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PMID: 20008565 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Valosin-containing protein (VCP) is required for autophagy and is disrupted in VCP disease.

The Journal of cell biology ·Vol. 187 ·No. 6 ·2009-12-14 ·Pages 875-88

Ju JS, Fuentealba RA, Miller SE, Jackson E, Piwnica-Worms D, Baloh RH, Weihl CC

Abstract

Mutations in valosin-containing protein (VCP) cause inclusion body myopathy (IBM), Paget's disease of the bone, and frontotemporal dementia (IBMPFD). Patient muscle has degenerating fibers, rimmed vacuoles (RVs), and sarcoplasmic inclusions containing ubiquitin and TDP-43 (TARDNA-binding protein 43). In this study, we find that IBMPFD muscle also accumulates autophagosome-associated proteins, Map1-LC3 (LC3), and p62/sequestosome, which localize to RVs. To test whether VCP participates in autophagy, we silenced VCP or expressed adenosine triphosphatase-inactive VCP. Under basal conditions, loss of VCP activity results in autophagosome accumulation. After autophagic induction, these autophagosomes fail to mature into autolysosomes and degrade LC3. Similarly, IBMPFD mutant VCP expression in cells and animals leads to the accumulation of nondegradative autophagosomes that coalesce at RVs and fail to degrade aggregated proteins. Interestingly, TDP-43 accumulates in the cytosol upon autophagic inhibition, similar to that seen after IBMPFD mutant expression. These data implicate VCP in autophagy and suggest that impaired autophagy explains the pathology seen in IBMPFD muscle, including TDP-43 accumulation.

MeSH Terms
Adaptor Proteins, Signal Transducing/metabolism Adenosine Triphosphatases/genetics,metabolism Animals Autophagy/genetics Biopsy Case-Control Studies Cell Cycle Proteins/genetics,metabolism Cell Line Chloroquine DNA-Binding Proteins/metabolism Disease Models, Animal Female Frontotemporal Dementia/chemically induced,enzymology,genetics,pathology Heat-Shock Proteins/metabolism Humans Mice Mice, Transgenic Microtubule-Associated Proteins/metabolism Mutation Myositis, Inclusion Body/chemically induced,enzymology,genetics,pathology Osteitis Deformans/chemically induced,enzymology,genetics,pathology Quadriceps Muscle/enzymology,pathology RNA Interference Recombinant Fusion Proteins/metabolism Sequestosome-1 Protein Transfection Ubiquitin/metabolism Valosin Containing Protein
Chemicals
Adaptor Proteins, Signal Transducing Cell Cycle Proteins DNA-Binding Proteins Heat-Shock Proteins MAP1LC3A protein, human Map1lc3b protein, mouse Microtubule-Associated Proteins Recombinant Fusion Proteins SQSTM1 protein, human Sequestosome-1 Protein Sqstm1 protein, mouse Ubiquitin Chloroquine Adenosine Triphosphatases VCP protein, human Valosin Containing Protein Vcp protein, mouse
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Ju Jeong-Sun
Department of Neurology, Washington University School of Medicine, St. Louis, MO 63110, USA.
Fuentealba Rodrigo A
Miller Sara E
Jackson Erin
Piwnica-Worms David
Baloh Robert H
Weihl Conrad C
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Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
1540-8140
Published
2009-12-14
Pages
875-88
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2806317
Subset
IM
Grants
NCI NIH HHS · P50 CA094056 · United States
NINDS NIH HHS · P30 NS057105 · United States
NIA NIH HHS · P50 AG005681 · United States
NIA NIH HHS · K08 AG026271 · United States
NIA NIH HHS · 5K08AG026271 · United States
NIA NIH HHS · R01AG031867 · United States
NCI NIH HHS · P50 CA94056 · United States
NIA NIH HHS · P50AG05681 · United States
NIA NIH HHS · R01 AG031867 · United States
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