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
References (33)
33 references, click to expand
-
Rotenone inhibition of spindle microtubule assembly in mammalian cells.
Exp Cell Res. 1974 Mar 30;85(1):41-6
PMID: 4857086
-
Phenotypic consequences of tubulin overproduction in Saccharomyces cerevisiae: differences between alpha-tubulin and beta-tubulin.
Mol Cell Biol. 1990 Oct;10(10):5295-304
PMID: 2204812
-
The alpha- and beta-tubulin folding pathways.
Trends Cell Biol. 1997 Dec;7(12):479-84
PMID: 17709011
-
The ubiquitin system.
Annu Rev Biochem. 1998;67:425-79
PMID: 9759494
-
Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase.
Nat Genet. 2000 Jul;25(3):302-5
PMID: 10888878
-
Microtubule assembly is directly affected by MPP(+)in vitro.
Cell Biol Int. 2001;25(10):981-4
PMID: 11589612
-
Dominant effects of tubulin overexpression in Saccharomyces cerevisiae.
Mol Cell Biol. 1989 Mar;9(3):1049-59
PMID: 2657385
-
A small amphipathic alpha-helical region is required for transcriptional activities and proteasome-dependent turnover of the tyrosine-phosphorylated Stat5.
EMBO J. 2000 Feb 1;19(3):392-9
PMID: 10654938
-
Microtubule transport in the axon.
Int Rev Cytol. 2002;212:41-62
PMID: 11804039
-
Autoregulation of tubulin expression is achieved through specific degradation of polysomal tubulin mRNAs.
Cell. 1987 Oct 23;51(2):283-92
PMID: 2444342
-
Complete genomic screen in Parkinson disease: evidence for multiple genes.
JAMA. 2001 Nov 14;286(18):2239-44
PMID: 11710888
-
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
-
Chronic systemic pesticide exposure reproduces features of Parkinson's disease.
Nat Neurosci. 2000 Dec;3(12):1301-6
PMID: 11100151
-
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
-
Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism.
Nature. 1998 Apr 9;392(6676):605-8
PMID: 9560156
-
Intermediate filament-ubiquitin diseases: implications for cell sanitization.
Biochem Soc Symp. 1989;55:193-201
PMID: 2559734
-
[3H]dihydrorotenone binding to NADH: ubiquinone reductase (complex I) of the electron transport chain: an autoradiographic study.
J Neurosci. 1996 Jun 15;16(12):3807-16
PMID: 8656275
-
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
-
Purification of brain microtubules and microtubule-associated protein 1 using taxol.
Methods Enzymol. 1986;134:104-15
PMID: 2881188
-
Ubiquitin is a common factor in intermediate filament inclusion bodies of diverse type in man, including those of Parkinson's disease, Pick's disease, and Alzheimer's disease, as well as Rosenthal fibres in cerebellar astrocytomas, cytoplasmic bodies in muscle, and mallory bodies in alcoholic liver disease.
J Pathol. 1988 May;155(1):9-15
PMID: 2837558
-
Rotenone inhibition of tubulin self-assembly.
Biochim Biophys Acta. 1978 Nov 1;543(4):590-4
PMID: 568944
-
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
-
Lactacystin, proteasome function, and cell fate.
J Biol Chem. 1998 Apr 10;273(15):8545-8
PMID: 9535824
-
Autoregulated control of tubulin synthesis in animal cells.
Curr Opin Cell Biol. 1989 Feb;1(1):10-4
PMID: 2629858
-
Parkin and the molecular pathways of Parkinson's disease.
Neuron. 2001 Sep 27;31(6):885-8
PMID: 11580890
-
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
-
Mechanisms of MPTP toxicity.
Mov Disord. 1998;13 Suppl 1:35-8
PMID: 9613716
-
Inhibition of ATP synthesis by 1-methyl-4-phenylpyridinium ion (MPP+) in isolated mitochondria from mouse brains.
Neurosci Lett. 1987 Oct 16;81(1-2):204-8
PMID: 3501080
-
Filaments of Lewy bodies contain insoluble cytoskeletal elements.
Am J Pathol. 1992 Apr;140(4):809-22
PMID: 1314025
-
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
-
Influence of MPP+ on the state of tubulin polymerisation in NGF-differentiated PC12 cells.
J Neurosci Res. 1999 Apr 1;56(1):28-35
PMID: 10213472
-
Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis.
Science. 1983 Feb 25;219(4587):979-80
PMID: 6823561
-
Microtubules and axonal growth.
Curr Opin Cell Biol. 1997 Feb;9(1):29-36
PMID: 9013665