Transcriptional programming of translation by BCL6 controls skeletal muscle proteostasis.
Journal
Nature metabolism
ISSN: 2522-5812
Titre abrégé: Nat Metab
Pays: Germany
ID NLM: 101736592
Informations de publication
Date de publication:
Feb 2024
Feb 2024
Historique:
received:
02
04
2022
accepted:
09
01
2024
medline:
28
2
2024
pubmed:
10
2
2024
entrez:
10
2
2024
Statut:
ppublish
Résumé
Skeletal muscle is dynamically controlled by the balance of protein synthesis and degradation. Here we discover an unexpected function for the transcriptional repressor B cell lymphoma 6 (BCL6) in muscle proteostasis and strength in mice. Skeletal muscle-specific Bcl6 ablation in utero or in adult mice results in over 30% decreased muscle mass and force production due to reduced protein synthesis and increased autophagy, while it promotes a shift to a slower myosin heavy chain fibre profile. Ribosome profiling reveals reduced overall translation efficiency in Bcl6-ablated muscles. Mechanistically, tandem chromatin immunoprecipitation, transcriptomic and translational analyses identify direct BCL6 repression of eukaryotic translation initiation factor 4E-binding protein 1 (Eif4ebp1) and activation of insulin-like growth factor 1 (Igf1) and androgen receptor (Ar). Together, these results uncover a bifunctional role for BCL6 in the transcriptional and translational control of muscle proteostasis.
Identifiants
pubmed: 38337096
doi: 10.1038/s42255-024-00983-3
pii: 10.1038/s42255-024-00983-3
pmc: PMC10949880
mid: NIHMS1966396
doi:
Substances chimiques
Transcription Factors
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
304-322Subventions
Organisme : NHLBI NIH HHS
ID : R56 HL158531
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK108987
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL061322
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS047726
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM008061
Pays : United States
Organisme : NIA NIH HHS
ID : R01 AG078174
Pays : United States
Organisme : BLRD VA
ID : I01 BX004898
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL166356
Pays : United States
Organisme : NIDDK NIH HHS
ID : R03 DK130908
Pays : United States
Informations de copyright
© 2024. This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply.
Références
Genome Res. 2018 Feb;28(2):243-255
pubmed: 29233921
Mol Metab. 2022 May;59:101456
pubmed: 35150906
Genes Dev. 2010 Dec 15;24(24):2760-5
pubmed: 21106671
Clin Sci (Lond). 1982 Dec;63(6):519-23
pubmed: 6181926
Cell. 2021 Sep 16;184(19):4919-4938.e22
pubmed: 34506722
Differentiation. 1998 Nov;64(1):33-44
pubmed: 9921651
J Muscle Res Cell Motil. 2019 Jun;40(2):127-140
pubmed: 31165949
Mol Cell. 2010 May 28;38(4):576-89
pubmed: 20513432
FASEB J. 2011 Mar;25(3):1028-39
pubmed: 21148113
J Cell Biol. 2013 Oct 28;203(2):345-57
pubmed: 24145169
Cell Host Microbe. 2015 Dec 9;18(6):723-35
pubmed: 26651948
Nature. 1997 May 1;387(6628):83-90
pubmed: 9139826
Br Med J (Clin Res Ed). 1984 Sep 8;289(6445):584-6
pubmed: 6087973
Cell Biosci. 2021 Mar 31;11(1):65
pubmed: 33789727
J Biol Chem. 2001 Dec 14;276(50):47277-84
pubmed: 11574538
Proc Natl Acad Sci U S A. 2018 Jan 23;115(4):E743-E752
pubmed: 29311302
Genome Biol. 2009;10(3):R25
pubmed: 19261174
FASEB J. 2009 Sep;23(9):3140-8
pubmed: 19417088
J Clin Invest. 2016 Sep 1;126(9):3351-62
pubmed: 27482887
Autophagy. 2010 Oct;6(7):929-35
pubmed: 20657169
Cell Rep. 2018 Dec 18;25(12):3283-3298.e6
pubmed: 30566857
Science. 1993 Oct 29;262(5134):747-50
pubmed: 8235596
Genome Biol. 2014;15(12):550
pubmed: 25516281
Cell. 1999 Mar 19;96(6):857-68
pubmed: 10102273
Nucleic Acids Res. 2020 Jul 2;48(W1):W218-W229
pubmed: 32427338
Int J Biochem Cell Biol. 2013 Oct;45(10):2191-9
pubmed: 23702032
Nat Genet. 2013 Nov;45(11):1309-18
pubmed: 24076600
J Pathol. 2010 Jun;221(2):117-24
pubmed: 20225337
Nucleic Acids Res. 2019 Jul 2;47(W1):W206-W211
pubmed: 31053864
Nucleic Acids Res. 1999 Oct 1;27(19):e27
pubmed: 10481039
Mol Cell Endocrinol. 2014 Sep;395(1-2):19-31
pubmed: 25088465
Trends Biochem Sci. 2007 Jun;32(6):279-85
pubmed: 17481902
Cell. 2013 Nov 7;155(4):934-47
pubmed: 24119843
Mol Cell Endocrinol. 2017 May 15;447:35-44
pubmed: 28237723
Science. 2009 Apr 10;324(5924):218-23
pubmed: 19213877
Nat Med. 2018 Jun;24(6):770-781
pubmed: 29875463
Mol Cell Biol. 2015 Apr;35(7):1125-38
pubmed: 25605333
F1000Prime Rep. 2014 Apr 01;6:20
pubmed: 24765525
Skelet Muscle. 2012 May 07;2(1):8
pubmed: 22564549
PLoS Biol. 2019 Oct 7;17(10):e3000467
pubmed: 31589602
Cell. 2009 Feb 20;136(4):731-45
pubmed: 19239892
Front Genet. 2019 May 03;10:421
pubmed: 31130993
Nucleic Acids Res. 2015 Jul 1;43(W1):W566-70
pubmed: 25969447
Biochim Biophys Acta. 2013 Jun-Jul;1829(6-7):666-79
pubmed: 23428348
Nucleic Acids Res. 2023 Jul 7;51(12):6461-6478
pubmed: 37224531
Curr Opin Genet Dev. 2001 Oct;11(5):497-504
pubmed: 11532390
Cell. 2010 Oct 1;143(1):35-45
pubmed: 20887891
Front Physiol. 2018 Aug 31;9:1220
pubmed: 30233398
Bioinformatics. 2013 Jan 1;29(1):15-21
pubmed: 23104886
Nat Rev Genet. 2009 Jan;10(1):32-42
pubmed: 19065135
Cell Rep. 2013 Aug 15;4(3):578-88
pubmed: 23911289
Elife. 2019 Apr 15;8:
pubmed: 30983568
Nat Biotechnol. 2010 May;28(5):495-501
pubmed: 20436461
Science. 2001 Nov 23;294(5547):1704-8
pubmed: 11679633
EMBO J. 2008 May 21;27(10):1481-90
pubmed: 18418387
Cell. 2017 Apr 6;169(2):361-371
pubmed: 28388417
J Natl Cancer Inst. 2015 Oct 12;107(12):djv274
pubmed: 26464423
Proc Natl Acad Sci U S A. 2019 Jun 4;116(23):11299-11308
pubmed: 31110021
Science. 1997 Apr 25;276(5312):589-92
pubmed: 9110977
J Appl Physiol (1985). 2015 Jul 1;119(1):16-26
pubmed: 25930021
J Biol Chem. 2018 Nov 30;293(48):18719-18729
pubmed: 30323064
Am J Physiol Endocrinol Metab. 2008 Jun;294(6):E1152-9
pubmed: 18445752
Cell. 2011 Nov 11;147(4):827-39
pubmed: 22078881
Wiley Interdiscip Rev RNA. 2016 Jan-Feb;7(1):53-70
pubmed: 26564736
Bioinformatics. 2017 Jan 1;33(1):139-141
pubmed: 27634950
Nat Rev Drug Discov. 2015 Jan;14(1):58-74
pubmed: 25549588
Curr Opin Clin Nutr Metab Care. 2013 May;16(3):243-50
pubmed: 23493017
Nat Genet. 1993 Sep;5(1):66-70
pubmed: 8220427
Nat Commun. 2021 Jan 12;12(1):330
pubmed: 33436614
Mol Cell Biol. 2012 Feb;32(4):880-96
pubmed: 22158971
Proc Natl Acad Sci U S A. 2013 Feb 5;110(6):2169-74
pubmed: 23345430
Am J Physiol Endocrinol Metab. 2006 May;290(5):E1048-56
pubmed: 16368786