Alterations in corticostriatal synaptic plasticity in mice overexpressing human α-synuclein

Neuroscience

Volumn 159, Issue 2, 2009, Pages 501-513

  Watson, J B ^a   Hatami, A ^a   David, H ^a   Masliah, E ^b   Roberts, K ^a   Evans, C E ^a   Levine, M S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

cAMP; chemLTP; facilitation; LTD; paired pulse; presynaptic

Indexed keywords

ADENYLATE CYCLASE; ALPHA SYNUCLEIN; CYCLIC AMP; FORSKOLIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN REGION; CONTROLLED STUDY; CORPUS STRIATUM; GENE MUTATION; GENE OVEREXPRESSION; MALE; MOUSE; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NONHUMAN; PARKINSON DISEASE; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ALPHA-SYNUCLEIN; ANIMALS; BIOPHYSICS; CEREBRAL CORTEX; CORPUS STRIATUM; CYCLIC AMP; ELECTRIC STIMULATION; FORSKOLIN; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; NEURAL PATHWAYS; NEURONAL PLASTICITY; NEURONS; PATCH-CLAMP TECHNIQUES; SYNAPSES;

EID: 60849116119     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.01.021     Document Type: Article

References (83)

1. Abeliovich A., Schmitz Y., Farinas I., Choi-Lundberg D., Ho W.H., Castillo P.E., Shinsky N., Verdugo J.M., Armanini M., Ryan A., Hynes M., Phillips H., Sulzer D., and Rosenthal A. Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 25 (2000) 239-252
2. Ade K.K., and Lovinger D.M. Anandamide regulates postnatal development of long-term synaptic plasticity in the rat dorsolateral striatum. J Neurosci 27 (2007) 2403-2409
3. Akopian G., Musleh W., Smith R., and Walsh J.P. Functional state of corticostriatal synapses determines their expression of short- and long-term plasticity. Synapse 38 (2000) 271-280
4. Bamford N.S., Zhang H., Schmitz Y., Wu N.-P., Cepeda C., Levine M.S., Schmauss C., Zakharenko S.S., Zablow L., and Sulzer D. Heterosynaptic dopamine neurotransmission selects sets of corticostriatal terminals. Neuron 42 (2004) 653-663
5. Berretta N., Nisticò R., Bernardi G., and Mercuri N.B. Synaptic plasticity in the basal ganglia: A similar code for physiological and pathological conditions. Prog Neurobiol 84 (2008) 343-362
6. Bonifati V. LRRK2 low-penetrance mutations (Gly201Ser) and risk alleles (Gly2385Arg)-linking familial and sporadic Parkinson's disease. Neurochem Res 32 (2007) 1700-1708
7. Braak H., Del Tredici K., Rub U., de Vos R.A., Steur E.N.J., and Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 24 (2003) 197-211
8. Cabin D.E., Shimazu K., Murphy D., Cole N.B., Gottschalk W., McIlwain K.L., Orrison B., Chen A., Ellis C.E., Paylor R., Lu B., and Nussbaum R.L. Synaptic vesicle depletion correlates with attenuated synaptic responses to prolonged repetitive stimulation in mice lacking α-synuclein. J Neurosci 22 (2002) 8797-8807
9. Calabresi P., Maj R., Pisani A., Mercuri N.B., and Bernardi G. Long-term synaptic depression in the striatum: physiological and pharmacological characterization. J Neurosci 12 (1992) 4224-4233
10. Calabresi P., Pisani A., Mercuri N.B., and Bernardi G. Long-term potentiation in the striatum is unmasked by removing the voltage-dependent magnesium block of the NMDA receptor channels. Eur J Neurosci 4 (1992) 929-935
11. Castillo P.E., Schoch S., Schmitz F., Südhof T.C., and Malenka R.C. RIM1alpha is required for presynaptic long-term potentiation. Nature 415 (2002) 327-330
12. Cepeda C., André V.M., Yamazaki I., Wu N., Kleiman-Weiner M., and Levine M.S. Differential electrophysiological properties of dopamine D1 and D2 receptor-containing striatal medium-sized spiny neurons. Eur J Neurosci 27 (2008) 671-682
13. Chandra S., Fornai F., Kwon H.-B., Yazdani U., Atasoy D., Liu X., Hammer R.E., Battaglia G., German D.C., Castillo P.E., and Südhof T.C. Double-knockout mice for α- and β-synucleins: effect on synaptic functions. Proc Natl Acad Sci U S A 101 (2004) 14966-14971
14. Choi S., and Lovinger D.M. Decreased probability of neurotransmitter release underlies striatal long-term depression and postnatal development of corticostriatal synapse. Proc Natl Acad Sci U S A 94 (1997) 2665-2670
15. Chotiner J.K., Khorasani H., Nairn A.C., O'Dell T.J., and Watson J.B. Adenylyl cyclase-dependent form of chemical long-term potentiation triggers translational regulation at the elongation step. Neuroscience 116 (2003) 743-752
16. Clayton D.F., and George J.M. The synucleins: a family of proteins involved in synaptic function, plasticity, neurodegeneration, and disease. Trends Neurosci 21 (1998) 249-254
17. Colwell C.S., and Levine M.S. Excitatory synaptic transmission in neostriatal neurons: regulation by cAMP-dependent mechanisms. J Neurosci 15 (1995) 1704-1713
18. Dauer W., and Przedborski S. Parkinson's disease: mechanisms and models. Neuron 39 (2003) 889-909
19. Dube L., Smith A.D., and Bolam J.P. Identification of synaptic terminals of thalamic or cortical origin in contact with distinct medium-size spiny neurons in the rat neostriatum. J Comp Neurol 267 (1988) 455-471
20. Farrer M., Maraganore D.M., Lockhart P., Singleton A., Lesnick T.G., de Andrade M., West A., de Silva R., Hardy J., and Hernandez D. α-Synuclein gene haplotypes are associated with Parkinson's disease. Hum Mol Genet 10 (2001) 1847-1851
21. Fernagut P.O., Hutson C.B., Fleming S.B., Tetreaut N.A., Salcedo J., Masliah E., and Chesselet M.F. Behavioral and histopathological consequences of paraquat intoxication in mice: effects of α-synuclein over-expression. Synapse 61 (2007) 991-1001
22. Fino E., Glowinski J., and Venance L. Bidirectional activity-dependence at corticostriatal synapses. J Neurosci 25 (2005) 11279-11287
23. Fisher R.S., Levine M.S., Sibley D.R., and Ariano M.A. D2 dopamine receptor protein location: Golgi impregnation-gold toned and ultrastructural analysis of the rat neostriatum. J Neurosci Res 38 (1994) 551-564
24. Fleming S.M., Salcedo J., Fernagut P.O., Rockenstein E., Masliah E., Levine M.S., and Chesselet M.F. Early and progressive sensorimotor anomalies in mice overexpressing wild-type human α-synuclein. J Neurosci 24 (2004) 9434-9440
25. Fleming S.M., Salcedo J., Hutson C.B., Rockenstein E., Masliah E., Levine M.S., and Chesselet M.F. Behavioral effects of dopaminergic agonists in transgenic mice overexpressing human wildtype α-synuclein. Neuroscience 142 (2006) 1245-1253
26. García-Junco-Clemente P., Linares-Clemente P., and Fernández-Chacón R. Active zones for presynaptic plasticity in the brain. Mol Psychiatry 10 (2005) 185-200
27. Geracitano R., Paolucci E., Prisco S., Guatteo E., Zona C., Longone P., Ammassari-Teule M., Bernardi G., Berretta N., and Mercuri N.B. Altered long-term corticostriatal synaptic plasticity in transgenic mice overexpressing human Cu/Zn superoxide dismutase (Gly93 → Ala) mutation. Neuroscience 118 (2003) 399-408
28. Giasson B.I., Covy J.P., Bonini N.M., Hurtig H.I., Farrer M.J., Trojanowski J.Q., and Van Deerlin V.M. Biochemical and pathological characterization of Lrrk2. Ann Neurol 59 (2006) 315-322
29. Goldberg M.S., Pisani A., Haburcak M., Vortherms T.A., Kitada T., Costa C., Tong Y., Martella G., Tscherter A., Martins A., Bernardi G., Roth B.I., Pothos E.N., Calabresi P., and Shen J. Dopaminergic deficits report and hypokinesia caused by inactivation of the familial Parkinsonism-linked gene DJ-1. Neuron 45 (2005) 489-496
30. Graybiel A.M., Ragsdale Jr. C.W., Yoneoka E.S., and Elde R.P. An immunohistochemical study of enkephalins and other neuropeptides in the striatum of the cat with evidence that the opiate peptides are arranged to form mosaic patterns in register with the striosomal compartments visible by acetylcholinesterase staining neurons and their striatal targets. Neuroscience 6 (1981) 377-397
31. Graybiel A.M., Aosaki T., Flaherty A., and Kimura M. The basal ganglia and adaptive motor control. Science 265 (1994) 826-831
32. Gureviciene I., Gurevicius K., and Tanila H. Role of α-synuclein in synaptic glutamate release. Neurobiol Dis 28 (2007) 83-89
33. Haber S.N. The primate basal ganglia: parallel and integrative networks. J Chem Neuroanat 26 (2003) 317-330
34. Holzmann C., Kruger R., Saecker A.M., Schmitt I., Schols L., Berger K., and Riess O. Polymorphisms of the α-synuclein promoter: expression analyses and association studies in Parkinson's disease. J Neural Transm 110 (2003) 67-76
35. Huang Y.Y., and Kandel E.R. Postsynaptic induction and PKA-dependent expression of LTP in the lateral amygdala. Neuron 21 (1998) 169-178
36. Hsu L.J., Mallory M., Xia Y., Veinbergs I., Hashimoto M., Yoshimoto M., Thal L.J., Saitoh T., and Masliah E. Expression patters of synucleins (non-Abeta component of Alzheimer's disease amyloid precursors protein/alpha-synuclein) during murine brain development. J Neurochem 71 (1998) 338-344
37. Johnson M.W., Chotiner J.K., and Watson J.B. Isolation and characterization of synaptoneurosomes from single rat hippocampal slices. J Neurosci Methods 77 (1997) 151-156
38. Kim S.J., Kima S.Y., Naa Y.-S., Leeb H.J., Chung K.C., and Baika J.-H. α-Synuclein enhances dopamine D2 receptor signaling. Brain Res 1124 (2006) 5-9
39. Klapstein G.J., Fisher R.S., Zanjani H., Cepeda C., Jokel E.S., Chesselet M.-F., and Levine M.S. Electrophysiological and morphological changes in striatal spiny neurons in R6/2 Huntington's disease transgenic mice. J Neurophysiol 86 (2001) 2667-2677
40. Kreitzer A.C., and Malenka R.C. Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson's disease models. Nature 445 (2007) 643-647
41. Kruger R., Kuhn W., Muller T., Woitalla D., Graeber M., Kosel S., Przuntek H., Epplen J.T., Schols L., and Riess O. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat Genet 18 (1998) 106-108
42. Larsen K.E., Schmitz Y., Troyer M.D., Mosharov E., Dietrich P., Quazi A.Z., Savalle M., Nemani V., Chaudhry F.A., Edwards R.H., Stefanis L., and Sulzer D. α-Synuclein overexpression in PC12 and chromaffin cells impairs catecholamine release by interfering with a late step in exocytosis. J Neurosci 26 (2006) 11915-11922
43. Linden D.J., and Ahn S. Activation of presynaptic cAMP-dependent protein kinase is required for induction of cerebellar long-term potentiation. J Neurosci 19 (1999) 10221-10227
44. Liu S., Ninan I., Antonova I., Battaglia F., Trinchese F., Narasanna A., Kolodilov N., Dauer W., Hawkins R.D., and Arancio O. Alpha-synuclein produces a long-lasting increase in neurotransmitter release. EMBO J 23 (2004) 4506-4516
45. Liu S., Fa M., Ninan I., Trinchese F., Dauer W., and Arancio O. α-Synuclein involvement in hippocampal synaptic plasticity: role of NO, cGMP, cGK and CaMKII. Eur J Neurosci 25 (2007) 3583-3596
46. Lobo M.K., Cui Y., Ostlund S.B., Balleine B.W., and Yang X.W. Genetic control of instrumental conditioning by striatopallidal neuron-specific S1P receptor Gpr6. Nat Neurosci 10 (2007) 1395-1397
47. Lonart G., Schoch S., Kaeser P.S., Larkin C.J., Sudhof T.C., and Linden D.J. Phosphorylation of RIM1alpha by PKA triggers presynaptic long-term potentiation at cerebellar parallel fiber synapses. Cell 115 (2003) 49-60
48. Lovinger D.M., Tyler E.C., and Merritt A. Short- and long-term synaptic depression in rat neostriatum. J Neurophysiol 70 (1993) 1937-1949
49. Mahon S., Deniau J.M., and Charpier S. Corticostriatal plasticity: life after the depression. Trends Neurosci 27 (2004) 460-467
50. 2+/calmodulin-dependent kinase II autophosphorylation. J Neurosci 19 (1999) 2500-2510
51. Malinow R., and Malenka R.C. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25 (2002) 103-126
52. Maroteaux L., and Scheller R.H. The rat brain synucleins: family of proteins transiently associated with neuronal membrane. Brain Res Mol Brain Res 11 (1991) 335-343
53. Matsuoka Y., Villa M., Lincoln S., McCormack A., Picciano M., LaFrancois J., Yu X., Dickson D., Langston W.J., McGowan E., Farrer M., Hardy J., Duff K., Przedborski S., and Di Monte D.A. Lack of nigral pathology in transgenic mice expressing human α-synuclein driven by the tyrosine hydroxylase promoter. Neurobiol Dis 8 (2001) 535-539
54. Murphy D.D., Rueter S.M., Trojanowski J.Q., and Lee V.M. Synucleins are developmentally expressed and α-synuclein regulates the size of the presynaptic vesicular pool in primary hippocampal neurons. J Neurosci 20 (2000) 3214-3220
55. Paisan-Ruiz C., Jain S., Evans E.W., Gilks W.P., Simon J., van der Brug M., Lopez 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., MartiMasso J.F., Perez-Tur J., Wood N.W., and Singleton A.B. Cloning of the gene containing mutations that cause PARK8-linked Parkinson's disease. Neuron 44 (2004) 595-600
56. Pals P., Lincoln S., Manning J., Heckman M., Skipper L., Hulihan M., Van den Broeck M., De Pooter T., Cras P., Crook J., Van Broeckhoven C., and Farrer M.J. α-Synuclein promoter confers susceptibility to Parkinson's disease. Ann Neurol 56 (2004) 591-595
57. Partridge J.G., Tang K.C., and Lovinger D.M. Regional and postnatal heterogeneity of activity-dependent long-term changes in synaptic efficacy in the dorsal striatum. J Neurophysiol 84 (2000) 1422-1429
58. Picconi B., Pisani A., Barone I., Bonsi P., Centonze D., Bernardi G., and Calabresi P. Review pathological synaptic plasticity in the striatum: implications for Parkinson's disease. Neurotoxicology 26 (2005) 779-783
59. 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 (1997) 2045-2047
60. Rockenstein E., Mallory M., Hashimoto M., Song D., Shults C.W., Lang I., and Masliah E. Differential neuropathological alterations in transgenic mice expressing alpha-synuclein from the platelet-derived growth factor and Thy-1 promoters. J Neurosci Res 68 (2002) 568-578
61. Singleton A.B., Farrer M., Johnson J., Singleton A., Hague S., Kachergus J., Hulihan M., Peuralinna T., Dutra A., Nussbaum R., Lincoln S., Crawley A., Hanson M., Maraganore D., Adler C., Cookson M.R., Muenter M., Baptista M., Miller D., Blancato J., et al. Alpha-synuclein locus triplication causes Parkinson's disease. Science 302 (2003) 841
62. Smith R., Musleh W., Akopian G., Buckwalter G., and Walsh J.P. Regional differences in the expression of corticostriatal synaptic plasticity. Neuroscience 106 (2001) 95-101
63. Spencer J.P., and Murphy K.P.S.J. Bi-directional changes in synaptic plasticity induced at corticostriatal synapses in vitro. Exp Brain Res 135 (2000) 497-503
64. Spencer J.P., and Murphy K.P.S.J. Activation of cyclic AMP-dependent protein kinase is required for long-term enhancement at corticostriatal synapses in rats. Neurosci Lett 329 (2002) 217-221
65. Spillantini M.G., Schmidt M.L., Lee V.M., Trojanowski J.Q., Jakes R., and Goedert M. α-Synuclein in Lewy bodies. Nature 388 (1997) 839-840
66. Steidl J.V., Gomez-Isla T., Mariash A., Ashe K.H., and Boland L.M. Altered short-term hippocampal synaptic plasticity in mutant α-synuclein transgenic mice. Neuroreport 14 (2003) 219-223
67. Stevens C.F. Neurotransmitter release at central synapses. Neuron 40 (2003) 381-388
68. Walsh J.P. Depression of excitatory input in rat striatal neurons. Brain Res 608 (1993) 123-128
69. Wang J.H., and Kelly P.T. Attenuation of paired-pulse facilitation associated with synaptic potentiation mediated by postsynaptic mechanisms. J Neurophysiol 78 (1997) 2707-2716
70. Wang Z., Kai L., Day M., Ronesi J., Yin H.H., Ding J., Tkatch T., Lovinger D.M., and Surmeier D.J. Dopaminergic control of corticostriatal long-term synaptic depression in medium spiny neurons is mediated by cholinergic interneurons. Neuron 50 (2006) 443-452
71. Watabe A.M., Zaki P.A., and O'Dell T.J. Coactivation of β-adrenergic and cholinergic receptors enhances the induction of long-term potentiation and synergistically activates mitogen-activated protein kinase in the hippocampal CA1 region. J Neurosci 20 (2000) 5924-5931
72. 2+/calmodulin-dependent protein kinase II. J Neurosci Res 70 (2002) 298-308
73. Watson J.B., Arnold M.M., Ho Y.-S., and O'Dell T.J. Age-dependent modulation of hippocampal long-term potentiation by antioxidant enzymes. J Neurosci Res 84 (2006) 1564-1574
74. Weisskopf M.G., Castillo P.E., Zalutsky R.A., and Nicholl R.A. Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP. Science 265 (1994) 1878-1882
75. Wickens J.R., Begg A.J., and Arbuthnott G.W. Dopamine reverses the depression of rat corticostriatal synapses which normally follows high-frequency stimulation of cortex in vitro. Neuroscience 70 (1996) 1-5
76. Wilson C.J. Morphology and synaptic connections of crossed corticostriatal neurons in the rat. J Comp Neurol 263 (1987) 567-580
77. Wu N.-P., Cepeda C., Masliah E., and Levine M.S. Abnormal glutamate and dopamine receptor function in the striatum of a-synuclein overexpressing mice. Soc Neurosci Abstr 85 (2005) 12
78. Yavich L., Tanila H., Vepsalainen S., and Jakala P. Role of α-synuclein in presynaptic dopamine recruitment. J Neurosci 24 (2004) 11165-11170
79. Yavich L., Oksman M., Tanila H., Kerokoski P., Hiltunen M., van Groen T., Puolivali J., Mannisto P.T., Garcia-Horsman A., MacDonald E., Beyreuther K., Hartmann T., and Jakala P. Locomotor activity and evoked dopamine release are reduced in mice overexpressing A30P-mutated human alpha-synuclein. Neurobiol Dis 20 (2005) 303-313
80. Zalutsky R.A., and Nicoll R.A. Comparison of two forms of long-term potentiation in single hippocampal neurons. Science 248 (1990) 1619-1624
81. Zarranz J.J., Alegre J., Gomez-Esteban J.C., Lezcano E., Ros R., Ampuero I., Vidal L., Hoenicka J., Rodriguez O., Atares B., Llorens V., Gomez Tortosa E., del Ser T., Munoz D.G., and de Yebenes J.G. The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann Neurol 55 (2004) 164-173
82. 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., Muller-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 (2004) 601-607
83. Zucker R.S., and Regehr W.G. Short-term synaptic plasticity. Annu Rev Physiol 64 (2002) 355-405