Cavin4 interacts with Bin1 to promote T-tubule formation and stability in developing skeletal muscle.


Journal

The Journal of cell biology
ISSN: 1540-8140
Titre abrégé: J Cell Biol
Pays: United States
ID NLM: 0375356

Informations de publication

Date de publication:
06 12 2021
Historique:
received: 09 05 2019
revised: 02 06 2021
accepted: 20 09 2021
entrez: 11 10 2021
pubmed: 12 10 2021
medline: 24 12 2021
Statut: ppublish

Résumé

The cavin proteins are essential for caveola biogenesis and function. Here, we identify a role for the muscle-specific component, Cavin4, in skeletal muscle T-tubule development by analyzing two vertebrate systems, mouse and zebrafish. In both models, Cavin4 localized to T-tubules, and loss of Cavin4 resulted in aberrant T-tubule maturation. In zebrafish, which possess duplicated cavin4 paralogs, Cavin4b was shown to directly interact with the T-tubule-associated BAR domain protein Bin1. Loss of both Cavin4a and Cavin4b caused aberrant accumulation of interconnected caveolae within the T-tubules, a fragmented T-tubule network enriched in Caveolin-3, and an impaired Ca2+ response upon mechanical stimulation. We propose a role for Cavin4 in remodeling the T-tubule membrane early in development by recycling caveolar components from the T-tubule to the sarcolemma. This generates a stable T-tubule domain lacking caveolae that is essential for T-tubule function.

Identifiants

pubmed: 34633413
pii: 212693
doi: 10.1083/jcb.201905065
pmc: PMC8513623
pii:
doi:

Substances chimiques

Adaptor Proteins, Signal Transducing 0
Bin1 protein, mouse 0
Cavin4 protein, mouse 0
Membrane Proteins 0
Muscle Proteins 0
Nerve Tissue Proteins 0
Tumor Suppressor Proteins 0
Zebrafish Proteins 0
bin1b protein, zebrafish 0
cavin4b protein, zebrafish 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2021 Lo et al.

Références

FEBS Lett. 1995 Nov 27;376(1-2):108-12
pubmed: 8521953
Elife. 2021 Apr 27;10:
pubmed: 33904409
Hum Mol Genet. 2005 Jul 1;14(13):1727-43
pubmed: 15888488
Traffic. 2008 Jun;9(6):893-909
pubmed: 18397183
Circ Cardiovasc Genet. 2011 Aug 1;4(4):349-58
pubmed: 21642240
Ann Biomed Eng. 1995 May-Jun;23(3):226-46
pubmed: 7631979
Hum Mol Genet. 2014 Jul 1;23(13):3566-78
pubmed: 24549043
EMBO J. 2009 Apr 22;28(8):1001-15
pubmed: 19262564
Dev Cell. 2015 Nov 23;35(4):513-25
pubmed: 26585296
Science. 2002 Aug 16;297(5584):1193-6
pubmed: 12183633
Science. 2001 Sep 28;293(5539):2449-52
pubmed: 11498544
J Physiol. 1975 Sep;250(3):513-39
pubmed: 1080806
J Cell Biol. 1975 Feb;64(2):493-7
pubmed: 1078824
Development. 2011 Oct;138(19):4193-8
pubmed: 21896629
Genome Res. 2003 Dec;13(12):2700-7
pubmed: 14613981
Prog Biophys Mol Biol. 2008 Oct-Nov;98(2-3):149-60
pubmed: 19351512
J Struct Biol. 2016 Oct;196(1):37-47
pubmed: 27343996
Traffic. 2000 Apr;1(4):326-41
pubmed: 11208118
Dev Biol. 1992 Dec;154(2):245-60
pubmed: 1426638
Proc Biol Sci. 2011 Sep 22;278(1719):2714-23
pubmed: 21697171
J Clin Invest. 2017 Dec 1;127(12):4477-4487
pubmed: 29130937
Mol Cell Biol. 2008 May;28(10):3424-36
pubmed: 18332105
Biomaterials. 2011 Aug;32(22):5304-10
pubmed: 21531457
Development. 2009 Oct;136(19):3367-76
pubmed: 19736328
J Cell Sci. 2008 Jun 15;121(Pt 12):2075-86
pubmed: 18505796
J Biol Chem. 2016 Jul 29;291(31):16307-17
pubmed: 27268056
Dev Dyn. 2007 Nov;236(11):3088-99
pubmed: 17937395
Am J Physiol Cell Physiol. 2008 Aug;295(2):C490-8
pubmed: 18508909
J Cell Biol. 1968 Jul;38(1):51-66
pubmed: 5691978
Elife. 2021 Feb 16;10:
pubmed: 33591275
PLoS One. 2010 Oct 29;5(10):e13763
pubmed: 21048941
Acta Biochim Biophys Sin (Shanghai). 2007 May;39(5):384-90
pubmed: 17492136
Methods Mol Biol. 2019;2025:403-421
pubmed: 31267464
J Struct Biol. 2008 Mar;161(3):298-313
pubmed: 18069000
Cell. 2011 Feb 4;144(3):402-13
pubmed: 21295700
PLoS Biol. 2018 Apr 5;16(4):e2005473
pubmed: 29621251
J Biol Chem. 2001 Jun 15;276(24):21425-33
pubmed: 11259414
Nat Cell Biol. 2009 Jul;11(7):807-14
pubmed: 19525939
J Cell Biol. 2015 Oct 12;211(1):53-61
pubmed: 26459598
Nat Commun. 2015 Jun 08;6:7378
pubmed: 26051838
Cell. 2008 Jan 11;132(1):113-24
pubmed: 18191225
Nucleic Acids Res. 2018 Jul 2;46(W1):W242-W245
pubmed: 29762716
Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8655-9
pubmed: 7567992
Proc Natl Acad Sci U S A. 2011 Jan 18;108(3):1176-81
pubmed: 21199938
J Mol Med (Berl). 2014 May;92(5):453-63
pubmed: 24590001
J Dev Biol. 2019 Jun 02;7(2):
pubmed: 31159511
Genome Biol. 2007;8 Suppl 1:S7
pubmed: 18047699
Curr Biol. 2017 Jul 10;27(13):1968-1981.e7
pubmed: 28648821
Elife. 2017 Dec 05;6:
pubmed: 29202928
Dev Biol. 1991 Aug;146(2):353-63
pubmed: 1864461
Nat Protoc. 2008;3(1):59-69
pubmed: 18193022
Tissue Cell. 1977;9(3):437-46
pubmed: 929575
Nucleic Acids Res. 2014 Jul;42(Web Server issue):W401-7
pubmed: 24861617
J Struct Biol. 2005 Oct;152(1):36-51
pubmed: 16182563
Hum Mol Genet. 2010 Jun 15;19(12):2433-44
pubmed: 20338942
Proc Natl Acad Sci U S A. 2020 Dec 1;117(48):30476-30487
pubmed: 33214152
Proc Natl Acad Sci U S A. 2014 Mar 11;111(10):3811-6
pubmed: 24567387
J Cell Biol. 1999 Jun 28;145(7):1443-59
pubmed: 10385524
Biochemistry. 2014 Nov 25;53(46):7297-309
pubmed: 25350771
Zebrafish. 2017 Feb;14(1):69-72
pubmed: 27631880
Biotechniques. 2013 Dec;55(6):314-6
pubmed: 24344681
J Cell Biol. 1997 Jun 16;137(6):1355-67
pubmed: 9182667
J Clin Lab Anal. 2018 Feb;32(2):
pubmed: 28594148
Biophys J. 2008 Aug;95(4):2053-62
pubmed: 18487298
Nat Commun. 2020 Jul 24;11(1):3711
pubmed: 32709891
Dev Dyn. 2007 Nov;236(11):3077-87
pubmed: 17948311
Cell Metab. 2008 Oct;8(4):310-7
pubmed: 18840361
PLoS Genet. 2016 Jun 13;12(6):e1006099
pubmed: 27294373
Hum Mol Genet. 2000 Dec 12;9(20):3047-54
pubmed: 11115849
J Cell Biol. 2009 Jun 29;185(7):1259-73
pubmed: 19546242
Mol Endocrinol. 2011 Feb;25(2):291-306
pubmed: 21239615
Circ Res. 1980 Feb;46(2):244-55
pubmed: 7351042
J Cell Biol. 2015 Aug 31;210(5):833-49
pubmed: 26323694
PLoS One. 2014 May 29;9(5):e98186
pubmed: 24873830
Dis Model Mech. 2012 Nov;5(6):726-32
pubmed: 23115202
J Cell Biol. 1997 Jan 13;136(1):137-54
pubmed: 9008709
Annu Rev Cell Dev Biol. 2018 Oct 6;34:111-136
pubmed: 30296391
J Proteome Res. 2020 Apr 3;19(4):1522-1532
pubmed: 32081002
J Biol Chem. 2004 Aug 27;279(35):36828-40
pubmed: 15199055
Biochem Biophys Res Commun. 2012 Jul 13;423(4):785-8
pubmed: 22713473
J Histochem Cytochem. 1994 Feb;42(2):155-66
pubmed: 8288861
J Gen Physiol. 2018 Feb 5;150(2):189-210
pubmed: 29317466
J Exp Biol. 2000 Feb;203(Pt 4):813-20
pubmed: 10648223

Auteurs

Harriet P Lo (HP)

Institute for Molecular Bioscience, The University of Queensland, Brisbane, Queensland, Australia.

Ye-Wheen Lim (YW)

Institute for Molecular Bioscience, The University of Queensland, Brisbane, Queensland, Australia.

Zherui Xiong (Z)

Institute for Molecular Bioscience, The University of Queensland, Brisbane, Queensland, Australia.

Nick Martel (N)

Institute for Molecular Bioscience, The University of Queensland, Brisbane, Queensland, Australia.

Charles Ferguson (C)

Institute for Molecular Bioscience, The University of Queensland, Brisbane, Queensland, Australia.

Nicholas Ariotti (N)

Institute for Molecular Bioscience, The University of Queensland, Brisbane, Queensland, Australia.

Jean Giacomotto (J)

Queensland Brain Institute, The University of Queensland, Brisbane, Queensland, Australia.
Queensland Centre for Mental Health Research, West Moreton Hospital and Health Service and University of Queensland, Brisbane, Queensland, Australia.

James Rae (J)

Institute for Molecular Bioscience, The University of Queensland, Brisbane, Queensland, Australia.

Matthias Floetenmeyer (M)

Centre for Microscopy and Microanalysis, The University of Queensland, Brisbane, Queensland, Australia.

Shayli Varasteh Moradi (SV)

CSIRO-Queensland University of Technology Synthetic Biology Alliance, ARC Centre of Excellence in Synthetic Biology, Centre for Agriculture and the Bioeconomy, School of Biology and Environmental Science, Queensland University of Technology, Brisbane, Queensland, Australia.

Ya Gao (Y)

Institute for Molecular Bioscience, The University of Queensland, Brisbane, Queensland, Australia.

Vikas A Tillu (VA)

Institute for Molecular Bioscience, The University of Queensland, Brisbane, Queensland, Australia.

Di Xia (D)

Genome Innovation Hub, The University of Queensland, Brisbane, Queensland, Australia.

Huang Wang (H)

Translational Research Institute, Mater Research Institute, The University of Queensland, Brisbane, Queensland, Australia.

Samira Rahnama (S)

CSIRO-Queensland University of Technology Synthetic Biology Alliance, ARC Centre of Excellence in Synthetic Biology, Centre for Agriculture and the Bioeconomy, School of Biology and Environmental Science, Queensland University of Technology, Brisbane, Queensland, Australia.

Susan J Nixon (SJ)

Institute for Molecular Bioscience, The University of Queensland, Brisbane, Queensland, Australia.

Michele Bastiani (M)

Institute for Molecular Bioscience, The University of Queensland, Brisbane, Queensland, Australia.

Ryan D Day (RD)

Institute for Molecular Bioscience, The University of Queensland, Brisbane, Queensland, Australia.

Kelly A Smith (KA)

Institute for Molecular Bioscience, The University of Queensland, Brisbane, Queensland, Australia.

Nathan J Palpant (NJ)

Institute for Molecular Bioscience, The University of Queensland, Brisbane, Queensland, Australia.

Wayne A Johnston (WA)

CSIRO-Queensland University of Technology Synthetic Biology Alliance, ARC Centre of Excellence in Synthetic Biology, Centre for Agriculture and the Bioeconomy, School of Biology and Environmental Science, Queensland University of Technology, Brisbane, Queensland, Australia.

Kirill Alexandrov (K)

CSIRO-Queensland University of Technology Synthetic Biology Alliance, ARC Centre of Excellence in Synthetic Biology, Centre for Agriculture and the Bioeconomy, School of Biology and Environmental Science, Queensland University of Technology, Brisbane, Queensland, Australia.

Brett M Collins (BM)

Institute for Molecular Bioscience, The University of Queensland, Brisbane, Queensland, Australia.

Thomas E Hall (TE)

Institute for Molecular Bioscience, The University of Queensland, Brisbane, Queensland, Australia.

Robert G Parton (RG)

Institute for Molecular Bioscience, The University of Queensland, Brisbane, Queensland, Australia.
Centre for Microscopy and Microanalysis, The University of Queensland, Brisbane, Queensland, Australia.

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