Overlapping functions of SIX homeoproteins during embryonic myogenesis.


Journal

PLoS genetics
ISSN: 1553-7404
Titre abrégé: PLoS Genet
Pays: United States
ID NLM: 101239074

Informations de publication

Date de publication:
06 2023
Historique:
received: 06 10 2022
accepted: 10 05 2023
revised: 14 06 2023
medline: 16 6 2023
pubmed: 2 6 2023
entrez: 2 6 2023
Statut: epublish

Résumé

Four SIX homeoproteins display a combinatorial expression throughout embryonic developmental myogenesis and they modulate the expression of the myogenic regulatory factors. Here, we provide a deep characterization of their role in distinct mouse developmental territories. We showed, at the hypaxial level, that the Six1:Six4 double knockout (dKO) somitic precursor cells adopt a smooth muscle fate and lose their myogenic identity. At the epaxial level, we demonstrated by the analysis of Six quadruple KO (qKO) embryos, that SIX are required for fetal myogenesis, and for the maintenance of PAX7+ progenitor cells, which differentiated prematurely and are lost by the end of fetal development in qKO embryos. Finally, we showed that Six1 and Six2 are required to establish craniofacial myogenesis by controlling the expression of Myf5. We have thus described an unknown role for SIX proteins in the control of myogenesis at different embryonic levels and refined their involvement in the genetic cascades operating at the head level and in the genesis of myogenic stem cells.

Identifiants

pubmed: 37267426
doi: 10.1371/journal.pgen.1010781
pii: PGENETICS-D-22-01142
pmc: PMC10266681
doi:

Substances chimiques

Homeodomain Proteins 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1010781

Informations de copyright

Copyright: © 2023 Wurmser et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

Cell Mol Life Sci. 2014 Jun;71(11):2149-64
pubmed: 24061537
Development. 2011 Jun;138(12):2401-15
pubmed: 21610022
Development. 2006 Sep;133(18):3723-32
pubmed: 16936075
Cell Rep. 2022 Feb 1;38(5):110323
pubmed: 35108532
Elife. 2016 Aug 24;5:
pubmed: 27554485
Development. 2007 Sep;134(17):3065-75
pubmed: 17652354
Nat Cell Biol. 2018 Jan;20(1):46-57
pubmed: 29255171
Exp Cell Res. 2010 Oct 15;316(17):2932-44
pubmed: 20696153
Dev Biol. 2009 Jul 15;331(2):152-66
pubmed: 19409884
Dev Cell. 2014 Feb 10;28(3):225-38
pubmed: 24525185
Development. 2017 Jun 1;144(11):2021-2031
pubmed: 28455376
PLoS One. 2013 Jun 28;8(6):e67762
pubmed: 23840772
Nature. 2005 Jan 20;433(7023):317-22
pubmed: 15568017
Nucleic Acids Res. 2016 Oct 14;44(18):8621-8640
pubmed: 27302134
Development. 2020 Oct 9;147(19):
pubmed: 32591430
Am J Anat. 1983 Nov;168(3):257-76
pubmed: 6650439
Proc Natl Acad Sci U S A. 2007 Jul 3;104(27):11310-5
pubmed: 17592144
Dev Biol. 2011 Nov 15;359(2):303-20
pubmed: 21884692
Development. 2020 Jun 26;147(12):
pubmed: 32541004
Dev Dyn. 2003 Dec;228(4):594-605
pubmed: 14648836
Development. 2012 Mar;139(5):958-67
pubmed: 22318627
EMBO J. 2006 Nov 1;25(21):5214-28
pubmed: 17036046
Hum Mol Genet. 2004 Nov 15;13(22):2829-40
pubmed: 15385444
Dev Biol. 2007 Apr 15;304(2):633-51
pubmed: 17292343
Development. 1998 Nov;125(21):4155-62
pubmed: 9753670
Skelet Muscle. 2021 Nov 19;11(1):26
pubmed: 34809717
Nature. 2015 Apr 23;520(7548):466-73
pubmed: 25903628
J Cell Sci. 2013 Apr 15;126(Pt 8):1868-80
pubmed: 23444384
Semin Cell Dev Biol. 2020 Aug;104:51-64
pubmed: 32247726
Development. 2005 May;132(9):2235-49
pubmed: 15788460
Development. 2006 Dec;133(24):4891-9
pubmed: 17107996
Genes Dev. 2005 Jun 15;19(12):1426-31
pubmed: 15964993
Skelet Muscle. 2018 Aug 24;8(1):27
pubmed: 30139374
Elife. 2022 Feb 28;11:
pubmed: 35225230
Nat Ecol Evol. 2019 Aug;3(8):1233-1240
pubmed: 31263232
Development. 2003 May;130(10):2239-52
pubmed: 12668636
Proc Natl Acad Sci U S A. 2006 Jan 24;103(4):945-50
pubmed: 16418263
Elife. 2019 Sep 19;8:
pubmed: 31535973
Skelet Muscle. 2016 Sep 05;6(1):30
pubmed: 27597886
Dev Biol. 2013 Dec 1;384(1):114-27
pubmed: 24055173
Cell. 2000 Sep 15;102(6):777-86
pubmed: 11030621
Development. 2016 Feb 15;143(4):595-608
pubmed: 26884396
Genesis. 2005 Apr;41(4):202-9
pubmed: 15789408
Nat Genet. 2000 May;25(1):105-9
pubmed: 10802667
J Clin Invest. 2011 Apr;121(4):1585-95
pubmed: 21364285
Development. 1999 Sep;126(18):4053-63
pubmed: 10457014
J Cell Biol. 2012 Sep 3;198(5):815-32
pubmed: 22945933
Nat Commun. 2020 Oct 9;11(1):5102
pubmed: 33037211
Nature. 2011 May 26;473(7348):532-5
pubmed: 21572437
Nature. 2005 Jun 16;435(7044):954-8
pubmed: 15843802
Nat Commun. 2020 Dec 8;11(1):6287
pubmed: 33293533
Dev Dyn. 2007 Feb;236(2):353-63
pubmed: 17117436
Curr Top Dev Biol. 2014;110:1-73
pubmed: 25248473
Curr Opin Cell Biol. 2000 Dec;12(6):725-30
pubmed: 11063939
FASEB J. 2015 Nov;29(11):4738-55
pubmed: 26229056
Nat Struct Mol Biol. 2013 Apr;20(4):447-53
pubmed: 23435380
Nature. 2005 Jun 16;435(7044):948-53
pubmed: 15843801
PLoS One. 2009;4(2):e4381
pubmed: 19198652
J Dent Res. 2019 May;98(5):572-579
pubmed: 30905259
Elife. 2018 Nov 19;7:
pubmed: 30451684
Dev Cell. 2010 Apr 20;18(4):662-74
pubmed: 20412780
Development. 2012 Jan;139(2):277-87
pubmed: 22129828
Nature. 2003 Nov 20;426(6964):247-54
pubmed: 14628042
Proc Natl Acad Sci U S A. 2007 Mar 13;104(11):4443-8
pubmed: 17360543
Proc Natl Acad Sci U S A. 2007 Jan 9;104(2):537-42
pubmed: 17194759
Development. 2005 Jan;132(2):345-57
pubmed: 15604102
Development. 2006 Jul;133(14):2731-45
pubmed: 16775000
Invest Ophthalmol Vis Sci. 2005 Nov;46(11):4200-8
pubmed: 16249499
Genes Dev. 2006 Sep 1;20(17):2450-64
pubmed: 16951257
Dev Biol. 2007 Feb 15;302(2):602-16
pubmed: 17098221
Dev Biol. 2007 Aug 15;308(2):281-93
pubmed: 17612520
Dev Growth Differ. 2016 Aug;58(6):546-61
pubmed: 27224259
PLoS Genet. 2020 Oct 30;16(10):e1009022
pubmed: 33125370
Cell Stem Cell. 2008 Aug 7;3(2):169-81
pubmed: 18682239
Cell Death Dis. 2018 Oct 25;9(11):1092
pubmed: 30361642
Dev Cell. 2012 Sep 11;23(3):469-81
pubmed: 22940113
Nat Commun. 2022 Feb 24;13(1):1039
pubmed: 35210422
Development. 2010 Nov;137(22):3847-56
pubmed: 20978076
Dev Cell. 2009 Jun;16(6):810-21
pubmed: 19531352
Curr Opin Cell Biol. 2021 Dec;73:110-116
pubmed: 34500235
Cell Regen. 2021 Oct 1;10(1):31
pubmed: 34595600
BMC Biol. 2014 Jul 12;12:53
pubmed: 25015411
Mol Cell Biol. 2001 May;21(10):3343-50
pubmed: 11313460
Dev Cell. 2015 Sep 28;34(6):694-704
pubmed: 26387456
Front Aging Neurosci. 2015 May 19;7:62
pubmed: 26042028
Science. 2002 Dec 20;298(5602):2378-81
pubmed: 12493912
Development. 2014 Aug;141(15):2959-71
pubmed: 25053429
Sci Adv. 2021 Jun 9;7(24):
pubmed: 34108202
Genes Dev. 2008 Jan 15;22(2):265-76
pubmed: 18198342
Genes Dev. 2009 Apr 15;23(8):997-1013
pubmed: 19346403
J Muscle Res Cell Motil. 2002;23(3):255-64
pubmed: 12500905
Dev Biol. 2010 Aug 15;344(2):720-30
pubmed: 20515681
Cell Rep. 2022 Aug 16;40(7):111219
pubmed: 35977485
Proc Natl Acad Sci U S A. 2015 Feb 3;112(5):1446-51
pubmed: 25605943
Semin Cell Dev Biol. 2019 Jul;91:31-44
pubmed: 29331210
Dev Dyn. 1999 Dec;216(4-5):385-97
pubmed: 10633858
Mech Dev. 2003 Jun;120(6):669-79
pubmed: 12834866
PLoS Genet. 2013 Apr;9(4):e1003425
pubmed: 23637613
BMC Dev Biol. 2010 Feb 22;10:21
pubmed: 20175910
J Cell Biol. 2008 Feb 11;180(3):607-18
pubmed: 18268106
Development. 1995 Mar;121(3):693-705
pubmed: 7720577
Nat Genet. 2000 May;25(1):110-4
pubmed: 10802668
Proc Natl Acad Sci U S A. 2007 Apr 3;104(14):5907-12
pubmed: 17384148
Development. 2016 Mar 1;143(5):872-9
pubmed: 26839363
Dev Biol. 2011 Jan 15;349(2):395-405
pubmed: 21035439
Dev Biol. 2010 Feb 15;338(2):168-82
pubmed: 19962975

Auteurs

Maud Wurmser (M)

Université de Paris Cité, Institut Cochin, INSERM, CNRS, Paris, France.

Rouba Madani (R)

Université de Paris Cité, Institut Cochin, INSERM, CNRS, Paris, France.

Nathalie Chaverot (N)

Université de Paris Cité, Institut Cochin, INSERM, CNRS, Paris, France.

Stéphanie Backer (S)

Université de Paris Cité, Institut Cochin, INSERM, CNRS, Paris, France.

Matthew Borok (M)

Univ Paris Est Creteil, INSERM, EnvA, EFS, AP-HP, IMRB, Creteil, France.

Matthieu Dos Santos (M)

Université de Paris Cité, Institut Cochin, INSERM, CNRS, Paris, France.

Glenda Comai (G)

Stem Cells & Development, Institut Pasteur, Paris, France.
CNRS UMR 3738, Institut Pasteur, Paris, France.

Shahragim Tajbakhsh (S)

Stem Cells & Development, Institut Pasteur, Paris, France.
CNRS UMR 3738, Institut Pasteur, Paris, France.

Frédéric Relaix (F)

Univ Paris Est Creteil, INSERM, EnvA, EFS, AP-HP, IMRB, Creteil, France.

Marc Santolini (M)

Université de Paris Cité, Interaction Data Lab, CRI Paris, INSERM. Paris, France.

Ramkumar Sambasivan (R)

Indian Institute of Science Education and Research (IISER) Tirupati, Tirupati, Andhra Pradesh, India.

Rulang Jiang (R)

Division of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, United States of America.
Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio, United States of America.

Pascal Maire (P)

Université de Paris Cité, Institut Cochin, INSERM, CNRS, Paris, France.

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