SNAI1 is upregulated during muscle regeneration and represses FGF21 and ATF3 expression by directly binding their promoters.
E box
endoplasmic reticulum stress
gene silencing
microarray analysis
muscle regeneration
myoblast differentiation
promoter
skeletal muscle
transcription
Journal
FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484
Informations de publication
Date de publication:
07 2022
07 2022
Historique:
revised:
19
05
2022
received:
09
02
2022
accepted:
26
05
2022
entrez:
21
6
2022
pubmed:
22
6
2022
medline:
23
6
2022
Statut:
ppublish
Résumé
During skeletal myogenesis, the zinc-finger transcription factors SNAI1 and SNAI2, are expressed in proliferating myoblasts and regulate the transition to terminally differentiated myotubes while repressing pro-differentiation genes. Here, we demonstrate that SNAI1 is upregulated in vivo during the early phase of muscle regeneration induced by bupivacaine injury. Using shRNA-mediated gene silencing in C2C12 myoblasts and whole-transcriptome microarray analysis, we identified a collection of genes belonging to the endoplasmic reticulum (ER) stress pathway whose expression, induced by myogenic differentiation, was upregulated in absence of SNAI1. Among these, key ER stress genes, such as Atf3, Ddit3/Chop, Hspa5/Bip, and Fgf21, a myokine involved in muscle differentiation, were strongly upregulated. Furthermore, by promoter mutant analysis and Chromatin immune precipitation assay, we demonstrated that SNAI1 represses Fgf21 and Atf3 in proliferating myoblasts by directly binding to multiple E boxes in their respective promoter regions. Together, these data describe a new regulatory mechanism of myogenic differentiation involving the direct repressive action of SNAI1 on ER stress and Fgf21 expression, ultimately contributing to maintaining the proliferative and undifferentiated state of myoblasts.
Identifiants
pubmed: 35726676
doi: 10.1096/fj.202200215R
doi:
Substances chimiques
Activating Transcription Factor 3
0
Snail Family Transcription Factors
0
fibroblast growth factor 21
0
Fibroblast Growth Factors
62031-54-3
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e22401Informations de copyright
© 2022 The Authors. The FASEB Journal published by Wiley Periodicals LLC on behalf of Federation of American Societies for Experimental Biology.
Références
Galvagni F, Lentucci C, Neri F, et al. Snai1 promotes ESC exit from the pluripotency by direct repression of self-renewal genes. Stem Cells. 2015;33:742-750.
Martinez-Estrada OM, Culleres A, Soriano FX, et al. The transcription factors Slug and Snail act as repressors of Claudin-1 expression in epithelial cells. Biochem J. 2006;394:449-457.
Peinado H, Ballestar E, Esteller M, Cano A. Snail mediates E-cadherin repression by the recruitment of the Sin3A/histone deacetylase 1 (HDAC1)/HDAC2 complex. Mol Cell Biol. 2004;24:306-319.
Soleimani VD, Yin H, Jahani-Asl A, et al. Snail regulates MyoD binding-site occupancy to direct enhancer switching and differentiation-specific transcription in myogenesis. Mol Cell. 2012;47:457-468.
Markan KR, Naber MC, Ameka MK, et al. Circulating FGF21 is liver derived and enhances glucose uptake during refeeding and overfeeding. Diabetes. 2014;63:4057-4063.
Izumiya Y, Bina HA, Ouchi N, Akasaki Y, Kharitonenkov A, Walsh K. FGF21 is an Akt-regulated myokine. FEBS Lett. 2008;582:3805-3810.
Ribas F, Villarroya J, Hondares E, Giralt M, Villarroya F. FGF21 expression and release in muscle cells: involvement of MyoD and regulation by mitochondria-driven signalling. Biochem J. 2014;463:191-199.
Liu X, Wang Y, Hou L, Xiong Y, Zhao S. Fibroblast Growth Factor 21 (FGF21) promotes formation of aerobic myofibers via the FGF21-SIRT1-AMPK-PGC1alpha pathway. J Cell Physiol. 2017;232:1893-1906.
Liu X, Wang Y, Zhao S, Li X. Fibroblast Growth Factor 21 promotes C2C12 cells myogenic differentiation by enhancing cell cycle exit. Biomed Res Int. 2017;2017:1648715.
Zhou S, Qian B, Wang L, Zhang C, Hogan MV, Li H. Altered bone-regulating myokine expression in skeletal muscle of Duchenne muscular dystrophy mouse models. Muscle Nerve. 2018;58(4):573-582.
Nakanishi K, Sudo T, Morishima N. Endoplasmic reticulum stress signaling transmitted by ATF6 mediates apoptosis during muscle development. J Cell Biol. 2005;169:555-560.
Nakanishi K, Dohmae N, Morishima N. Endoplasmic reticulum stress increases myofiber formation in vitro. FASEB J. 2007;21:2994-3003.
He S, Fu T, Yu Y, et al. IRE1alpha regulates skeletal muscle regeneration through Myostatin mRNA decay. J Clin Invest. 2021;131(17):e143737.
Malhotra JD, Kaufman RJ. The endoplasmic reticulum and the unfolded protein response. Semin Cell Dev Biol. 2007;18:716-731.
Wu J, Kaufman RJ. From acute ER stress to physiological roles of the unfolded protein response. Cell Death Differ. 2006;13(3):374-384.
Wang M, Kaufman RJ. The impact of the endoplasmic reticulum protein-folding environment on cancer development. Nat Rev Cancer. 2014;14(9):581-597.
Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol. 2012;13(2):89-102.
Tan YY, Zhang Y, Li B, et al. PERK signaling controls myoblast differentiation by regulating MicroRNA networks. Front Cell Dev Biol. 2021;9:670435.
Shi L, Zhou B, Li P, et al. MicroRNA-128 targets myostatin at coding domain sequence to regulate myoblasts in skeletal muscle development. Cell Signal. 2015;27(9):1895-1904.
Alter J, Bengal E. Stress-induced C/EBP homology protein (CHOP) represses MyoD transcription to delay myoblast differentiation. PLoS One. 2011;6(12):e29498.
Galvagni F, Cantini M, Oliviero S. The utrophin gene is transcriptionally up-regulated in regenerating muscle. J Biol Chem. 2002;277:19106-19113.
Yaffe D, Saxel O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature. 1977;270:725-727.
Galvagni F, Oliviero S. Utrophin transcription is activated by an intronic enhancer. J Biol Chem. 2000;275:3168-3172.
Anselmi F, Orlandini M, Rocchigiani M, et al. c-ABL modulates MAP kinases activation downstream of VEGFR-2 signaling by direct phosphorylation of the adaptor proteins GRB2 and NCK1. Angiogenesis. 2012;15:187-197.
Salameh A, Galvagni F, Anselmi F, De Clemente C, Orlandini M, Oliviero S. Growth factor stimulation induces cell survival by c-Jun. ATF2-dependent activation of Bcl-XL. J Biol Chem. 2010;285:23096-23104.
Haring M, Offermann S, Danker T, Horst I, Peterhansel C, Stam M. Chromatin immunoprecipitation: optimization, quantitative analysis and data normalization. Plant Methods. 2007;3:11.
Zink W, Graf BM, Sinner B, Martin E, Fink RH, Kunst G. Differential effects of bupivacaine on intracellular Ca2+ regulation: potential mechanisms of its myotoxicity. Anesthesiology. 2002;97:710-716.
Zheng H, Shen M, Zha YL, et al. PKD1 phosphorylation-dependent degradation of SNAIL by SCF-FBXO11 regulates epithelial-mesenchymal transition and metastasis. Cancer Cell. 2014;26(3):358-373.
Kleger A, Loebnitz C, Pusapati GV, et al. Protein kinase D2 is an essential regulator of murine myoblast differentiation. PLoS One. 2011;6(1):e14599.
Peiró S, Escrivà M, Puig I, et al. Snail1 transcriptional repressor binds to its own promoter and controls its expression. Nucleic Acids Res. 2006;34(7):2077-2084.
Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4:44-57.
Supek F, Bosnjak M, Skunca N, Smuc T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One. 2011;6:e21800.
Edagawa M, Kawauchi J, Hirata M, et al. Role of activating transcription factor 3 (ATF3) in endoplasmic reticulum (ER) stress-induced sensitization of p53-deficient human colon cancer cells to tumor necrosis factor (TNF)-related apoptosis-inducing ligand (TRAIL)-mediated apoptosis through up-regulation of death receptor 5 (DR5) by zerumbone and celecoxib. J Biol Chem. 2014;289:21544-21561.
Wan XS, Lu XH, Xiao YC, et al. ATF4- and CHOP-dependent induction of FGF21 through endoplasmic reticulum stress. Biomed Res Int. 2014;2014:807874.
Schaap FG, Kremer AE, Lamers WH, Jansen PL, Gaemers IC. Fibroblast growth factor 21 is induced by endoplasmic reticulum stress. Biochimie. 2013;95:692-699.
Guardiola O, Andolfi G, Tirone M, Iavarone F, Brunelli S, Minchiotti G. Induction of acute skeletal muscle regeneration by cardiotoxin injection. J Vis Exp. 2017;119:54515.
Seale P, Ishibashi J, Holterman C, Rudnicki MA. Muscle satellite cell-specific genes identified by genetic profiling of MyoD-deficient myogenic cell. Dev Biol. 2004;275:287-300.
Miller KJ, Thaloor D, Matteson S, Pavlath GK. Hepatocyte growth factor affects satellite cell activation and differentiation in regenerating skeletal muscle. Am J Physiol Cell Physiol. 2000;278:174-C181.
Leshem Y, Spicer DB, Gal-Levi R, Halevy O. Hepatocyte growth factor (HGF) inhibits skeletal muscle cell differentiation: a role for the bHLH protein twist and the cdk inhibitor p27. J Cell Physiol. 2000;184:101-109.
Anastasi S, Giordano S, Sthandier O, et al. A natural hepatocyte growth factor/scatter factor autocrine loop in myoblast cells and the effect of the constitutive met kinase activation on myogenic differentiation. J Cell Biol. 1997;137:1057-1068.
Contreras O, Cordova-Casanova A, Brandan E. PDGF-PDGFR network differentially regulates the fate, migration, proliferation, and cell cycle progression of myogenic cells. Cell Signal. 2021;84:110036.
Shan T, Xu Z, Wu W, Liu J, Wang Y. Roles of Notch1 signaling in regulating satellite cell fates choices and postnatal skeletal myogenesis. J Cell Physiol. 2017;232:2964-2967.
Lee NK, Skinner JP, Zajac JD, MacLean HE. Ornithine decarboxylase is upregulated by the androgen receptor in skeletal muscle and regulates myoblast proliferation. Am J Physiol Endocrinol Metab. 2011;301:172-E179.
Kitzmann M, Vandromme M, Schaeffer V, et al. cdk1- and cdk2-mediated phosphorylation of MyoD Ser200 in growing C2 myoblasts: role in modulating MyoD half-life and myogenic activity. Mol Cell Biol. 1999;19:3167-3176.
Correra RM, Ollitrault D, Valente M, et al. The imprinted gene Pw1/Peg3 regulates skeletal muscle growth, satellite cell metabolic state, and self-renewal. Sci Rep. 2018;8:14649-x.
Bengal E, Ransone L, Scharfmann R, et al. Functional antagonism between c-Jun and MyoD proteins: a direct physical association. Cell. 1992;68:507-519.
El Haddad M, Notarnicola C, Evano B, et al. Retinoic acid maintains human skeletal muscle progenitor cells in an immature state. Cell Mol Life Sci. 2017;74:1923-1936.
Li H, Sun H, Qian B, et al. Increased expression of FGF-21 negatively affects bone homeostasis in dystrophin/utrophin double knockout mice. J Bone Miner Res. 2020;35:738-752.
Morville T, Sahl RE, Trammell SA, et al. Divergent effects of resistance and endurance exercise on plasma bile acids, FGF19, and FGF21 in humans. JCI Insight. 2018;3(15):e122737.
Sun H, Sherrier M, Li H. Skeletal muscle and bone - emerging targets of Fibroblast Growth Factor-21. Front Physiol. 2021;12:625287.
Yu Y, He J, Li S, et al. Fibroblast growth factor 21 (FGF21) inhibits macrophage-mediated inflammation by activating Nrf2 and suppressing the NF-kappaB signaling pathway. Int Immunopharmacol. 2016;38:144-152.
Li H, Wu G, Fang Q, et al. Fibroblast growth factor 21 increases insulin sensitivity through specific expansion of subcutaneous fat. Nat Commun. 2018;9:272-279.
Contreras-Shannon V, Ochoa O, Reyes-Reyna SM, et al. Fat accumulation with altered inflammation and regeneration in skeletal muscle of CCR2−/− mice following ischemic injury. Am J Physiol Cell Physiol. 2007;292:953-C967.
Shireman PK, Contreras-Shannon V, Ochoa O, Karia BP, Michalek JE, McManus LM. MCP-1 deficiency causes altered inflammation with impaired skeletal muscle regeneration. J Leukoc Biol. 2007;81:775-785.
Summan M, Warren GL, Mercer RR, et al. Macrophages and skeletal muscle regeneration: a clodronate-containing liposome depletion study. Am J Physiol Regul Integr Comp Physiol. 2006;290:1488-R1495.
Pimorady-Esfahani A, Grounds MD, McMenamin PG. Macrophages and dendritic cells in normal and regenerating murine skeletal muscle. Muscle Nerve. 1997;20:158-166.
McLennan IS. Degenerating and regenerating skeletal muscles contain several subpopulations of macrophages with distinct spatial and temporal distributions. J Anat. 1996;188(Pt 1):17-28.
Bencze M, Negroni E, Vallese D, et al. Proinflammatory macrophages enhance the regenerative capacity of human myoblasts by modifying their kinetics of proliferation and differentiation. Mol Ther. 2012;20:2168-2179.
Arnold L, Henry A, Poron F, et al. Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J Exp Med. 2007;204:1057-1069.
Wek RC, Jiang HY, Anthony TG. Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans. 2006;34:7-11.
Ku HC, Cheng CF. Master regulator activating transcription factor 3 (ATF3) in metabolic homeostasis and cancer. Front Endocrinol (Lausanne). 2020;11:556.
Luo S, Baumeister P, Yang S, Abcouwer SF, Lee AS. Induction of Grp78/BiP by translational block: activation of the Grp78 promoter by ATF4 through and upstream ATF/CRE site independent of the endoplasmic reticulum stress elements. J Biol Chem. 2003;278:37375-37385.