16. Conn P.J., Battaglia G., Marino M.J., and Nicoletti F. Metabotropic glutamate receptors in the basal ganglia motor circuit. Nat. Rev., Neurosci. 6 10 (2005) 787-798
17. Cookson M.R., Dauer W., Dawson T., Fon E.A., Guo M., and Shen J. The roles of kinases in familial Parkinson's disease. J. Neurosci. 27 44 (2007) 11865-11868
18. Corti C., Battaglia G., Molinaro G., Riozzi B., Pittaluga A., Corsi M., Mugnaini M., Nicoletti F., and Bruno V. The use of knock-out mice unravels distinct roles for mGlu2 and mGlu3 metabotropic glutamate receptors in mechanisms of neurodegeneration/neuroprotection. J. Neurosci. 27 31 (2007) 8297-8308
19. David H.N., and Abraini J.H. Blockade of the locomotor stimulant effects of amphetamine by group I, group II, and group III metabotropic glutamate receptor ligands in the rat nucleus accumbens: possible interactions with dopamine receptors. Neuropharmacology 44 6 (2003) 717-727
20. Dawson L., Chadha A., Megalou M., and Duty S. The group II metabotropic glutamate receptor agonist, DCG-IV, alleviates akinesia following intranigral or intraventricular administration in the reserpine-treated rat. Br. J. Pharmacol. 129 3 (2000) 541-546
21. Gautier C.A., Kitada T., and Shen J. Loss of PINK1 causes mitochondrial functional defects and increased sensitivity to oxidative stress. Proc. Natl. Acad. Sci. U. S. A. 105 32 (2008) 11364-11369
22. Goldberg M.S., Fleming S.M., Palacino J.J., Cepeda C., Lam H.A., Bhatnagar A., Meloni E.G., Wu N., Ackerson L.C., Klapstein G.J., Gajendiran M., Roth B.L., Chesselet M.F., Maidment N.T., Levine M.S., and Shen J. Parkin-deficient mice exhibit nigrostriatal deficits but not loss of dopaminergic neurons. J. Biol. Chem. 278 44 (2003) 43628-43635
23. Greenamyre J.T. Glutamatergic influences on the basal ganglia. Clin. Neuropharmacol. 24 2 (2001) 65-70
24. Gubellini P., Eusebio A., Oueslati A., Melon C., Kerkerian-Le Goff L., and Salin P. Chronic high-frequency stimulation of the subthalamic nucleus and L-DOPA treatment in experimental parkinsonism: effects on motor behaviour and striatal glutamate transmission. Eur. J. Neurosci. 24 6 (2006) 1802-1814
25. Jiang Z.G., and North R.A. Membrane properties and synaptic responses of rat striatal neurones in vitro. J. Physiol. 443 (1991) 533-553
26. Kawaguchi Y. Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J. Neurosci. 13 11 (1993) 4908-4923
27. Kitada T., Asakawa S., Hattori N., Matsumine H., Yamamura Y., Minoshima S., Yokochi M., Mizuno Y., and Shimizu N. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392 6676 (1998) 605-608
28. Kitada T., Pisani A., Porter D.R., Yamaguchi H., Tscherter A., Martella G., Bonsi P., Zhang C., Pothos E.N., and Shen J. Impaired dopamine release and synaptic plasticity in the striatum of PINK1-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 104 27 (2007) 11441-11446
29. Kitada T., Pisani A., Karouani M., Martella G., Platania P., Madeo G., Pothos E.N., and Shen J. Impaired catecholamine release in the striatum of parkin mutant mice. The 38th Society for Neurosceince Annual Meeting, Washington DC (2008)
30. Klein C., Lohmann-Hedrich K., Rogaeva E., Schlossmacher M.G., and Lang A.E. Deciphering the role of heterozygous mutations in genes associated with parkinsonism. Lancet Neurol. 6 7 (2007) 652-662
31. Konieczny J., Ossowska K., Wolfarth S., and Pilc A. LY354740, a group II metabotropic glutamate receptor agonist with potential antiparkinsonian properties in rats. Naunyn-Schmiedeberg's Arch. Pharmacol. 358 4 (1998) 500-502
32. Lovinger D.M., and McCool B.A. Metabotropic glutamate receptor-mediated presynaptic depression at corticostriatal synapses involves mGLuR2 or 3. J. Neurophysiol. 73 3 (1995) 1076-1083
33. Meshul C.K., Emre N., Nakamura C.M., Allen C., Donohue M.K., and Buckman J.F. Time-dependent changes in striatal glutamate synapses following a 6-hydroxydopamine lesion. Neuroscience 88 1 (1999) 1-16
34. Morishima Y., Miyakawa T., Furuyashiki T., Tanaka Y., Mizuma H., and Nakanishi S. Enhanced cocaine responsiveness and impaired motor coordination in metabotropic glutamate receptor subtype 2 knockout mice. Proc. Natl. Acad. Sci. U. S. A. 102 11 (2005) 4170-4175
35. Murray T.K., Messenger M.J., Ward M.A., Woodhouse S., Osborne D.J., Duty S., and O'Neill M.J. Evaluation of the mGluR2/3 agonist LY379268 in rodent models of Parkinson's disease. Pharmacol. Biochem. Behav. 73 2 (2002) 455-466
36. Paisán-Ruíz C., Jain S., Evans E.W., Gilks W.P., Simón J., van der Brug M., López de Munain A., Aparicio S., Gil A.M., Khan N., Johnson J., Martinez J.R., Nicholl D., Carrera I.M., Pena A.S., de Silva R., Lees A., Martí-Massó J.F., Pérez-Tur J., Wood N.W., and Singleton A.B. Cloning of the gene containing mutations that cause PARK8-linked Parkinson's disease. Neuron 44 4 (2004) 595-600
37. Park J., Lee S.B., Lee S., Kim Y., Song S., Kim S., Bae E., Kim J., Shong M., Kim J.M., and Chung J. Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 441 7097 (2006) 1157-1161
38. Phillips T., Rees S., Augood S., Waldvogel H., Faull R., Svendsen C., and Emson P. Localization of metabotropic glutamate receptor type 2 in the human brain. Neuroscience 95 4 (2000) 1139-1156
39. Picconi B., Pisani A., Centonze D., Battaglia G., Storto M., Nicoletti F., Bernardi G., and Calabresi P. Striatal metabotropic glutamate receptor function following experimental parkinsonism and chronic levodopa treatment. Brain 125 Pt 12 (2002) 2635-2645
40. Pisani A., Calabresi P., Centonze D., and Bernardi G. Activation of group III metabotropic glutamate receptors depresses glutamatergic transmission at corticostriatal synapse. Neuropharmacology 36 6 (1997) 845-851
41. Pisani A., Bonsi P., Centonze D., Bernardi G., and Calabresi P. Functional coexpression of excitatory mGluR1 and mGluR5 on striatal cholinergic interneurons. Neuropharmacology 40 3 (2001) 460-463
42. Pisani A., Gubellini P., Bonsi P., Conquet F., Picconi B., Centonze D., Bernardi G., and Calabresi P. Metabotropic glutamate receptor 5 mediates the potentiation of N-methyl-d-aspartate responses in medium spiny striatal neurons. Neuroscience 106 3 (2001) 579-587
43. Pisani A., Bonsi P., Catania M.V., Giuffrida R., Morari M., Marti M., Centonze D., Bernardi G., Kingston A.E., and Calabresi P. Metabotropic glutamate 2 receptors modulate synaptic inputs and calcium signals in striatal cholinergic interneurons. J. Neurosci. 22 14 (2002) 6176-6185
44. Pisani A., Bernardi G., Ding J., and Surmeier D.J. Re-emergence of striatal cholinergic interneurons in movement disorders. Trends Neurosci. 30 10 (2007) 545-553
45. Polymeropoulos M.H., Lavedan C., Leroy E., Ide S.E., Dehejia A., Dutra A., Pike B., Root H., Rubenstein J., Boyer R., Stenroos E.S., Chandrasekharappa S., Athanassiadou A., Papapetropoulos T., Johnson W.G., Lazzarini A.M., Duvoisin R.C., Di Iorio G., Golbe L.I., and Nussbaum R.L. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276 5321 (1997) 2045-2047
46. Poole A.C., Thomas R.E., Andrews L.A., McBride H.M., Whitworth A.J., and Pallanck L.J. The PINK1/Parkin pathway regulates mitochondrial morphology. Proc. Natl. Acad. Sci. U. S. A 105 5 (2008) 1638-1643
47. Samadi P., Grégoire L., Morissette M., Calon F., Tahar A.H., Bélanger N., Dridi M., Bédard P.J., and Di Paolo T. Basal ganglia group II metabotropic glutamate receptors specific binding in non-human primate model of L-Dopa-induced dyskinesias. Neuropharmacology 54 2 (2008) 258-268
48. Schulz P.E., Cook E.P., and Johnston D. Changes in paired-pulse facilitation suggest presynaptic involvement in long-term potentiation. J. Neurosci. 14 9 (1994) 5325-5337
49. Sherer T.B., Richardson J.R., Testa C.M., Seo B.B., Panov A.V., Yagi T., Matsuno-Yagi A., Miller G.W., and Greenamyre J.T. Mechanism of toxicity of pesticides acting at complex I: relevance to environmental etiologies of Parkinson's disease. J. Neurochem. 100 6 (2007) 1469-1479
50. Smith A.D., and Bolam J.P. The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurones. Trends Neurosci. 13 7 (1990) 259-265
51. Smith Y., Charara A., Paquet M., Kieval J.Z., Paré J.F., Hanson J.E., Hubert G.W., Kuwajima M., and Levey A.I. Ionotropic and metabotropic GABA and glutamate receptors in primate basal ganglia. J. Chem. Neuroanat. 22 1-2 (2001) 13-42
52. Testa C.M., Friberg I.K., Weiss S.W., and Standaert D.G. Immunohistochemical localization of metabotropic glutamate receptors mGluR1a and mGluR2/3 in the rat basal ganglia. J. Comp. Neurol. 390 1 (1998) 5-19
53. Valente E.M., Abou-Sleiman P.M., Caputo V., Muqit M.M., Harvey K., Gispert S., Ali Z., Del Turco D., Bentivoglio A.R., Healy D.G., Albanese A., Nussbaum R., González-Maldonado R., Deller T., Salvi S., Cortelli P., Gilks W.P., Latchman D.S., Harvey R.J., Dallapiccola B., Auburger G., and Wood N.W. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 304 5674 (2004) 1158-1160
54. Varrone A., Pellecchia M.T., Amboni M., Sansone V., Salvatore E., Ghezzi D., Garavaglia B., Brice A., Brunetti A., Bonavita V., De Michele G., Salvatore M., Pappatà S., and Barone P. Imaging of dopaminergic dysfunction with [123I]FP-CIT SPECT in early-onset parkin disease. Neurology 63 11 (2004) 2097-2103
55. Zimprich A., Biskup S., Leitner P., Lichtner P., Farrer M., Lincoln S., Kachergus J., Hulihan M., Uitti R.J., Calne D.B., Stoessl A.J., Pfeiffer R.F., Patenge N., Carbajal I.C., Vieregge P., Asmus F., Müller-Myhsok B., Dickson D.W., Meitinger T., Strom T.M., Wszolek Z.K., and Gasser T. Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology. Neuron 44 4 (2004) 601-607