Home LiteratureArticle Details
PMID: 17097639 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Parkin is an E3 ubiquitin-ligase for normal and mutant ataxin-2 and prevents ataxin-2-induced cell death.

Experimental neurology ·Vol. 203 ·No. 2 ·2007-02-00 ·Pages 531-41

Huynh DP, Nguyen DT, Pulst-Korenberg JB, Brice A, Pulst SM

Abstract

Expansion of the polyQ repeat in ataxin-2 results in degeneration of Purkinje neurons and other neuronal groups including the substantia nigra in patients with spinocerebellar ataxia type 2 (SCA2). In animal and cell models, overexpression of mutant ataxin-2 induces cell dysfunction and death, but little is known about steady-state levels of normal and mutant ataxin-2 and cellular mechanisms regulating their abundance. Based on preliminary findings that ataxin-2 interacted with parkin, an E3 ubiquitin ligase mutated in an autosomal recessive form of Parkinsonism, we sought to determine whether parkin played a role in regulating the steady-state levels of ataxin-2. Parkin interacted with the N-terminal half of normal and mutant ataxin-2, and ubiquitinated the full-length form of both wild-type and mutant ataxin-2. Parkin also regulated the steady-state levels of endogenous ataxin-2 in PC12 cells with regulatable parkin expression. Parkin reduced abnormalities in Golgi morphology induced by mutant ataxin-2 and decreased ataxin-2 induced cytotoxicity. In brains of SCA2 patients, parkin labeled cytoplasmic ataxin-2 aggregates in Purkinje neurons. These studies suggest a role for parkin in regulating the intracellular levels of both wild-type and mutant ataxin-2, and in rescuing cells from ataxin-2-induced cytotoxicity. The role of parkin variants in modifying the SCA2 phenotype and its use as a therapeutic target should be further investigated.

MeSH Terms
Animals Ataxins Blotting, Western Cell Death/physiology Cell Line Cell Survival Cytoplasm/metabolism Fluorescent Antibody Technique Humans Immunoprecipitation Mice Nerve Tissue Proteins/genetics,physiology Purkinje Cells/metabolism Transfection Trypan Blue Ubiquitin-Protein Ligases/metabolism,physiology
Chemicals
Ataxins Nerve Tissue Proteins Ubiquitin-Protein Ligases parkin protein Trypan Blue
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Huynh Duong P
Rose Moss Laboratory for Parkinson and Neurodegenerative Diseases, Burns and Allen Research Institute, and Division of Neurology, Cedars-Sinai Medical Center, USA.
Nguyen Dung T
Pulst-Korenberg Johannes B
Brice Alexis
Pulst Stefan-M
References (49)
49 references, click to expand
  1. Expression of ataxin-2 in brains from normal individuals and patients with Alzheimer's disease and spinocerebellar ataxia 2.
    Ann Neurol. 1999 Feb;45(2):232-41 PMID: 9989626
  2. Ataxin-1 nuclear localization and aggregation: role in polyglutamine-induced disease in SCA1 transgenic mice.
    Cell. 1998 Oct 2;95(1):41-53 PMID: 9778246
  3. Spinocerebellar ataxia type 2 (SCA2) with white matter involvement.
    Neurosci Lett. 2005 Jun 24;381(3):247-51 PMID: 15896478
  4. Familial-associated mutations differentially disrupt the solubility, localization, binding and ubiquitination properties of parkin.
    Hum Mol Genet. 2005 Sep 1;14(17):2571-86 PMID: 16049031
  5. Accumulation of the authentic parkin substrate aminoacyl-tRNA synthetase cofactor, p38/JTV-1, leads to catecholaminergic cell death.
    J Neurosci. 2005 Aug 31;25(35):7968-78 PMID: 16135753
  6. Spinocerebellar ataxia type 2: polyQ repeat variation in the CACNA1A calcium channel modifies age of onset.
    Brain. 2005 Oct;128(Pt 10):2297-303 PMID: 16000334
  7. Proteomic analysis of parkin knockout mice: alterations in energy metabolism, protein handling and synaptic function.
    J Neurochem. 2005 Dec;95(5):1259-76 PMID: 16150055
  8. Leucine-rich repeat kinase 2 (LRRK2) interacts with parkin, and mutant LRRK2 induces neuronal degeneration.
    Proc Natl Acad Sci U S A. 2005 Dec 20;102(51):18676-81 PMID: 16352719
  9. Identification of far upstream element-binding protein-1 as an authentic Parkin substrate.
    J Biol Chem. 2006 Jun 16;281(24):16193-6 PMID: 16672220
  10. Activity-dependent dynamics and sequestration of proteasomes in dendritic spines.
    Nature. 2006 Jun 29;441(7097):1144-8 PMID: 16810255
  11. Proteasome inhibition triggers activity-dependent increase in the size of the recycling vesicle pool in cultured hippocampal neurons.
    J Neurosci. 2006 Nov 1;26(44):11333-41 PMID: 17079661
  12. Neuronal intranuclear inclusions in spinocerebellar ataxia type 2.
    Ann Neurol. 2000 Apr;47(4):550 PMID: 10762173
  13. Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase.
    Nat Genet. 2000 Jul;25(3):302-5 PMID: 10888878
  14. Nuclear localization or inclusion body formation of ataxin-2 are not necessary for SCA2 pathogenesis in mouse or human.
    Nat Genet. 2000 Sep;26(1):44-50 PMID: 10973246
  15. Spinocerebellar ataxia type 2 with parkinsonism in ethnic Chinese.
    Neurology. 2000 Sep 26;55(6):800-5 PMID: 10993999
  16. Protein aggregation and pathogenesis of Huntington's disease: mechanisms and correlations.
    Biol Chem. 2000 Sep-Oct;381(9-10):937-42 PMID: 11076024
  17. Parkin is associated with actin filaments in neuronal and nonneural cells.
    Ann Neurol. 2000 Nov;48(5):737-44 PMID: 11079537
  18. 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
  19. 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
  20. SCA17, a novel autosomal dominant cerebellar ataxia caused by an expanded polyglutamine in TATA-binding protein.
    Hum Mol Genet. 2001 Jul 1;10(14):1441-8 PMID: 11448935
  21. Over-expression of inducible HSP70 chaperone suppresses neuropathology and improves motor function in SCA1 mice.
    Hum Mol Genet. 2001 Jul 1;10(14):1511-8 PMID: 11448943
  22. 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
  23. Non-expanded polyglutamine proteins in intranuclear inclusions of hereditary ataxias--triple-labeling immunofluorescence study.
    Acta Neuropathol. 2001 Aug;102(2):149-52 PMID: 11563629
  24. Parkin ubiquitinates the alpha-synuclein-interacting protein, synphilin-1: implications for Lewy-body formation in Parkinson disease.
    Nat Med. 2001 Oct;7(10):1144-50 PMID: 11590439
  25. SCA1 molecular genetics: a history of a 13 year collaboration against glutamines.
    Hum Mol Genet. 2001 Oct 1;10(20):2307-11 PMID: 11673415
  26. Differential expression and tissue distribution of parkin isoforms during mouse development.
    Brain Res Dev Brain Res. 2001 Oct 24;130(2):173-81 PMID: 11675120
  27. Spinocerebellar ataxia type 2 presenting as familial levodopa-responsive parkinsonism.
    Ann Neurol. 2001 Dec;50(6):812-5 PMID: 11761482
  28. Mechanisms underlying ubiquitination.
    Annu Rev Biochem. 2001;70:503-33 PMID: 11395416
  29. Paradoxical absence of nuclear inclusion in cerebellar Purkinje cells of hereditary ataxias linked to CAG expansion.
    J Neurol Neurosurg Psychiatry. 2002 Oct;73(4):450-2 PMID: 12235319
  30. Parkin prevents mitochondrial swelling and cytochrome c release in mitochondria-dependent cell death.
    Hum Mol Genet. 2003 Mar 1;12(5):517-26 PMID: 12588799
  31. Parkin binds to alpha/beta tubulin and increases their ubiquitination and degradation.
    J Neurosci. 2003 Apr 15;23(8):3316-24 PMID: 12716939
  32. The p38 subunit of the aminoacyl-tRNA synthetase complex is a Parkin substrate: linking protein biosynthesis and neurodegeneration.
    Hum Mol Genet. 2003 Jun 15;12(12):1427-37 PMID: 12783850
  33. Parkin facilitates the elimination of expanded polyglutamine proteins and leads to preservation of proteasome function.
    J Biol Chem. 2003 Jun 13;278(24):22044-55 PMID: 12676955
  34. Expansion of the polyQ repeat in ataxin-2 alters its Golgi localization, disrupts the Golgi complex and causes cell death.
    Hum Mol Genet. 2003 Jul 1;12(13):1485-96 PMID: 12812977
  35. How much phenotypic variation can be attributed to parkin genotype?
    Ann Neurol. 2003 Aug;54(2):176-85 PMID: 12891670
  36. The autosomal recessive juvenile Parkinson disease gene product, parkin, interacts with and ubiquitinates synaptotagmin XI.
    Hum Mol Genet. 2003 Oct 15;12(20):2587-97 PMID: 12925569
  37. Parkin-deficient mice exhibit nigrostriatal deficits but not loss of dopaminergic neurons.
    J Biol Chem. 2003 Oct 31;278(44):43628-35 PMID: 12930822
  38. A product of the human gene adjacent to parkin is a component of Lewy bodies and suppresses Pael receptor-induced cell death.
    J Biol Chem. 2003 Dec 19;278(51):51901-10 PMID: 14532270
  39. Complex phenotypes in an Indian family with homozygous SCA2 mutations.
    Ann Neurol. 2004 Jan;55(1):130-3 PMID: 14705123
  40. Parkin genetics: one model for Parkinson's disease.
    Hum Mol Genet. 2004 Apr 1;13 Spec No 1:R127-33 PMID: 14976155
  41. Mitochondrial dysfunction and oxidative damage in parkin-deficient mice.
    J Biol Chem. 2004 Apr 30;279(18):18614-22 PMID: 14985362
  42. Nitrosative stress linked to sporadic Parkinson's disease: S-nitrosylation of parkin regulates its E3 ubiquitin ligase activity.
    Proc Natl Acad Sci U S A. 2004 Jul 20;101(29):10810-4 PMID: 15252205
  43. Moderate expansion of a normally biallelic trinucleotide repeat in spinocerebellar ataxia type 2.
    Nat Genet. 1996 Nov;14(3):269-76 PMID: 8896555
  44. Identification of the spinocerebellar ataxia type 2 gene using a direct identification of repeat expansion and cloning technique, DIRECT.
    Nat Genet. 1996 Nov;14(3):277-84 PMID: 8896556
  45. Cloning of the gene for spinocerebellar ataxia 2 reveals a locus with high sensitivity to expanded CAG/glutamine repeats.
    Nat Genet. 1996 Nov;14(3):285-91 PMID: 8896557
  46. Intranuclear inclusions of expanded polyglutamine protein in spinocerebellar ataxia type 3.
    Neuron. 1997 Aug;19(2):333-44 PMID: 9292723
  47. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain.
    Science. 1997 Sep 26;277(5334):1990-3 PMID: 9302293
  48. Spinocerebellar ataxia type 2. Genotype and phenotype in German kindreds.
    Arch Neurol. 1997 Sep;54(9):1073-80 PMID: 9311350
  49. A wide variety of mutations in the parkin gene are responsible for autosomal recessive parkinsonism in Europe. French Parkinson's Disease Genetics Study Group and the European Consortium on Genetic Susceptibility in Parkinson's Disease.
    Hum Mol Genet. 1999 Apr;8(4):567-74 PMID: 10072423
Article Info
Journal
Experimental neurology
Abbr.
Exp Neurol
ISSN
0014-4886
Published
2007-02-00
Epub
2006-00-09
Pages
531-41
Language
English
Region
United States
NLM ID
0370712
PMCID
PMC2788988
Subset
IM
Grants
NINDS NIH HHS · R21 NS048083 · United States
NINDS NIH HHS · K01 NS047548 · United States
NINDS NIH HHS · K01-NS047548-01A1 · United States
NIA NIH HHS · P50 AG16570 · United States
NINDS NIH HHS · R01-NS33124 · United States
NINDS NIH HHS · K01 NS047548-01A1 · United States
NINDS NIH HHS · K01 NS047548-03 · United States
NIA NIH HHS · P50 AG016570 · United States
NINDS NIH HHS · P50NS038367 · United States
NINDS NIH HHS · R01 NS033123 · United States
NINDS NIH HHS · P50 NS038367 · United States
NINDS NIH HHS · K01 NS047548-02 · United States
NINDS NIH HHS · R21NS048083 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]