ZAKβ is activated by cellular compression and mediates contraction-induced MAP kinase signaling in skeletal muscle.


Journal

The EMBO journal
ISSN: 1460-2075
Titre abrégé: EMBO J
Pays: England
ID NLM: 8208664

Informations de publication

Date de publication:
01 09 2022
Historique:
revised: 28 05 2022
received: 12 05 2022
accepted: 22 06 2022
pubmed: 29 7 2022
medline: 9 9 2022
entrez: 28 7 2022
Statut: ppublish

Résumé

Mechanical inputs give rise to p38 and JNK activation, which mediate adaptive physiological responses in various tissues. In skeletal muscle, contraction-induced p38 and JNK signaling ensure adaptation to exercise, muscle repair, and hypertrophy. However, the mechanisms by which muscle fibers sense mechanical load to activate this signaling have remained elusive. Here, we show that the upstream MAP3K ZAKβ is activated by cellular compression induced by osmotic shock and cyclic compression in vitro, and muscle contraction in vivo. This function relies on ZAKβ's ability to recognize stress fibers in cells and Z-discs in muscle fibers when mechanically perturbed. Consequently, ZAK-deficient mice present with skeletal muscle defects characterized by fibers with centralized nuclei and progressive adaptation towards a slower myosin profile. Our results highlight how cells in general respond to mechanical compressive load and how mechanical forces generated during muscle contraction are translated into MAP kinase signaling.

Identifiants

pubmed: 35899396
doi: 10.15252/embj.2022111650
pmc: PMC9434084
doi:

Substances chimiques

Mitogen-Activated Protein Kinases EC 2.7.11.24
p38 Mitogen-Activated Protein Kinases EC 2.7.11.24
MAP Kinase Kinase Kinases EC 2.7.11.25
ZAK protein, mouse EC 2.7.11.25

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

e111650

Informations de copyright

© 2022 The Authors. Published under the terms of the CC BY NC ND 4.0 license.

Références

Small. 2020 Jan;16(2):e1903857
pubmed: 31782912
Nat Commun. 2020 Jan 15;11(1):282
pubmed: 31941964
Ann Rheum Dis. 2010 Jan;69 Suppl 1:i77-82
pubmed: 19995751
Toxins (Basel). 2016 Sep 02;8(9):
pubmed: 27598200
J Appl Physiol (1985). 2017 Aug 1;123(2):460-472
pubmed: 28572498
Nat Cell Biol. 2016 Aug;18(8):864-75
pubmed: 27398909
Nat Rev Cancer. 2009 Aug;9(8):537-49
pubmed: 19629069
PLoS One. 2012;7(5):e36964
pubmed: 22615857
J Biol Chem. 1999 Feb 12;274(7):4341-6
pubmed: 9933636
EMBO J. 2019 Dec 16;38(24):e102578
pubmed: 31381180
J Cell Physiol. 2002 Apr;191(1):95-104
pubmed: 11920685
J Muscle Res Cell Motil. 2009;30(5-6):171-85
pubmed: 19830582
Nat Cell Biol. 2003 Dec;5(12):1104-10
pubmed: 14634666
Nat Protoc. 2009;4(6):928-38
pubmed: 19478808
Nat Commun. 2020 Feb 7;11(1):787
pubmed: 32034161
Brain. 2017 Jan;140(1):37-48
pubmed: 27816943
Front Physiol. 2019 Jan 30;10:42
pubmed: 30761018
Trends Biochem Sci. 2017 Jan;42(1):57-71
pubmed: 27743844
J Biol Chem. 2002 Apr 19;277(16):13873-82
pubmed: 11836244
Cell. 2020 May 14;181(4):800-817.e22
pubmed: 32302590
EMBO J. 1998 May 1;17(9):2596-606
pubmed: 9564042
J Appl Physiol (1985). 2007 Jul;103(1):388-95
pubmed: 17303713
Emerg Top Life Sci. 2018 Dec;2(5):713-725
pubmed: 31693005
J Exp Biol. 2018 Aug 1;221(Pt 15):
pubmed: 29844202
Nucleic Acids Res. 2020 Nov 4;48(19):10648-10661
pubmed: 32941609
Nat Commun. 2018 Aug 2;9(1):3030
pubmed: 30072727
Nature. 2017 Jun 8;546(7657):307-311
pubmed: 28562590
Nature. 2020 Dec;588(7837):290-295
pubmed: 33057202
Bioinformatics. 2017 Jan 1;33(1):135-136
pubmed: 27605098
Nat Commun. 2021 Feb 8;12(1):869
pubmed: 33558521
Physiol Rev. 2008 Oct;88(4):1379-406
pubmed: 18923185
J Biol Chem. 2006 Sep 29;281(39):28802-10
pubmed: 16893890
Mol Cell Proteomics. 2019 May;18(5):1027-1035
pubmed: 30833379
Cell. 2014 Jul 31;158(3):633-46
pubmed: 25083873
Blood. 2008 Dec 15;112(13):4961-70
pubmed: 18818394
Front Physiol. 2020 Aug 31;11:813
pubmed: 32982762
Nature. 2020 Aug;584(7820):268-273
pubmed: 32728211
J Physiol. 2017 Jun 15;595(12):3949-3958
pubmed: 28098356
Cell. 2020 Jul 23;182(2):404-416.e14
pubmed: 32610081
Cold Spring Harb Perspect Med. 2018 Jun 1;8(6):
pubmed: 28490543
J Biol Chem. 2008 Nov 28;283(48):33080-6
pubmed: 18829460
Nat Protoc. 2014 Aug;9(8):1956-68
pubmed: 25058643
Biochem Biophys Res Commun. 2011 May 6;408(2):202-7
pubmed: 21371434
J Cell Biochem. 2010 Feb 15;109(3):460-7
pubmed: 20024954
Mol Biol Cell. 2017 Oct 1;28(20):2661-2675
pubmed: 28768826
Proc Natl Acad Sci U S A. 2015 Jan 6;112(1):154-9
pubmed: 25535389
Mol Cell Proteomics. 2020 Apr;19(4):716-729
pubmed: 32051234
Cell. 2000 Oct 13;103(2):239-52
pubmed: 11057897
Mol Cell. 2020 May 21;78(4):700-713.e7
pubmed: 32289254
Nat Methods. 2016 Sep;13(9):731-40
pubmed: 27348712
Genome Res. 2016 Feb;26(2):183-91
pubmed: 26755636
Front Physiol. 2018 Jul 05;9:824
pubmed: 30026699
J Biol Chem. 2019 Nov 15;294(46):17395-17408
pubmed: 31586031
EMBO J. 2022 Sep 1;41(17):e111650
pubmed: 35899396
Front Biosci. 2007 Jan 01;12:174-91
pubmed: 17127292
Cell Metab. 2015 Nov 3;22(5):922-35
pubmed: 26437602
Nat Rev Mol Cell Biol. 2019 Aug;20(8):457-473
pubmed: 31182865
J Med Chem. 2017 Jul 13;60(13):5927-5932
pubmed: 28586211

Auteurs

Cathrine Nordgaard (C)

Center for Healthy Aging, Department of Cellular and Molecular Medicine, University of Copenhagen, Copenhagen, Denmark.

Anna Constance Vind (AC)

Center for Healthy Aging, Department of Cellular and Molecular Medicine, University of Copenhagen, Copenhagen, Denmark.

Amy Stonadge (A)

Department of Biology, University of York, York, UK.

Rasmus Kjøbsted (R)

Department of Nutrition, Exercise and Sports, University of Copenhagen, Copenhagen, Denmark.

Goda Snieckute (G)

Center for Healthy Aging, Department of Cellular and Molecular Medicine, University of Copenhagen, Copenhagen, Denmark.

Pedro Antas (P)

Stem Cell and Cancer Biology Laboratory, The Francis Crick Institute, London, UK.

Melanie Blasius (M)

Center for Healthy Aging, Department of Cellular and Molecular Medicine, University of Copenhagen, Copenhagen, Denmark.

Marie Sofie Reinert (MS)

Center for Healthy Aging, Department of Cellular and Molecular Medicine, University of Copenhagen, Copenhagen, Denmark.

Ana Martinez Del Val (AM)

Mass Spectrometry for Quantitative Proteomics, Proteomics Program, Faculty of Health and Medical Sciences, The Novo Nordisk Foundation Center for Protein Research, University of Copenhagen, Copenhagen, Denmark.

Dorte Breinholdt Bekker-Jensen (DB)

Mass Spectrometry for Quantitative Proteomics, Proteomics Program, Faculty of Health and Medical Sciences, The Novo Nordisk Foundation Center for Protein Research, University of Copenhagen, Copenhagen, Denmark.

Peter Haahr (P)

Division of Biochemistry, The Netherlands Cancer Institute, Amsterdam, The Netherlands.

Yekaterina A Miroshnikova (YA)

Stem Cells and Metabolism Research Program, Faculty of Medicine and Helsinki Institute of Life Science, University of Helsinki, Helsinki, Finland.

Abdelghani Mazouzi (A)

Division of Biochemistry, The Netherlands Cancer Institute, Amsterdam, The Netherlands.

Sarah Falk (S)

Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.

Emeline Perrier-Groult (E)

Institut de Biologie et Chimie des Protéines, CNRS UMR5305, Lyon, France.

Christopher Tiedje (C)

Center for Healthy Aging, Department of Cellular and Molecular Medicine, University of Copenhagen, Copenhagen, Denmark.

Xiang Li (X)

Department of Biology, University of York, York, UK.

Jens Rithamer Jakobsen (JR)

Department of Orthopedic Surgery M, Institute of Sports Medicine Copenhagen, Bispebjerg Hospital, Copenhagen, Denmark.

Nicolas Oldenburg Jørgensen (NO)

Department of Nutrition, Exercise and Sports, University of Copenhagen, Copenhagen, Denmark.

Jørgen Fp Wojtaszewski (JF)

Department of Nutrition, Exercise and Sports, University of Copenhagen, Copenhagen, Denmark.

Frederic Mallein-Gerin (F)

Institut de Biologie et Chimie des Protéines, CNRS UMR5305, Lyon, France.

Jesper Løvind Andersen (JL)

Center for Healthy Aging, Department of Cellular and Molecular Medicine, University of Copenhagen, Copenhagen, Denmark.
Department of Orthopedic Surgery M, Institute of Sports Medicine Copenhagen, Bispebjerg Hospital, Copenhagen, Denmark.

Cristian Pablo Pennisi (CP)

Regenerative Medicine Group, Department of Health Science and Technology, Aalborg University, Aalborg, Denmark.

Christoffer Clemmensen (C)

Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.

Moustapha Kassem (M)

Department of Cellular and Molecular Medicine, Novo Nordisk Foundation Center for Stem Cell Biology (DanStem), University of Copenhagen, Copenhagen, Denmark.
Department of Endocrinology and Metabolism, University Hospital of Odense and University of Southern Denmark, Odense, Denmark.

Abbas Jafari (A)

Department of Cellular and Molecular Medicine, Novo Nordisk Foundation Center for Stem Cell Biology (DanStem), University of Copenhagen, Copenhagen, Denmark.

Thijn Brummelkamp (T)

Division of Biochemistry, The Netherlands Cancer Institute, Amsterdam, The Netherlands.
Oncode Institute, Division of Biochemistry, The Netherlands Cancer Institute, Amsterdam, The Netherlands.
CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences, Vienna, Austria.
Cancer Genomics Center, Amsterdam, The Netherlands.

Vivian Sw Li (VS)

Stem Cell and Cancer Biology Laboratory, The Francis Crick Institute, London, UK.

Sara A Wickström (SA)

Stem Cells and Metabolism Research Program, Faculty of Medicine and Helsinki Institute of Life Science, University of Helsinki, Helsinki, Finland.

Jesper Velgaard Olsen (JV)

Mass Spectrometry for Quantitative Proteomics, Proteomics Program, Faculty of Health and Medical Sciences, The Novo Nordisk Foundation Center for Protein Research, University of Copenhagen, Copenhagen, Denmark.

Gonzalo Blanco (G)

Department of Biology, University of York, York, UK.

Simon Bekker-Jensen (S)

Center for Healthy Aging, Department of Cellular and Molecular Medicine, University of Copenhagen, Copenhagen, Denmark.

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Classifications MeSH