Home LiteratureArticle Details
PMID: 12000718 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Parkin localizes to the Lewy bodies of Parkinson disease and dementia with Lewy bodies.

The American journal of pathology ·Vol. 160 ·No. 5 ·2002-05-00 ·Pages 1655-67

Schlossmacher MG, Frosch MP, Gai WP, Medina M, Sharma N, Forno L, Ochiishi T, Shimura H, Sharon R, Hattori N, Langston JW, Mizuno Y, Hyman BT, Selkoe DJ, Kosik KS

Abstract

Mutations in alpha-synuclein (alpha S) and parkin cause heritable forms of Parkinson disease (PD). We hypothesized that neuronal parkin, a known E3 ubiquitin ligase, facilitates the formation of Lewy bodies (LBs), a pathological hallmark of PD. Here, we report that affinity-purified parkin antibodies labeled classical LBs in substantia nigra sections from four related human disorders: sporadic PD, inherited alphaS-linked PD, dementia with LBs (DLB), and LB-positive, parkin-linked PD. Anti-parkin antibodies also detected LBs in entorhinal and cingulate cortices from DLB brain and alphaS inclusions in sympathetic gangliocytes from sporadic PD. Double labeling with confocal microscopy of DLB midbrain sections revealed that approximately 90% of anti-alpha S-reactive LBs were also detected by a parkin antibody to amino acids 342 to 353. Accordingly, parkin proteins, including the 53-kd mature isoform, were present in affinity-isolated LBs from DLB cortex. Fluorescence resonance energy transfer and immunoelectron microscopy showed that alphaS and parkin co-localized within brainstem and cortical LBs. Biochemically, parkin appeared most enriched in cytosolic and postsynaptic fractions of adult rat brain, but also in purified, alpha S-rich presynaptic elements that additionally contained parkin's E2-binding partner, UbcH7. We conclude that parkin and UbcH7 are present with alphaS in subcellular compartments of normal brain and that parkin frequently co-localizes with alpha S aggregates in the characteristic LB inclusions of PD and DLB. These results suggest that functional parkin proteins may be required during LB formation.

MeSH Terms
Amino Acid Sequence Animals Brain/metabolism,pathology COS Cells Cell Line Humans Immunohistochemistry Lewy Bodies/chemistry,pathology,ultrastructure Lewy Body Disease/metabolism,pathology Ligases/analysis,genetics,immunology Microscopy, Confocal Microscopy, Electron Molecular Sequence Data Mutation Parkinson Disease/metabolism,pathology Rats Rats, Sprague-Dawley Tumor Cells, Cultured Ubiquitin-Protein Ligases
Chemicals
Ubiquitin-Protein Ligases parkin protein Ligases
Authors & Affiliations
15 authors, click to expand affiliations / ORCID
Schlossmacher Michael G
Department of Neurology, Center for Neurologic Diseases, Brigham and Women's Hospital, Boston, Massachusetts 02115, USA. schloss@cnd.bwh.harvard.edu
Frosch Matthew P
Gai Wei Ping
Medina Miguel
Sharma Nutan
Forno Lysia
Ochiishi Tomoyo
Shimura Hideki
Sharon Ronit
Hattori Nobutaka
Langston J William
Mizuno Yoshikuni
Hyman Bradley T
Selkoe Dennis J
Kosik Kenneth S
References (59)
59 references, click to expand
  1. An autopsy case of autosomal-recessive juvenile parkinsonism with a homozygous exon 4 deletion in the parkin gene.
    Mov Disord. 2000 Sep;15(5):884-8 PMID: 11009195
  2. Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase.
    Nat Genet. 2000 Jul;25(3):302-5 PMID: 10888878
  3. Parkin is associated with actin filaments in neuronal and nonneural cells.
    Ann Neurol. 2000 Nov;48(5):737-44 PMID: 11079537
  4. PSD-95 involvement in maturation of excitatory synapses.
    Science. 2000 Nov 17;290(5495):1364-8 PMID: 11082065
  5. In situ and in vitro study of colocalization and segregation of alpha-synuclein, ubiquitin, and lipids in Lewy bodies.
    Exp Neurol. 2000 Dec;166(2):324-33 PMID: 11085897
  6. 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
  7. 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
  8. A ubiquitin-like system mediates protein lipidation.
    Nature. 2000 Nov 23;408(6811):488-92 PMID: 11100732
  9. Subcellular localization of alpha-synuclein in primary neuronal cultures: effect of missense mutations.
    J Neural Transm Suppl. 2000;(58):53-63 PMID: 11128613
  10. Clinical and pathologic abnormalities in a family with parkinsonism and parkin gene mutations.
    Neurology. 2001 Feb 27;56(4):555-7 PMID: 11222808
  11. Accumulation of alpha-synuclein in autonomic nerves in pure autonomic failure.
    Neurology. 2001 Apr 10;56(7):980-1 PMID: 11294945
  12. Features of the parkin/ariadne-like ubiquitin ligase, HHARI, that regulate its interaction with the ubiquitin-conjugating enzyme, Ubch7.
    J Biol Chem. 2001 Jun 1;276(22):19640-7 PMID: 11278816
  13. Parkin is associated with cellular vesicles.
    J Neurochem. 2001 Jul;78(1):42-54 PMID: 11432972
  14. A close association of torsinA and alpha-synuclein in Lewy bodies: a fluorescence resonance energy transfer study.
    Am J Pathol. 2001 Jul;159(1):339-44 PMID: 11438481
  15. 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
  16. Familial juvenile parkinsonism: clinical and pathologic study in a family.
    Neurology. 1994 Mar;44(3 Pt 1):437-41 PMID: 8145912
  17. Electron microscopy of Lewy bodies in the amygdala-parahippocampal region. Comparison with inclusion bodies in the MPTP-treated squirrel monkey.
    Adv Neurol. 1996;69:217-28 PMID: 8615131
  18. Consensus guidelines for the clinical and pathologic diagnosis of dementia with Lewy bodies (DLB): report of the consortium on DLB international workshop.
    Neurology. 1996 Nov;47(5):1113-24 PMID: 8909416
  19. Clinical genetic analysis of Parkinson's disease in the Contursi kindred.
    Ann Neurol. 1996 Nov;40(5):767-75 PMID: 8957018
  20. In situ molecular association of dystrophin with actin revealed by sensitized emission immuno-resonance energy transfer.
    Proc Natl Acad Sci U S A. 1997 May 27;94(11):5685-90 PMID: 9159133
  21. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease.
    Science. 1997 Jun 27;276(5321):2045-7 PMID: 9197268
  22. Alpha-synuclein in Lewy bodies.
    Nature. 1997 Aug 28;388(6645):839-40 PMID: 9278044
  23. 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
  24. alpha-Synuclein occurs in lipid-rich high molecular weight complexes, binds fatty acids, and shows homology to the fatty acid-binding proteins.
    Proc Natl Acad Sci U S A. 2001 Jul 31;98(16):9110-5 PMID: 11481478
  25. Zinc finger proteins as potential targets for toxic metal ions: differential effects on structure and function.
    Antioxid Redox Signal. 2001 Aug;3(4):625-34 PMID: 11554449
  26. Lewy bodies and parkinsonism in families with parkin mutations.
    Ann Neurol. 2001 Sep;50(3):293-300 PMID: 11558785
  27. 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
  28. Alpha-synuclein has an altered conformation and shows a tight intermolecular interaction with ubiquitin in Lewy bodies.
    Acta Neuropathol. 2001 Oct;102(4):329-34 PMID: 11603807
  29. Parkin is linked to the ubiquitin pathway.
    J Mol Med (Berl). 2001 Sep;79(9):482-94 PMID: 11692161
  30. Parkin and CASK/LIN-2 associate via a PDZ-mediated interaction and are co-localized in lipid rafts and postsynaptic densities in brain.
    J Biol Chem. 2002 Jan 4;277(1):486-91 PMID: 11679592
  31. Immunocytochemical localization of synphilin-1, an alpha-synuclein-associated protein, in neurodegenerative disorders.
    Acta Neuropathol. 2002 Mar;103(3):209-14 PMID: 11907799
  32. Brain dopamine and the syndromes of Parkinson and Huntington. Clinical, morphological and neurochemical correlations.
    J Neurol Sci. 1973 Dec;20(4):415-55 PMID: 4272516
  33. Presenile dementia with Alzheimer-, Pick- and Lewy-body changes.
    Acta Neuropathol. 1976 Nov 15;36(3):221-33 PMID: 188300
  34. Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation.
    J Cell Biol. 1983 May;96(5):1374-88 PMID: 6404912
  35. 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
  36. Subcellular localization of wild-type and Parkinson's disease-associated mutant alpha -synuclein in human and transgenic mouse brain.
    J Neurosci. 2000 Sep 1;20(17):6365-73 PMID: 10964942
  37. The lore of the RINGs: substrate recognition and catalysis by ubiquitin ligases.
    Trends Cell Biol. 2000 Oct;10(10):429-39 PMID: 10998601
  38. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease.
    Nat Genet. 1998 Feb;18(2):106-8 PMID: 9462735
  39. A large kindred with autosomal dominant Parkinson's disease.
    Ann Neurol. 1990 Mar;27(3):276-82 PMID: 2158268
  40. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism.
    Nature. 1998 Apr 9;392(6676):605-8 PMID: 9560156
  41. 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
  42. Accuracy of the clinical diagnoses of Lewy body disease, Parkinson disease, and dementia with Lewy bodies: a clinicopathologic study.
    Arch Neurol. 1998 Jul;55(7):969-78 PMID: 9678315
  43. Multiple-system atrophy: a new alpha-synuclein disease?
    Lancet. 1998 Aug 15;352(9127):547-8 PMID: 9716068
  44. Pathologic and biochemical studies of juvenile parkinsonism linked to chromosome 6q.
    Neurology. 1998 Sep;51(3):890-2 PMID: 9748052
  45. 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
  46. 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
  47. Lewy body-type degeneration in cardiac plexus in Parkinson's and incidental Lewy body diseases.
    Neurology. 1999 Apr 12;52(6):1269-71 PMID: 10214756
  48. Immunohistochemical and subcellular localization of Parkin protein: absence of protein in autosomal recessive juvenile parkinsonism patients.
    Ann Neurol. 1999 May;45(5):668-72 PMID: 10319893
  49. The septin CDCrel-1 binds syntaxin and inhibits exocytosis.
    Nat Neurosci. 1999 May;2(5):434-9 PMID: 10321247
  50. A novel transactivation domain in parkin.
    Trends Biochem Sci. 1999 Jun;24(6):229-31 PMID: 10366851
  51. Characterization and autophosphorylation of Ca2+/calmodulin-dependent protein kinase in the postsynaptic density of the rat forebrain.
    Brain Res. 1993 Apr 30;610(1):97-107 PMID: 8390910
  52. Mutation of the E6-AP ubiquitin ligase reduces nuclear inclusion frequency while accelerating polyglutamine-induced pathology in SCA1 mice.
    Neuron. 1999 Dec;24(4):879-92 PMID: 10624951
  53. [Two cases of sporadic juvenile Parkinson's disease caused by homozygous deletion of Parkin gene].
    No To Shinkei. 1999 Dec;51(12):1061-4 PMID: 10654303
  54. Temporal accrual of complement proteins in amyloid plaques in Down's syndrome with Alzheimer's disease.
    Am J Pathol. 2000 Feb;156(2):489-99 PMID: 10666378
  55. New animal models for Parkinson's disease.
    Cell. 2000 Apr 14;101(2):115-8 PMID: 10786830
  56. Association between early-onset Parkinson's disease and mutations in the parkin gene.
    N Engl J Med. 2000 May 25;342(21):1560-7 PMID: 10824074
  57. Ubiquitin and its kin: how close are the family ties?
    Trends Cell Biol. 2000 Aug;10(8):335-42 PMID: 10884686
  58. Microtubule-associated protein 1B is a component of cortical Lewy bodies and binds alpha-synuclein filaments.
    J Biol Chem. 2000 Jul 14;275(28):21500-7 PMID: 10764738
  59. Autosomal recessive juvenile parkinsonism: a key to understanding nigral degeneration in sporadic Parkinson's disease.
    Neuropathology. 2000 Sep;20 Suppl:S85-90 PMID: 11037196
Article Info
Journal
The American journal of pathology
Abbr.
Am J Pathol
ISSN
0002-9440
Published
2002-05-00
Pages
1655-67
Language
English
Region
United States
NLM ID
0370502
PMCID
PMC1850875
Subset
IM
Grants
NINDS NIH HHS · NS02127 · United States
NINDS NIH HHS · P50 NS038375 · United States
NINDS NIH HHS · NS38375 · United States
NINDS NIH HHS · P50 NS038372 · United States
NINDS NIH HHS · NS38372 · United States
NINDS NIH HHS · K08 NS002127 · 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: product@genelibs.com