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Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 900))

Abstract

Satellite cells are the “currency” for the muscle growth that is critical to meat production in many species, as well as to phenotypic distinctions in development at the level of species or taxa, and for human muscle growth, function and regeneration. Careful research on the activation and behaviour of satellite cells, the stem cells in skeletal muscle, including cross-species comparisons, has potential to reveal the mechanisms underlying pathological conditions in animals and humans, and to anticipate implications of development, evolution and environmental change on muscle function and animal performance.

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References

  • Alfaro LA, Dick SA, Siegel AL, Anonuevo AS, McNagny KM, Megeney LA, Cornelison DD, Rossi FM (2011) CD34 promotes satellite cell motility and entry into proliferation to facilitate efficient skeletal muscle regeneration. Stem Cells 29(12):2030–2041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allen RE, Boxhorn LK (1989) Regulation of skeletal muscle satellite cell proliferation and differentiation by transforming growth factor-beta, insulin-like growth factor I, and fibroblast growth factor. J Cell Physiol 138(2):311–315

    Article  CAS  PubMed  Google Scholar 

  • Allen RE, Rankin LL (1990) Regulation of satellite cells during skeletal muscle growth and development. Proc Soc Exp Biol Med 194(2):81–86

    Article  CAS  PubMed  Google Scholar 

  • Allen RE, Merkel RA, Young RB (1979) Cellular aspects of muscle growth: myogenic cell proliferation. J Anim Sci 49(1):115–127

    CAS  PubMed  Google Scholar 

  • Allen DL, Monke SR, Talmadge RJ, Roy RR, Edgerton VR (1995a) Plasticity of myonuclear number in hypertrophied and atrophied mammalian skeletal muscle fibers. J Appl Physiol 78(5):1969–1976

    CAS  PubMed  Google Scholar 

  • Allen RE, Sheehan SM, Taylor RG, Kendall TL, Rice GM (1995b) Hepatocyte growth factor activates quiescent skeletal muscle satellite cells in vitro. J Cell Physiol 165(2):307–312

    Article  CAS  PubMed  Google Scholar 

  • Anastasi S, Giordano S, Sthandier O, Gambarotta G, Maione R, Comoglio P, Amati P (1997) 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 137(5):1057–1068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson JE (2000) A role for nitric oxide in muscle repair: nitric oxide-mediated activation of muscle satellite cells. Mol Biol Cell 11(5):1859–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson JE (2006) The satellite cell as a companion in skeletal muscle plasticity: currency, conveyance, clue, connector and colander. J Exp Biol 209(Pt 12):2276–2292

    Google Scholar 

  • Anderson J, Pilipowicz O (2002) Activation of muscle satellite cells in single-fiber cultures. Nitric Oxide 7(1):36–41

    Article  CAS  PubMed  Google Scholar 

  • Anderson JE, Wozniak AC (2004) Satellite cell activation on fibers: modeling events in vivo – an invited review. Can J Physiol Pharmacol 82(5):300–310

    Article  CAS  PubMed  Google Scholar 

  • Anderson JE, Bressler BH, Ovalle WK (1988) Functional regeneration in the hindlimb skeletal muscle of the mdx mouse. J Muscle Res Cell Motil 9(6):499–515

    Article  CAS  PubMed  Google Scholar 

  • Anderson JE, Liu L, Kardami E (1991) Distinctive patterns of basic fibroblast growth factor (bFGF) distribution in degenerating and regenerating areas of dystrophic (mdx) striated muscles. Dev Biol 147(1):96–109

    Article  CAS  PubMed  Google Scholar 

  • Anderson JE, McIntosh LM, Moor AN, Yablonka-Reuveni Z (1998) Levels of MyoD protein expression following injury of mdx and normal limb muscle are modified by thyroid hormone. J Histochem Cytochem 46(1):59–67

    Article  CAS  PubMed  Google Scholar 

  • Anderson JE, Wozniak AC, Mizunoya W (2012) Single muscle-fiber isolation and culture for cellular, molecular, pharmacological, and evolutionary studies. Methods Mol Biol 798:85–102

    Article  CAS  PubMed  Google Scholar 

  • Andres-Mateos E, Brinkmeier H, Burks TN, Mejias R, Files DC, Steinberger M, Soleimani A, Marx R, Simmers JL, Lin B, Hedderick EF, Marr TG, Lin BM, Hourde C, Leinwand LA, Kuhl D, Foller M, Vogelsang S, Hernandez-Diaz I, Vaughan DK, de la Rosa DA, Lang F, Cohn RD (2013) Activation of serum/glucocorticoid-induced kinase 1 (SGK1) is important to maintain skeletal muscle homeostasis and prevent atrophy. EMBO Mol Med 5(1):80–91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arber S, Burden SJ, Harris AJ (2002) Patterning of skeletal muscle. Curr Opin Neurobiol 12(1):100–103

    Article  CAS  PubMed  Google Scholar 

  • Argiles JM, Orpi M, Busquets S, Lopez-Soriano FJ (2012) Myostatin: more than just a regulator of muscle mass. Drug Discov Today 17(13–14):702–709

    Google Scholar 

  • Asano T, Kaneko E, Shinozaki S, Imai Y, Shibayama M, Chiba T, Ai M, Kawakami A, Asaoka H, Nakayama T, Mano Y, Shimokado K (2007) Hyperbaric oxygen induces basic fibroblast growth factor and hepatocyte growth factor expression, and enhances blood perfusion and muscle regeneration in mouse ischemic hind limbs. Circ J 71(3):405–411

    Article  CAS  PubMed  Google Scholar 

  • Atkins C, Pezzementi L (1993) Developmental changes in the molecular forms of acetylcholinesterase during the life-cycle of the lamprey Petromyzon marinus. Comp Biochem Physiol B: Biochem Mol Biol 106:369–372

    CAS  Google Scholar 

  • Barbero A, Benelli R, Minghelli S, Tosetti F, Dorcaratto A, Ponzetto C, Wernig A, Cullen MJ, Albini A, Noonan DM (2001) Growth factor supplemented matrigel improves ectopic skeletal muscle formation–a cell therapy approach. J Cell Physiol 186(2):183–192

    Article  CAS  PubMed  Google Scholar 

  • Barresi R, Campbell KP (2006) Dystroglycan: from biosynthesis to pathogenesis of human disease. J Cell Sci 119(Pt 2):199–207

    Article  CAS  PubMed  Google Scholar 

  • Beauchamp JR, Morgan JE, Pagel CN, Partridge TA (1999) Dynamics of myoblast transplantation reveal a discrete minority of precursors with stem cell-like properties as the myogenic source. J Cell Biol 144(6):1113–1122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bischoff R (1986a) A satellite cell mitogen from crushed adult muscle. Dev Biol 115(1):140–147

    Article  CAS  PubMed  Google Scholar 

  • Bischoff R (1986b) Proliferation of muscle satellite cells on intact myofibers in culture. Dev Biol 115(1):129–139

    Article  CAS  PubMed  Google Scholar 

  • Bischoff R (1990) Cell cycle commitment of rat muscle satellite cells. J Cell Biol 111(1):201–207

    Article  CAS  PubMed  Google Scholar 

  • Bischoff R, Heintz C (1994) Enhancement of skeletal muscle regeneration. Dev Dyn 201(1):41–54

    Article  CAS  PubMed  Google Scholar 

  • bou-Khalil R, Mounier R, Chazaud B (2010) Regulation of myogenic stem cell behavior by vessel cells: the “menage a trois” of satellite cells, periendothelial cells and endothelial cells. Cell Cycle 9(5):892–896

    Article  Google Scholar 

  • Brack AS, Murphy-Seiler F, Hanifi J, Deka J, Eyckerman S, Keller C, Aguet M, Rando TA (2009) BCL9 is an essential component of canonical Wnt signaling that mediates the differentiation of myogenic progenitors during muscle regeneration. Dev Biol 335(1):93–105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brenman JE, Chao DS, Xia H, Aldape K, Bredt DS (1995) Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell 82(5):743–752

    Article  CAS  PubMed  Google Scholar 

  • Brooks NE, Myburgh KH, Storey KB (2011) Myostatin levels in skeletal muscle of hibernating ground squirrels. J Exp Biol 214(15):2522–2527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burke B, Roux KJ (2009) Nuclei take a position: managing nuclear location. Dev Cell 17(5):587–597

    Article  CAS  PubMed  Google Scholar 

  • Busetto G, Buffelli M, Cangiano L, Cangiano A (2003) Effects of evoked and spontaneous motoneuronal firing on synapse competition and elimination in skeletal muscle. J Neurocytol 32(5–8):795–802

    Article  CAS  PubMed  Google Scholar 

  • Campbell KP, Stull JT (2003) Skeletal muscle basement membrane-sarcolemma-cytoskeleton interaction minireview series. J Biol Chem 278(15):12599–12600

    Article  CAS  PubMed  Google Scholar 

  • Casar JC, Cabello-Verrugio C, Olguin H, Aldunate R, Inestrosa NC, Brandan E (2004) Heparan sulfate proteoglycans are increased during skeletal muscle regeneration: requirement of syndecan-3 for successful fiber formation. J Cell Sci 117(Pt 1):73–84

    Article  CAS  PubMed  Google Scholar 

  • Cassano M, Biressi S, Finan A, Benedetti L, Omes C, Boratto R, Martin F, Allegretti M, Broccoli V, Cusella De AG, Comoglio PM, Basilico C, Torrente Y, Michieli P, Cossu G, Sampaolesi M (2008) Magic-factor 1, a partial agonist of Met, induces muscle hypertrophy by protecting myogenic progenitors from apoptosis. Plos One 3(9):e3223

    Google Scholar 

  • Charge SB, Rudnicki MA (2004) Cellular and molecular regulation of muscle regeneration. Physiol Rev 84(1):209–238

    Article  CAS  PubMed  Google Scholar 

  • Chazaud B (2010) Dual effect of HGF on satellite/myogenic cell quiescence. Focus on “High concentrations of HGF inhibit skeletal muscle satellite cell proliferation in vitro by inducing expression of myostatin: a possible mechanism for reestablishing satellite cell quiescence in vivo”. Am J Physiol Cell Physiol 298(3):C448–C449

    Article  CAS  PubMed  Google Scholar 

  • Collins CA, Partridge TA (2005) Self-renewal of the adult skeletal muscle satellite cell. Cell Cycle 4(10):1338–1341

    Article  CAS  PubMed  Google Scholar 

  • Collins CA, Olsen I, Zammit PS, Heslop L, Petrie A, Partridge TA, Morgan JE (2005) Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 122(2):289–301

    Article  CAS  PubMed  Google Scholar 

  • Collins CA, Zammit PS, Perez RA, Morgan JE, Partridge TA (2007) A population of myogenic stem cells that survives skeletal muscle aging. Stem Cells 25:885–894

    Article  CAS  PubMed  Google Scholar 

  • Cornelison DD, Filla MS, Stanley HM, Rapraeger AC, Olwin BB (2001) Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration. Dev Biol 239(1):79–94

    Article  CAS  PubMed  Google Scholar 

  • Cornelison DD, Wilcox-Adelman SA, Goetinck PF, Rauvala H, Rapraeger AC, Olwin BB (2004) Essential and separable roles for Syndecan-3 and Syndecan-4 in skeletal muscle development and regeneration. Genes Dev 18(18):2231–2236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corrigan LJ, Lucas MC, Winfield IJ, Hoelzel AR (2011) Environmental factors associated with genetic and phenotypic divergence among sympatric populations of Arctic charr (Salvelinus alpinus). J Evol Biol 24:1906–1917

    Article  CAS  PubMed  Google Scholar 

  • Corti S, Salani S, Del BR, Sironi M, Strazzer S, D’Angelo MG, Comi GP, Bresolin N, Scarlato G (2001) Chemotactic factors enhance myogenic cell migration across an endothelial monolayer. Exp Cell Res 268(1):36–44

    Article  CAS  PubMed  Google Scholar 

  • Crisp M, Liu Q, Roux K, Rattner JB, Shanahan C, Burke B, Stahl PD, Hodzic D (2006) Coupling of the nucleus and cytoplasm: role of the LINC complex. J Cell Biol 172(1):41–53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dhawan J, Rando TA (2005) Stem cells in postnatal myogenesis: molecular mechanisms of satellite cell quiescence, activation and replenishment. Trends Cell Biol 15(12):666–673

    Article  CAS  PubMed  Google Scholar 

  • Do MK, Sato Y, Shimizu N, Suzuki T, Shono J, Mizunoya W, Nakamura M, Ikeuchi Y, Anderson JE, Tatsumi R (2011) Growth factor regulation of neural chemorepellent Sema3A expression in satellite cell cultures. Am J Physiol Cell Physiol 301(5):C1270–C1279

    Article  CAS  PubMed  Google Scholar 

  • Do MK, Suzuki T, Gerelt B, Sato Y, Mizunoya W, Nakamura M, Ikeuchi Y, Anderson JE, Tatsumi R (2012) Time-coordinated prevalence of extracellular HGF, FGF2 and TGF-beta3 in crush-injured skeletal muscle. Anim Sci J 83(10):712–717

    Google Scholar 

  • Dumont NA, Wang YX, von Maltazahn J, Pasut A, Bentzinger CF, Brun CE, Rudnicki MA (2015) Dystrophin expression in muscle stem cells regulates their polarity and asymmetric division. Nat Med 21(12):1455–1463

    Article  CAS  PubMed  Google Scholar 

  • Durbeej M, Campbell KP (2002) Muscular dystrophies involving the dystrophin-glycoprotein complex: an overview of current mouse models. Curr Opin Genet Dev 12(3):349–361

    Article  CAS  PubMed  Google Scholar 

  • Duxson MJ, Sheard PW (1995) Formation of new myotubes occurs exclusively at the multiple innervation zones of an embryonic large muscle. Dev Dyn 204(4):391–405

    Article  CAS  PubMed  Google Scholar 

  • Duxson MJ, Ross JJ, Harris AJ (1986) Transfer of differentiated synaptic terminals from primary myotubes to new-formed muscle cells during embryonic development in the rat. Neurosci Lett 71(2):147–152

    Article  CAS  PubMed  Google Scholar 

  • Ervasti JM, Campbell KP (1991) Membrane organization of the dystrophin-glycoprotein complex. Cell 66(6):1121–1131

    Article  CAS  PubMed  Google Scholar 

  • Ervasti JM, Campbell KP (1993) A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol 122(4):809–823

    Article  CAS  PubMed  Google Scholar 

  • Ferrara N, Gerber HP, LeCouter J (2003) The biology of VEGF and its receptors. Nat Med 9(6):669–676

    Article  CAS  PubMed  Google Scholar 

  • Fibbi G, D’Alessio S, Pucci M, Cerletti M, Del RM (2002) Growth factor-dependent proliferation and invasion of muscle satellite cells require the cell-associated fibrinolytic system. Biol Chem 383(1):127–136

    Article  CAS  PubMed  Google Scholar 

  • Flann KL, Rathbone CR, Cole LC, Liu X, Allen RE, Rhoads RP (2014) Hypoxia simultaneously alters satellite cell-mediated angiogenesis and hepatocyte growth factor expression. J Cell Physiol 229(5):572–579

    Article  CAS  PubMed  Google Scholar 

  • Florini JR, Magri KA (1989) Effects of growth factors on myogenic differentiation. Am J Physiol 256(4) Pt 1:C701–C711

    Google Scholar 

  • Fukada S, Morikawa D, Yamamoto Y, Yoshida T, Sumie N, Yamaguchi M, Ito T, Miyagoe-Suzuki Y, Takeda S, Tsujikawa K, Yamamoto H (2010) Genetic background affects properties of satellite cells and mdx phenotypes. Am J Pathol 176(5):2414–2424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fukada S, Ma Y, Ohtani T, Watanabe Y, Murakami S, Yamaguchi M (2013) Isolation, characterization, and molecular regulation of muscle stem cells. Front Physiol 4:317

    Article  PubMed  PubMed Central  Google Scholar 

  • Gal-Levi R, Leshem Y, Aoki S, Nakamura T, Halevy O (1998) Hepatocyte growth factor plays a dual role in regulating skeletal muscle satellite cell proliferation and differentiation. Biochim Biophys Acta 1402(1):39–51

    Article  CAS  PubMed  Google Scholar 

  • Grounds MD (1987) Phagocytosis of necrotic muscle in muscle isografts is influenced by the strain, age, and sex of host mice. J Pathol 153(1):71–82

    Article  CAS  PubMed  Google Scholar 

  • Grounds MD, McGeachie JK (1987) A model of myogenesis in vivo, derived from detailed autoradiographic studies of regenerating skeletal muscle, challenges the concept of quantal mitosis. Cell Tissue Res 250(3):563–569

    Article  CAS  PubMed  Google Scholar 

  • Grounds MD, McGeachie JK (1992) Skeletal muscle regeneration after crush injury in dystrophic mdx mice: an autoradiographic study. Muscle Nerve 15(5):580–586

    Article  CAS  PubMed  Google Scholar 

  • Grounds MD, Garrett KL, Lai MC, Wright WE, Beilharz MW (1992) Identification of skeletal muscle precursor cells in vivo by use of MyoD1 and myogenin probes. Cell Tissue Res 267(1):99–104

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez J, Cabrera D, Brandan E (2014) Glypican-1 regulates myoblast response to HGF via Met in a lipid raft-dependent mechanism: effect on migration of skeletal muscle precursor cells. Skelet Muscle 4(1):5

    Google Scholar 

  • Hall TE, Smith P, Johnston IA (2004) Stages of embryonic development in the Atlantic cod Gadus morhua. J Morphol 259(3):255–270

    Article  PubMed  Google Scholar 

  • Hara M, Tabata K, Suzuki T, Do MK, Mizunoya W, Nakamura M, Nishimura S, Tabata S, Ikeuchi Y, Sunagawa K, Anderson JE, Allen RE, Tatsumi R (2012) Calcium influx through a possible coupling of cation channels impacts skeletal muscle satellite cell activation in response to mechanical stretch. Am J Physiol Cell Physiol 302(12):C1741–C1750

    Article  CAS  PubMed  Google Scholar 

  • Harris AJ, Duxson MJ, Fitzsimons RB, Rieger F (1989) Myonuclear birthdates distinguish the origins of primary and secondary myotubes in embryonic mammalian skeletal muscles. Development 107(4):771–784

    CAS  PubMed  Google Scholar 

  • Hayashi S, Aso H, Watanabe K, Nara H, Rose MT, Ohwada S, Yamaguchi T (2004) Sequence of IGF-I, IGF-II, and HGF expression in regenerating skeletal muscle. Histochem Cell Biol 122(5):427–434

    Article  CAS  PubMed  Google Scholar 

  • Heslop L, Morgan JE, Partridge TA (2000) Evidence for a myogenic stem cell that is exhausted in dystrophic muscle. J Cell Sci 113(Pt 12):2299–2308

    CAS  PubMed  Google Scholar 

  • Huang Z, Chen X, Yu B, He J, Chen D (2012) MicroRNA-27a promotes myoblast proliferation by targeting myostatin. Biochem Biophys Res Commun 423(2):265–269

    Article  CAS  PubMed  Google Scholar 

  • Ieronimakis N, Balasundaram G, Rainey S, Srirangam K, Yablonka-Reuveni Z, Reyes M (2010) Absence of CD34 on murine skeletal muscle satellite cells marks a reversible state of activation during acute injury. PLoS One 5(6):e10920

    Google Scholar 

  • Janke A, Upadhaya R, Snow WM, Anderson JE (2013) A new look at cytoskeletal NOS-1 and â-dystroglycan changes in developing muscle and brain in control and mdx dystrophic mice. Dev Dyn 242(12):1369–1381. doi:10.1002/dvdy.24031

    Google Scholar 

  • Jansen JK, Fladby T (1990) The perinatal reorganization of the innervation of skeletal muscle in mammals. Prog Neurobiol 34(1):39–90

    Article  CAS  PubMed  Google Scholar 

  • Jennische E, Ekberg S, Matejka GL (1993) Expression of hepatocyte growth factor in growing and regenerating rat skeletal muscle. Am J Physiol 265(1) Pt 1;C122–C128

    Google Scholar 

  • Johnson SE, Allen RE (1993) Proliferating cell nuclear antigen (PCNA) is expressed in activated rat skeletal muscle satellite cells. J Cell Physiol 154(1):39–43

    Article  CAS  PubMed  Google Scholar 

  • Johnson SE, Allen RE (1995) Activation of skeletal muscle satellite cells and the role of fibroblast growth factor receptors. Exp Cell Res 219(2):449–453

    Article  CAS  PubMed  Google Scholar 

  • Johnston IA (2006) Environment and plasticity of myogenesis in teleost fish. J Exp Biol 209(Pt 12):2249–2264

    Article  CAS  PubMed  Google Scholar 

  • Johnston IA, Hall TE (2004) Mechanisms of muscle development and responses to temperature change in fish larvae. In: Govoni JJ (ed) Development of form and function in fishes and the question of larval adaptation [40], pp 85–116. American Fisheries Society Symposium. Ref Type: Serial (Book, Monograph)

    Google Scholar 

  • Johnston IA, Lee HT, Macqueen DJ, Paranthaman K, Kawashima C, Anwar A, Kinghorn JR, Dalmay T (2009) Embryonic temperature affects muscle fibre recruitment in adult zebrafish: genome-wide changes in gene and microRNA expression associated with the transition from hyperplastic to hypertrophic growth phenotypes. J Exp Biol 212(Pt 12):1781–1793

    Article  CAS  PubMed  Google Scholar 

  • Johnston IA, Bower NI, Macqueen DJ (2011) Growth and the regulation of myotomal muscle mass in teleost fish. J Exp Biol 214(Pt 10):1617–1628

    Article  CAS  PubMed  Google Scholar 

  • Karalaki M, Fili S, Philippou A, Koutsilieris M (2009) Muscle regeneration: cellular and molecular events. In Vivo 23(5):779–796

    CAS  PubMed  Google Scholar 

  • Kawamura K, Takano K, Suetsugu S, Kurisu S, Yamazaki D, Miki H, Takenawa T, Endo T (2004) N-WASP and WAVE2 acting downstream of phosphatidylinositol 3-kinase are required for myogenic cell migration induced by hepatocyte growth factor. J Biol Chem 279(52):54862–54871

    Article  CAS  PubMed  Google Scholar 

  • Kuang S, Kuroda K, Le GF, Rudnicki MA (2007) Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129(5):999–1010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee AS, Anderson JE, Joya JE, Head SI, Pather N, Kee AJ, Gunning PW, Hardeman EC (2013) Aged skeletal muscle retains the ability to fully regenerate functional architecture. Bioarchitecture 3(2):25–37

    Article  PubMed  PubMed Central  Google Scholar 

  • Leiter JR, Anderson JE (2010) Satellite cells are increasingly refractory to activation by nitric oxide and stretch in aged mouse-muscle cultures. Int J Biochem Cell Biol 42:132–136

    Article  CAS  PubMed  Google Scholar 

  • Leiter JR, Peeler J, Anderson JE (2011) Exercise-induced muscle growth is muscle-specific and age-dependent. Muscle Nerve 43(6):828–838

    Article  PubMed  Google Scholar 

  • Leiter JR, Upadhaya R, Anderson JE (2012) Nitric oxide and voluntary exercise together promote quadriceps hypertrophy and increase vascular density in female 18-mo-old mice. Am J Physiol Cell Physiol 302(9):C1306–C1315

    Article  CAS  PubMed  Google Scholar 

  • Leshem Y, Spicer DB, Gal-Levi R, Halevy O (2000) Hepatocyte growth factor (HGF) inhibits skeletal muscle cell differentiation: a role for the bHLH protein twist and the cdk inhibitor p27. J Cell Physiol 184(1):101–109

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Peng J, Wang G, Yang Q, Yu H, Guo Q, Wang A, Zhao B, Lu S (2008) Effects of local release of hepatocyte growth factor on peripheral nerve regeneration in acellular nerve grafts. Exp Neurol 214(1):47–54

    Article  CAS  PubMed  Google Scholar 

  • Lin DC, Hershey JD, Mattoon JS, Robbins CT (2012) Skeletal muscles of hibernating brown bears are unusually resistant to effects of denervation. J Exp Biol 215(12):2081–2087

    Article  PubMed  Google Scholar 

  • Lomo T (2003) What controls the position, number, size, and distribution of neuromuscular junctions on rat muscle fibers? J Neurocytol 32(5–8):835–848

    Article  CAS  PubMed  Google Scholar 

  • Luo D, Renault VM, Rando TA (2005) The regulation of Notch signaling in muscle stem cell activation and postnatal myogenesis. Semin Cell Dev Biol 16(4-5):612–622

    Article  CAS  PubMed  Google Scholar 

  • Matsumura K, Ohlendieck K, Ionasescu VV, Tome FM, Nonaka I, Burghes AH, Mora M, Kaplan JC, Fardeau M, Campbell KP (1993) The role of the dystrophin-glycoprotein complex in the molecular pathogenesis of muscular dystrophies. Neuromuscul Disord 3(5–6):533–535

    Article  CAS  PubMed  Google Scholar 

  • Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mauro A, Shafiq SA, Milhorat AT (1970) Regeneration of striated muscle, and myogenesis. Ekcerpta Medica, Amsterdam

    Google Scholar 

  • McGeachie JK, Grounds MD (1987) Initiation and duration of muscle precursor replication after mild and severe injury to skeletal muscle of mice. An autoradiographic study. Cell Tissue Res 248(1):125–130

    Article  CAS  PubMed  Google Scholar 

  • McIntosh L, Granberg KE, Briere KM, Anderson JE (1998a) Nuclear magnetic resonance spectroscopy study of muscle growth, mdx dystrophy and glucocorticoid treatments: correlation with repair. NMR Biomed 11(1):1–10

    Article  CAS  PubMed  Google Scholar 

  • McIntosh LM, Baker RE, Anderson JE (1998b) Magnetic resonance imaging of regenerating and dystrophic mouse muscle. Biochem Cell Biol 76(2–3):532–541

    Article  CAS  PubMed  Google Scholar 

  • McIntosh LM, Garrett KL, Megeney L, Rudnicki MA, Anderson JE (1998c) Regeneration and myogenic cell proliferation correlate with taurine levels in dystrophin- and MyoD-deficient muscles. Anat Rec 252(2):311–324

    Article  CAS  PubMed  Google Scholar 

  • Merly F, Lescaudron L, Rouaud T, Crossin F, Gardahaut MF (1999) Macrophages enhance muscle satellite cell proliferation and delay their differentiation. Muscle Nerve 22(6):724–732

    Article  CAS  PubMed  Google Scholar 

  • Merrifield P, Atkinson BG (2000) Phylogenetic diversity of myosin expression in muscle. Microsc Res Tech 50(6):425–429

    Article  CAS  PubMed  Google Scholar 

  • Meyerrochow VB, Ingram JR (1993) Red white muscle distribution and fiber growth dynamics – a comparison between Lacustrine and Riverine populations of the Southern smelt Retropinna-Retropinna Richardson. Proc Biol Sci 252(1334):85–92

    Article  CAS  Google Scholar 

  • Miller KJ, Thaloor D, Matteson S, Pavlath GK (2000) Hepatocyte growth factor affects satellite cell activation and differentiation in regenerating skeletal muscle. Am J Physiol Cell Physiol 278(1):C174–C181

    CAS  PubMed  Google Scholar 

  • Missias AC, Chu GC, Klocke BJ, Sanes JR, Merlie JP (1996) Maturation of the acetylcholine receptor in skeletal muscle: regulation of the AChR gamma-to-epsilon switch. Dev Biol 179(1):223–238

    Article  CAS  PubMed  Google Scholar 

  • Moor AN, Rector ES, Anderson JE (2000) Cell cycle behavior and MyoD expression in response to T3 differ in normal and mdx dystrophic primary muscle cell cultures. Microsc Res Tech 48(3–4):204–212

    Article  CAS  PubMed  Google Scholar 

  • Mylona E, Jones KA, Mills ST, Pavlath GK (2006) CD44 regulates myoblast migration and differentiation. J Cell Physiol 209(2):314–321

    Article  CAS  PubMed  Google Scholar 

  • O’Brien LE, Tang K, Kats ES, Schutz-Geschwender A, Lipschutz JH, Mostov KE (2004) ERK and MMPs sequentially regulate distinct stages of epithelial tubule development. Dev Cell 7(1):21–32

    Article  PubMed  Google Scholar 

  • Paul AC, Sheard PW, Duxson MJ (2004) Development of a mammalian series-fibered muscle. Anat Rec A Discov Mol Cell Evol Biol 278(2):571–578

    Article  PubMed  Google Scholar 

  • Peplow PV, Chatterjee MP (2013) A review of the influence of growth factors and cytokines in in vitro human keratinocyte migration. Cytokine 62(1):1–21

    Article  CAS  PubMed  Google Scholar 

  • Pezzementi L, Chatonnet A (2010) Evolution of cholinesterases in the animal kingdom. Chem Biol Interact 187:27–33. Ref Type: Journal (Full)

    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(3):427–441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Price ER, Bauchinger U, Zajac DM, Cerasale DJ, McFarlan JT, Gerson AR, McWilliams SR, Guglielmo CG (2011) Migration- and exercise-induced changes to flight muscle size in migratory birds and association with IGF1 and myostatin mRNA expression. J Exp Biol 214(17):2823–2831

    Article  CAS  PubMed  Google Scholar 

  • Ramani VC, Purushothaman A, Stewart MD, Thompson CA, Vlodavsky I, Au JL, Sanderson RD (2013) The heparanase/syndecan-1 axis in cancer: mechanisms and therapies. FEBS J 280(10):2294–2306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rapraeger AC (2000) Syndecan-regulated receptor signaling. J Cell Biol 149(5):995–998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reed SA, Sandesara PB, Senf SM, Judge AR (2012) Inhibition of FoxO transcriptional activity prevents muscle fiber atrophy during cachexia and induces hypertrophy. FASEB J 26(3):987–1000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roux KJ, Crisp ML, Liu Q, Kim D, Kozlov S, Stewart CL, Burke B (2009) Nesprin 4 is an outer nuclear membrane protein that can induce kinesin-mediated cell polarization. Proc Natl Acad Sci U S A 106(7):2194–2199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rudnicki MA, Le GF, McKinnell I, Kuang S (2008) The molecular regulation of muscle stem cell function. Cold Spring Harb Symp Quant Biol 73:323–331

    Article  CAS  PubMed  Google Scholar 

  • Sakaguchi S, Shono JI, Suzuki T, Sawano S, Anderson JE, Do MK, Ohtsubo H, Mizunoya W, Sato Y, Nakamura M, Furuse M, Yamada K, Ikeuchi Y, Tatsumi R (2014) Implication of anti-inflammatory macrophages in regenerative moto-neuritogenesis: promotion of myoblast migration and neural chemorepellent semaphorin 3A expression in injured muscle. Int J Biochem Cell Biol 54:272–285

    Article  CAS  PubMed  Google Scholar 

  • Seale P, Rudnicki MA (2000) A new look at the origin, function, and “stem-cell” status of muscle satellite cells. Dev Biol 218(2):115–124

    Article  CAS  PubMed  Google Scholar 

  • Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA (2000) Pax7 is required for the specification of myogenic satellite cells. Cell 102(6):777–786

    Article  CAS  PubMed  Google Scholar 

  • Sebastian S, Sreenivas P, Sambasivan R, Cheedipudi S, Kandalla P, Pavlath GK, Dhawan J (2009) MLL5, a trithorax homolog, indirectly regulates H3K4 methylation, represses cyclin A2 expression, and promotes myogenic differentiation. Proc Natl Acad Sci U S A 106(12):4719–4724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sellathurai J, Cheedipudi S, Dhawan J, Schroder HD (2013) A novel in vitro model for studying quiescence and activation of primary isolated human myoblasts. Plos One 8(5):e64067

    Google Scholar 

  • Sheehan SM, Tatsumi R, Temm-Grove CJ, Allen RE (2000) HGF is an autocrine growth factor for skeletal muscle satellite cells in vitro. Muscle Nerve 23(2):239–245

    Article  CAS  PubMed  Google Scholar 

  • Siegel AL, Atchison K, Fisher KE, Davis GE, Cornelison DD (2009) 3D timelapse analysis of muscle satellite cell motility. Stem Cells 27(10):2527–2538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siegel AL, Kuhlmann PK, Cornelison DD (2011) Muscle satellite cell proliferation and association: new insights from myofiber time-lapse imaging. Skelet Muscle 1(1):1–7

    Article  Google Scholar 

  • Smith CK, Janney MJ, Allen RE (1994) Temporal expression of myogenic regulatory genes during activation, proliferation, and differentiation of rat skeletal muscle satellite cells. J Cell Physiol 159(2):379–385

    Article  CAS  PubMed  Google Scholar 

  • Smythe GM, Shavlakadze T, Roberts P, Davies MJ, McGeachie JK, Grounds MD (2008) Age influences the early events of skeletal muscle regeneration: studies of whole muscle grafts transplanted between young (8 weeks) and old (13–21 months) mice. Exp Gerontol 43(6):550–562

    Article  CAS  PubMed  Google Scholar 

  • Snow WM, Anderson JE, Jakobson LS (2013a) Neuropsychological and neurobehavioral functioning in Duchenne muscular dystrophy: a review. Neurosci Biobehav Rev 37(5):743–752

    Article  PubMed  Google Scholar 

  • Snow WM, Fry M, Anderson JE (2013b) Increased density of dystrophin protein in the lateral versus the vermal mouse cerebellum. Cell Mol Neurobiol 33(4):513–520

    Article  CAS  PubMed  Google Scholar 

  • Srivastava S, Mishra RK, Dhawan J (2010) Regulation of cellular chromatin state: insights from quiescence and differentiation. Organogenesis 6(1):37–47

    Article  PubMed  PubMed Central  Google Scholar 

  • Stark DA, Karvas RM, Siegel AL, Cornelison DD (2011) Eph/ephrin interactions modulate muscle satellite cell motility and patterning. Development 138(24):5279–5289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Starr DA, Fischer JA (2005) KASH ’n Karry: the KASH domain family of cargo-specific cytoskeletal adaptor proteins. Bioessays 27(11):1136–1146

    Article  CAS  PubMed  Google Scholar 

  • Steinbacher P, Marschallinger J, Obermayer A, Neuhofer A, Sanger AM, Stoiber W (2011) Temperature-dependent modification of muscle precursor cell behaviour is an underlying reason for lasting effects on muscle cellularity and body growth of teleost fish. J Exp Biol 214(Pt 11):1791–1801

    Article  PubMed  PubMed Central  Google Scholar 

  • Subramaniam S, Sreenivas P, Cheedipudi S, Reddy VR, Shashidhara LS, Chilukoti RK, Mylavarapu M, Dhawan J (2013) Distinct transcriptional networks in quiescent myoblasts: a role for Wnt signaling in reversible vs. irreversible arrest. Plos One 8(6):e65097

    Google Scholar 

  • Sugiura T, Kawaguchi Y, Soejima M, Katsumata Y, Gono T, Baba S, Kawamoto M, Murakawa Y, Yamanaka H, Hara M (2010) Increased HGF and c-Met in muscle tissues of polymyositis and dermatomyositis patients: beneficial roles of HGF in muscle regeneration. Clin Immunol 136(3):387–399

    Article  CAS  PubMed  Google Scholar 

  • Sumino Y, Hirata Y, Sato F, Mimata H (2007) Growth mechanism of satellite cells in human urethral rhabdosphincter. Neurourol Urodyn 26(4):552–561

    Article  CAS  PubMed  Google Scholar 

  • Suzuki S, Yamanouchi K, Soeta C, Katakai Y, Harada R, Naito K, Tojo H (2002) Skeletal muscle injury induces hepatocyte growth factor expression in spleen. Biochem Biophys Res Commun 292(3):709–714

    Article  CAS  PubMed  Google Scholar 

  • Suzuki T, Do MK, Sato Y, Ojima K, Hara M, Mizunoya W, Nakamura M, Furuse M, Ikeuchi Y, Anderson JE, Tatsumi R (2013) Comparative analysis of semaphorin 3A in soleus and EDL muscle satellite cells in vitro toward understanding its role in modulating myogenin expression. Int J Biochem Cell Biol 45(2):476–482

    Article  CAS  PubMed  Google Scholar 

  • Tatsumi R (2010) Mechano-biology of skeletal muscle hypertrophy and regeneration: possible mechanism of stretch-induced activation of resident myogenic stem cells. Anim Sci J 81(1):11–20

    Article  CAS  PubMed  Google Scholar 

  • Tatsumi R, Allen RE (2004) Active hepatocyte growth factor is present in skeletal muscle extracellular matrix. Muscle Nerve 30(5):654–658

    Article  CAS  PubMed  Google Scholar 

  • Tatsumi R, Anderson JE, Nevoret CJ, Halevy O, Allen RE (1998) HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev Biol 194(1):114–128

    Article  CAS  PubMed  Google Scholar 

  • Tatsumi R, Sheehan SM, Iwasaki H, Hattori A, Allen RE (2001) Mechanical stretch induces activation of skeletal muscle satellite cells in vitro. Exp Cell Res 267(1):107–114

    Article  CAS  PubMed  Google Scholar 

  • Tatsumi R, Hattori A, Ikeuchi Y, Anderson JE, Allen RE (2002) Release of hepatocyte growth factor from mechanically stretched skeletal muscle satellite cells and role of pH and nitric oxide. Mol Biol Cell 13(8):2909–2918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tatsumi R, Sankoda Y, Anderson JE, Sato Y, Mizunoya W, Shimizu N, Suzuki T, Yamada M, Rhoads RP Jr, Ikeuchi Y, Allen RE (2009a) Possible implication of satellite cells in regenerative motoneuritogenesis: HGF upregulates neural chemorepellent Sema3A during myogenic differentiation. Am J Physiol Cell Physiol 297(2):C238–C252

    Article  CAS  PubMed  Google Scholar 

  • Tatsumi R, Wuollet al, Tabata K, Nishimura S, Tabata S, Mizunoya W, Ikeuchi Y, Allen RE (2009b) A role for calcium-calmodulin in regulating nitric oxide production during skeletal muscle satellite cell activation. Am J Physiol Cell Physiol 296(4):C922–C929

    Google Scholar 

  • Thomas M, Langley B, Berry C, Sharma M, Kirk S, Bass J, Kambadur R (2000) Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. J Biol Chem 275(51):40235–40243

    Article  CAS  PubMed  Google Scholar 

  • Trusolino L, Bertotti A, Comoglio PM (2010) MET signalling: principles and functions in development, organ regeneration and cancer. Nat Rev Mol Cell Biol 11(12):834–848

    Article  CAS  PubMed  Google Scholar 

  • Tzur YB, Wilson KL, Gruenbaum Y (2006) SUN-domain proteins: ‘Velcro’ that links the nucleoskeleton to the cytoskeleton. Nat Rev Mol Cell Biol 7(10):782–788

    Article  CAS  PubMed  Google Scholar 

  • Villena J, Brandan E (2004) Dermatan sulfate exerts an enhanced growth factor response on skeletal muscle satellite cell proliferation and migration. J Cell Physiol 198(2):169–178

    Article  CAS  PubMed  Google Scholar 

  • Volonte D, Liu Y, Galbiati F (2005) The modulation of caveolin-1 expression controls satellite cell activation during muscle repair. FASEB J 19(2):237–239

    CAS  PubMed  Google Scholar 

  • Watanabe I, Okada S (1967) Stationary phase of cultured mammalian cells (L5178Y). J Cell Biol 35(2):285–294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Webster MT, Fan CM (2013) c-MET regulates myoblast motility and myocyte fusion during adult skeletal muscle regeneration. PLoS One 8(11):e81757

    Google Scholar 

  • Williams RS, Annex BH (2004) Plasticity of myocytes and capillaries: a possible coordinating role for VEGF. Circ Res 95(1):7–8

    Article  CAS  PubMed  Google Scholar 

  • Wozniak AC, Anderson JE (2005) Single-fiber isolation and maintenance of satellite cell quiescence. Biochem Cell Biol 83(5):674–676

    Article  CAS  PubMed  Google Scholar 

  • Wozniak AC, Anderson JE (2007) Nitric oxide-dependence of satellite stem cell activation and quiescence on normal skeletal muscle fibers. Dev Dyn 236(1):240–250

    Article  CAS  PubMed  Google Scholar 

  • Wozniak AC, Anderson JE (2009) The dynamics of the nitric oxide release-transient from stretched muscle cells. Int J Biochem Cell Biol 41(3):625–631

    Article  CAS  PubMed  Google Scholar 

  • Wozniak AC, Pilipowicz O, Yablonka-Reuveni Z, Greenway S, Craven S, Scott E, Anderson JE (2003) C-met expression and mechanical activation of satellite cells on cultured muscle fibers. J Histochem Cytochem 51(11):1437–1445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wozniak AC, Kong J, Bock E, Pilipowicz O, Anderson JE (2005) Signaling satellite-cell activation in skeletal muscle: markers, models, stretch, and potential alternate pathways. Muscle Nerve 31(3):283–300

    Article  CAS  PubMed  Google Scholar 

  • Wund MA, Baker JA, Clancy B, Golub JL, Foster SA (2008) A test of the “Flexible stem” model of evolution: ancestral plasticity, genetic accommodation, and morphological divergence in the threespine stickleback radiation. Am Nat 172:449–462

    Article  PubMed  Google Scholar 

  • Xie G, Karaca G, Swiderska-Syn M, Michelotti GA, Kruger L, Chen Y, Premont RT, Choi SS, Diehl AM (2013) Cross-talk between notch and hedgehog regulates hepatic stellate cell fate. Hepatology 58(5):1801–1813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yablonka-Reuveni Z (2011) The skeletal muscle satellite cell: still young and fascinating at 50. J Histochem Cytochem 59(12):1041–1059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamada M, Tatsumi R, Yamanouchi K, Hosoyama T, Shiratsuchi S, Sato A, Mizunoya W, Ikeuchi Y, Furuse M, Allen RE (2010) High concentrations of HGF inhibit skeletal muscle satellite cell proliferation in vitro by inducing expression of myostatin: a possible mechanism for reestablishing satellite cell quiescence in vivo. Am J Physiol Cell Physiol 298(3):C465–C476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Anderson JE (2014) Satellite cell activation and populations on single muscle-fiber cultures from adult zebrafish (Danio rerio). J Exp Biol 217(Pt 11):1910–1917

    Article  PubMed  Google Scholar 

  • Zhang X, Xu R, Zhu B, Yang X, Ding X, Duan S, Xu T, Zhuang Y, Han M (2007) Syne-1 and Syne-2 play crucial roles in myonuclear anchorage and motor neuron innervation. Development 134(5):901–908

    Article  CAS  PubMed  Google Scholar 

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Anderson, J.E. (2016). Hepatocyte Growth Factor and Satellite Cell Activation. In: White, J., Smythe, G. (eds) Growth Factors and Cytokines in Skeletal Muscle Development, Growth, Regeneration and Disease. Advances in Experimental Medicine and Biology, vol 900. Springer, Cham. https://doi.org/10.1007/978-3-319-27511-6_1

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