Membrane Tension Gates ERK-Mediated Regulation of Pluripotent Cell Fate.

Beta-catenin Cell fate choice Cell surface mechanics ERK Embryonic stem cells Endocytosis Membrane tension mechanical signalling pluripotency

Journal

Cell stem cell
ISSN: 1875-9777
Titre abrégé: Cell Stem Cell
Pays: United States
ID NLM: 101311472

Informations de publication

Date de publication:
04 02 2021
Historique:
received: 03 12 2019
revised: 18 09 2020
accepted: 28 10 2020
pubmed: 21 11 2020
medline: 20 5 2021
entrez: 20 11 2020
Statut: ppublish

Résumé

Cell fate transitions are frequently accompanied by changes in cell shape and mechanics. However, how cellular mechanics affects the instructive signaling pathways controlling cell fate is poorly understood. To probe the interplay between shape, mechanics, and fate, we use mouse embryonic stem cells (ESCs), which change shape as they undergo early differentiation. We find that shape change is regulated by a β-catenin-mediated decrease in RhoA activity and subsequent decrease in the plasma membrane tension. Strikingly, preventing a decrease in membrane tension results in early differentiation defects in ESCs and gastruloids. Decreased membrane tension facilitates the endocytosis of FGF signaling components, which activate ERK signaling and direct the exit from the ESC state. Increasing Rab5a-facilitated endocytosis rescues defective early differentiation. Thus, we show that a mechanically triggered increase in endocytosis regulates early differentiation. Our findings are of fundamental importance for understanding how cell mechanics regulates biochemical signaling and therefore cell fate.

Identifiants

pubmed: 33217323
pii: S1934-5909(20)30534-8
doi: 10.1016/j.stem.2020.10.018
pmc: PMC7875115
pii:
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

273-284.e6

Subventions

Organisme : Medical Research Council
ID : MC_PC_12009
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 203151/Z/16/Z
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_00012/5
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_PC_17230
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_12018/5
Pays : United Kingdom

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Interests The authors declare no competing interests.

Références

Bioinformatics. 2015 Jan 15;31(2):166-9
pubmed: 25260700
Nucleic Acids Res. 2015 Jan;43(Database issue):D662-9
pubmed: 25352552
Nat Protoc. 2009;4(1):44-57
pubmed: 19131956
Nat Commun. 2018 Oct 11;9(1):4217
pubmed: 30310066
Nature. 2006 Apr 20;440(7087):1069-72
pubmed: 16547516
Nat Commun. 2017 May 17;8:15206
pubmed: 28513598
PLoS Biol. 2010 Nov 30;8(11):e1000544
pubmed: 21151339
Dev Cell. 2004 Apr;6(4):483-95
pubmed: 15068789
EMBO Rep. 2018 Aug;19(8):
pubmed: 29895711
J Cell Biol. 2000 Jul 10;150(1):193-203
pubmed: 10893267
Cell Stem Cell. 2019 Jul 3;25(1):23-38.e8
pubmed: 31080134
Nat Mater. 2019 Nov;18(11):1252-1263
pubmed: 31332337
Curr Biol. 2013 Aug 5;23(15):1409-17
pubmed: 23831292
Genome Biol. 2014;15(12):550
pubmed: 25516281
Nature. 1981 Jul 9;292(5819):154-6
pubmed: 7242681
Curr Opin Cell Biol. 2014 Dec;31:92-7
pubmed: 25269668
Cell Stem Cell. 2021 Feb 4;28(2):209-216.e4
pubmed: 33207217
Development. 2019 Jun 3;146(12):
pubmed: 31064783
Dev Cell. 2015 Nov 9;35(3):366-82
pubmed: 26555056
Nat Methods. 2010 Mar;7(3):168-9
pubmed: 20195247
Curr Opin Cell Biol. 2011 Aug;23(4):393-403
pubmed: 21474295
Biophys J. 2011 Mar 2;100(5):L25-7
pubmed: 21354386
Cell. 2013 May 23;153(5):948-62
pubmed: 23706734
Open Biol. 2019 Jan 31;9(1):180203
pubmed: 30958114
Nature. 2017 Mar 2;543(7643):118-121
pubmed: 28199303
Sci Signal. 2009 Apr 14;2(66):ra16
pubmed: 19366994
Cell Stem Cell. 2016 Oct 6;19(4):462-475
pubmed: 27452175
Cell Stem Cell. 2009 Jul 2;5(1):17-26
pubmed: 19570510
Nat Cell Biol. 2017 Jun;19(6):689-697
pubmed: 28530659
Semin Cell Dev Biol. 2017 Nov;71:30-41
pubmed: 28851599
Nature. 2008 May 22;453(7194):519-23
pubmed: 18497825
Cell Stem Cell. 2018 Jan 4;22(1):35-49.e7
pubmed: 29249464
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Sci Rep. 2015 Oct 05;5:14700
pubmed: 26435322
Nature. 2019 Sep;573(7772):130-134
pubmed: 31413369
Nat Rev Mol Cell Biol. 2016 Mar;17(3):170-82
pubmed: 26818440
J Vis Exp. 2015 Nov 24;(105):
pubmed: 26650833
Development. 2007 Aug;134(16):2895-902
pubmed: 17660198
J Cell Biol. 2000 Jan 10;148(1):127-36
pubmed: 10629223
Small GTPases. 2014;5(1):e28195
pubmed: 25763873
Cell. 2002 Mar 22;108(6):837-47
pubmed: 11955436
Cell. 2006 Aug 25;126(4):677-89
pubmed: 16923388
Development. 2009 Oct;136(19):3215-22
pubmed: 19710168
Nat Rev Mol Cell Biol. 2012 Sep;13(9):591-600
pubmed: 22895435
Nat Cell Biol. 2010 Jul;12(7):711-8
pubmed: 20581838
Bioinformatics. 2010 Apr 1;26(7):873-81
pubmed: 20147302
Dev Cell. 2016 Sep 26;38(6):571-3
pubmed: 27676427
Curr Biol. 2009 Sep 15;19(17):R790-9
pubmed: 19906581
Nucleic Acids Res. 2009 Jan;37(1):1-13
pubmed: 19033363
Nat Neurosci. 2016 Dec;19(12):1592-1598
pubmed: 27643431
Development. 2019 Mar 26;146(6):
pubmed: 30914406
Trends Cell Biol. 2013 Feb;23(2):47-53
pubmed: 23122885
Nature. 2019 Sep;573(7772):69-74
pubmed: 31435009
Proc Natl Acad Sci U S A. 1975 Dec;72(12):5099-102
pubmed: 1108013
Nat Rev Mol Cell Biol. 2008 Sep;9(9):730-6
pubmed: 18628785
Nat Cell Biol. 2011 Jun 19;13(7):838-45
pubmed: 21685889
Cold Spring Harb Symp Quant Biol. 1995;60:567-71
pubmed: 8824429
Development. 2014 May;141(9):1814-20
pubmed: 24718989
Nat Rev Mol Cell Biol. 2009 Sep;10(9):609-22
pubmed: 19696798
Dev Cell. 2017 Jun 5;41(5):511-526.e4
pubmed: 28552557
Mol Pharm. 2016 Feb 1;13(2):357-368
pubmed: 26702793
Exp Cell Res. 2017 Sep 1;358(1):20-30
pubmed: 28363828
Development. 2017 Nov 1;144(21):3894-3906
pubmed: 28951435
J Cell Biol. 1998 Feb 9;140(3):647-57
pubmed: 9456324
Genome Res. 2016 Oct;26(10):1342-1354
pubmed: 27486082
Am J Physiol Cell Physiol. 2002 Jul;283(1):C235-43
pubmed: 12055092
J Cell Biol. 2017 Sep 4;216(9):2959-2977
pubmed: 28687667
Development. 2017 Apr 1;144(7):1221-1234
pubmed: 28174249
Curr Biol. 2014 May 19;24(10):R484-94
pubmed: 24845681
Cell Logist. 2012 Oct 1;2(4):203-208
pubmed: 23538558
Proc Natl Acad Sci U S A. 2009 Jul 21;106(29):11972-7
pubmed: 19574460
Int J Biochem Cell Biol. 2013 Nov;45(11):2698-705
pubmed: 23871934

Auteurs

Henry De Belly (H)

MRC Laboratory for Molecular Cell Biology, University College London, Gower Street, London WC1E 6BT, UK; Wellcome/MRC Cambridge Stem Cell Research Institute, Puddicombe Way, University of Cambridge, Cambridge CB2 0AW, UK; Department of Physiology, Development, and Neuroscience, Downing Street, University of Cambridge, Cambridge CB2 3DY, UK.

Aki Stubb (A)

Department of Physiology, Development, and Neuroscience, Downing Street, University of Cambridge, Cambridge CB2 3DY, UK.

Ayaka Yanagida (A)

Wellcome/MRC Cambridge Stem Cell Research Institute, Puddicombe Way, University of Cambridge, Cambridge CB2 0AW, UK; Living Systems Institute, University of Exeter, Exeter EX4 4QD, UK.

Céline Labouesse (C)

Wellcome/MRC Cambridge Stem Cell Research Institute, Puddicombe Way, University of Cambridge, Cambridge CB2 0AW, UK.

Philip H Jones (PH)

Department of Physics & Astronomy, University College London, Gower Street, London WC1E 6BT, UK.

Ewa K Paluch (EK)

MRC Laboratory for Molecular Cell Biology, University College London, Gower Street, London WC1E 6BT, UK; Department of Physiology, Development, and Neuroscience, Downing Street, University of Cambridge, Cambridge CB2 3DY, UK. Electronic address: ekp25@cam.ac.uk.

Kevin J Chalut (KJ)

Wellcome/MRC Cambridge Stem Cell Research Institute, Puddicombe Way, University of Cambridge, Cambridge CB2 0AW, UK. Electronic address: kc370@cam.ac.uk.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH