Dynamics of huntingtin protein interactions in the striatum identifies candidate modifiers of Huntington disease.

AMPA receptors Arp2/3 D. melanogaster LuTHy SNARE immunoaffinity purification-mass spectrometry label-free quantification metabolic labeling protein interactions synaptic biology vesicular trafficking

Journal

Cell systems
ISSN: 2405-4720
Titre abrégé: Cell Syst
Pays: United States
ID NLM: 101656080

Informations de publication

Date de publication:
20 04 2022
Historique:
received: 15 06 2021
revised: 18 11 2021
accepted: 24 01 2022
pubmed: 13 2 2022
medline: 26 4 2022
entrez: 12 2 2022
Statut: ppublish

Résumé

Huntington disease (HD) is a monogenic neurodegenerative disorder with one causative gene, huntingtin (HTT). Yet, HD pathobiology is multifactorial, suggesting that cellular factors influence disease progression. Here, we define HTT protein-protein interactions (PPIs) perturbed by the mutant protein with expanded polyglutamine in the mouse striatum, a brain region with selective HD vulnerability. Using metabolically labeled tissues and immunoaffinity purification-mass spectrometry, we establish that polyglutamine-dependent modulation of HTT PPI abundances and relative stability starts at an early stage of pathogenesis in a Q140 HD mouse model. We identify direct and indirect PPIs that are also genetic disease modifiers using in-cell two-hybrid and behavioral assays in HD human cell and Drosophila models, respectively. Validated, disease-relevant mHTT-dependent interactions encompass mediators of synaptic neurotransmission (SNAREs and glutamate receptors) and lysosomal acidification (V-ATPase). Our study provides a resource for understanding mHTT-dependent dysfunction in cortico-striatal cellular networks, partly through impaired synaptic communication and endosomal-lysosomal system. A record of this paper's Transparent Peer Review process is included in the supplemental information.

Identifiants

pubmed: 35148841
pii: S2405-4712(22)00040-0
doi: 10.1016/j.cels.2022.01.005
pmc: PMC9317655
mid: NIHMS1780257
pii:
doi:

Substances chimiques

Huntingtin Protein 0

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

304-320.e5

Subventions

Organisme : NIA NIH HHS
ID : R01 AG057339
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS077926
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS090914
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2022 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

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Auteurs

Todd M Greco (TM)

Department of Molecular Biology, Princeton University, Washington Road, Princeton, NJ, USA.

Christopher Secker (C)

Neuroproteomics, Max Delbrück Centre for Molecular Medicine, Berlin, Germany.

Eduardo Silva Ramos (ES)

Neuroproteomics, Max Delbrück Centre for Molecular Medicine, Berlin, Germany.

Joel D Federspiel (JD)

Department of Molecular Biology, Princeton University, Washington Road, Princeton, NJ, USA.

Jeh-Ping Liu (JP)

Department of Neuroscience, University of Virginia School of Medicine, Charlottesville, VA, USA.

Alma M Perez (AM)

Jan and Dan Duncan Neurological Research Institute, Houston, TX, USA; Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA.

Ismael Al-Ramahi (I)

Jan and Dan Duncan Neurological Research Institute, Houston, TX, USA; Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA.

Jeffrey P Cantle (JP)

Department of Psychology, Western Washington University, Bellingham, WA, USA.

Jeffrey B Carroll (JB)

Department of Psychology, Western Washington University, Bellingham, WA, USA.

Juan Botas (J)

Jan and Dan Duncan Neurological Research Institute, Houston, TX, USA; Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA.

Scott O Zeitlin (SO)

Department of Neuroscience, University of Virginia School of Medicine, Charlottesville, VA, USA.

Erich E Wanker (EE)

Neuroproteomics, Max Delbrück Centre for Molecular Medicine, Berlin, Germany.

Ileana M Cristea (IM)

Department of Molecular Biology, Princeton University, Washington Road, Princeton, NJ, USA. Electronic address: icristea@princeton.edu.

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