Constitutive Notch Activation Upregulates Pax7 and Promotes the Self-Renewal of Skeletal Muscle Satellite Cells

REFERENCES

• Acharyya S, et al. 2010. TNF inhibits Notch-1 in skeletal muscle cells by Ezh2 and DNA methylation mediated repression: implications in duchenne muscular dystrophy. PLoS One 5:e12479. https://doi.org/10.1371/journal.pone.0012479.
   PubMed Web of Science ®Google Scholar
• Bjornson CR, et al. 2011. Notch signaling is necessary to maintain quiescence in adult muscle stem cells. Stem Cells 30:232–242.
   Google Scholar
• Brack AS, Conboy IM, Conboy MJ, Shen J, Rando TA. 2008. A temporal switch from notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis. Cell Stem Cell 2:50–59.
   PubMedGoogle Scholar
• Buas MF, Kabak S, Kadesch T. 2010. The Notch effector Hey1 associates with myogenic target genes to repress myogenesis. J. Biol. Chem. 285:1249–1258.
   PubMedGoogle Scholar
• Carlson BM. 2003. Muscle regeneration in amphibians and mammals: passing the torch. Dev. Dyn. 226:167–181.
   PubMed Web of Science ®Google Scholar
• Carlson ME, Hsu M, Conboy IM. 2008. Imbalance between pSmad3 and Notch induces CDK inhibitors in old muscle stem cells. Nature 454:528–532.
   PubMedGoogle Scholar
• Charge SB, Brack AS, Hughes SM. 2002. Aging-related satellite cell differentiation defect occurs prematurely after Ski-induced muscle hypertrophy. Am. J. Physiol. Cell Physiol. 283:C1228–C1241.
   PubMedGoogle Scholar
• Conboy IM, Conboy MJ, Smythe GM, Rando TA. 2003. Notch-mediated restoration of regenerative potential to aged muscle. Science 302:1575–1577.
   PubMed Web of Science ®Google Scholar
• Conboy IM, et al. 2005. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433:760–764.
   PubMed Web of Science ®Google Scholar
• Conboy IM, Rando TA. 2002. The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev. Cell 3:397–409.
   PubMed Web of Science ®Google Scholar
• Cornelison DD, et al. 2004. Essential and separable roles for Syndecan-3 and Syndecan-4 in skeletal muscle development and regeneration. Genes Dev. 18:2231–2236.
   PubMed Web of Science ®Google Scholar
• Delfini MC, Hirsinger E, Pourquie O, Duprez D. 2000. Delta 1-activated notch inhibits muscle differentiation without affecting Myf5 and Pax3 expression in chick limb myogenesis. Development 127:5213–5224.
   PubMedGoogle Scholar
• Fuentealba L, Carey DJ, Brandan E. 1999. Antisense inhibition of syndecan-3 expression during skeletal muscle differentiation accelerates myogenesis through a basic fibroblast growth factor-dependent mechanism. J. Biol. Chem. 274:37876–37884.
   PubMedGoogle Scholar
• Fukada S, et al. 2011. Hesr1 and Hesr3 are essential to generate undifferentiated quiescent satellite cells and to maintain satellite cell numbers. Development 138:4609–4619.
   PubMedGoogle Scholar
• Gustafsson MV, et al. 2005. Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev. Cell 9:617–628.
   PubMed Web of Science ®Google Scholar
• Halevy O, et al. 2004. Pattern of Pax7 expression during myogenesis in the posthatch chicken establishes a model for satellite cell differentiation and renewal. Dev. Dyn. 231:489–502.
   PubMed Web of Science ®Google Scholar
• Jory A, et al. 2009. Numb promotes an increase in skeletal muscle progenitor cells in the embryonic somite. Stem Cells 27:2769–2780.
   PubMedGoogle Scholar
• Jouve C, et al. 2000. Notch signalling is required for cyclic expression of the hairy-like gene HES1 in the presomitic mesoderm. Development 127:1421–1429.
   PubMedGoogle Scholar
• Kitamoto T, Hanaoka K. 2010. Notch3 null mutation in mice causes muscle hyperplasia by repetitive muscle regeneration. Stem Cells 28:2205–2216.
   PubMedGoogle Scholar
• Kopan R, Ilagan MX. 2009. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137:216–233.
   PubMed Web of Science ®Google Scholar
• Kopan R, Nye JS, Weintraub H. 1994. The intracellular domain of mouse Notch: a constitutively activated repressor of myogenesis directed at the basic helix-loop-helix region of MyoD. Development 120:2385–2396.
   PubMed Web of Science ®Google Scholar
• Kuang S, Charge SB, Seale P, Huh M, Rudnicki MA. 2006. Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis. J. Cell Biol. 172:103–113.
   PubMed Web of Science ®Google Scholar
• Kuang S, Kuroda K, Le Grand F, Rudnicki MA. 2007. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129:999–1010.
   PubMed Web of Science ®Google Scholar
• Kuroda K, et al. 1999. Delta-induced Notch signaling mediated by RBP-J inhibits MyoD expression and myogenesis. J. Biol. Chem. 274:7238–7244.
   PubMed Web of Science ®Google Scholar
• Leimeister C, Externbrink A, Klamt B, Gessler M. 1999. Hey genes: a novel subfamily of hairy- and Enhancer of split-related genes specifically expressed during mouse embryogenesis. Mech. Dev. 85:173–177.
   PubMed Web of Science ®Google Scholar
• Lepper C, Conway SJ, Fan CM. 2009. Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature 460:627–631.
   PubMed Web of Science ®Google Scholar
• Lepper C, Partridge TA, Fan CM. 2011. An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development 138:3639–3646.
   PubMed Web of Science ®Google Scholar
• Mourikis P, et al. 2012. A critical requirement for Notch signaling in maintenance of the quiescent skeletal muscle stem cell state. Stem Cells 30:243–252.
   PubMed Web of Science ®Google Scholar
• Murphy MM, Lawson JA, Mathew SJ, Hutcheson DA, Kardon G. 2011. Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration. Development 138:3625–3637.
   PubMed Web of Science ®Google Scholar
• Murtaugh LC, Stanger BZ, Kwan KM, Melton DA. 2003. Notch signaling controls multiple steps of pancreatic differentiation. Proc. Natl. Acad. Sci. U. S. A. 100:14920–14925.
   PubMed Web of Science ®Google Scholar
• Nishijo K, et al. 2009. Biomarker system for studying muscle, stem cells, and cancer in vivo. FASEB J. 23:2681–2690.
   PubMedGoogle Scholar
• Olguin HC, Olwin BB. 2004. Pax-7 up-regulation inhibits myogenesis and cell cycle progression in satellite cells: a potential mechanism for self-renewal. Dev. Biol. 275:375–388.
   PubMed Web of Science ®Google Scholar
• Olguin HC, Patzlaff NE, Olwin BB. 2011. Pax7-FKHR transcriptional activity is enhanced by transcriptionally repressed MyoD. J. Cell. Biochem. 112:1410–1417.
   PubMed Web of Science ®Google Scholar
• Olguin HC, Yang Z, Tapscott SJ, Olwin BB. 2007. Reciprocal inhibition between Pax7 and muscle regulatory factors modulates myogenic cell fate determination. J. Cell Biol. 177:769–779.
   PubMed Web of Science ®Google Scholar
• Oustanina S, Hause G, Braun T. 2004. Pax7 directs postnatal renewal and propagation of myogenic satellite cells but not their specification. EMBO J. 23:3430–3439.
   PubMed Web of Science ®Google Scholar
• Pan D, Fujimoto M, Lopes A, Wang YX. 2009. Twist-1 is a PPARδ-inducible, negative-feedback regulator of PGC-1α in brown fat metabolism. Cell 137:73–86.
   PubMed Web of Science ®Google Scholar
• Pisconti A, Cornelison DD, Olguin HC, Antwine TL, Olwin BB. 2010. Syndecan-3 and Notch cooperate in regulating adult myogenesis. J. Cell Biol. 190:427–441.
   PubMedGoogle Scholar
• Pourquie O. 2011. Vertebrate segmentation: from cyclic gene networks to scoliosis. Cell 145:650–663.
   PubMed Web of Science ®Google Scholar
• Relaix F, et al. 2006. Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. J. Cell Biol. 172:91–102.
   PubMed Web of Science ®Google Scholar
• Rios AC, Serralbo O, Salgado D, Marcelle C. 2011. Neural crest regulates myogenesis through the transient activation of NOTCH. Nature 473:532–535.
   PubMedGoogle Scholar
• Rosenblatt JD, Lunt AI, Parry DJ, Partridge TA. 1995. Culturing satellite cells from living single muscle fiber explants. In Vitro Cell. Dev. Biol. Anim. 31:773–779.
   PubMed Web of Science ®Google Scholar
• Sambasivan R, et al. 2011. Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration. Development 138:3647–3656.
   PubMed Web of Science ®Google Scholar
• Schultz E, Lipton BH. 1982. Skeletal muscle satellite cells: changes in proliferation potential as a function of age. Mech. Ageing Dev. 20:377–383.
   PubMed Web of Science ®Google Scholar
• Schuster-Gossler K, Cordes R, Gossler A. 2007. Premature myogenic differentiation and depletion of progenitor cells cause severe muscle hypotrophy in Delta1 mutants. Proc. Natl. Acad. Sci. U. S. A. 104:537–542.
   PubMedGoogle Scholar
• Schwanbeck R, Martini S, Bernoth K, Just U. 2011. The Notch signaling pathway: molecular basis of cell context dependency. Eur. J. Cell Biol. 90:572–581.
   PubMed Web of Science ®Google Scholar
• Seale P, et al. 2000. Pax7 is required for the specification of myogenic satellite cells. Cell 102:777–786.
   PubMed Web of Science ®Google Scholar
• Shinin V, Gayraud-Morel B, Gomes D, Tajbakhsh S. 2006. Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat. Cell Biol. 8:677–687.
   PubMed Web of Science ®Google Scholar
• Song Y, McFarland DC, Velleman SG. 2011. Role of syndecan-4 side chains in turkey satellite cell growth and development. Dev. Growth Differ. 53:97–109.
   PubMedGoogle Scholar
• Sun D, Li H, Zolkiewska A. 2008. The role of Delta-like 1 shedding in muscle cell self-renewal and differentiation. J. Cell Sci. 121:3815–3823.
   PubMedGoogle Scholar
• Vasyutina E, et al. 2007. RBP-J (Rbpsuh) is essential to maintain muscle progenitor cells and to generate satellite cells. Proc. Natl. Acad. Sci. U. S. A. 104:4443–4448.
   PubMedGoogle Scholar
• Waddell JN, et al. 2010. Dlk1 is necessary for proper skeletal muscle development and regeneration. PLoS One 5:e15055. https://doi.org/10.1371/journal.pone.0015055.
   PubMed Web of Science ®Google Scholar
• Walker L, et al. 1999. The Notch/Jagged pathway inhibits proliferation of human hematopoietic progenitors in vitro. Stem Cells 17:162–171.
   PubMed Web of Science ®Google Scholar
• Weng AP, et al. 2006. c-Myc is an important direct target of Notch1 in T-cell acute lymphoblastic leukemia/lymphoma. Genes Dev. 20:2096–2109.
   PubMed Web of Science ®Google Scholar
• Wilson-Rawls J, Molkentin JD, Black BL, Olson EN. 1999. Activated notch inhibits myogenic activity of the MADS-box transcription factor myocyte enhancer factor 2C. Mol. Cell. Biol. 19:2853–2862.
   PubMedGoogle Scholar
• Zammit PS, et al. 2004. Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J. Cell Biol. 166:347–357.
   PubMed Web of Science ®Google Scholar