Homotypic fibrillization of TMEM106B across diverse neurodegenerative diseases.


Journal

Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066

Informations de publication

Date de publication:
14 04 2022
Historique:
received: 25 01 2022
revised: 14 02 2022
accepted: 23 02 2022
pubmed: 6 3 2022
medline: 20 4 2022
entrez: 5 3 2022
Statut: ppublish

Résumé

Misfolding and aggregation of disease-specific proteins, resulting in the formation of filamentous cellular inclusions, is a hallmark of neurodegenerative disease with characteristic filament structures, or conformers, defining each proteinopathy. Here we show that a previously unsolved amyloid fibril composed of a 135 amino acid C-terminal fragment of TMEM106B is a common finding in distinct human neurodegenerative diseases, including cases characterized by abnormal aggregation of TDP-43, tau, or α-synuclein protein. A combination of cryoelectron microscopy and mass spectrometry was used to solve the structures of TMEM106B fibrils at a resolution of 2.7 Å from postmortem human brain tissue afflicted with frontotemporal lobar degeneration with TDP-43 pathology (FTLD-TDP, n = 8), progressive supranuclear palsy (PSP, n = 2), or dementia with Lewy bodies (DLB, n = 1). The commonality of abundant amyloid fibrils composed of TMEM106B, a lysosomal/endosomal protein, to a broad range of debilitating human disorders indicates a shared fibrillization pathway that may initiate or accelerate neurodegeneration.

Identifiants

pubmed: 35247328
pii: S0092-8674(22)00259-8
doi: 10.1016/j.cell.2022.02.026
pmc: PMC9018563
mid: NIHMS1784277
pii:
doi:

Substances chimiques

Amyloid 0
DNA-Binding Proteins 0
Membrane Proteins 0
Nerve Tissue Proteins 0
TMEM106B protein, human 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

1346-1355.e15

Subventions

Organisme : NIA NIH HHS
ID : R01 AG063780
Pays : United States
Organisme : NINDS NIH HHS
ID : U01 NS110438
Pays : United States
Organisme : CIHR
ID : 74580
Pays : Canada
Organisme : NINDS NIH HHS
ID : U54 NS110435
Pays : United States
Organisme : NIA NIH HHS
ID : RF1 AG061829
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

Published by Elsevier Inc.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Références

Cell. 2020 Feb 20;180(4):633-644.e12
pubmed: 32032505
J Comput Chem. 2004 Oct;25(13):1605-12
pubmed: 15264254
Neurology. 2011 Feb 1;76(5):467-74
pubmed: 21178100
Commun Biol. 2021 Jul 15;4(1):874
pubmed: 34267316
Elife. 2018 Nov 09;7:
pubmed: 30412051
J Mol Biol. 2015 Jan 30;427(2):478-90
pubmed: 25451785
Brain Pathol. 2021 May;31(3):e12945
pubmed: 33709463
J Biol Chem. 2014 Jul 11;289(28):19670-80
pubmed: 24872421
Nature. 2022 May;605(7909):304-309
pubmed: 35344984
Brain. 2011 Mar;134(Pt 3):808-15
pubmed: 21354975
EMBO J. 2014 Mar 3;33(5):450-67
pubmed: 24357581
EMBO Rep. 2020 Oct 5;21(10):e50197
pubmed: 32761777
Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W526-31
pubmed: 15215442
Nature. 2018 Sep;561(7721):137-140
pubmed: 30158706
Nature. 2017 Jul 13;547(7662):185-190
pubmed: 28678775
Annu Rev Neurosci. 2001;24:1121-59
pubmed: 11520930
J Biol Chem. 2012 Jun 1;287(23):19355-65
pubmed: 22511793
J Struct Biol. 2016 Jan;193(1):1-12
pubmed: 26592709
Mol Cell Neurosci. 2014 Jul;61:226-40
pubmed: 25066864
Acta Neuropathol Commun. 2013 Jul 11;1:36
pubmed: 24252750
Cell Rep. 2020 Mar 10;30(10):3506-3519.e6
pubmed: 32160553
Acta Crystallogr D Biol Crystallogr. 2010 Jan;66(Pt 1):12-21
pubmed: 20057044
Transl Psychiatry. 2021 Jan 11;11(1):27
pubmed: 33431793
Brain Pathol. 2021 Mar;31(2):223-238
pubmed: 33016371
Nature. 2013 Sep 5;501(7465):45-51
pubmed: 24005412
Front Immunol. 2020 May 19;11:931
pubmed: 32508827
Proc Natl Acad Sci U S A. 2021 Jan 12;118(2):
pubmed: 33361332
Nat Methods. 2020 Jan;17(1):79-85
pubmed: 31768063
J Struct Biol. 2017 Jun;198(3):163-176
pubmed: 28193500
Acta Crystallogr D Struct Biol. 2018 Jun 1;74(Pt 6):531-544
pubmed: 29872004
Proc Natl Acad Sci U S A. 2020 Jan 21;117(3):1496-1503
pubmed: 31896580
Nat Biotechnol. 2008 Dec;26(12):1367-72
pubmed: 19029910
Neuron. 2011 Oct 20;72(2):245-56
pubmed: 21944778
Elife. 2019 Feb 05;8:
pubmed: 30720432
Proc Natl Acad Sci U S A. 2013 Apr 2;110(14):5468-73
pubmed: 23513222
Nature. 2021 Oct;598(7880):359-363
pubmed: 34588692
J Neurochem. 2013 Sep;126(6):781-91
pubmed: 23742080
Nature. 2021 Aug;596(7873):583-589
pubmed: 34265844
Nat Genet. 2010 Mar;42(3):234-9
pubmed: 20154673
Protein Sci. 2005 Nov;14(11):2915-8
pubmed: 16199659
Front Mol Neurosci. 2020 Oct 16;13:586731
pubmed: 33177989
Curr Opin Struct Biol. 2019 Oct;58:34-42
pubmed: 31200186
Front Mol Neurosci. 2020 Mar 11;13:37
pubmed: 32218723
Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):486-501
pubmed: 20383002
Nature. 2022 Jan;601(7891):139-143
pubmed: 34880495
Brain. 2020 Jul 1;143(7):2255-2271
pubmed: 32572497
Acta Neuropathol. 2007 Jul;114(1):5-22
pubmed: 17579875
Nature. 2022 May;605(7909):310-314
pubmed: 35344985
Front Neurosci. 2020 Nov 04;14:581936
pubmed: 33250706
Nature. 2006 Aug 24;442(7105):916-9
pubmed: 16862116
Acta Neuropathol. 2011 Jul;122(1):111-3
pubmed: 21644037
Genomics Proteomics Bioinformatics. 2020 Feb;18(1):52-64
pubmed: 32413515
Cell Rep. 2021 Mar 16;34(11):108843
pubmed: 33730588
Sci Transl Med. 2016 May 11;8(338):338ra66
pubmed: 27169802
Nat Methods. 2017 Apr;14(4):331-332
pubmed: 28250466
Acta Neuropathol. 2021 Mar;141(3):327-339
pubmed: 33386471
Nature. 2020 Sep;585(7825):464-469
pubmed: 32461689
Nature. 2020 Apr;580(7802):283-287
pubmed: 32050258
Acta Neuropathol. 2012 Jan;123(1):1-11
pubmed: 22101365
Science. 2005 Jan 14;307(5707):262-5
pubmed: 15653506
Nature. 2019 Apr;568(7752):420-423
pubmed: 30894745
IUCrJ. 2021 Dec 01;9(Pt 1):86-97
pubmed: 35059213
Nucleic Acids Res. 2018 Jan 4;46(D1):D624-D632
pubmed: 29145643
J Phys Chem B. 2005 Oct 20;109(41):19043-5
pubmed: 16853453
Brain. 2022 May 24;145(4):1257-1263
pubmed: 34999780

Auteurs

Andrew Chang (A)

Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY 10027, USA; Department of Biochemistry and Molecular Biophysics, Columbia University, New York, NY 10032, USA; Taub Institute for Research on Alzheimer's Disease and the Aging Brain, Columbia University Irving Medical Center, 630 West 168th Street, New York, NY 10032, USA.

Xinyu Xiang (X)

Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY 10027, USA; Department of Biochemistry and Molecular Biophysics, Columbia University, New York, NY 10032, USA; Taub Institute for Research on Alzheimer's Disease and the Aging Brain, Columbia University Irving Medical Center, 630 West 168th Street, New York, NY 10032, USA; Department of Structural Biology, Stanford University School of Medicine, Stanford, CA 94305, USA.

Jing Wang (J)

Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY 10027, USA; Department of Biochemistry and Molecular Biophysics, Columbia University, New York, NY 10032, USA; Taub Institute for Research on Alzheimer's Disease and the Aging Brain, Columbia University Irving Medical Center, 630 West 168th Street, New York, NY 10032, USA.

Carolyn Lee (C)

Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY 10027, USA; Department of Biochemistry and Molecular Biophysics, Columbia University, New York, NY 10032, USA; Taub Institute for Research on Alzheimer's Disease and the Aging Brain, Columbia University Irving Medical Center, 630 West 168th Street, New York, NY 10032, USA; Department of Microbiology & Immunology, Columbia University, New York, NY 10032, USA.

Tamta Arakhamia (T)

Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY 10027, USA; Department of Biochemistry and Molecular Biophysics, Columbia University, New York, NY 10032, USA; Taub Institute for Research on Alzheimer's Disease and the Aging Brain, Columbia University Irving Medical Center, 630 West 168th Street, New York, NY 10032, USA.

Marija Simjanoska (M)

Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY 10027, USA; Department of Biochemistry and Molecular Biophysics, Columbia University, New York, NY 10032, USA; Taub Institute for Research on Alzheimer's Disease and the Aging Brain, Columbia University Irving Medical Center, 630 West 168th Street, New York, NY 10032, USA.

Chi Wang (C)

Department of Biochemistry and Molecular Biophysics, Columbia University, New York, NY 10032, USA.

Yari Carlomagno (Y)

Department of Neuroscience, Mayo Clinic, Jacksonville, FL 32224, USA.

Guoan Zhang (G)

Proteomics and Metabolomics Core Facility, Weill Cornell Medicine, New York, NY 10021, USA.

Shikhar Dhingra (S)

Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY 10027, USA.

Manon Thierry (M)

Centre for Cognitive Neurology, Department of Neurology, New York University School of Medicine, New York, NY 10016, USA.

Jolien Perneel (J)

Applied and Translational Neurogenomics, VIB Center for Molecular Neurology, VIB, Antwerp, Belgium; Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium.

Bavo Heeman (B)

Applied and Translational Neurogenomics, VIB Center for Molecular Neurology, VIB, Antwerp, Belgium; Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium.

Lauren M Forgrave (LM)

Department of Pathology and Laboratory Medicine, University of British Columbia, Vancouver, BC V6T 2B5, Canada; Department of Pathology and Laboratory Medicine, St. Paul's Hospital, Providence Health Care, Vancouver, Canada.

Michael DeTure (M)

Department of Neuroscience, Mayo Clinic, Jacksonville, FL 32224, USA.

Mari L DeMarco (ML)

Department of Pathology and Laboratory Medicine, University of British Columbia, Vancouver, BC V6T 2B5, Canada; Department of Pathology and Laboratory Medicine, St. Paul's Hospital, Providence Health Care, Vancouver, Canada.

Casey N Cook (CN)

Department of Neuroscience, Mayo Clinic, Jacksonville, FL 32224, USA.

Rosa Rademakers (R)

Applied and Translational Neurogenomics, VIB Center for Molecular Neurology, VIB, Antwerp, Belgium; Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium.

Dennis W Dickson (DW)

Department of Neuroscience, Mayo Clinic, Jacksonville, FL 32224, USA.

Leonard Petrucelli (L)

Department of Neuroscience, Mayo Clinic, Jacksonville, FL 32224, USA.

Michael H B Stowell (MHB)

Department of Molecular, Cellular and Developmental Biology, University of Colorado Boulder, Boulder, CO 80309, USA. Electronic address: stowellm@colorado.edu.

Ian R A Mackenzie (IRA)

Department of Pathology and Laboratory Medicine, University of British Columbia, Vancouver, BC V6T 2B5, Canada. Electronic address: ian.mackenzie@vch.ca.

Anthony W P Fitzpatrick (AWP)

Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY 10027, USA; Department of Biochemistry and Molecular Biophysics, Columbia University, New York, NY 10032, USA; Taub Institute for Research on Alzheimer's Disease and the Aging Brain, Columbia University Irving Medical Center, 630 West 168th Street, New York, NY 10032, USA. Electronic address: anthony.fitzpatrick@columbia.edu.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH