Synaptic vesicle trafficking and Parkinson's disease

Developmental Neurobiology

Volumn 72, Issue 1, 2012, Pages 134-144

  Esposito, Giovanni ^a,b   Ana Clara, Fernandes ^a,b   Verstreken, Patrik ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

synuclein; Endocytosis; Exocytosis; SNARE complex; Synaptic vesicle

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALPHA SYNUCLEIN; DOPAMINE; DYNAMIN; ENDOPHILIN; LEUCINE RICH REPEAT KINASE 2; MITOCHONDRIAL DNA; PARKIN; RAB PROTEIN; SNARE PROTEIN; SYNAPSIN; SYNAPTOTAGMIN;

ALZHEIMER DISEASE; DEGENERATIVE DISEASE; DOPAMINERGIC NERVE CELL; ENDOCYTOSIS; EXOCYTOSIS; GENE MUTATION; HUMAN; MEMBRANE TRANSPORT; NERVE CELL DEGENERATION; NERVE ENDING; NEUROLOGIC DISEASE; NEUROPATHOLOGY; NEUROTRANSMITTER RELEASE; PARKINSON DISEASE; PRIORITY JOURNAL; REVIEW; SYNAPSE VESICLE;

ANIMALS; HUMANS; NERVE TISSUE PROTEINS; PARKINSON DISEASE; PROTEIN TRANSPORT; SYNAPSES; SYNAPTIC VESICLES;

EID: 83455225173     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20916     Document Type: Review

References (131)

1. Abeliovich A, Schmitz Y, Farinas I, Choi-Lundberg D, Ho WH, Castillo PE, Shinsky N, et al. 2000. Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 25: 239-252.
2. Akbergenova Y, Bykhovskaia M. 2007. Synapsin maintains the reserve vesicle pool and spatial segregation of the recycling pool in Drosophila presynaptic boutons. Brain Res 1178: 52-64.
3. Antunes F, Nunes C, Laranjinha J, Cadenas E. 2005. Redox interactions of nitric oxide with dopamine and its derivatives. Toxicology 208: 207-212.
4. Auffret A, Mariani J, Rovira C. 2010. Age-related progressive synaptic dysfunction: The critical role of presenilin 1. Rev Neurosci 21: 239-250.
5. Baldelli P, Fassio A, Valtorta F, Benfenati F. 2007. Lack of synapsin I reduces the readily releasable pool of synaptic vesicles at central inhibitory synapses. J Neurosci 27: 13520-13531.
6. Beites CL, Xie H, Bowser R, Trimble WS. 1999. The septin CDCrel-1 binds syntaxin and inhibits exocytosis. Nat Neurosci 2: 434-439.
7. Bertram L, Lill CM, Tanzi RE. 2010. The genetics of Alzheimer disease: Back to the future. Neuron 68: 270-281.
8. Bisaglia M, Greggio E, Maric D, Miller DW, Cookson MR, Bubacco L. 2010. Alpha-synuclein overexpression increases dopamine toxicity in BE2-M17 cells. BMC Neurosci 11: 41.
9. Biskup S, Moore DJ, Celsi F, Higashi S, West AB, Andrabi SA, Kurkinen K, et al. 2006. Localization of LRRK2 to membranous and vesicular structures in mammalian brain. Ann Neurol 60: 557-569.
10. Bove J, Prou D, Perier C, Przedborski S. 2005. Toxin-induced models of Parkinson's disease. Neuro Rx 2: 484-494.
11. Bredesen DE, Rao RV, Mehlen P. 2006. Cell death in the nervous system. Nature 443: 796-802.
12. Burre J, Sharma M, Tsetsenis T, Buchman V, Etherton MR, Sudhof TC. 2010. Alpha-synuclein promotes SNARE-complex assembly in vivo and in vitro. Science 329: 1663-1667.
13. Caballol N, Marti MJ, Tolosa E. 2007. Cognitive dysfunction and dementia in Parkinson disease. Mov Disord. 22 Suppl 17: S358-S366.
14. Cabin DE, Shimazu K, Murphy D, Cole NB, Gottschalk W, McIlwain KL, Orrison B, et al. 2002. Synaptic vesicle depletion correlates with attenuated synaptic responses to prolonged repetitive stimulation in mice lacking alpha-synuclein. J Neurosci 22: 8797-8807.
15. Cajigas IJ, Will T, Schuman EM. 2010. Protein homeostasis and synaptic plasticity. EMBO J 29: 2746-2752.
16. Carney DS, Davies BA, Horazdovsky BF. 2006. Vps9 domain-containing proteins: Activators of Rab5 GTPases from yeast to neurons. Trends Cell Biol 16: 27-35.
17. Chandra S, Gallardo G, Fernandez-Chacon R, Schluter OM, Sudhof TC. 2005. Alpha-synuclein cooperates with CSPalpha in preventing neurodegeneration. Cell 123: 383-396.
18. Chen L, Feany MB. 2005. Alpha-synuclein phosphorylation controls neurotoxicity and inclusion formation in a Drosophila model of Parkinson disease. Nat Neurosci 8: 657-663.
19. Chung CY, Koprich JB, Hallett PJ, Isacson O. 2009. Functional enhancement and protection of dopaminergic terminals by RAB3B overexpression. Proc Natl Acad Sci U S A 106: 22474-22479.
20. Chung KK, Zhang Y, Lim KL, Tanaka Y, Huang H, Gao J, Ross CA, et al. 2001. Parkin ubiquitinates the alpha-synuclein-interacting protein, synphilin-1: Implications for Lewy-body formation in Parkinson disease. Nat Med 7: 1144-1150.
21. Clayton DF, George JM. 1998. The synucleins: A family of proteins involved in synaptic function, plasticity, neurodegeneration and disease. Trends Neurosci 21: 249-254.
22. Conway KA, Lee SJ, Rochet JC, Ding TT, Williamson RE, Lansbury PTJr. 2000. Acceleration of oligomerization, not fibrillization, is a shared property of both alpha-synuclein mutations linked to early-onset Parkinson's disease: Implications for pathogenesis and therapy. Proc Natl Acad Sci U S A 97: 571-576.
23. Conway KA, Rochet JC, Bieganski RM, Lansbury PTJr. 2001. Kinetic stabilization of the alpha-synuclein protofibril by a dopamine-alpha-synuclein adduct. Science 294: 1346-1349.
24. Cookson MR, Bandmann O. 2010. Parkinson's disease: Insights from pathways. Hum Mol Genet 19: R21-27.
25. Cremona O, Di Paolo G, Wenk MR, Luthi A, Kim WT, Takei K, Daniell L, et al. 1999. Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 99: 179-188.
26. Dalfo E, Gomez-Isla T, Rosa JL, Nieto Bodelon M, Cuadrado Tejedor M, Barrachina M, Ambrosio S, et al. 2004. Abnormal alpha-synuclein interactions with Rab proteins in alpha-synuclein A30P transgenic mice. J Neuropathol Exp Neurol 63: 302-313.
27. Davie CA. 2008. A review of Parkinson's disease. Br Med Bull 86: 109-127.
28. de Castro IP, Martins LM, Loh SH. 2011. Mitochondrial quality control and Parkinson's disease: A pathway unfolds. Mol Neurobiol 43: 80-86.
29. de Hoop MJ, Huber LA, Stenmark H, Williamson E, Zerial M, Parton RG, Dotti CG. 1994. The involvement of the small GTP-binding protein Rab5a in neuronal endocytosis. Neuron 13: 11-22.
30. de Lau LM, Breteler MM. 2006. Epidemiology of Parkinson's disease. Lancet Neurol 5: 525-535.
31. Dittman J, Ryan TA. 2009. Molecular circuitry of endocytosis at nerve terminals. Annu Rev Cell Dev Biol 25: 133-160.
32. Dong Z, Ferger B, Paterna JC, Vogel D, Furler S, Osinde M, Feldon J, et al. 2003. Dopamine-dependent neurodegeneration in rats induced by viral vector-mediated overexpression of the parkin target protein, CDCrel-1. Proc Natl Acad Sci U S A 100: 12438-12443.
33. Douglas PM, Dillin A. 2010. Protein homeostasis and aging in neurodegeneration. J Cell Biol 190: 719-729.
34. Elbaz A, Dufouil C, Alperovitch A. 2007. Interaction between genes and environment in neurodegenerative diseases. C R Biol 330: 318-328.
35. Evergren E, Benfenati F, Shupliakov O. 2007. The synapsin cycle: A view from the synaptic endocytic zone. J Neurosci Res 85: 2648-2656.
36. Fahn S. 2003. Description of Parkinson's disease as a clinical syndrome. Ann N Y Acad Sci 991: 1-14.
37. Fernandez-Chacon R, Wolfel M, Nishimune H, Tabares L, Schmitz F, Castellano-Munoz M, Rosenmund C, et al. 2004. The synaptic vesicle protein CSP alpha prevents presynaptic degeneration. Neuron 42: 237-251.
38. Fischer von Mollard G, Stahl B, Walch-Solimena C, Takei K, Daniels L, Khoklatchev A, De Camilli P, et al. 1994. Localization of Rab5 to synaptic vesicles identifies endosomal intermediate in synaptic vesicle recycling pathway. Eur J Cell Biol 65: 319-326.
39. Funayama M, Hasegawa K, Ohta E, Kawashima N, Komiyama M, Kowa H, Tsuji S, et al. 2005. An LRRK2 mutation as a cause for the parkinsonism in the original PARK8 family. Ann Neurol 57: 918-921.
40. Gad H, Ringstad N, Low P, Kjaerulff O, Gustafsson J, Wenk M, Di Paolo G, et al. 2000. Fission and uncoating of synaptic clathrin-coated vesicles are perturbed by disruption of interactions with the SH3 domain of endophilin. Neuron 27: 301-312.
41. Geppert M, Bolshakov VY, Siegelbaum SA, Takei K, De Camilli P, Hammer RE, Sudhof TC. 1994. The role of Rab3A in neurotransmitter release. Nature 369: 493-497.
42. Geppert M, Goda Y, Stevens CF, Sudhof TC. 1997. The small GTP-binding protein Rab3A regulates a late step in synaptic vesicle fusion. Nature 387: 810-814.
43. Gilks WP, Abou-Sleiman PM, Gandhi S, Jain S, Singleton A, Lees AJ, Shaw K, et al. 2005. A common LRRK2 mutation in idiopathic Parkinson's disease. Lancet 365: 415-416.
44. Gitler D, Cheng Q, Greengard P, Augustine GJ. 2008. Synapsin IIa controls the reserve pool of glutamatergic synaptic vesicles. J Neurosci 28: 10835-10843.
45. Goldberg MS, Lansbury PTJr. 2000. Is there a cause-and-effect relationship between alpha-synuclein fibrillization and Parkinson's disease? Nat Cell Biol 2: E115-E119.
46. Greggio E, Cookson MR. 2009. Leucine-rich repeat kinase 2 mutations and Parkinson's disease: Three questions. ASN Neuro 1.
47. Guichet A, Wucherpfennig T, Dudu V, Etter S, Wilsch-Brauniger M, Hellwig A, Gonzalez-Gaitan M, et al. 2002. Essential role of endophilin A in synaptic vesicle budding at the Drosophila neuromuscular junction. EMBO J 21: 1661-1672.
48. Hampe C, Ardila-Osorio H, Fournier M, Brice A, Corti O. 2006. Biochemical analysis of Parkinson's disease-causing variants of Parkin, an E3 ubiquitin-protein ligase with monoubiquitylation capacity. Hum Mol Genet 15: 2059-2075.
49. Healy DG, Wood NW, Schapira AH. 2008. Test for LRRK2 mutations in patients with Parkinson's disease. Pract Neurol 8: 381-385.
50. Helton TD, Otsuka T, Lee MC, Mu Y, Ehlers MD. 2008. Pruning and loss of excitatory synapses by the parkin ubiquitin ligase. Proc Natl Acad Sci U S A 105: 19492-19497.
51. Higashi S, Biskup S, West AB, Trinkaus D, Dawson VL, Faull RL, Waldvogel HJ, et al. 2007. Localization of Parkinson's disease-associated LRRK2 in normal and pathological human brain. Brain Res 1155: 208-219.
52. Hobson RJ, Liu Q, Watanabe S, Jorgensen EM. 2010. Complexin Maintains Vesicles in the Primed State in C. elegans. Curr Biol 21: 106-113.
53. Huynh DP, Scoles DR, Nguyen D, Pulst SM. 2003. The autosomal recessive juvenile Parkinson disease gene product, parkin, interacts with and ubiquitinates synaptotagmin XI. Hum Mol Genet 12: 2587-2597.
54. Iwai A, Masliah E, Yoshimoto M, Ge N, Flanagan L, de Silva HA, Kittel A, Saitoh T. 1995. The precursor protein of non-A beta component of Alzheimer's disease amyloid is a presynaptic protein of the central nervous system. Neuron 14: 467-475.
55. Jankovic J. 2008. Parkinson's disease: Clinical features and diagnosis. J Neurol Neurosurg Psychiatry 79: 368-376.
56. Jiang H, Ren Y, Zhao J, Feng J. 2004. Parkin protects human dopaminergic neuroblastoma cells against dopamine-induced apoptosis. Hum Mol Genet 13: 1745-1754.
57. Kamp F, Beyer K. 2006. Binding of alpha-synuclein affects the lipid packing in bilayers of small vesicles. J Biol Chem 281: 9251-9259.
58. Kasprowicz J, Kuenen S, Miskiewicz K, Habets RL, Smitz L, Verstreken P. 2008. Inactivation of clathrin heavy chain inhibits synaptic recycling but allows bulk membrane uptake. J Cell Biol 182: 1007-1016.
59. Katz B, Miledi R. 1968. The effect of local blockage of motor nerve terminals. J Physiol 199: 729-741.
60. Koh TW, Verstreken P, Bellen HJ. 2004. Dap160/intersectin acts as a stabilizing scaffold required for synaptic development and vesicle endocytosis. Neuron 43: 193-205.
61. Kruger R, Kuhn W, Muller T, Woitalla D, Graeber M, Kosel S, Przuntek H, et al. 1998. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat Genet 18: 106-108.
62. Kuromi H, Kidokoro Y. 2000. Tetanic stimulation recruits vesicles from reserve pool via a cAMP-mediated process in Drosophila synapses. Neuron 27: 133-143.
63. Labandeira-Garcia JL. 2010. Dopamine-derived neurotoxicity and Parkinson's disease. In: Endogenous Toxins. Weinheim: Wiley-VCH Verlag GmbH & Co. KGaA.
64. Lesage S, Brice A. 2009. Parkinson's disease: From monogenic forms to genetic susceptibility factors. Hum Mol Genet 18: R48-R59.
65. Lotharius J, Brundin P. 2002. Pathogenesis of Parkinson's disease: Dopamine, vesicles and alpha-synuclein. Nat Rev Neurosci 3: 932-942.
66. Mahoney TR, Liu Q, Itoh T, Luo S, Hadwiger G, Vincent R, Wang ZW, et al. 2006. Regulation of synaptic transmission by RAB-3 and RAB-27 in Caenorhabditis elegans. Mol Biol Cell 17: 2617-2625.
67. Martin JA, Hu Z, Fenz KM, Fernandez J, Dittman JS. 2010. Complexin has opposite effects on two modes of synaptic vesicle fusion. Curr Biol 21: 97-105.
68. Mata IF, Wedemeyer WJ, Farrer MJ, Taylor JP, Gallo KA. 2006. LRRK2 in Parkinson's disease: Protein domains and functional insights. Trends Neurosci 29: 286-293.
69. Matthies HJ, Moore JL, Saunders C, Matthies DS, Lapierre LA, Goldenring JR, Blakely RD, et al. 2010. Rab11 supports amphetamine-stimulated norepinephrine transporter trafficking. J Neurosci 30: 7863-7877.
70. McLean PJ, Kawamata H, Ribich S, Hyman BT. 2000. Membrane association and protein conformation of alpha-synuclein in intact neurons. Effect of Parkinson's disease-linked mutations. J Biol Chem 275: 8812-8816.
71. Melrose HL, Kent CB, Taylor JP, Dachsel JC, Hinkle KM, Lincoln SJ, Mok SS, et al. 2007. A comparative analysis of leucine-rich repeat kinase 2 (Lrrk2) expression in mouse brain and Lewy body disease. Neuroscience 147: 1047-1058.
72. Menegon A, Bonanomi D, Albertinazzi C, Lotti F, Ferrari G, Kao HT, Benfenati F, et al. 2006. Protein kinase A-mediated synapsin I phosphorylation is a central modulator of Ca2+-dependent synaptic activity. J Neurosci 26: 11670-11681.
73. Milnerwood AJ, Raymond LA. 2010. Early synaptic pathophysiology in neurodegeneration: Insights from Huntington's disease. Trends Neurosci 33: 513-523.
74. Morais VA, Verstreken P, Roethig A, Smet J, Snellinx A, Vanbrabant M, Haddad D, et al. 2009. Parkinson's disease mutations in PINK1 result in decreased Complex I activity and deficient synaptic function. EMBO Mol Med 1: 99-111.
75. Mosharov EV, Staal RG, Bove J, Prou D, Hananiya A, Markov D, Poulsen N, et al. 2006. Alpha-synuclein overexpression increases cytosolic catecholamine concentration. J Neurosci 26: 9304-9311.
76. Munoz-Soriano V, Paricio N. 2007. Overexpression of Septin 4, the Drosophila homologue of human CDCrel-1, is toxic for dopaminergic neurons. Eur J Neurosci 26: 3150-3158.
77. Murphy DD, Rueter SM, Trojanowski JQ, Lee VM. 2000. Synucleins are developmentally expressed, and alpha-synuclein regulates the size of the presynaptic vesicular pool in primary hippocampal neurons. J Neurosci 20: 3214-3220.
78. Narendra DP, Youle RJ. 2011. Targeting mitochondrial dysfunction: Role for PINK1 and Parkin in mitochondrial quality control. Antioxid Redox Signal 14: 1929-1938.
79. Nemani VM, Lu W, Berge V, Nakamura K, Onoa B, Lee MK, Chaudhry FA, et al. 2010. Increased expression of alpha-synuclein reduces neurotransmitter release by inhibiting synaptic vesicle reclustering after endocytosis. Neuron 65: 66-79.
80. Ng EL, Tang BL. 2008. Rab GTPases and their roles in brain neurons and glia. Brain Res Rev 58: 236-246.
81. Nizami S, Lee VW, Davies J, Long P, Jovanovic JN, Sihra TS. 2010. Presynaptic roles of intracellular Ca(2+) stores in signalling and exocytosis. Biochem Soc Trans 38: 529-535.
82. Nonet ML, Staunton JE, Kilgard MP, Fergestad T, Hartwieg E, Horvitz HR, Jorgensen EM, et al. 1997. Caenorhabditis elegans rab-3 mutant synapses exhibit impaired function and are partially depleted of vesicles. J Neurosci 17: 8061-8073.
83. Obeso JA, Rodriguez-Oroz MC, Goetz CG, Marin C, Kordower JH, Rodriguez M, Hirsch EC, et al. 2010. Missing pieces in the Parkinson's disease puzzle. Nat Med 16: 653-661.
84. Oorschot DE. 1996. Total number of neurons in the neostriatal, pallidal, subthalamic, and substantia nigral nuclei of the rat basal ganglia: A stereological study using the cavalieri and optical disector methods. J Comp Neurol 366: 580-599.
85. Outeiro TF, Lindquist S. 2003. Yeast cells provide insight into alpha-synuclein biology and pathobiology. Science 302: 1772-1775.
86. Paisan-Ruiz C, Jain S, Evans EW, Gilks WP, Simon J, van der Brug M, Lopez de Munain A, et al. 2004. Cloning of the gene containing mutations that cause PARK8-linked Parkinson's disease. Neuron 44: 595-600.
87. Palop JJ, Mucke L. 2010. Amyloid-beta-induced neuronal dysfunction in Alzheimer's disease: From synapses toward neural networks. Nat Neurosci 13: 812-818.
88. Park J, Kim Y, Chung J. 2009. Mitochondrial dysfunction and Parkinson's disease genes: Insights from Drosophila. Dis Model Mech 2: 336-340.
89. Perrin RJ, Woods WS, Clayton DF, George JM. 2000. Interaction of human alpha-Synuclein and Parkinson's disease variants with phospholipids. Structural analysis using site-directed mutagenesis. J Biol Chem 275: 34393-34398.
90. Perrin RJ, Woods WS, Clayton DF, George JM. 2001. Exposure to long chain polyunsaturated fatty acids triggers rapid multimerization of synucleins. J Biol Chem 276: 41958-41962.
91. Piccoli G, Condliffe SB, Bauer M, Giesert F, Boldt K, De Astis S, Meixner A, et al. 2011. LRRK2 controls synaptic vesicle storage and mobilization within the recycling pool. J Neurosci 31: 2225-2237.
92. Plowey ED, Chu CT. 2011. Synaptic dysfunction in genetic models of Parkinson's disease: A role for autophagy? Neurobiol Dis 43: 60-67.
93. Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, Dutra A, Pike B, et al. 1997. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276: 2045-2047.
94. Ringstad N, Nemoto Y, De Camilli P. 1997. The SH3p4/Sh3p8/SH3p13 protein family: Binding partners for synaptojanin and dynamin via a Grb2-like Src homology 3 domain. Proc Natl Acad Sci U S A 94: 8569-8574.
95. Rizo J, Rosenmund C. 2008. Synaptic vesicle fusion. Nat Struct Mol Biol 15: 665-674.
96. Roberts RC, Force M, Kung L. 2002. Dopaminergic synapses in the matrix of the ventrolateral striatum after chronic haloperidol treatment. Synapse 45: 78-85.
97. Roux A, Uyhazi K, Frost A, De Camilli P. 2006. GTP-dependent twisting of dynamin implicates constriction and tension in membrane fission. Nature 441: 528-531.
98. Rubinsztein DC. 2006. The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 443: 780-786.
99. Sakane A, Manabe S, Ishizaki H, Tanaka-Okamoto M, Kiyokage E, Toida K, Yoshida T, et al. 2006. Rab3 GTPase-activating protein regulates synaptic transmission and plasticity through the inactivation of Rab3. Proc Natl Acad Sci U S A 103: 10029-10034.
100. Satake W, Nakabayashi Y, Mizuta I, Hirota Y, Ito C, Kubo M, Kawaguchi T, et al. 2009. Genome-wide association study identifies common variants at four loci as genetic risk factors for Parkinson's disease. Nat Genet 41: 1303-1307.
101. Scott DA, Tabarean I, Tang Y, Cartier A, Masliah E, Roy S. 2010. A pathologic cascade leading to synaptic dysfunction in alpha-synuclein-induced neurodegeneration. J Neurosci 30: 8083-8095.
102. Shimura H, Hattori N, Kubo S, Mizuno Y, Asakawa S, Minoshima S, Shimizu N, et al. 2000. Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nat Genet 25: 302-305.
103. Shin N, Jeong H, Kwon J, Heo HY, Kwon JJ, Yun HJ, Kim CH, et al. 2008. LRRK2 regulates synaptic vesicle endocytosis. Exp Cell Res 314: 2055-2065.
104. Simon-Sanchez J, Schulte C, Bras JM, Sharma M, Gibbs JR, Berg D, Paisan-Ruiz C, et al. 2009. Genome-wide association study reveals genetic risk underlying Parkinson's disease. Nat Genet 41: 1308-1312.
105. Singleton AB, Farrer M, Johnson J, Singleton A, Hague S, Kachergus J, Hulihan M, et al. 2003. alpha-Synuclein locus triplication causes Parkinson's disease. Science 302: 841.
106. Slepnev VI, De Camilli P. 2000. Accessory factors in clathrin-dependent synaptic vesicle endocytosis. Nat Rev Neurosci 1: 161-172.
107. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, Goedert M. 1997. Alpha-synuclein in Lewy bodies. Nature 388: 839-840.
108. Sriram SR, Li X, Ko HS, Chung KK, Wong E, Lim KL, Dawson VL, Dawson TM. 2005. Familial-associated mutations differentially disrupt the solubility, localization, binding and ubiquitination properties of parkin. Hum Mol Genet 14: 2571-2586.
109. Star EN, Newton AJ, Murthy VN. 2005. Real-time imaging of Rab3a and Rab5a reveals differential roles in presynaptic function. J Physiol 569: 103-117.
110. Sudhof TC. 2004. The synaptic vesicle cycle. Annu Rev Neurosci 27: 509-547.
111. Sudhof TC, Rothman JE. 2009. Membrane fusion: Grappling with SNARE and SM proteins. Science 323: 474-477.
112. Takahashi N, Miner LL, Sora I, Ujike H, Revay RS, Kostic V, Jackson-Lewis V, et al. 1997. VMAT2 knockout mice: Heterozygotes display reduced amphetamine-conditioned reward, enhanced amphetamine locomotion, and enhanced MPTP toxicity. Proc Natl Acad Sci U S A 94: 9938-9943.
113. Trempe JF, Chen CX, Grenier K, Camacho EM, Kozlov G, McPherson PS, Gehring K, et al. 2009. SH3 domains from a subset of BAR proteins define a Ubl-binding domain and implicate parkin in synaptic ubiquitination. Mol Cell 36: 1034-1047.
114. Uytterhoeven V, Kuenen S, Kasprowicz J, Miskiewicz K Verstreken P. 2011. Loss of skywalker reveals synaptic endosomes as sorting stations for synaptic vesicle proteins. Cell 145: 117-132.
115. Verstreken P, Kjaerulff O, Lloyd TE, Atkinson R, Zhou Y, Meinertzhagen IA, Bellen HJ. 2002. Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release. Cell 109: 101-112.
116. Verstreken P, Koh TW, Schulze KL, Zhai RG, Hiesinger PR, Zhou Y, Mehta SQ, et al. 2003. Synaptojanin is recruited by endophilin to promote synaptic vesicle uncoating. Neuron 40: 733-748.
117. Verstreken P, Ly CV, Venken KJ, Koh TW, Zhou Y, Bellen HJ. 2005. Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 47: 365-378.
118. Vos M, Lauwers E, Verstreken P. 2010. Synaptic mitochondria in synaptic transmission and organization of vesicle pools in health and disease. Frontiers in Synaptic Neuroscience 3: 12.
119. Wang C, Tan JM, Ho MW, Zaiden N, Wong SH, Chew CL, Eng PW, et al. 2005. Alterations in the solubility and intracellular localization of parkin by several familial Parkinson's disease-linked point mutations. J Neurochem 93: 422-431.
120. Wang CT, Grishanin R, Earles CA, Chang PY, Martin TF, Chapman ER, Jackson MB. 2001. Synaptotagmin modulation of fusion pore kinetics in regulated exocytosis of dense-core vesicles. Science 294: 1111-1115.
121. Wersinger C, Banta M, Sidhu A. 2004. Comparative analyses of alpha-synuclein expression levels in rat brain tissues and transfected cells. Neurosci Lett 358: 95-98.
122. Wucherpfennig T, Wilsch-Brauninger M, Gonzalez-Gaitan M. 2003. Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J Cell Biol 161: 609-624.
123. Xiong Y, Coombes CE, Kilaru A, Li X, Gitler AD, Bowers WJ, Dawson VL, et al. 2010. GTPase activity plays a key role in the pathobiology of LRRK2. PLoS Genet 6: e1000902.
124. Yi JJ, Ehlers MD. 2005. Ubiquitin and protein turnover in synapse function. Neuron 47: 629-632.
125. Yoshihara M, Suzuki K, Kidokoro Y. 2000. Two independent pathways mediated by cAMP and protein kinase A enhance spontaneous transmitter release at Drosophila neuromuscular junctions. J Neurosci 20: 8315-8322.
126. Yu E, Kanno E, Choi S, Sugimori M, Moreira JE, Llinas RR, Fukuda M. 2008. Role of Rab27 in synaptic transmission at the squid giant synapse. Proc Natl Acad Sci U S A 105: 16003-16008.
127. Zarow C, Lyness SA, Mortimer JA, Chui HC. 2003. Neuronal loss is greater in the locus coeruleus than nucleus basalis and substantia nigra in Alzheimer and Parkinson diseases. Arch Neurol 60: 337-341.
128. Zarranz JJ, Alegre J, Gomez-Esteban JC, Lezcano E, Ros R, Ampuero I, Vidal L, et al. 2004. The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann Neurol 55: 164-173.
129. Zhang Y, Gao J, Chung KK, Huang H, Dawson VL, Dawson TM. 2000. Parkin functions as an E2-dependent ubiquitin- protein ligase and promotes the degradation of the synaptic vesicle-associated protein, CDCrel-1. Proc Natl Acad Sci U S A 97: 13354-13359.
130. Zimprich A, Biskup S, Leitner P, Lichtner P, Farrer M, Lincoln S, Kachergus J, et al. 2004. Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology. Neuron 44: 601-7.
131. Zinsmaier KE, Eberle KK, Buchner E, Walter N, Benzer S. 1994. Paralysis and early death in cysteine string protein mutants of Drosophila. Science 263: 977-980.