Parkin and α-synuclein: Opponent Actions in the Pathogenesis of Parkinson's Disease

Neuroscientist

Volumn 10, Issue 1, 2004, Pages 63-72

  Baptista, Melisa J ^a   Cookson, Mark R ^a   Miller, David W ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

Lewy bodies; Mitochondria; Parkin; Proteasome; Synapses; Synuclein

Indexed keywords

ALPHA SYNUCLEIN; GENE PRODUCT; PARKIN;

DISEASE ASSOCIATION; GENE EXPRESSION; MITOCHONDRION; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

ALPHA-SYNUCLEIN; ANIMALS; HUMANS; NERVE TISSUE PROTEINS; PARKINSON DISEASE; SYNUCLEINS; UBIQUITIN-PROTEIN LIGASES;

EID: 1642498210     PISSN: 10738584     EISSN: None     Source Type: Journal    
DOI: 10.1177/1073858403260392     Document Type: Review

References (61)

1. Abeliovich A, Schmitz Y, Farinas I, Choi-Lundberg D, Ho WH, Castillo PE, and others. 2000. Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 25:239-52.
2. Ahn BH, Rhim H, Kim SY, Sung YM, Lee MY, Choi JY, and others. 2002. Alpha-synuclein interacts with phospholipase D isozymes and inhibits pervanadate-induced phospholipase D activation in human embryonic kidney-293 cells. J Biol Chem 277:12334-42.
3. Auluck PK, Chan HY, Trojanowski JQ, Lee VM, Bonini NM. 2002. Chaperone suppression of alpha-synuclein toxicity in a Drosophila model for Parkinson's disease. Science 295:865-68.
4. Baptista MJ, O'Farrell C, Daya S, Ahmad R, Miller DW, Hardy J, and others. 2003. Co-ordinate transcriptional regulation of dopamine synthesis genes by alpha-synuclein in human neuroblastoma cell lines. J Neurochem 85:957-68.
5. Beites CL, Xie H, Bowser R, Trimble WS. 1999. The septin CDCrel-1 binds syntaxin and inhibits exocytosis. Nat Neurosci 2:434-9.
6. Bence NF, Sampat RM, Kopito RR. 2001. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292:1552-5.
7. Bonifati V, Rizzu P, van Baren MJ, Schaap O, Breedveld GJ, Krieger E, and others. 2003. Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science 299:256-9.
8. Braak H, Braak E. 2000. Pathoanatomy of Parkinson's disease. J Neurol 247(suppl 2):3-10.
9. Cabin DE, Shimazu K, Murphy D, Cole NB, Gottschalk W, Mcllwain KL, and others. 2002. Synaptic vesicle depletion correlates with attenuated synaptic responses to prolonged repetitive stimulation in mice lacking alpha-synuclein. J Neurosci 22:8797-807.
10. Chung KK, Zhang Y, Lim KL, Tanaka Y, Huang H, Gao J, and others. 2001. Parkin ubiquitinates the alpha-synuclein-interacting protein, synphilin-1: implications for Lewy-body formation in Parkinson disease. Nat Med 7:1144-50.
11. Clayton DF, George JM. 1998. The synucleins: a family of proteins involved in synaptic function, plasticity, neurodegeneration and disease. Trends Neurosci 21:249-54.
12. Conway KA, Rochet JC, Bieganski RM, Lansbury PT Jr. 2001. Kinetic stabilization of the alpha-synuclein protofibril by a dopamine-alpha-synuclein adduct. Science 294:1346-9.
13. Cookson MR. 2003. Parkin's substrates and the pathways leading to neuronal damage. Neuromolecular Med 3:1-13.
14. Darios F, Corti O, Lucking CB, Hampe C, Muriel MP, Abbas N, and others. 2003. Parkin prevents mitochondrial swelling and cytochrome c release in mitochondria-dependent cell death. Hum Mol Genet 12:517-26.
15. Dauer W, Kholodilov N, Vila M, Trillat AC, Goodchild R, Larsen KE, and others. 2002. Resistance of alpha-synuclein null mice to the parkinsonian neurotoxin MPTP. Proc Natl Acad Sci U S A 99:14524-9.
16. Davidson WS, Jonas A, Clayton DF, George JM. 1998. Stabilization of alpha-synuclein secondary structure upon binding to synthetic membranes. J Biol Chem 273:9443-9.
17. Di Monte DA. 2003. The environment and Parkinson's disease: is the nigrostriatal system preferentially targeted by neurotoxins? Lancet Neurol 2:531-8.
18. Goldberg MS, Fleming SM, Palacino JJ, Cepeda C, Lam HA, Bhatnagar A, and others. 2003. Parkin-deficient mice exhibit nigrostriatal deficits but not loss of dopaminergic neurons. J Biol Chem 278:43628-35.
19. Greene JC, Whitworth AJ, Kuo I, Andrews LA, Feany MB, Pallanck LJ. 2003. Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc Natl Acad Sci U S A 100:4078-83.
20. Gwinn-Hardy K. 2002. Genetics of parkinsonism. Mov Disord 17:645-56.
21. Hashimoto M, Hsu LJ, Rockenstein E, Takenouchi T, Mallory M, Masliah E. 2002. Alpha-synuclein protects against oxidative stress via inactivation of the c-Jun N-terminal kinase stress-signaling pathway in neuronal cells. J Biol Chem 277:11465-72.
22. Hashimoto M, Takenouchi T, Rockenstein E, Masliah E. 2003. Alpha-synuclein up-regulates expression of caveolin-1 and down-regulates extracellular signal-regulated kinase activity in B 103 neuroblastoma cells: role in the pathogenesis of Parkinson's disease. J Neurochem 85:1468-79.
23. Ichimura T, Isobe T, Okuyama T, Takahashi N, Araki K, Kuwano R, and others. 1988. Molecular cloning of cDNA coding for brain-specific 14-3-3 protein, a protein kinase-dependent activator of tyrosine and tryptophan hydroxylases. Proc Natl Acad Sci U S A 85:7084-8.
24. Impey S, Fong AL, Wang Y, Cardinaux JR, Fass DM, Obrietan K, and others. 2002. Phosphorylation of CBP mediates transcriptional activation by neural activity and CaM kinase IV. Neuron 34:235-44.
25. Irizarry MC, Kim TW, McNamara M, Tanzi RE, George JM, Clayton DF, and others. 1996. Characterization of the precursor protein of the non-A beta component of senile plaques (NACP) in the human central nervous system. J Neuropathol Exp Neurol 55:889-95.
26. Itier JM, Ibanez P, Mena MA, Abbas N, Cohen-Salmon C, Bohme GA, and others. 2003. Parkin gene inactivation alters behaviour and dopamine neurotransmission in the mouse. Hum Mol Genet 12:2277-91.
27. Iwai A, Masliah E, Yoshimoto M, Ge N, Flanagan L, de Silva HA, and others. 1995. The precursor protein of non-A beta component of Alzheimer's disease amyloid is a presynaptic protein of the central nervous system. Neuron 14:467-75.
28. Iwata A, Maruyama M, Kanazawa I, Nukina N. 2001. Alpha-synuclein affects the MAPK pathway and accelerates cell death. J Biol Chem 276:45320-9.
29. Jensen PH, Nielsen MS, Jakes R, Dotti CG, Goedert M. 1998. Binding of alpha-synuclein to brain vesicles is abolished by familial Parkinson's disease mutation. J Biol Chem 273:26292-4.
30. Khan NL, Brooks DJ, Pavese N, Sweeney MG, Wood NW, Lees AJ, and others. 2002. Progression of nigrostriatal dysfunction in a parkin kindred: an [18F] dopa PET and clinical study. Brain 125:2248-56.
31. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, and others. 1998. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392:605-8.
32. Lee FJ, Liu F, Pristupa ZB, Niznik HB. 2001. Direct binding and functional coupling of alpha-synuclein to the dopamine transporters accelerate dopamine-induced apoptosis. Faseb J 15:916-26.
33. Lehmensiek V, Tan EM, Schwarz J, Storch A. 2002. Expression of mutant alpha-synucleins enhances dopamine transporter-mediated MPP+ toxicity in vitro. Neuroreport 13:1279-83.
34. Lotharius J, Barg S, Wiekop P, Lundberg C, Raymon HK, Brundin P. 2002. Effect of mutant alpha-synuclein on dopamine homeostasis in a new human mesencephalic cell line. J Biol Chem 277:38884-94.
35. Lotharius J, Brundin P. 2002. Pathogenesis of Parkinson's disease: dopamine, vesicles and alpha-synuclein. Nat Rev Neurosci 3:932-42.
36. McLean PJ, Ribich S, Hyman BT. 2000. Subcellular localization of alpha-synuclein in primary neuronal cultures: effect of missense mutations. J Neural Transm Suppl: 53-63.
37. Miller DW, Ahmad R, Hague S, Baptista MJ, Canet-Aviles R, McLendon C, and others. 2003. L166P mutant DJ-1, causative for recessive Parkinson's disease, is degraded through the ubiquitin-proteasome system. J Biol Chem 278:36588-95.
38. 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 20:3214-20.
39. Peng XR, Jia Z, Zhang Y, Ware J, Trimble WS. 2002. The septin CDCrel-1 is dispensable for normal development and neurotransmitter release. Mol Cell Biol 22:378-87.
40. Perez RG, Waymire JC, Lin E, Liu JJ, Guo F, Zigmond MJ. 2002. A role for alpha-synuclein in the regulation of dopamine biosynthesis. J Neurosci 22:3090-9.
41. Petrucelli L, O'Farrell C, Lockhart PJ, Baptista M, Kehoe K, Vink L, and others. 2002. Parkin protects against the toxicity associated with mutant alpha-synuclein: proteasome dysfunction selectively affects catecholaminergic neurons. Neuron 36:1007-19.
42. Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, Dutra A, and others. 1997. Mutation in the α-synuclein gene identified in families with Parkinson's disease. Science 276:2045-7.
43. Scherzer CR, Jensen RV, Gullans SR, Feany MB. 2003. Gene expression changes presage neurodegeneration in a Drosophila model of Parkinson's disease. Hum Mol Genet 12:2457-66.
44. Seo JH, Rah JC, Choi SH, Shin JK, Min K, Kim HS, and others. 2002. Alpha-synuclein regulates neuronal survival via Bcl-2 family expression and PI3/Akt kinase pathway. Faseb J 16:1826-8.
45. Sharon R, Bar-Joseph I, Frosch MP, Walsh DM, Hamilton JA, Selkoe DJ. 2003. The formation of highly soluble oligomers of alpha-synuclein is regulated by fatty acids and enhanced in Parkinson's disease. Neuron 37:583-95.
46. Shimura H, Schlossmacher MG, Hattori N, Frosch MP, Trockenbacher A, Schneider R, and others. 2001. Ubiquitination of a new form of alpha-synuclein by parkin from human brain: implications for Parkinson's disease. Science 293:263-9.
47. Singleton AB, Farrer M, Johnson J, Singleton A, Hagu, S, Kachergus J, and others. 2003. α-synuclein locus triplication causes Parkinson's disease. Science 301:841.
48. Snyder H, Mensah K, Theisler C, Lee J, Matouschek A, Wolozin B. 2003. Aggregated and monomeric alpha-synuclein bind to the S6' proteasomal protein and inhibit proteasomal function. J Biol Chem 278:11753-9.
49. Solano SM, Miller DW, Augood SJ, Young AB, Penney JB Jr. 2000. Expression of alpha-synuclein, parkin, and ubiquitin carboxy-terminal hydrolase L1 mRNA in human brain: genes associated with familial Parkinson's disease. Ann Neurol 47:201-10.
50. Staropoli JF, McDermott C, Martinat C, Schulman B, Demireva E, Abeliovich A. 2003. Parkin is a component of an SCF-like ubiquitin ligase complex and protects postmitotic neurons from kainate excitotoxicity. Neuron 37:735-49.
51. Stokes AH, Hastings TG, Vrana KE. 1999. Cytotoxic and genotoxic potential of dopamine. J Neurosci Res 55:659-65.
52. Tanaka Y, Engelender S, Igarashi S, Rao RK, Wanner T, Tanzi RE, and others. 2001. Inducible expression of mutant alpha-synuclein decreases proteasome activity and increases sensitivity to mitochondria-dependent apoptosis. Hum Mol Genet 10:919-26.
53. Taylor JP, Hardy J, Fischbeck KH. 2002. Toxic proteins in neurodegenerative disease. Science 296:1991-5.
54. Tsai YC, Fishman PS, Thakor NV, Oyler GA. 2003. Parkin facilitates the elimination of expanded polyglutamine proteins and leads to preservation of proteasome function. J Biol Chem 278:22044-55.
55. Uversky VN. 2003. A protein-chameleon: conformational plasticity of alpha-synuclein, a disordered protein involved in neurodegenerative disorders. J Biomol Struct Dyn 21:211-34.
56. Volles MJ, Lansbury PT Jr. 2003. Zeroing in on the pathogenic form of alpha-synuclein and its mechanism of neurotoxicity in Parkinson's disease. Biochemistry 42:7871-8.
57. Wersinger C, Prou D, Vernier P, Sidhu A. 2003. Modulation of dopamine transporter function by alpha-synuclein is altered by impairment of cell adhesion and by induction of oxidative stress. Faseb J 17:2151-3.
58. Wersinger C, Sidhu A. 2003. Attenuation of dopamine transporter activity by alpha-synuclein. Neurosci Lett 340:189-92.
59. Xu J, Kao SY, Lee FJS, Song W, Jin LW, Yankner BA. 2002. Dopamine-dependent neurotoxicity of α-synuclein: a mechanism for selective neurodegeneration in Parkinson disease. Nat Med 8:600-6.
60. Yang Y, Nishimura I, Imai Y, Takahashi R, Lu B. 2003. Parkin suppresses dopaminergic neuron-selective neurotoxicity induced by Pael-R in Drosophila. Neuron 37:911-24.
61. 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 97:13354-9.