FoxO maintains a genuine muscle stem-cell quiescent state
until geriatric age
  • 1.

    Hwang, A. B. & Brack, A. S. Muscle stem cells and aging. Curr. Top. Dev. Biol. 126, 299–322 (2018).

    PubMed  Article  Google Scholar 

  • 2.

    Sousa-Victor, P., Garcia-Prat, L., Serrano, A. L., Perdiguero, E. & Munoz-Canoves, P. Muscle stem cell aging: regulation and rejuvenation. Trends Endocrinol. Metab. 26, 287–296 (2015).

    CAS  PubMed  Article  Google Scholar 

  • 3.

    Brack, A. S. & Rando, T. A. Tissue-specific stem cells: lessons from the skeletal muscle satellite cell. Cell Stem Cell 10, 504–514 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 4.

    Feige, P., Brun, C. E., Ritso, M. & Rudnicki, M. A. Orienting muscle stem cells for regeneration in homeostasis, aging, and disease. Cell Stem Cell 23, 653–664 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 5.

    Chakkalakal, J. V., Jones, K. M., Basson, M. A. & Brack, A. S. The aged niche disrupts muscle stem cell quiescence. Nature 490, 355–360 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 6.

    Dell’Orso, S. et al. Single cell analysis of adult mouse skeletal muscle stem cells in homeostatic and regenerative conditions. Development 146, dev.174177 (2019).

  • 7.

    Giordani, L. et al. High-dimensional single-cell cartography reveals novel skeletal muscle-resident cell populations. Mol. Cell 74, 609–621 (2019).

    CAS  PubMed  Article  Google Scholar 

  • 8.

    Kuang, S., Kuroda, K., Le Grand, F. & Rudnicki, M. A. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129, 999–1010 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 9.

    Rocheteau, P., Gayraud-Morel, B., Siegl-Cachedenier, I., Blasco, M. A. & Tajbakhsh, S. A subpopulation of adult skeletal muscle stem cells retains all template DNA strands after cell division. Cell 148, 112–125 (2012).

    CAS  PubMed  Article  Google Scholar 

  • 10.

    Scaramozza, A. et al. Lineage tracing reveals a subset of reserve muscle stem cells capable of clonal expansion under stress. Cell Stem Cell https://doi.org/10.1016/j.stem.2019.03.020 (2019).

  • 11.

    Der Vartanian, A. et al. PAX3 confers functional heterogeneity in skeletal muscle stem cell responses to environmental stress. Cell Stem Cell https://doi.org/10.1016/j.stem.2019.03.019 (2019).

  • 12.

    De Micheli, A. J. et al. Single-cell analysis of the muscle stem cell hierarchy identifies heterotypic communication signals involved in skeletal muscle regeneration. Cell Rep. 30, 3583–3595 (2020).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 13.

    Toro-Dominguez, D. et al. ImaGEO: integrative gene expression meta-analysis from GEO database. Bioinformatics 35, 880–882 (2019).

    CAS  PubMed  Article  Google Scholar 

  • 14.

    Sidney, L. E., Branch, M. J., Dunphy, S. E., Dua, H. S. & Hopkinson, A. Concise review: evidence for CD34 as a common marker for diverse progenitors. Stem Cells 32, 1380–1389 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 15.

    Beauchamp, J. R. et al. Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J. Cell Biol. 151, 1221–1234 (2000).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 16.

    van Velthoven, C. T. J., de Morree, A., Egner, I. M., Brett, J. O. & Rando, T. A. Transcriptional profiling of quiescent muscle stem cells in vivo. Cell Rep. 21, 1994–2004 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 17.

    Garcia-Prat, L. et al. Autophagy maintains stemness by preventing senescence. Nature 529, 37–42 (2016).

    CAS  PubMed  Article  Google Scholar 

  • 18.

    Sousa-Victor, P. et al. Geriatric muscle stem cells switch reversible quiescence into senescence. Nature 506, 316–321 (2014).

    CAS  PubMed  Article  Google Scholar 

  • 19.

    Alfaro, L. A. et al. CD34 promotes satellite cell motility and entry into proliferation to facilitate efficient skeletal muscle regeneration. Stem Cells 29, 2030–2041 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 20.

    Lee, J. Y. et al. Clonal isolation of muscle-derived cells capable of enhancing muscle regeneration and bone healing. J. Cell Biol. 150, 1085–1100 (2000).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 21.

    Reimand, J. et al. Pathway enrichment analysis and visualization of omics data using g:Profiler, GSEA, Cytoscape and EnrichmentMap. Nat. Protoc. 14, 482–517 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 22.

    Nichols, J. & Smith, A. Naive and primed pluripotent states. Cell Stem Cell 4, 487–492 (2009).

    CAS  PubMed  Article  Google Scholar 

  • 23.

    Abou-Khalil, R. et al. Autocrine and paracrine angiopoietin 1/Tie-2 signaling promotes muscle satellite cell self-renewal. Cell Stem Cell 5, 298–309 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 24.

    Kitamoto, T. & Hanaoka, K. Notch3 null mutation in mice causes muscle hyperplasia by repetitive muscle regeneration. Stem Cells 28, 2205–2216 (2010).

    CAS  PubMed  Article  Google Scholar 

  • 25.

    Evano, B. & Tajbakhsh, S. Skeletal muscle stem cells in comfort and stress. NPJ Regen. Med. 3, 24 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  • 26.

    Mourikis, P. & Tajbakhsh, S. Distinct contextual roles for notch signalling in skeletal muscle stem cells. BMC Dev. Biol. 14, 2 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 27.

    White, R. B., Bierinx, A. S., Gnocchi, V. F. & Zammit, P. S. Dynamics of muscle fibre growth during postnatal mouse development. BMC Dev. Biol. 10, 21 (2010).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 28.

    Day, K., Shefer, G., Shearer, A. & Yablonka-Reuveni, Z. The depletion of skeletal muscle satellite cells with age is concomitant with reduced capacity of single progenitors to produce reserve progeny. Dev. Biol. 340, 330–343 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 29.

    Liu, W. et al. Loss of adult skeletal muscle stem cells drives age-related neuromuscular junction degeneration. eLife 6, e26464 (2017).

  • 30.

    Gopinath, S. D., Webb, A. E., Brunet, A. & Rando, T. A. FOXO3 promotes quiescence in adult muscle stem cells during the process of self-renewal. Stem Cell Rep. 2, 414–426 (2014).

    CAS  Article  Google Scholar 

  • 31.

    Kalamakis, G. et al. Quiescence modulates stem cell maintenance and regenerative capacity in the aging brain. Cell 176, 1407–1419 (2019).

    CAS  PubMed  Article  Google Scholar 

  • 32.

    Ravichandran, S., Hartmann, A. & Del Sol, A. SigHotSpotter: scRNA-seq-based computational tool to control cell subpopulation phenotypes for cellular rejuvenation strategies. Bioinformatics https://doi.org/10.1093/bioinformatics/btz827 (2019).

  • 33.

    Alessi, D. R. et al. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 15, 6541–6551 (1996).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 34.

    Yun, B. G. & Matts, R. L. Hsp90 functions to balance the phosphorylation state of Akt during C2C12 myoblast differentiation. Cell Signal. 17, 1477–1485 (2005).

    CAS  PubMed  Article  Google Scholar 

  • 35.

    Stitt, T. N. et al. The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol. Cell 14, 395–403 (2004).

    CAS  PubMed  Article  Google Scholar 

  • 36.

    Ascenzi, F. et al. Effects of IGF-1 isoforms on muscle growth and sarcopenia. Aging Cell 18, e12954 (2019).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 37.

    Dell’Orso, S. et al. Correction: single cell analysis of adult mouse skeletal muscle stem cells in homeostatic and regenerative conditions (doi: 10.1242/dev.174177). Development 146, dev.181743 (2019).

  • 38.

    Li, Y. et al. A programmable fate decision landscape underlies single-cell aging in yeast. Science 369, 325–329 (2020).

    CAS  PubMed  Google Scholar 

  • 39.

    Baghdadi, M. B. et al. Reciprocal signalling by Notch–Collagen V–CALCR retains muscle stem cells in their niche. Nature 557, 714–718 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 40.

    Bjornson, C. R. et al. Notch signaling is necessary to maintain quiescence in adult muscle stem cells. Stem Cells 30, 232–242 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 41.

    Mourikis, P. et al. A critical requirement for notch signaling in maintenance of the quiescent skeletal muscle stem cell state. Stem Cells 30, 243–252 (2012).

    CAS  PubMed  Article  Google Scholar 

  • 42.

    Webb, A. E. et al. FOXO3 shares common targets with ASCL1 genome-wide and inhibits ASCL1-dependent neurogenesis. Cell Rep. 4, 477–491 (2013).

    CAS  PubMed  Article  Google Scholar 

  • 43.

    Wilhelm, K. et al. FOXO1 couples metabolic activity and growth state in the vascular endothelium. Nature 529, 216–220 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 44.

    Tierney, M. T., Stec, M. J., Rulands, S., Simons, B. D. & Sacco, A. Muscle stem cells exhibit distinct clonal dynamics in response to tissue repair and homeostatic aging. Cell Stem Cell 22, 119–127 (2018).

    CAS  PubMed  Article  Google Scholar 

  • 45.

    Alvarez, S. et al. Replication stress caused by low MCM expression limits fetal erythropoiesis and hematopoietic stem cell functionality. Nat. Commun. 6, 8548 (2015).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 46.

    Sambasivan, R. et al. Distinct regulatory cascades govern extraocular and pharyngeal arch muscle progenitor cell fates. Dev. Cell 16, 810–821 (2009).

    CAS  PubMed  Article  Google Scholar 

  • 47.

    Paik, J. H. et al. FoxOs are lineage-restricted redundant tumor suppressors and regulate endothelial cell homeostasis. Cell 128, 309–323 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 48.

    Suelves, M. et al. uPA deficiency exacerbates muscular dystrophy in MDX mice. J. Cell Biol. 178, 1039–1051 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 49.

    Moyle, L. A. & Zammit, P. S. Isolation, culture and immunostaining of skeletal muscle fibres to study myogenic progression in satellite cells. Methods Mol. Biol. 1210, 63–78 (2014).

    CAS  PubMed  Article  Google Scholar 

  • 50.

    Sacco, A. et al. Short telomeres and stem cell exhaustion model Duchenne muscular dystrophy in mdx/mTR mice. Cell 143, 1059–1071 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 51.

    Weintraub, H. et al. The myoD gene family: nodal point during specification of the muscle cell lineage. Science 251, 761–766 (1991).

    CAS  PubMed  Article  Google Scholar 

  • 52.

    Perdiguero, E., Ruiz-Bonilla, V., Serrano, A. L. & Munoz-Canoves, P. Genetic deficiency of p38α reveals its critical role in myoblast cell cycle exit: the p38α-JNK connection. Cell Cycle 6, 1298–1303 (2007).

    CAS  PubMed  Article  Google Scholar 

  • 53.

    Garcia-Prat, L., Munoz-Canoves, P. & Martinez-Vicente, M. Monitoring autophagy in muscle stem cells. Methods Mol. Biol. 1556, 255–280 (2017).

    PubMed  Article  CAS  Google Scholar 

  • 54.

    Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 55.

    Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y. & Greenleaf, W. J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10, 1213–1218 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 56.

    Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 57.

    Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545–15550 (2005).

    CAS  Article  Google Scholar 

  • 58.

    Kuleshov, M. V. et al. Enrichr: a comprehensive gene set enrichment analysis web server 2016 update. Nucleic Acids Res. 44, W90–W97 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 59.

    Shih, H. Y. et al. Developmental acquisition of regulomes underlies innate lymphoid cell functionality. Cell 165, 1120–1133 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 60.

    Xu, H. et al. FastUniq: a fast de novo duplicates removal tool for paired short reads. PLoS ONE 7, e52249 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 61.

    Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 62.

    Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576–589 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 63.

    Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 64.

    Shen, L., Shao, N., Liu, X. & Nestler, E. ngs.plot: Quick mining and visualization of next-generation sequencing data by integrating genomic databases. BMC Genomics 15, 284 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Read original article here.