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PMID: 12716939 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Parkin binds to alpha/beta tubulin and increases their ubiquitination and degradation.

Ren Y, Zhao J, Feng J

Abstract

In addition to inhibiting the mitochondrial respiratory chain, toxins known to cause Parkinson's disease (PD), such as 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine and rotenone, also strongly depolymerize microtubules and increase tubulin degradation. Microtubules are polymers of tubulin alpha/beta heterodimers, whose correct folding requires coordinated actions of cellular chaperonins and cofactors. Misfolded tubulin monomers are highly toxic and quickly degraded through a hitherto unknown mechanism. Here we report that parkin, a protein-ubiquitin E3 ligase linked to PD, was tightly bound to microtubules in taxol-mediated microtubule coassembly assays. In lysates from the rat brain or transfected human embryonic kidney (HEK) 293 cells, alpha-tubulin and beta-tubulin were strongly coimmunoprecipitated with parkin at 4 degrees C in the presence of colchicine, a condition in which tubulin exits as alpha/beta heterodimers. At the subcellular level, parkin exhibited punctate immunostaining along microtubules in rat brain sections, cultured primary neurons, glial cells, and cell lines. This pattern of subcellular localization was abolished in cells treated with the microtubule-depolymerizing drug colchicine. The binding between parkin and tubulin apparently led to increased ubiquitination and accelerated degradation of alpha- and beta-tubulins in HEK293 cells. Similarly ubiquitinated tubulins were also observed in rat brain lysates. Furthermore, parkin mutants found in PD patients did not ubiquitinate or degrade either tubulin. Taken together, our results show that parkin is a novel tubulin-binding protein, as well as a microtubule-associated protein. Its ability to enhance the ubiquitination and degradation of misfolded tubulins may play a significant role in protecting neurons from toxins that cause PD.

MeSH Terms
Animals Antibody Specificity Cells, Cultured Colchicine/pharmacology Dimerization Fibroblasts/drug effects,metabolism Humans Kidney/cytology,metabolism Ligases/genetics,metabolism Male Mice Microtubule-Associated Proteins/metabolism Microtubules/drug effects,metabolism Mutation Nerve Tissue Proteins/biosynthesis Neuroblastoma/drug therapy,metabolism Neurons/cytology,drug effects,metabolism Paclitaxel/pharmacology Parkinson Disease/genetics,metabolism Protein Binding Rats Rats, Sprague-Dawley Tubulin/metabolism Ubiquitin-Protein Ligases Ubiquitins/metabolism
Chemicals
MAP1A protein, human MAP1A protein, mouse Map1a protein, rat Microtubule-Associated Proteins Nerve Tissue Proteins Tubulin Ubiquitins postsynaptic density proteins Ubiquitin-Protein Ligases parkin protein Ligases Paclitaxel Colchicine
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Ren Yong
Department of Physiology and Biophysics, State University of New York at Buffalo, Buffalo, New York 14214, USA.
Zhao Jinghui
Feng Jian
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Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2003-04-15
Pages
3316-24
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC1876717
Subset
IM
Grants
NINDS NIH HHS · R01 NS041722 · United States
NINDS NIH HHS · NS41722 · United States
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