Staufen1 Inhibits MyoD Translation to Actively Maintain Muscle Stem Cell Quiescence

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2017 Oct 27

PMID 29073096

Citations 44

Authors

Antoine de Morree

Cindy T J van Velthoven

Qiang Gan

Jayesh S Salvi

Julian D D Klein

Igor Akimenko

Marco Quarta

Stefano Biressi

Thomas A Rando

Affiliations

Soon will be listed here.

Abstract

Tissue regeneration depends on the timely activation of adult stem cells. In skeletal muscle, the adult stem cells maintain a quiescent state and proliferate upon injury. We show that muscle stem cells (MuSCs) use direct translational repression to maintain the quiescent state. High-resolution single-molecule and single-cell analyses demonstrate that quiescent MuSCs express high levels of Myogenic Differentiation 1 (MyoD) transcript in vivo, whereas MyoD protein is absent. RNA pulldowns and costainings show that MyoD mRNA interacts with Staufen1, a potent regulator of mRNA localization, translation, and stability. Staufen1 prevents MyoD translation through its interaction with the MyoD 3'-UTR. MuSCs from Staufen1 heterozygous (Staufen1) mice have increased MyoD protein expression, exit quiescence, and begin proliferating. Conversely, blocking MyoD translation maintains the quiescent phenotype. Collectively, our data show that MuSCs express MyoD mRNA and actively repress its translation to remain quiescent yet primed for activation.

Citing Articles

Effects of radial extracorporeal shock wave with different frequencies on acute skeletal muscle injury in rabbits.

Wang S, Huang S, Xu X, Liu R Sci Rep. 2024; 14(1):21276.

PMID: 39261623 PMC: 11391075. DOI: 10.1038/s41598-024-72371-6.

Spermidine-eIF5A axis is essential for muscle stem cell activation via translational control.

Zhang Q, Han W, Wu R, Deng S, Meng J, Yang Y Cell Discov. 2024; 10(1):94.

PMID: 39251577 PMC: 11383958. DOI: 10.1038/s41421-024-00712-w.

The artemisinin-induced dormant stages of Plasmodium falciparum exhibit hallmarks of cellular quiescence/senescence and drug resilience.

Tripathi J, Stoklasa M, Nayak S, Low K, Lee E, Duong Tien Q Nat Commun. 2024; 15(1):7485.

PMID: 39209862 PMC: 11362153. DOI: 10.1038/s41467-024-51846-0.

The E3 ubiquitin ligase Nedd4L preserves skeletal muscle stem cell quiescence by inhibiting their activation.

Blackburn D, Sahinyan K, Hernandez-Corchado A, Lazure F, Richard V, Raco L iScience. 2024; 27(7):110241.

PMID: 39015146 PMC: 11250905. DOI: 10.1016/j.isci.2024.110241.

Dual-specificity phosphatases 13 and 27 as key switches in muscle stem cell transition from proliferation to differentiation.

Hayashi T, Sadaki S, Tsuji R, Okada R, Fuseya S, Kanai M Stem Cells. 2024; 42(9):830-847.

PMID: 38975693 PMC: 11384902. DOI: 10.1093/stmcls/sxae045.

References

Gerhart J, Neely C, Elder J, Pfautz J, Perlman J, Narciso L . Cells that express MyoD mRNA in the epiblast are stably committed to the skeletal muscle lineage. J Cell Biol. 2007; 178(4):649-60. PMC: 2064471. DOI: 10.1083/jcb.200703060. View

Rosenblatt J, Lunt A, Parry D, Partridge T . Culturing satellite cells from living single muscle fiber explants. In Vitro Cell Dev Biol Anim. 1995; 31(10):773-9. DOI: 10.1007/BF02634119. View

Rouskin S, Zubradt M, Washietl S, Kellis M, Weissman J . Genome-wide probing of RNA structure reveals active unfolding of mRNA structures in vivo. Nature. 2013; 505(7485):701-5. PMC: 3966492. DOI: 10.1038/nature12894. View

Brack A, Rando T . Tissue-specific stem cells: lessons from the skeletal muscle satellite cell. Cell Stem Cell. 2012; 10(5):504-14. PMC: 3348769. DOI: 10.1016/j.stem.2012.04.001. View

Dugre-Brisson S, Elvira G, Boulay K, Chatel-Chaix L, Mouland A, DesGroseillers L . Interaction of Staufen1 with the 5' end of mRNA facilitates translation of these RNAs. Nucleic Acids Res. 2005; 33(15):4797-812. PMC: 1193567. DOI: 10.1093/nar/gki794. View

Robinson M, McCarthy D, Smyth G . edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2009; 26(1):139-40. PMC: 2796818. DOI: 10.1093/bioinformatics/btp616. View

Liu L, Cheung T, Charville G, Rando T . Isolation of skeletal muscle stem cells by fluorescence-activated cell sorting. Nat Protoc. 2015; 10(10):1612-24. PMC: 4793971. DOI: 10.1038/nprot.2015.110. View

Quarta M, Brett J, DiMarco R, de Morree A, Boutet S, Chacon R . An artificial niche preserves the quiescence of muscle stem cells and enhances their therapeutic efficacy. Nat Biotechnol. 2016; 34(7):752-9. PMC: 4942359. DOI: 10.1038/nbt.3576. View

Heraud-Farlow J, Kiebler M . The multifunctional Staufen proteins: conserved roles from neurogenesis to synaptic plasticity. Trends Neurosci. 2014; 37(9):470-9. PMC: 4156307. DOI: 10.1016/j.tins.2014.05.009. View

10.

Crist C, Montarras D, Buckingham M . Muscle satellite cells are primed for myogenesis but maintain quiescence with sequestration of Myf5 mRNA targeted by microRNA-31 in mRNP granules. Cell Stem Cell. 2012; 11(1):118-26. DOI: 10.1016/j.stem.2012.03.011. View

11.

Yin H, Price F, Rudnicki M . Satellite cells and the muscle stem cell niche. Physiol Rev. 2013; 93(1):23-67. PMC: 4073943. DOI: 10.1152/physrev.00043.2011. View

12.

Boonsanay V, Zhang T, Georgieva A, Kostin S, Qi H, Yuan X . Regulation of Skeletal Muscle Stem Cell Quiescence by Suv4-20h1-Dependent Facultative Heterochromatin Formation. Cell Stem Cell. 2015; 18(2):229-42. DOI: 10.1016/j.stem.2015.11.002. View

13.

Rodgers J, King K, Brett J, Cromie M, Charville G, Maguire K . mTORC1 controls the adaptive transition of quiescent stem cells from G0 to G(Alert). Nature. 2014; 510(7505):393-6. PMC: 4065227. DOI: 10.1038/nature13255. View

14.

Cornelison D, Wold B . Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol. 1997; 191(2):270-83. DOI: 10.1006/dbio.1997.8721. View

15.

Hausburg M, Doles J, Clement S, Cadwallader A, Hall M, Blackshear P . Post-transcriptional regulation of satellite cell quiescence by TTP-mediated mRNA decay. Elife. 2015; 4:e03390. PMC: 4415119. DOI: 10.7554/eLife.03390. View

16.

Conboy I, Rando T . The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev Cell. 2002; 3(3):397-409. DOI: 10.1016/s1534-5807(02)00254-x. View

17.

Murphy M, Lawson J, Mathew S, Hutcheson D, Kardon G . Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration. Development. 2011; 138(17):3625-37. PMC: 3152921. DOI: 10.1242/dev.064162. View

18.

Ravel-Chapuis A, Crawford T, Blais-Crepeau M, Belanger G, Richer C, Jasmin B . The RNA-binding protein Staufen1 impairs myogenic differentiation via a c-myc-dependent mechanism. Mol Biol Cell. 2014; 25(23):3765-78. PMC: 4230783. DOI: 10.1091/mbc.E14-04-0895. View

19.

Kanisicak O, Mendez J, Yamamoto S, Yamamoto M, Goldhamer D . Progenitors of skeletal muscle satellite cells express the muscle determination gene, MyoD. Dev Biol. 2009; 332(1):131-41. PMC: 2728477. DOI: 10.1016/j.ydbio.2009.05.554. View

20.

Dobin A, Davis C, Schlesinger F, Drenkow J, Zaleski C, Jha S . STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2012; 29(1):15-21. PMC: 3530905. DOI: 10.1093/bioinformatics/bts635. View