Mice lacking α-synuclein display functional deficits in the nigrostriatal dopamine system

Neuron

Volumn 25, Issue 1, 2000, Pages 239-252

  Abeliovich, Asa ^a   Schmitz, Yvonne ^d   Fariñas, Isabel ^b   Choi Lundberg, Derek ^c   Ho, Wei Hsien ^c   Castillo, Pablo E ^e   Shinsky, Natasha ^c   Garcia Verdugo, Jose Manuel ^b   Armanini, Mark ^c   Ryan, Anne ^c   Hynes, Mary ^c   Phillips, Heidi ^c   Sulzer, David ^d   Rosenthal, Arnon ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF VALENCIA   (Spain)

^c GENENTECH INC   (United States)

^d NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; CALCIUM; DOPAMINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOPAMINE RELEASE; DOPAMINE UPTAKE; DOPAMINERGIC NERVE CELL; ELECTROSTIMULATION; FEMALE; LOCOMOTION; MALE; MOTOR DYSFUNCTION; MOUSE; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; SYNAPTIC TRANSMISSION;

EID: 0034077041     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80886-7     Document Type: Article

References (52)

1. Buchman, V.L., Hunter, H.J., Pinon, L.G.P., Thompson, J., Primalova, E.M., Ninkina, N.N., and Davies, A.M. (1998). Persyn, a member of the synuclein family, has a distinct pattern of expression in the developing nervous system. J. Neurosci. 18, 9335-9341.
2. Castillo, P.E., Janz, R., Südhof, T.C., Tzounopoulos, T., Malenka, R.C., and Nicoll, R.A. (1997). Rab3A is essential for mossy fibre longterm potentiation in the hippocampus. Nature 388, 590-593.
3. Clayton, D.F., and George, J.M. (1998). The synucleins: A family of proteins involved in synaptic function, plasticity, neurodegeneration, and disease. Trends Neurosci. 21, 249-254.
4. Cohen, F.E., and Prusiner, S.B. (1998). Pathologic conformations of prion proteins. Annu. Rev. Biochem. 67, 793-819.
5. Conway, K.A., Harper, J.D., and Lansbury, P.T. (1998). Accelerated in vitro fibril formation by a mutant linked to early-onset Parkinson's disease. Nat. Med. 4, 1318-1320.
6. Davidson, W.S., Jonas, A., Clayton, D.F., and George, J.M. (1998). Stabilization of α-synuclein secondary structure upon binding to synthetic membranes. J. Biol. Chem. 273, 9443-9449.
7. DiFiglia, M., Sapp, E., Chase, K.O., Davies, S.W., Bates, G.P., Vonsattel, J.P., and Aronin, N. (1997). Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277, 1990-1993.
8. Dittman, J.S., and Regehr, W.G. (1998). Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to Purkinje cell synapse. J. Neurosci. 18, 6147-6162.
9. Fon, E.A., Pothos, E.N., Sun, B.-C., Killeen, N., Sulzer, D., and Edwards, R.H. (1997). Vesicular transport regulates monoamine storage and release but is not essential for amphetamine action. Neuron 19, 1271-1283.
10. Frohman, M.A., and Morris, A.J. (1996). Phospholipid signaling: Rho is only ARF the story. Curr. Biol. 6, 945-947.
11. Garris, P.A., Ciolkowski, E.L., and Wightman, R.M. (1994). Heterogeneity of evoked dopamine overflow in striatal and striatoamygdaloid regions. Neuroscience 59, 417-427.
12. Garris, P.A., Kilpatrick, M., Bunin, M.A., Michael, D., Walker, Q.D., and Wightman, R.M. (1999). Dissociation of dopamine release in the nucleus accumbens from intracranial self-stimulation. Nature 398, 67-69.
13. George, J.M., Jin, W.S., Woods, W.S., and Clayton, D.F. (1995). Characterization of a novel protein regulated during the critical period for song learning in the zebra finch. Neuron 15, 361-372.
14. Goda, Y., and Südhof, T.C. (1997). Calcium regulation of neurotransmitter release: Reliably reliable? Curr. Opin. Cell Biol. 9, 513-518.
15. Gomis, A., Burrone, J., and Lagnado, L. (1999). Two actions of calcium regulate the supply of releasable vesicles at the ribbon synapse of retinal bipolar cells. J. Neurosci. 19, 6309-6317.
16. Grace, A.A., and Bunney, B.S. (1984). The control of firing pattern in nigral dopamine neurons: Burst firing. J. Neurosci. 4, 2877-2890.
17. Hong, M., Zhukareva, V., Vogelsberg-Ragaglia, V., Wszolek, Z., Reed, L., Miller, B.I., Geschwind, D.H., Bird, T.D., McKeel, D., Goate, A., et al. (1998). Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17. Science 282, 1914-1917.
18. Horger, B.A., Nishimura, M.C., Armanini, M.P., Wang, L.C., Poulsen, K.T., Rosenblad, C., Kirik, D., Moffat, B., Simmons, L., Johnson, E., et al. (1998). Neurturin exerts potent actions on survival and function of midbrain dopaminergic neurons. J. Neurosci. 18, 4929-4937.
19. Hynes, M., Poulsen, K., Tessier-Lavigne, M., and Rosenthal, A. (1995). Control of neuronal diversity by the floor plate: Contact-mediated induction of midbrain dopaminergic neurons. Cell 80, 95-101.
20. Iwai, A., Masliah, E., Yoshimoto, M., Ge, N., Flanagan, L., de Silva, H.A., Kittle, A., and Saito, T. (1995). The precursor protein of non-Aβ component of Alzheimer's disease amyloid is a presynaptic protein of the central nervous system. Neuron 14, 467-475.
21. Jakes, R., Spillantini, M.G., and Goedert, M. (1994). Identification of 2 distinct synucleins from human brain. FEBS Lett. 345, 27-32.
22. Jenco, J.M., Rawlingson, A., Daniels, B., and Morris, A.J. (1998). Regulation of phospholipase D2: Selective inhibition of mammalian phospholipase D isoenzymes by α- and β-synucleins. Biochemistry 37, 4901-4909.
23. Jensen, P.H., Sorensen, E.S., Peterson, T.E., Gliemann, J., and Rasumussen, L.K. (1995). Residues in the synuclein consensus motif of α-synuclein fragment, NAC, participate in the transglutaminase-catalysed cross-linking to Alzheimer-disease amyloid βA4 peptide. Biochem. J. 310, 91-94.
24. Jensen, P.H., Hojrup, P., Hager, H., Nielsen, M.S., Jacobsen, L., Olesen, O.F., Gliemann, J., and Jakes, R. (1997). Binding of Aβ to α- and β-synucleins: Identification of segments in α-synuclein/NAC precursor that bind Aβ and NAC. Biochem. J. 323, 539-546.
25. Jones, S.R., Gainetdinov, R.R., Wightman, R.M., and Caron, M.G. (1998). Mechanisms of amphetamine action revealed in mice lacking the dopamine transporter. J. Neurosci. 18, 1979-1986.
26. Kennedy, R.J., Jones, S.R., and Wightman, R.M. (1992). Dynamic observations of dopamine autoreceptor effects in rat striatal slices. J. Neurochem. 59, 449-455.
27. Klein, J., Chalifa, V., Liscovitch, M., and Loffelholz, K. (1995). Role of phospholipase D activation in nervous system physiology and pathophysiology. J. Neurochem. 65, 1445-1455.
28. Krüger, R., Kühn, W., Müller, T., Woitalla, D., Graeber, M., Kösel, S., Przuntek, H., Epplen, J.T., Schöls, L., and Riess, O. (1998). Ala30Pro mutation in the gene encoding α-synuclein in Parkinson's disease. Nat. Genet. 18, 106-108.
29. Lavedan, C. (1998). The synuclein family. Genome Res. 8, 871-880.
30. Maroteaux, L., and Scheller, R.H. (1991). The rat brain synucleins; family of proteins transiently associated with neuronal membrane. Brain Res. Mol. Brain Res. 11, 335-343.
31. Maroteaux, L., Campanelli, J.T., and Scheller, R.H. (1988). Synuclein: A neuron-specific protein localized to the nucleus and presynaptic nerve terminal. J. Neurosci. 8, 2804-2815.
32. Mezey, E., Dehejia, A., Harta, G., Papp, M.I., Polymeropoulos, M.H., and Brownstein, M.J. (1998). α-Synuclein in neurodegenerative disorders: Murderer or accomplice? Nat. Med. 4, 755-756.
33. Moore, M.W., Klein, R.D., Fariñas, I., Sauer, H., Armanini, M., Phillips, H., Reichardt, L.F., Ryan, A.M., Carver-Moore, K., and Rosenthal, A. (1996). Renal and neuronal abnormalities in mice lacking GDNF. Nature 382, 76-79.
34. Ostrerova, N., Petrucelli, L., Farrer, M., Mehta, N., Choi, P., Hardy, J., and Wolozin, B. (1999). α-Synuclein shares physical and functional homology with 14-3-3 protein. J. Neurosci. 19, 5782-5791.
35. Paik, S.R., Lee, J.-H., Kim, D.-H., Chang, C.-S., and Kim, Y.-S. (1998). Self-oligomerization of NACP, the precursor protein of the non-amyloid β-/A4 (Aβ) component of Alzheimer's disease amyloid, observed in the presence of a C-terminal Aβ fragment (residues 25-35). FEBS Lett. 421, 73-76.
36. Polymeropoulos, M.H., Lavedan, C., Leroy, E., Ide, S.E., Dehejia, A., Dutra, A., Pike, B., Root, H., Rubenstein, J., Boyer, R., et al. (1997). Mutations in the α-synuclein gene identified in families with Parkinson's disease. Science 276, 2045-2047.
37. Rebec, G.V., Grabner, C.P., Pierce, R.C., and Bardo, M.T. (1997). Transient increases in catecholamine activity in medial prefrontal cortex and nucleus accumbens shell during novelty. Neuroscience 76, 707-714.
38. Schlüter, O.M., Schnell, E., Verhage, M., Tzonopoulos, T., Nicoll, R.A., Janz, R., Malenka, R.C., Geppert, M., and Südhof, T.C. (1999). Rabphilin knock-out mice reveal that rabphilin is not required for Rab3 function in regulating neurotransmitter release. J. Neurosci. 19, 5834-5846.
39. Seiden, L.S., Sabol, K.E., and Ricaurte, G.A. (1993). Amphetamine: Effects on catecholamine systems and behavior. Annu. Rev. Pharmacol. Toxicol. 32, 639-677.
40. Spillantini, M.G., Crowther, R.A., Jakes, R., Hasegawa, M., and Goedert, M. (1998). α-Synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with Lewy bodies. Proc. Natl. Acad. Sci. USA 95, 6469-6473.
41. Starke, K., Gothert, M., and Kilbinger, H. (1989). Modulation of presynaptic release by presynaptic autoreceptors. J. Neurochem. 2, 449-455.
42. Stevens, C.F., and Tsujimoto, T. (1995). Estimates for the pool size of releasable quanta at a single central synapse and for the time required to fill the pool. Proc. Natl. Acad. Sci. USA 92, 846-849.
43. Stevens, C.F., and Wesseling, J.F. (1998). Activity-dependent modulation of the rat at which synaptic vesicles become available to undergo exocytosis. Neuron 21, 415-424.
44. Südhof, T.C. (1995). The synaptic vesicle cycle: A cascade of protein - Protein interactions. Nature 375, 645-653.
45. Sulzer, D., Chen, T.-K., Lau, Y.Y., Kristensen, H., Rayport, S., and Ewing, A. (1995). Amphetamine redistributes dopamine from synaptic vesicles to the cytosol and promotes reverse transport. J. Neurosci. 15, 4102-4108.
46. Tong, G., Malenka, R.C., and Nicoll, R.A. (1996). Long-term potentiation in cultures of single hippocampal granule cells: A presynaptic form of plasticity. Neuron 16, 1147-1157.
47. Ueda, K., Fukushima, H., Masliah, E., Xia, Y., Iwai, A., Yoshimoto, M., Otero, D.A.C., Kondo, J., Ihara, Y., and Saitoh, T. (1993). Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer's disease. Proc. Natl. Acad. Sci. USA 90,11282-11286.
48. Wang, L.-Y., and Kaczmarek, L.K. (1998). High-frequencyfiring helps replenish the readily releasable pool of synaptic vesicles. Nature 394, 384-388.
49. Weinreb, P.H., Zhen, W., Poon, A.W., Conway, K.A., and Lansbury, P.T. (1996). NACP, a protein implicated in Alzheimer's disease and learning, is natively unfolded. Biochemistry 35, 13709-13715.
50. Wightman, R.M., and Zimmerman, J.B. (1990). Control of dopamine extracellular concentration in rat striatum by impulse flow and uptake. Brain Res. Brain Res. Rev. 15, 135-144.
51. Williams, G.W., and Goldman-Rakic, P.S. (1995). Modulation of memory fields by dopamine D1 receptors in prefrontal cortex. Nature 376, 572-575.
52. Wise, R.A. (1996). Addictive drugs and brain stimulation reward. Annu. Rev. Neurosci. 19, 319-340.