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PMID: 11739566 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Expression of A53T mutant but not wild-type alpha-synuclein in PC12 cells induces alterations of the ubiquitin-dependent degradation system, loss of dopamine release, and autophagic cell death.

Stefanis L, Larsen KE, Rideout HJ, Sulzer D, Greene LA

Abstract

Alpha-synuclein mutations have been identified in certain families with Parkinson's disease (PD), and alpha-synuclein is a major component of Lewy bodies. Other genetic data indicate that the ubiquitin-dependent proteolytic system is involved in PD pathogenesis. We have generated stable PC12 cell lines expressing wild-type or A53T mutant human alpha-synuclein. Lines expressing mutant but not wild-type alpha-synuclein show: (1) disruption of the ubiquitin-dependent proteolytic system, manifested by small cytoplasmic ubiquitinated aggregates and by an increase in polyubiquitinated proteins; (2) enhanced baseline nonapoptotic death; (3) marked accumulation of autophagic-vesicular structures; (4) impairment of lysosomal hydrolysis and proteasomal function; and (5) loss of catecholamine-secreting dense core granules and an absence of depolarization-induced dopamine release. Such findings raise the possibility that the primary abnormality in these cells may involve one or more deficits in the lysosomal and/or proteasomal degradation pathways, which in turn lead to loss of dopaminergic capacity and, ultimately, to death. These cells may serve as a model to study the effects of aberrant alpha-synuclein on dopaminergic cell function and survival.

MeSH Terms
Amino Acid Substitution Animals Autophagy/drug effects,physiology Cathepsin D/metabolism Cell Death/physiology Cells, Cultured Clone Cells/cytology,drug effects,metabolism Cysteine Endopeptidases/metabolism Cysteine Proteinase Inhibitors/pharmacology Cytoplasm/metabolism,ultrastructure Dopamine/metabolism Fluorescent Dyes Humans Lysosomes/metabolism,ultrastructure Macromolecular Substances Multienzyme Complexes/metabolism Mutagenesis, Site-Directed Nerve Tissue Proteins/biosynthesis,genetics PC12 Cells/cytology,drug effects,metabolism Parkinson Disease/metabolism Proteasome Endopeptidase Complex Proteins/metabolism Rats Synucleins Transfection Ubiquitin/metabolism alpha-Synuclein
Chemicals
Cysteine Proteinase Inhibitors Fluorescent Dyes Macromolecular Substances Multienzyme Complexes Nerve Tissue Proteins Proteins SNCA protein, human Snca protein, rat Synucleins Ubiquitin alpha-Synuclein Cysteine Endopeptidases Cathepsin D Proteasome Endopeptidase Complex Dopamine
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Stefanis L
Department of Pathology, Columbia University, New York, New York 10032, USA. ls76@columbia.edu
Larsen K E
Rideout H J
Sulzer D
Greene L A
References (71)
71 references, click to expand
  1. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease.
    Science. 1997 Jun 27;276(5321):2045-7 PMID: 9197268
  2. The ubiquitin pathway in Parkinson's disease.
    Nature. 1998 Oct 1;395(6701):451-2 PMID: 9774100
  3. Sensitivity to MPTP is not increased in Parkinson's disease-associated mutant alpha-synuclein transgenic mice.
    J Neurochem. 2001 May;77(4):1181-4 PMID: 11359883
  4. Effect of the overexpression of wild-type or mutant alpha-synuclein on cell susceptibility to insult.
    J Neurochem. 2001 Feb;76(4):998-1009 PMID: 11181819
  5. Proteasome inhibitors which induce neurite outgrowth from PC12h cells cause different subcellular accumulations of multi-ubiquitin chains.
    Neurochem Res. 1998 Nov;23(11):1435-43 PMID: 9814555
  6. Structural abnormalities associated with congenital megacolon in transgenic mice that overexpress the Hoxa-4 gene.
    Dev Dyn. 1993 Sep;198(1):28-53 PMID: 7904838
  7. Induction of neuronal death by alpha-synuclein.
    Eur J Neurosci. 2000 Aug;12(8):3073-7 PMID: 10971650
  8. 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. 2000 Nov 21;97(24):13354-9 PMID: 11078524
  9. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor.
    Proc Natl Acad Sci U S A. 1976 Jul;73(7):2424-8 PMID: 1065897
  10. Ultrastructure of Lewy bodies in the stellate ganglion.
    Acta Neuropathol. 1976 Mar 30;34(3):183-97 PMID: 178142
  11. Degradation of alpha-synuclein by proteasome.
    J Biol Chem. 1999 Nov 26;274(48):33855-8 PMID: 10567343
  12. Rat alpha-synuclein interacts with Tat binding protein 1, a component of the 26S proteasomal complex.
    J Neurochem. 2000 Nov;75(5):2221-4 PMID: 11032911
  13. An ultrastructural and immunohistochemical study of PC12 cells during apoptosis induced by serum deprivation with special reference to autophagy and lysosomal cathepsins.
    Arch Histol Cytol. 1998 Dec;61(5):395-403 PMID: 9990423
  14. Nerve growth factor withdrawal-induced cell death in neuronal PC12 cells resembles that in sympathetic neurons.
    J Cell Biol. 1992 Dec;119(6):1669-80 PMID: 1469055
  15. Inducible expression of mutant alpha-synuclein decreases proteasome activity and increases sensitivity to mitochondria-dependent apoptosis.
    Hum Mol Genet. 2001 Apr 15;10(9):919-26 PMID: 11309365
  16. Structural aspects of autophagy.
    Adv Exp Med Biol. 1996;389:103-11 PMID: 8860999
  17. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease.
    Nat Genet. 1998 Feb;18(2):106-8 PMID: 9462735
  18. Neurite outgrowth in PC12 cells. Distinguishing the roles of ubiquitylation and ubiquitin-dependent proteolysis.
    J Biol Chem. 1999 Apr 23;274(17):11789-95 PMID: 10206996
  19. Caspase-dependent and -independent death of camptothecin-treated embryonic cortical neurons.
    J Neurosci. 1999 Aug 1;19(15):6235-47 PMID: 10414953
  20. Synaptic vesicle transporter expression regulates vesicle phenotype and quantal size.
    J Neurosci. 2000 Oct 1;20(19):7297-306 PMID: 11007887
  21. Exposure of cells to nonlethal concentrations of hydrogen peroxide induces degeneration-repair mechanisms involving lysosomal destabilization.
    Free Radic Biol Med. 1995 Dec;19(6):813-22 PMID: 8582654
  22. Induction of CPP32-like activity in PC12 cells by withdrawal of trophic support. Dissociation from apoptosis.
    J Biol Chem. 1996 Nov 29;271(48):30663-71 PMID: 8940042
  23. alpha-synuclein promotes mitochondrial deficit and oxidative stress.
    Am J Pathol. 2000 Aug;157(2):401-10 PMID: 10934145
  24. Multiple agents rescue PC12 cells from serum-free cell death by translation- and transcription-independent mechanisms.
    J Neurosci. 1991 Aug;11(8):2552-63 PMID: 1714494
  25. alpha-Synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with lewy bodies.
    Proc Natl Acad Sci U S A. 1998 May 26;95(11):6469-73 PMID: 9600990
  26. Fatal attractions: abnormal protein aggregation and neuron death in Parkinson's disease and Lewy body dementia.
    Cell Death Differ. 1998 Oct;5(10):832-7 PMID: 10203692
  27. Mutated alpha-synuclein gene in two Greek kindreds with familial PD: incomplete penetrance?
    Neurology. 1999 Feb;52(3):651-4 PMID: 10025809
  28. Regulation of quantal size by presynaptic mechanisms.
    Rev Neurosci. 2000;11(2-3):159-212 PMID: 10718152
  29. A new inhibitor of the chymotrypsin-like activity of the multicatalytic proteinase complex (20S proteasome) induces accumulation of ubiquitin-protein conjugates in a neuronal cell.
    J Neurochem. 1994 Oct;63(4):1578-81 PMID: 7931314
  30. Alpha-synuclein in Lewy bodies.
    Nature. 1997 Aug 28;388(6645):839-40 PMID: 9278044
  31. Mutant and wild type human alpha-synucleins assemble into elongated filaments with distinct morphologies in vitro.
    J Biol Chem. 1999 Mar 19;274(12):7619-22 PMID: 10075647
  32. The A53T alpha-synuclein mutation increases iron-dependent aggregation and toxicity.
    J Neurosci. 2000 Aug 15;20(16):6048-54 PMID: 10934254
  33. Synuclein-1 is selectively up-regulated in response to nerve growth factor treatment in PC12 cells.
    J Neurochem. 2001 Feb;76(4):1165-76 PMID: 11181836
  34. Dopaminergic loss and inclusion body formation in alpha-synuclein mice: implications for neurodegenerative disorders.
    Science. 2000 Feb 18;287(5456):1265-9 PMID: 10678833
  35. Ubiquitination of a new form of alpha-synuclein by parkin from human brain: implications for Parkinson's disease.
    Science. 2001 Jul 13;293(5528):263-9 PMID: 11431533
  36. Proteasomal function is impaired in substantia nigra in Parkinson's disease.
    Neurosci Lett. 2001 Jan 19;297(3):191-4 PMID: 11137760
  37. Huntingtin expression stimulates endosomal-lysosomal activity, endosome tubulation, and autophagy.
    J Neurosci. 2000 Oct 1;20(19):7268-78 PMID: 11007884
  38. Ubiquitin-mediated proteolysis centers in HeLa cells: indication from studies of an inhibitor of the chymotrypsin-like activity of the proteasome.
    Eur J Cell Biol. 1996 Nov;71(3):311-8 PMID: 8929570
  39. Programmed cell death (PCD). Apoptosis, autophagic PCD, or others?
    Ann N Y Acad Sci. 2000;926:1-12 PMID: 11193023
  40. An unfolded putative transmembrane polypeptide, which can lead to endoplasmic reticulum stress, is a substrate of Parkin.
    Cell. 2001 Jun 29;105(7):891-902 PMID: 11439185
  41. Expression of mutant alpha-synuclein causes increased susceptibility to dopamine toxicity.
    Hum Mol Genet. 2000 Nov 1;9(18):2683-9 PMID: 11063727
  42. Enhanced vulnerability to oxidative stress by alpha-synuclein mutations and C-terminal truncation.
    Neuroscience. 2000;97(2):279-84 PMID: 10799759
  43. Dopamine (3-hydroxytyramine) and brain function.
    Pharmacol Rev. 1966 Jun;18(2):925-64 PMID: 5328389
  44. Nerve growth factor prevents the death and stimulates the neuronal differentiation of clonal PC12 pheochromocytoma cells in serum-free medium.
    J Cell Biol. 1978 Sep;78(3):747-55 PMID: 701359
  45. Routes of excretion of neuronal lysosomal dense bodies after ventricular infusion of leupeptin in the rat: a study using ubiquitin and PGP 9.5 immunocytochemistry.
    J Neurocytol. 1993 Sep;22(9):779-91 PMID: 8270961
  46. alpha-Synuclein shares physical and functional homology with 14-3-3 proteins.
    J Neurosci. 1999 Jul 15;19(14):5782-91 PMID: 10407019
  47. Developmental cell death: morphological diversity and multiple mechanisms.
    Anat Embryol (Berl). 1990;181(3):195-213 PMID: 2186664
  48. p53-dependent induction of apoptosis by proteasome inhibitors.
    J Biol Chem. 1997 May 16;272(20):12893-6 PMID: 9148891
  49. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism.
    Nature. 1998 Apr 9;392(6676):605-8 PMID: 9560156
  50. Failure of the ubiquitin-proteasome system in Parkinson's disease.
    Nat Rev Neurosci. 2001 Aug;2(8):589-94 PMID: 11484002
  51. Alpha-synuclein overexpression promotes aggregation of mutant huntingtin.
    Biochem J. 2000 Mar 15;346 Pt 3:577-81 PMID: 10698681
  52. Apoptosis and autophagy in nigral neurons of patients with Parkinson's disease.
    Histol Histopathol. 1997 Jan;12(1):25-31 PMID: 9046040
  53. Autophagy is activated by apoptotic signalling in sympathetic neurons: an alternative mechanism of death execution.
    Mol Cell Neurosci. 1999 Sep;14(3):180-98 PMID: 10576889
  54. Proteasomal inhibition leads to formation of ubiquitin/alpha-synuclein-immunoreactive inclusions in PC12 cells.
    J Neurochem. 2001 Aug;78(4):899-908 PMID: 11520910
  55. Sensitization of neuronal cells to oxidative stress with mutated human alpha-synuclein.
    J Neurochem. 2000 Dec;75(6):2546-54 PMID: 11080208
  56. Ubiquitinated protein conjugates are specifically enriched in the lysosomal system of fibroblasts.
    FEBS Lett. 1990 Feb 26;261(2):365-8 PMID: 2155827
  57. Aggregation of alpha-synuclein in Lewy bodies of sporadic Parkinson's disease and dementia with Lewy bodies.
    Am J Pathol. 1998 Apr;152(4):879-84 PMID: 9546347
  58. Alpha-synuclein and the Parkinson's disease-related mutant Ala53Thr-alpha-synuclein do not undergo proteasomal degradation in HEK293 and neuronal cells.
    Neurosci Lett. 2000 May 12;285(2):79-82 PMID: 10793231
  59. Aurintricarboxylic acid rescues PC12 cells and sympathetic neurons from cell death caused by nerve growth factor deprivation: correlation with suppression of endonuclease activity.
    J Cell Biol. 1991 Oct;115(2):461-71 PMID: 1655805
  60. Accelerated in vitro fibril formation by a mutant alpha-synuclein linked to early-onset Parkinson disease.
    Nat Med. 1998 Nov;4(11):1318-20 PMID: 9809558
  61. Parkin suppresses unfolded protein stress-induced cell death through its E3 ubiquitin-protein ligase activity.
    J Biol Chem. 2000 Nov 17;275(46):35661-4 PMID: 10973942
  62. The synucleins: a family of proteins involved in synaptic function, plasticity, neurodegeneration and disease.
    Trends Neurosci. 1998 Jun;21(6):249-54 PMID: 9641537
  63. Activation of the cell death program by inhibition of proteasome function.
    Proc Natl Acad Sci U S A. 1997 Feb 4;94(3):855-60 PMID: 9023346
  64. Caspase-2 (Nedd-2) processing and death of trophic factor-deprived PC12 cells and sympathetic neurons occur independently of caspase-3 (CPP32)-like activity.
    J Neurosci. 1998 Nov 15;18(22):9204-15 PMID: 9801360
  65. Overexpression of human alpha-synuclein causes dopamine neuron death in rat primary culture and immortalized mesencephalon-derived cells.
    Brain Res. 2000 Jun 2;866(1-2):33-43 PMID: 10825478
  66. Lack of nigral pathology in transgenic mice expressing human alpha-synuclein driven by the tyrosine hydroxylase promoter.
    Neurobiol Dis. 2001 Jun;8(3):535-9 PMID: 11442360
  67. Ubiquitin, lysosomes, and neurodegenerative diseases.
    Ann N Y Acad Sci. 1992 Dec 31;674:149-60 PMID: 1337689
  68. The ubiquitin-proteasome pathway: on protein death and cell life.
    EMBO J. 1998 Dec 15;17(24):7151-60 PMID: 9857172
  69. Synucleins in synaptic plasticity and neurodegenerative disorders.
    J Neurosci Res. 1999 Oct 1;58(1):120-9 PMID: 10491577
  70. Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase.
    Nat Genet. 2000 Jul;25(3):302-5 PMID: 10888878
  71. Vesicular transport regulates monoamine storage and release but is not essential for amphetamine action.
    Neuron. 1997 Dec;19(6):1271-83 PMID: 9427250
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2001-12-15
Pages
9549-60
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6763041
Subset
IM
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