The structural basis of lipid scrambling and inactivation in the endoplasmic reticulum scramblase TMEM16K.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
02 09 2019
Historique:
received: 14 10 2018
accepted: 01 08 2019
entrez: 4 9 2019
pubmed: 4 9 2019
medline: 31 12 2019
Statut: epublish

Résumé

Membranes in cells have defined distributions of lipids in each leaflet, controlled by lipid scramblases and flip/floppases. However, for some intracellular membranes such as the endoplasmic reticulum (ER) the scramblases have not been identified. Members of the TMEM16 family have either lipid scramblase or chloride channel activity. Although TMEM16K is widely distributed and associated with the neurological disorder autosomal recessive spinocerebellar ataxia type 10 (SCAR10), its location in cells, function and structure are largely uncharacterised. Here we show that TMEM16K is an ER-resident lipid scramblase with a requirement for short chain lipids and calcium for robust activity. Crystal structures of TMEM16K show a scramblase fold, with an open lipid transporting groove. Additional cryo-EM structures reveal extensive conformational changes from the cytoplasmic to the ER side of the membrane, giving a state with a closed lipid permeation pathway. Molecular dynamics simulations showed that the open-groove conformation is necessary for scramblase activity.

Identifiants

pubmed: 31477691
doi: 10.1038/s41467-019-11753-1
pii: 10.1038/s41467-019-11753-1
pmc: PMC6718402
doi:

Substances chimiques

ANO10 protein, human 0
Anoctamins 0
Lipids 0
Phospholipid Transfer Proteins 0
Calcium SY7Q814VUP

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3956

Subventions

Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/P01948X/1
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/I019855/1
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : NIGMS NIH HHS
ID : P41 GM103311
Pays : United States
Organisme : British Heart Foundation
ID : FS/17/45/33102
Pays : United Kingdom
Organisme : NIGMS NIH HHS
ID : T32 GM008539
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM106717
Pays : United States

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Auteurs

Simon R Bushell (SR)

Structural Genomics Consortium, Nuffield Department of Medicine, University of Oxford, Old Road Campus Research Building, Roosevelt Drive, Oxford, OX3 7DQ, UK.

Ashley C W Pike (ACW)

Structural Genomics Consortium, Nuffield Department of Medicine, University of Oxford, Old Road Campus Research Building, Roosevelt Drive, Oxford, OX3 7DQ, UK.

Maria E Falzone (ME)

Department of Biochemistry, Weill Cornell Medical School, 1300 York Avenue, New York, NY, 10065, USA.

Nils J G Rorsman (NJG)

Department of Pharmacology, University of Oxford, Mansfield Road, Oxford, OX1 3QT, UK.
OxSyBio, Atlas Building, Harwell Campus, Didcot, Oxfordshire, OX11 0QX, UK.

Chau M Ta (CM)

Department of Pharmacology, University of Oxford, Mansfield Road, Oxford, OX1 3QT, UK.
Department of Cardiology, Washington University in St. Louis, St. Louis, MO, 63110, USA.

Robin A Corey (RA)

Department of Biochemistry, University of Oxford, South Parks Road, Oxford, OX1 3QT, UK.

Thomas D Newport (TD)

Department of Biochemistry, University of Oxford, South Parks Road, Oxford, OX1 3QT, UK.
Oxford Nanopore Technologies, Oxford Science Park, Oxford, OX4 4DQ, UK.

John C Christianson (JC)

Nuffield Department of Rheumatology, Orthopaedics and Musculoskeletal Sciences, University of Oxford, Windmill Road, Oxford, OX3 7LD, UK.

Lara F Scofano (LF)

Department of Pharmacology, University of Oxford, Mansfield Road, Oxford, OX1 3QT, UK.

Chitra A Shintre (CA)

Structural Genomics Consortium, Nuffield Department of Medicine, University of Oxford, Old Road Campus Research Building, Roosevelt Drive, Oxford, OX3 7DQ, UK.
Vertex Pharmaceuticals Ltd, Milton Park, Oxfordshire, OX14 4RW, UK.

Annamaria Tessitore (A)

Structural Genomics Consortium, Nuffield Department of Medicine, University of Oxford, Old Road Campus Research Building, Roosevelt Drive, Oxford, OX3 7DQ, UK.
Nuffield Division of Clinical Laboratory Sciences, Oxford University, Oxford, OX3 9DU, UK.

Amy Chu (A)

Structural Genomics Consortium, Nuffield Department of Medicine, University of Oxford, Old Road Campus Research Building, Roosevelt Drive, Oxford, OX3 7DQ, UK.
Department of Biochemistry, Oxford University, Oxford, OX1 3QT, UK.

Qinrui Wang (Q)

Structural Genomics Consortium, Nuffield Department of Medicine, University of Oxford, Old Road Campus Research Building, Roosevelt Drive, Oxford, OX3 7DQ, UK.
Department of Biochemistry, University of Oxford, South Parks Road, Oxford, OX1 3QT, UK.

Leela Shrestha (L)

Structural Genomics Consortium, Nuffield Department of Medicine, University of Oxford, Old Road Campus Research Building, Roosevelt Drive, Oxford, OX3 7DQ, UK.

Shubhashish M M Mukhopadhyay (SMM)

Structural Genomics Consortium, Nuffield Department of Medicine, University of Oxford, Old Road Campus Research Building, Roosevelt Drive, Oxford, OX3 7DQ, UK.

James D Love (JD)

Department of Biochemistry, Albert Einstein College of Medicine, 1300 Morris Park Avenue, Bronx, NY, 10461-1602, USA.
Novo Nordisk A/S, Novo Nordisk Park, 2760, Måløv, Denmark.

Nicola A Burgess-Brown (NA)

Structural Genomics Consortium, Nuffield Department of Medicine, University of Oxford, Old Road Campus Research Building, Roosevelt Drive, Oxford, OX3 7DQ, UK.

Rebecca Sitsapesan (R)

Department of Pharmacology, University of Oxford, Mansfield Road, Oxford, OX1 3QT, UK.

Phillip J Stansfeld (PJ)

Department of Biochemistry, University of Oxford, South Parks Road, Oxford, OX1 3QT, UK.

Juha T Huiskonen (JT)

Division of Structural Biology, Wellcome Centre for Human Genetics, University of Oxford, Roosevelt Drive, Oxford, OX3 7BN, UK.

Paolo Tammaro (P)

Department of Pharmacology, University of Oxford, Mansfield Road, Oxford, OX1 3QT, UK.

Alessio Accardi (A)

Department of Biochemistry, Weill Cornell Medical School, 1300 York Avenue, New York, NY, 10065, USA.
Department of Anesthesiology, Weill Cornell Medical School, 25 East 68th Street, New York, NY, 10065, USA.
Department of Physiology and Biophysics, Weill Cornell Medical School, 1300 York Avenue, New York, NY, 10065, USA.

Elisabeth P Carpenter (EP)

Structural Genomics Consortium, Nuffield Department of Medicine, University of Oxford, Old Road Campus Research Building, Roosevelt Drive, Oxford, OX3 7DQ, UK. liz.carpenter@sgc.ox.ac.uk.

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Classifications MeSH