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Research Paper - Basic Science

Autophagy controls neonatal myogenesis by regulating the GH-IGF1 system through a NFE2L2- and DDIT3-mediated mechanism

, , ORCID Icon, , , , , , , , & ORCID Icon show all
Pages 58-77 | Received 27 Sep 2017, Accepted 24 Jul 2018, Published online: 10 Sep 2018

References

  • Murphy M, Kardon G. Origin of vertebrate limb muscle: the role of progenitor and myoblast populations. Curr Top Dev Biol. 2011;96:1–32. PubMed PMID: 21621065.
  • Messina G, Cossu G. The origin of embryonic and fetal myoblasts: a role of Pax3 and Pax7. Genes Dev. 2009 Apr 15;23(8):902–905. PubMed PMID: 19390084.
  • Biressi S, Molinaro M, Cossu G. Cellular heterogeneity during vertebrate skeletal muscle development. Dev Biol. 2007 Aug 15;308(2):281–293. PubMed PMID: 17612520.
  • Mauro A. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol. 1961 Feb;9:493–495. PubMed PMID: 13768451; PubMed Central PMCID: PMC2225012.
  • Biressi S, Tagliafico E, Lamorte G, et al. Intrinsic phenotypic diversity of embryonic and fetal myoblasts is revealed by genome-wide gene expression analysis on purified cells. Dev Biol. 2007 Apr 15;304(2):633–651. PubMed PMID: 17292343.
  • Ono Y, Calhabeu F, Morgan JE, et al. BMP signalling permits population expansion by preventing premature myogenic differentiation in muscle satellite cells. Cell Death Differ. 2011 Feb;18(2):222–234. PubMed PMID: 20689554; PubMed Central PMCID: PMC3044455.
  • Perez-Ruiz A, Ono Y, Gnocchi VF, et al. beta-Catenin promotes self-renewal of skeletal-muscle satellite cells. J Cell Sci. 2008 May 01;121(Pt 9):1373–1382. PubMed PMID: 18397993.
  • Hutcheson DA, Zhao J, Merrell A, et al. Embryonic and fetal limb myogenic cells are derived from developmentally distinct progenitors and have different requirements for beta-catenin. Genes Dev. 2009 Apr 15;23(8):997–1013. PubMed PMID: 19346403; PubMed Central PMCID: PMC2675868.
  • Mathew SJ, Hansen JM, Merrell AJ, et al. Connective tissue fibroblasts and Tcf4 regulate myogenesis. Development. 2011 Jan;138(2):371–384. PubMed PMID: 21177349; PubMed Central PMCID: PMC3005608.
  • Guan JL, Simon AK, Prescott M, et al. Autophagy in stem cells. Autophagy. 2013 Jun 01;9(6):830–849. PubMed PMID: 23486312; PubMed Central PMCID: PMC3672294.
  • Singh R, Cuervo AM. Autophagy in the cellular energetic balance. Cell Metab. 2011 May 04;13(5):495–504. PubMed PMID: 21531332; PubMed Central PMCID: PMC3099265.
  • Mizushima N, Levine B, Cuervo AM, et al. Autophagy fights disease through cellular self-digestion. Nature. 2008 Feb 28;451(7182):1069–1075. PubMed PMID: 18305538; PubMed Central PMCID: PMC2670399.
  • Phadwal K, Watson AS, Simon AK. Tightrope act: autophagy in stem cell renewal, differentiation, proliferation, and aging. Cell Mol Life Sci. 2013 Jan;70(1):89–103. PubMed PMID: 22669258; PubMed Central PMCID: PMC3535400.
  • Fortini P, Ferretti C, Iorio E, et al. The fine tuning of metabolism, autophagy and differentiation during in vitro myogenesis. Cell Death Dis. 2016 Mar;31(7):e2168. PubMed PMID: 27031965; PubMed Central PMCID: PMC4823951.
  • Sin J, Andres AM, Taylor DJ, et al. Mitophagy is required for mitochondrial biogenesis and myogenic differentiation of C2C12 myoblasts. Autophagy. 2016;12(2):369–380. PubMed PMID: 26566717; PubMed Central PMCID: PMC4836019.
  • Tang AH, Rando TA. Induction of autophagy supports the bioenergetic demands of quiescent muscle stem cell activation. EMBO J. 2014 Dec 01;33(23):2782–2797. PubMed PMID: 25316028; PubMed Central PMCID: PMC4282556.
  • Garcia-Prat L, Martinez-Vicente M, Perdiguero E, et al. Autophagy maintains stemness by preventing senescence. Nature. 2016 Jan 07;529(7584):37–42. PubMed PMID: 26738589.
  • Martinez-Lopez N, Athonvarangkul D, Sahu S, et al. Autophagy in Myf5+ progenitors regulates energy and glucose homeostasis through control of brown fat and skeletal muscle development. EMBO Rep. 2013 Sep;14(9):795–803. PubMed PMID: 23907538; PubMed Central PMCID: PMC3790054.
  • Haldar M, Karan G, Tvrdik P, et al. Two cell lineages, myf5 and myf5-independent, participate in mouse skeletal myogenesis. Dev Cell. 2008 Mar;14(3):437–445. PubMed PMID: 18331721; PubMed Central PMCID: PMC2917991.
  • Relaix F, Rocancourt D, Mansouri A, et al. Divergent functions of murine Pax3 and Pax7 in limb muscle development. Genes Dev. 2004 May 01;18(9):1088–1105. PubMed PMID: 15132998; PubMed Central PMCID: PMC406297.
  • Lepper C, Conway SJ, Fan CM. Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature. 2009 Jul 30;460(7255):627–631. PubMed PMID: 19554048; PubMed Central PMCID: PMC2767162.
  • Lepper C, Fan CM. Inducible lineage tracing of Pax7-descendant cells reveals embryonic origin of adult satellite cells. Genesis. 2010 Jul;48(7):424–436. PubMed PMID: 20641127; PubMed Central PMCID: PMC3113517.
  • Masiero E, Agatea L, Mammucari C, et al. Autophagy is required to maintain muscle mass. Cell Metab. 2009 Dec;10(6):507–515; S1550–4131(09)00310–6 [pii]. PubMed PMID: 19945408; eng.
  • Mavalli MD, DiGirolamo DJ, Fan Y, et al. Distinct growth hormone receptor signaling modes regulate skeletal muscle development and insulin sensitivity in mice. J Clin Invest. 2010 Nov;120(11):4007–4020. PubMed PMID: 20921627; PubMed Central PMCID: PMC2964973.
  • Sotiropoulos A, Ohanna M, Kedzia C, et al. Growth hormone promotes skeletal muscle cell fusion independent of insulin-like growth factor 1 up-regulation. Proc Natl Acad Sci U S A. 2006 May 09;103(19):7315–7320. PubMed PMID: 16670201; PubMed Central PMCID: PMC1456062.
  • Kim H, Barton E, Muja N, et al. Intact insulin and insulin-like growth factor-I receptor signaling is required for growth hormone effects on skeletal muscle growth and function in vivo. Endocrinology. 2005 Apr;146(4):1772–1779. PubMed PMID: 15618350.
  • Schiaffino S, Mammucari C. Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skelet Muscle. 2011 Jan 24;1(1):4. PubMed PMID: 21798082; PubMed Central PMCID: PMC3143906.
  • Klover P, Hennighausen L. Postnatal body growth is dependent on the transcription factors signal transducers and activators of transcription 5a/b in muscle: a role for autocrine/paracrine insulin-like growth factor I. Endocrinology. 2007 Apr;148(4):1489–1497. PubMed PMID: 17158201.
  • Davey HW, Xie T, McLachlan MJ, et al. STAT5b is required for GH-induced liver IGF-I gene expression. Endocrinology. 2001 Sep;142(9):3836–3841. PubMed PMID: 11517160.
  • Klover P, Chen W, Zhu BM, et al. Skeletal muscle growth and fiber composition in mice are regulated through the transcription factors STAT5a/b: linking growth hormone to the androgen receptor. FASEB J. 2009 Sep;23(9):3140–3148. PubMed PMID: 19417088; PubMed Central PMCID: PMC2735360.
  • MacLean HE, Chiu WS, Notini AJ, et al. Impaired skeletal muscle development and function in male, but not female, genomic androgen receptor knockout mice. FASEB J. 2008 Aug;22(8):2676–2689. PubMed PMID: 18390925.
  • Frost RA, Nystrom GJ, Lang CH. Regulation of IGF-I mRNA and signal transducers and activators of transcription-3 and −5 (Stat-3 and −5) by GH in C2C12 myoblasts. Endocrinology. 2002 Feb;143(2):492–503. PubMed PMID: 11796503.
  • Sadowski CL, Wheeler TT, Wang LH, et al. GH regulation of IGF-I and suppressor of cytokine signaling gene expression in C2C12 skeletal muscle cells. Endocrinology. 2001 Sep;142(9):3890–3900. PubMed PMID: 11517167.
  • Li Z, Gilbert JA, Zhang Y, et al. An HMGA2-IGF2BP2 axis regulates myoblast proliferation and myogenesis. Dev Cell. 2012 Dec 11;23(6):1176–1188. PubMed PMID: 23177649; PubMed Central PMCID: PMC3645921.
  • Fukada S, Uezumi A, Ikemoto M, et al. Molecular signature of quiescent satellite cells in adult skeletal muscle. Stem Cells. 2007 Oct;25(10):2448–2459. PubMed PMID: 17600112.
  • Lin S, Li H, Mu H, et al. Let-7b regulates the expression of the growth hormone receptor gene in deletion-type dwarf chickens. BMC Genomics. 2012 Jul;10(13):306. PubMed PMID: 22781587; PubMed Central PMCID: PMC3428657.
  • Elzein S, Goodyer CG. Regulation of human growth hormone receptor expression by microRNAs. Mol Endocrinol. 2014 Sep;28(9):1448–1459. PubMed PMID: 25073105.
  • Wei Y, Puzhko S, Wabitsch M, et al. Transcriptional regulation of the human growth hormone receptor (hGHR) gene V2 promoter by transcriptional activators and repressor. Mol Endocrinol. 2009 Mar;23(3):373–387. PubMed PMID: 19116245.
  • Oyadomari S, Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 2004 Apr;11(4):381–389. PubMed PMID: 14685163.
  • Szegezdi E, Logue SE, Gorman AM, et al. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep. 2006 Sep;7(9):880–885. PubMed PMID: 16953201; PubMed Central PMCID: PMC1559676.
  • Zong ZH, Du ZX, Li N, et al. Implication of Nrf2 and ATF4 in differential induction of CHOP by proteasome inhibition in thyroid cancer cells. Biochim Biophys Acta. 2012 Aug;1823(8):1395–1404. PubMed PMID: 22691366.
  • Cullinan SB, Diehl JA. PERK-dependent activation of Nrf2 contributes to redox homeostasis and cell survival following endoplasmic reticulum stress. J Biol Chem. 2004 May 7;279(19):20108–20117. PubMed PMID: 14978030.
  • Jiang T, Harder B, Rojo de la Vega M, et al. p62 links autophagy and Nrf2 signaling. Free Radic Biol Med. 2015 Nov;88(Pt B):199–204. PubMed PMID: 26117325; PubMed Central PMCID: PMC4628872.
  • Liu JP, Baker J, Perkins AS, et al. Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell. 1993 Oct 08;75(1):59–72. PubMed PMID: 8402901.
  • Horibe T, Hoogenraad NJ. The chop gene contains an element for the positive regulation of the mitochondrial unfolded protein response. PLoS One. 2007 Sep 12;2(9):e835. PubMed PMID: 17848986; PubMed Central PMCID: PMC1950685.
  • Touvier T, De Palma C, Rigamonti E, et al. Muscle-specific Drp1 overexpression impairs skeletal muscle growth via translational attenuation. Cell Death Dis. 2015;6:e1663. PubMed PMID: 25719247.
  • Ubeda M, Habener JF. CHOP gene expression in response to endoplasmic-reticular stress requires NFY interaction with different domains of a conserved DNA-binding element. Nucleic Acids Res. 2000 Dec 15;28(24):4987–4997. PubMed PMID: 11121490; PubMed Central PMCID: PMC115245.
  • Guyton KZ, Xu Q, Holbrook NJ. Induction of the mammalian stress response gene GADD153 by oxidative stress: role of AP-1 element. Biochem J. 1996 Mar 1;314(Pt 2):547–554. PubMed PMID: 8670069; PubMed Central PMCID: PMC1217084.
  • Cullinan SB, Zhang D, Hannink M, et al. Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Mol Cell Biol. 2003 Oct;23(20):7198–7209. PubMed PMID: 14517290; PubMed Central PMCID: PMC230321
  • Kim KH, Jeong YT, Oh H, et al. Autophagy deficiency leads to protection from obesity and insulin resistance by inducing Fgf21 as a mitokine. Nat Med. 2013 Jan;19(1):83–92. PubMed PMID: 23202295.
  • Komatsu M, Waguri S, Ueno T, et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol. 2005 May 09;169(3):425–434. PubMed PMID: 15866887; PubMed Central PMCID: PMC2171928.
  • Pajtler K, Bohrer A, Maurer J, et al. Production of chick embryo extract for the cultivation of murine neural crest stem cells. Journal Visualized Experiments: JoVE. 2010 Nov;27(45). PubMed PMID: 21178955; PubMed Central PMCID: PMC3159602. DOI:10.3791/2380.
  • Perrotta C, Buonanno F, Zecchini S, et al. Climacostol reduces tumour progression in a mouse model of melanoma via the p53-dependent intrinsic apoptotic programme. Sci Rep. 2016 Jun;07(6):27281. PubMed PMID: 27271364; PubMed Central PMCID: PMC4895139.
  • De Palma C, Morisi F, Pambianco S, et al. Deficient nitric oxide signalling impairs skeletal muscle growth and performance: involvement of mitochondrial dysregulation. Skelet Muscle. 2014;4(1):22. PubMed PMID: 25530838; PubMed Central PMCID: PMC4272808.
  • De Palma C, Di Paola R, Perrotta C, et al. Ibuprofen-arginine generates nitric oxide and has enhanced anti-inflammatory effects. Pharmacological Res. 2009;60(4):221–228.
  • Pambianco S, Giovarelli M, Perrotta C, et al. Reversal of defective mitochondrial biogenesis in limb-girdle muscular dystrophy 2D by independent modulation of histone and PGC-1alpha acetylation. Cell Rep. 2016 Dec 13;17(11):3010–3023. PubMed PMID: 27974213.
  • De Palma C, Morisi F, Cheli S, et al. Autophagy as a new therapeutic target in Duchenne muscular dystrophy. Cell Death Dis. 2012;3:11.
  • Miglietta D, De Palma C, Sciorati C, et al. Naproxcinod shows significant advantages over naproxen in the mdx model of duchenne muscular dystrophy. Orphanet J Rare Dis. 2015;10(1):101. PubMed PMID: 26296873; PubMed Central PMCID: PMC4546261. .
  • Buono R, Vantaggiato C, Pisa V, et al. Nitric oxide sustains long-term skeletal muscle regeneration by regulating fate of satellite cells via signaling pathways requiring Vangl2 and cyclic GMP. Stem Cells. 2012 Feb;30(2):197–209. PubMed PMID: 22084027; PubMed Central PMCID: PMC3378700.

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