Oscillations of Delta-like1 regulate the balance between differentiation and maintenance of muscle stem cells.


Journal

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

Informations de publication

Date de publication:
26 02 2021
Historique:
received: 06 05 2020
accepted: 04 02 2021
entrez: 27 2 2021
pubmed: 28 2 2021
medline: 16 3 2021
Statut: epublish

Résumé

Cell-cell interactions mediated by Notch are critical for the maintenance of skeletal muscle stem cells. However, dynamics, cellular source and identity of functional Notch ligands during expansion of the stem cell pool in muscle growth and regeneration remain poorly characterized. Here we demonstrate that oscillating Delta-like 1 (Dll1) produced by myogenic cells is an indispensable Notch ligand for self-renewal of muscle stem cells in mice. Dll1 expression is controlled by the Notch target Hes1 and the muscle regulatory factor MyoD. Consistent with our mathematical model, our experimental analyses show that Hes1 acts as the oscillatory pacemaker, whereas MyoD regulates robust Dll1 expression. Interfering with Dll1 oscillations without changing its overall expression level impairs self-renewal, resulting in premature differentiation of muscle stem cells during muscle growth and regeneration. We conclude that the oscillatory Dll1 input into Notch signaling ensures the equilibrium between self-renewal and differentiation in myogenic cell communities.

Identifiants

pubmed: 33637744
doi: 10.1038/s41467-021-21631-4
pii: 10.1038/s41467-021-21631-4
pmc: PMC7910593
doi:

Substances chimiques

Calcium-Binding Proteins 0
Dlk1 protein, mouse 0
Hes1 protein, mouse 0
MyoD Protein 0
MyoD1 myogenic differentiation protein 0
Transcription Factor HES-1 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1318

Commentaires et corrections

Type : ErratumIn

Références

Dev Dyn. 2005 Oct;234(2):332-8
pubmed: 16127714
Cell. 1997 Nov 28;91(5):639-48
pubmed: 9393857
Stem Cells. 2012 Feb;30(2):232-42
pubmed: 22045613
J Vis Exp. 2019 Dec 12;(154):
pubmed: 31885384
EMBO J. 2015 May 12;34(10):1417-33
pubmed: 25828096
Development. 2008 Aug;135(15):2531-41
pubmed: 18579678
Nat Cell Biol. 2016 Sep;18(9):930-40
pubmed: 27548913
Dev Cell. 2010 Apr 20;18(4):662-74
pubmed: 20412780
Genes Dev. 2014 Aug 1;28(15):1641-6
pubmed: 25085416
J Biol Chem. 1999 Mar 12;274(11):7238-44
pubmed: 10066785
Science. 2002 Oct 25;298(5594):840-3
pubmed: 12399594
Dev Cell. 2009 Jun;16(6):810-21
pubmed: 19531352
Nature. 2020 Apr;580(7801):113-118
pubmed: 31915384
Development. 2014 Jul;141(14):2780-90
pubmed: 25005473
Dev Cell. 2020 Mar 23;52(6):731-747.e8
pubmed: 32059775
Cell Stem Cell. 2018 Oct 4;23(4):530-543.e9
pubmed: 30290177
Proc Natl Acad Sci U S A. 2011 Feb 22;108(8):3300-5
pubmed: 21300886
Science. 2005 Sep 23;309(5743):2064-7
pubmed: 16141372
Development. 2019 Oct 14;146(20):
pubmed: 31519691
Nat Commun. 2013;4:2869
pubmed: 24287629
Development. 1997 Mar;124(6):1139-48
pubmed: 9102301
Dev Growth Differ. 2020 Jan;62(1):59-66
pubmed: 31489617
Methods Mol Biol. 2014;1187:169-79
pubmed: 25053489
Development. 2011 Nov;138(21):4609-19
pubmed: 21989910
Nat Immunol. 2004 Jun;5(6):638-44
pubmed: 15146182
Cell. 2000 Sep 15;102(6):777-86
pubmed: 11030621
Genes Dev. 2016 Jan 1;30(1):102-16
pubmed: 26728556
Cell Rep. 2017 Nov 14;21(7):1994-2004
pubmed: 29141228
Exp Cell Res. 2010 Nov 1;316(18):3028-33
pubmed: 20452344
Proc Natl Acad Sci U S A. 2007 Jul 3;104(27):11292-7
pubmed: 17592117
Science. 2012 Jun 15;336(6087):1440-4
pubmed: 22700930
Dev Cell. 2002 Sep;3(3):397-409
pubmed: 12361602
Cell. 1993 Dec 31;75(7):1351-9
pubmed: 8269513
Genes Dev. 2019 May 1;33(9-10):524-535
pubmed: 30862660
Development. 2001 Jan;128(1):107-16
pubmed: 11092816
J Biol Chem. 2007 Feb 2;282(5):3058-65
pubmed: 17158101
J Biol Chem. 1994 Feb 18;269(7):5150-6
pubmed: 7906273
Development. 2005 Jun;132(12):2685-95
pubmed: 15930108
Development. 2011 Sep;138(17):3625-37
pubmed: 21828091
Cell. 2018 Feb 8;172(4):869-880.e19
pubmed: 29398116
Elife. 2018 Oct 05;7:
pubmed: 30289388
Proc Natl Acad Sci U S A. 2007 Mar 13;104(11):4443-8
pubmed: 17360543
Neuron. 2008 Apr 10;58(1):52-64
pubmed: 18400163
Proc Natl Acad Sci U S A. 2007 Jan 9;104(2):537-42
pubmed: 17194759
Dev Cell. 2012 Sep 11;23(3):469-81
pubmed: 22940113
Genes Dev. 2017 Mar 1;31(5):524-535
pubmed: 28373207
Science. 1999 Apr 30;284(5415):770-6
pubmed: 10221902
Curr Top Dev Biol. 1991;25:177-225
pubmed: 1743056
Mech Dev. 2001 Nov;109(1):61-8
pubmed: 11677053
J Histochem Cytochem. 2006 Nov;54(11):1177-91
pubmed: 16899758
Annu Rev Genet. 1990;24:387-407
pubmed: 2128440
Science. 2013 Dec 6;342(6163):1203-8
pubmed: 24179156
Development. 2012 Dec;139(24):4536-48
pubmed: 23136394
Cell Rep. 2020 Feb 4;30(5):1491-1503.e6
pubmed: 32023464
FEBS Lett. 2003 Apr 24;541(1-3):176-7
pubmed: 12706840
Dev Biol. 2000 Dec 15;228(2):151-65
pubmed: 11112321
Curr Biol. 2003 Aug 19;13(16):1409-13
pubmed: 12932324
Development. 2000 Dec;127(23):5213-24
pubmed: 11060246
Cell Rep. 2017 Nov 14;21(7):1982-1993
pubmed: 29141227
Cell. 2007 Jun 1;129(5):999-1010
pubmed: 17540178
Proc Natl Acad Sci U S A. 2005 May 17;102(20):7063-8
pubmed: 15883385
Curr Top Dev Biol. 2014;110:263-83
pubmed: 25248479
PLoS Genet. 2013;9(2):e1003273
pubmed: 23459255
J Cell Biol. 2010 Jan 11;188(1):39-48
pubmed: 20048262
Phys Rev Lett. 2000 Oct 16;85(16):3381-4
pubmed: 11030901
Science. 2005 Sep 23;309(5743):2010-3
pubmed: 16179466
Nat Rev Mol Cell Biol. 2006 Sep;7(9):678-89
pubmed: 16921404

Auteurs

Yao Zhang (Y)

Developmental Biology/Signal Transduction, Max-Delbrück-Center for Molecular Medicine, Berlin, Germany. Yao.Zhang@mdc-berlin.de.

Ines Lahmann (I)

Developmental Biology/Signal Transduction, Max-Delbrück-Center for Molecular Medicine, Berlin, Germany.

Katharina Baum (K)

Mathematical Modelling of Cellular Processes, Max-Delbrück-Center for Molecular Medicine, Berlin, Germany.
Hasso Plattner Institute, Digital Engineering Faculty, University of Potsdam, Potsdam, Germany.

Hiromi Shimojo (H)

Institute for Frontier Life and Medical Sciences, Kyoto University, Kyoto, Japan.
Graduate School of Frontier Biosciences, Osaka University, Osaka, Japan.

Philippos Mourikis (P)

Univ Paris Est Creteil, INSERM, IMRB, Creteil, France.

Jana Wolf (J)

Mathematical Modelling of Cellular Processes, Max-Delbrück-Center for Molecular Medicine, Berlin, Germany.
Department of Mathematics and Computer Science, Free University Berlin, Berlin, Germany.

Ryoichiro Kageyama (R)

Institute for Frontier Life and Medical Sciences, Kyoto University, Kyoto, Japan.

Carmen Birchmeier (C)

Developmental Biology/Signal Transduction, Max-Delbrück-Center for Molecular Medicine, Berlin, Germany. cbirch@mdc-berlin.de.
Neurowissenschaftliches Forschungzentrum, NeuroCure Cluster of Excellence, Charité-Universitätsmedizin Berlin, Berlin, Germany. cbirch@mdc-berlin.de.

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