PINK1 heterozygous mutations induce subtle alterations in dopamine-dependent synaptic plasticity

Movement Disorders

Volumn 29, Issue 1, 2014, Pages 41-53

  Madeo, Graziella ^a   Schirinzi, Tommaso ^a   Martella, Giuseppina ^a   Latagliata, E Claudio ^b,c   Puglisi, Francesca ^a   Shen, Jie ^d   Valente, Enza Maria ^e,f   Federici, Mauro ^b   Mercuri, Nicola B ^a,b   Puglisi Allegra, Stefano ^b,c   Bonsi, Paola ^b   Pisani, Antonio ^a,b  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d HARVARD MEDICAL SCHOOL   (United States)

^e CASA SOLLIEVO DELLA SOFFERENZA HOSPITAL   (Italy)

^f UNIVERSITY OF SALERNO   (Italy)

Author keywords

Autosomal recessive Parkinson's disease; Heterozygous mutations; PINK1; Striatum; Synaptic plasticity

Indexed keywords

DOPAMINE; DOPAMINE RECEPTOR; MONOAMINE OXIDASE B INHIBITOR; PARKIN; PHOSPHATASE AND TENSIN HOMOLOG INDUCED PUTATIVE KINASE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; ENDOPHENOTYPE; GENE; GENE MUTATION; HETEROZYGOTE; LOCOMOTION; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MOTOR COORDINATION; MOUSE; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; STIMULUS RESPONSE;

AUTOSOMAL RECESSIVE PARKINSON'S DISEASE; HETEROZYGOUS MUTATIONS; PINK1; STRIATUM; SYNAPTIC PLASTICITY;

ANIMALS; CEREBRAL CORTEX; CORPUS STRIATUM; DOPAMINE; MICE; MICE, KNOCKOUT; MOTOR ACTIVITY; NEURONAL PLASTICITY; PROTEIN KINASES; RECEPTORS, DOPAMINE; ROTAROD PERFORMANCE TEST; SUBSTANTIA NIGRA; SYNAPSES;

EID: 84892946302     PISSN: 08853185     EISSN: 15318257     Source Type: Journal    
DOI: 10.1002/mds.25724     Document Type: Article

References (70)

1. Puschmann A. Monogenic Parkinson's disease and parkinsonism: clinical phenotypes and frequencies of known mutations. Parkinsonism Rel Dis 2013;19:407-415.
2. Samaranch L, Lorenzo-Betancor O, Arbelo JM, et al. PINK1-linked parkinsonism is associated with Lewy body pathology. Brain 2010;133:1128-1142.
3. Marongiu R, Ferraris A, Ialongo T, et al. PINK1 heterozygous rare variants: prevalence, significance and phenotypic spectrum [serial online]. Hum Mutat 2008;29:565.
4. Ibanez P, Lesage S, Lohmann E, et al. Mutational analysis of the PINK1 gene in early-onset parkinsonism in Europe and North Africa. Brain 2006;129:686-694.
5. Dauer W, Przedborski S. Parkinson's disease: mechanisms and models. Neuron 2003;39:889-909.
6. Calabresi P, Di Filippo M, Gallina A, et al. New synaptic and molecular targets for neuroprotection in Parkinson's disease. Mov Disord 2013;28:51-60.
7. Morrish PK, Sawle GV, Brooks DJ. Regional changes in [18F]dopa metabolism in the striatum in Parkinson's disease. Brain 1996;119(pt 6):2097-2103.
8. Hilker R, Schweitzer K, Coburger S, et al. Nonlinear progression of Parkinson disease as determined by serial positron emission tomographic imaging of striatal fluorodopa F 18 activity. Arch Neurol 2005;62:378-382.
9. van Nuenen BF, Weiss MM, Bloem BR, et al. Heterozygous carriers of a Parkin or PINK1 mutation share a common functional endophenotype. Neurology 2009;72:1041-1047.
10. van Nuenen BF, van Eimeren T, van der Vegt JP, et al. Mapping preclinical compensation in Parkinson's disease: an imaging genomics approach. Mov Disord 2009;24(suppl 2):S703-S710.
11. Eggers C, Schmidt A, Hagenah J, et al. Progression of subtle motor signs in PINK1 mutation carriers with mild dopaminergic deficit. Neurology 2010;74:1798-1805.
12. Khan NL, Valente EM, Bentivoglio AR, et al. Clinical and subclinical dopaminergic dysfunction in PARK6-linked parkinsonism: an 18F-dopa PET study. Ann Neurol 2002;52:849-853.
13. Fiorio M, Valente EM, Gambarin M, et al. Subclinical sensory abnormalities in unaffected PINK1 heterozygotes. J Neurol 2008;255:1372-1377.
14. Kitada T, Pisani A, Porter DR, et al. Impaired dopamine release and synaptic plasticity in the striatum of PINK1-deficient mice. Proc Natl Acad Sci U S A 2007;104:11441-11446.
15. Mercuri NB, Scarponi M, Bonci A, Siniscalchi A, Bernardi G. Monoamine oxidase inhibition causes a long-term prolongation of the dopamine-induced responses in rat midbrain dopaminergic cells. J Neurosci 1997;17:2267-2272.
16. Goldberg MS, Pisani A, Haburcak M, et al. Nigrostriatal dopaminergic deficits and hypokinesia caused by inactivation of the familial Parkinsonism-linked gene DJ-1. Neuron 2005;45:489-496.
17. Martella G, Tassone A, Sciamanna G, et al. Impairment of bidirectional synaptic plasticity in the striatum of a mouse model of DYT1 dystonia: role of endogenous acetylcholine. Brain 2009;132(pt 9):2336-2349.
18. Ding J, Peterson JD, Surmeier DJ. Corticostriatal and thalamostriatal synapses have distinctive properties. J Neurosci 2008;28:6483-6492.
19. Cossart R, Hirsch JC, Cannon RC, et al. Distribution of spontaneous currents along the somato-dendritic axis of rat hippocampal CA1 pyramidal neurons. Neuroscience 2000;99:593-603.
20. Cuomo D, Martella G, Barabino E, et al. Metabotropic glutamate receptor subtype 4 selectively modulates both glutamate and GABA transmission in the striatum: implications for Parkinson's disease treatment. J Neurochem 2009;109:1096-1105.
21. Mercuri NB, Stratta F, Calabresi P, Bonci A, Bernardi G. Activation of metabotropic glutamate receptors induces an inward current in rat dopamine mesencephalic neurons. Neuroscience 1993;56:399-407.
22. Mercuri NB, Bonci A, Johnson SW, Stratta F, Calabresi P, Bernardi G. Effects of anoxia on rat midbrain dopamine neurons. J Neurophysiol 1994;71:1165-1173.
23. Napolitano F, Bonito-Oliva A, Federici M, et al. Role of aberrant striatal dopamine D1 receptor/cAMP/protein kinase A/DARPP32 signaling in the paradoxical calming effect of amphetamine. J Neurosci 2010;30:11043-11056.
24. Mercuri NB, Bonci A, Calabresi P, Stefani A, Bernardi G. Properties of the hyperpolarization-activated cation current Ih in rat midbrain dopaminergic neurons. Eur J Neurosci 1995;7:462-469.
25. Kawagoe KT, Wightman RM. Characterization of amperometry for in vivo measurement of dopamine dynamics in the rat brain. Talanta 1994;41:865-874.
26. Schmitz Y, Lee CJ, Schmauss C, Gonon F, Sulzer D. Amphetamine distorts stimulation-dependent dopamine overflow: effects on D2 auto-receptors, transporters, and synaptic vesicle stores. J Neurosci 2001;21:5916-5924.
27. Sciamanna G, Tassone A, Mandolesi G, et al. Cholinergic dysfunction alters synaptic integration between thalamostriatal and corticostriatal inputs in DYT1 dystonia. J Neurosci 2012;32:11991-12004.
28. Ventura R, Alcaro A, Cabib S, Conversi D, Mandolesi L, Puglisi-Allegra S. Dopamine in the medial prefrontal cortex controls genotype-dependent effects of amphetamine on mesoaccumbens dopamine release and locomotion. Neuropsychopharmacology 2004;29:72-80.
29. Spink AJ, Tegelenbosch RA, Buma MO, Noldus LP. The EthoVision video tracking system-a tool for behavioral phenotyping of transgenic mice. Physiol Behav 2001;73:731-744.
30. Glasl L, Kloos K, Giesert F, et al. Pink1-deficiency in mice impairs gait, olfaction and serotonergic innervation of the olfactory bulb. Exp Neurol 2012;235:214-227.
31. Grinberg LT, Rueb U, Alho AT, Heinsen H. Brainstem pathology and non-motor symptoms in PD. J Neurol Sci 2010;289(1-2):81-88.
32. Jellinger KA. Synuclein deposition and non-motor symptoms in Parkinson disease. J Neurol Sci 2011;310(1-2):107-111.
33. Smith GA, Isacson O, Dunnett SB. The search for genetic mouse models of prodromal Parkinson's disease. Exp Neurol 2012;237:267-273.
34. Lacey MG, Mercuri NB, North RA. Dopamine acts on D2 receptors to increase potassium conductance in neurones of the rat substantia nigra zona compacta. J Physiol 1987;392:397-416.
35. Kitada T, Pisani A, Karouani M, et al. Impaired dopamine release and synaptic plasticity in the striatum of Parkin -/- mice. J Neurochem 2009;110:613-621.
36. Tozzi A, de Iure A, Di Filippo M, et al. the distinct role of medium spiny neurons and cholinergic interneurons in the D2/A2A receptor interaction in the striatum: implications for Parkinson's disease. J Neurosci 2011;31:1850-1862.
37. Calabresi P, Pisani A, Mercuri NB, Bernardi G. Long-term potentiation in the striatum is unmasked by removing the voltage-dependent magnesium block of NMDA receptor channels. Eur J Neurosci 1992;4:929-935.
38. Centonze D, Gubellini P, Picconi B, et al. An abnormal striatal synaptic plasticity may account for the selective neuronal vulnerability in Huntington's disease. Neurol Sci 2001;22:61-62.
39. Kerr JN, Wickens JR. Dopamine D-1/D-5 receptor activation is required for long-term potentiation in the rat neostriatum in vitro. J Neurophysiol 2001;85:117-124.
40. Ledonne A, Berretta N, Davoli A, Rizzo GR, Bernardi G, Mercuri NB. Electrophysiological effects of trace amines on mesencephalic dopaminergic neurons [serial online]. Front Syst Neurosci 2011;5:56.
41. Dimpfel W, Hoffmann JA. Electropharmacograms of rasagiline, its metabolite aminoindan and selegiline in the freely moving rat. Neuropsychobiology 2010;62:213-220.
42. Schapira AHV. Monoamine oxidase B inhibitors for the treatment of Parkinson's disease. CNS Drugs 2011;25:1061-1071.
43. Engberg G, Elebring T, Nissbrandt H. Deprenyl (selegiline), a selective MAO-B inhibitor with active metabolites; effects on locomotor activity, dopaminergic neurotransmission and firing rate of nigral dopamine neurons. J Pharmacol Exp Ther 1991;259:841-847.
44. Madeo G, Martella G, Schirinzi T, Ponterio G, Shen J, Bonsi P, Pisani A. Aberrant striatal synaptic plasticity in monogenic parkinsonisms. Neuroscience 2012;211:126-135.
45. Picconi B, Piccoli G, Calabresi P. Synaptic dysfunction in Parkinson's disease. Adv Exp Med Biol 2012;970:553-572.
46. Klein C, Lohmann-Hedrich K, Rogaeva E, Schlossmacher MG, Lang AE. Deciphering the role of heterozygous mutations in genes associated with parkinsonism. Lancet Neurol 2007;6:652-662.
47. Hilker R, Klein C, Ghaemi M, et al. Positron emission tomographic analysis of the nigrostriatal dopaminergic system in familial parkinsonism associated with mutations in the parkin gene. Ann Neurol 2001;49:367-376.
48. Khan NL, Scherfler C, Graham E, et al. Dopaminergic dysfunction in unrelated, asymptomatic carriers of a single parkin mutation. Neurology 2005;64:134-136.
49. Walter U, Klein C, Hilker R, Benecke R, Pramstaller PP, Dressler D. Brain parenchyma sonography detects preclinical parkinsonism. Mov Disord 2004;1912:1445-1449.
50. Paille V, Picconi B, Bagetta V, et al. Distinct levels of dopamine denervation differentially alter striatal synaptic plasticity and NMDA receptor subunit composition. J Neurosci 2010;30:14182-14193.
51. Agid Y. Parkinson's disease: pathophysiology. Lancet 1991;337:1321-1324.
52. Bezard E, Dovero S, Prunier C, et al. Relationship between the appearance of symptoms and the level of nigrostriatal degeneration in a progressive 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-lesioned macaque model of Parkinson's disease. J. Neurosci 2001;21:6853-6861.
53. Buhmann C, Binkofski F, Klein C, et al. Motor reorganization in asymptomatic carriers of a single mutant Parkin allele: a human model for presymptomatic parkinsonism. Brain 2005;128:2281-2290.
54. Schneider SA, Talelli P, Cheeran BJ, et al. Motor cortical physiology in patients and asymptomatic carriers of parkin gene mutations. Mov Disord 2008;23:1812-1819.
55. Khan NL, Brooks DJ, Pavese N, et al. Progression of nigrostriatal dysfunction in a Parkin kindred: an [18F]dopa PET and clinical study. Brain 2002;125:2248-2256.
56. Kuromi H, Kidokoro Y. Exocytosis and endocytosis of synaptic vesicles and functional roles of vesicle pools: lessons from the Drosophila neuromuscular junction. Neuroscientist 2005;11:138-147.
57. Rizzoli SO, Betz WJ. Synaptic vesicle pools. Nat Rev Neurosci 2005;6:57-69.
58. Gautier CA, Kitada T, Shen J. Loss of PINK1 causes mitochondrial functional defects and increased sensitivity to oxidative stress. Proc Natl Acad Sci U S A 2008;105:11364-11369.
59. Morais VA, Verstreken P, Roethig A, et al. Parkinson's disease mutations in PINK1 result in decreased complex I activity and deficient synaptic function. EMBO Mol Med 2090;1:99-111.
60. Vos M, Lauwers E, Verstreken P. Synaptic mitochondria in synaptic transmission and organization of vesicle pools in health and disease [serial online]. Front Synaptic Neurosci 2010;2:139.
61. Mochida S. Activity-dependent regulation of synaptic vesicle exocytosis and presynaptic short-term plasticity. Neurosci Res 2011;70:16-23.
62. Ivannikov MV, Sugimori M, Llinas RR. Synaptic vesicle exocytosis in hippocampal synaptosomes correlates directly with total mitochondrial volume. J Mol Neurosci 2013;49:223-230.
63. Calabresi P, Picconi B, Tozzi A, Di Filippo M. Dopamine-mediated regulation of corticostriatal synaptic plasticity. Trends Neurosci 2007;30:211-219.
64. Nicola SM, Surmeier J, Malenka RC. Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu Rev Neurosci 2000;23:185-215.
65. Parker EM, Cubeddu LX. Comparative effects of amphetamine, phenylethylamine and related drugs on dopamine efflux, dopamine uptake and mazindol binding. J Pharmacol Exp Ther 1988;245:199-210.
66. Bailey BA, Philips SR, Boulton AA. In vivo release of endogenous dopamine, 5-hydroxytryptamine and some of their metabolites from rat caudate nucleus by phenylethylamine. Neurochem Res 1987;12:173-178.
67. Geracitano R, Federici M, Prisco S, Bernardi G, Mercuri NB. Inhibitory effects of trace amines on rat midbrain dopaminergic neurons. Neuropharmacology 2004;46:807-814.
68. Reynolds GP, Elsworth JD, Blau K, Sandler M, Lees AJ, Stern GM. Deprenyl is metabolized to methamphetamine and amphetamine in man. Br J Clin. Pharmacol 1978;6:542-544.
69. Simpson LL. Evidence that deprenyl, a type B monoamine oxidase inhibitor, is an indirectly acting sympathomimetic amine. Biochem Pharmacol 1978;27:1591-1595.
70. Youdim MB, Gross A, Finberg JP. Rasagiline [N-propargyl-1R(fl)-aminoindan], a selective and potent inhibitor of mitochondrial monoamine oxidase B. Br J Pharmacol 2001;132:500-506.