In vitro indeterminate teleost myogenesis appears to be dependent on Pax3

  • Jacob Michael Froehlich
  • Nicholas J. Galt
  • Matthew J. Charging
  • Ben M. Meyer
  • Peggy R. BigaEmail author


The zebrafish (Danio rerio) has been used extensively as a model system for developmental studies but, unlike most teleost fish, it grows in a determinate-like manner. A close relative, the giant danio (Devario cf. aequipinnatus), grows indeterminately, displaying both hyperplasia and hypertrophy of skeletal myofibers as an adult. To better understand adult muscle hyperplasia, a postlarval/postnatal process that closely resembles secondary myogenesis during development, we characterized the expression of Pax3/7, c-Met, syndecan-4, Myf5, MyoD1, myogenin, and myostatin during in vitro myogenesis, a technique that allows for the complete progression of myogenic precursor cells to myotubes. Pax7 appears to be expressed only in newly activated MPCs while Pax3 is expressed through most of the myogenic program, as are c-Met and syndecan-4. MyoD1 appears important in all stages of myogenesis, while Myf5 is likely expressed at low to background levels, and myogenin expression is enriched in myotubes. Myostatin, like MyoD1, appears to be ubiquitous at all stages. This is the first comprehensive report of key myogenic factor expression patterns in an indeterminate teleost, one that strongly suggests that Pax3 and/or Myf5 may be involved in the regulation of this paradigm. Further, it validates this species as a model organism for studying adult myogenesis in vitro, especially mechanisms underlying nascent myofiber recruitment.


Myogenesis Zebrafish Giant danio Indeterminate growth Pax3 



We would like to thank Drs. Josep Planas and Juan Castillo for their assistance and direction with the primary myoblast cultures, as well as Zachary Fowler, Brooke Franzen, Nathan Froehlich, Kira Marshall, Ethan Remily, and Sinibaldo Romero for their technical assistance in isolating MPCs from numerous fish. Thanks are also due to Dr. Jodie Haring, Dr. Joseph Provost, and Naomi Light for their assistance in cell imaging. Funds for this work were provided to PRB by the Center for Protease Research NIH Grant # 2P20 RR015566, NIH NIAMS Grant # R03AR055350, and NDSU Advance FORWARD NSF Grant #HRD-0811239. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the NIH.


  1. Alfei L.; Maggi F.; Parvopassu F.; Bertoncello G.; De Vita R. Postlarval muscle growth in fish: a DNA flow cytometric and morphometric analysis. Basic Appl Histochem 33(2): 147–158; 1989.PubMedGoogle Scholar
  2. Allen R. E.; Sheehan S. M.; Taylor R. G.; Kendall T. L.; Rice G. M. Hepatocyte growth factor activates quiescent skeletal muscle satellite cells in vitro. J. Cell. Physiol. 165(2): 307–312; 1995.PubMedCrossRefGoogle Scholar
  3. Anastasi S.; Giordano S.; Sthandier O.; Gambarotta G.; Maione R.; Comoglio P.; Amati P. 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; 1997.PubMedCrossRefGoogle Scholar
  4. Andres V.; Walsh K. Myogenin expression, cell cycle withdrawal, and phenotypic differentiation are temporally separable events that precede cell fusion upon myogenesis. J. Cell Biol. 132(4): 657–666; 1996.PubMedCrossRefGoogle Scholar
  5. Beauchamp J. R.; Heslop L.; Yu D. S.; Tajbakhsh S.; Kelly R. G.; Wernig A.; Buckingham M. E.; Partridge T. A.; Zammit P. S. Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J. Cell Biol. 151(6): 1221–1234; 2000.PubMedCrossRefGoogle Scholar
  6. Biga P. R.; Cain K. D.; Hardy R. W.; Schelling G. T.; Overturf K.; Roberts S. B.; Goetz F. W.; Ott T. L. Growth hormone differentially regulates muscle myostatin1 and −2 and increases circulating cortisol in rainbow trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 138(1): 32–41; 2004.PubMedCrossRefGoogle Scholar
  7. Biga P. R.; Goetz F. W. Zebrafish and giant danio as models for muscle growth: determinate vs. indeterminate growth as determined by morphometric analysis. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291(5): R1327–1337; 2006.PubMedCrossRefGoogle Scholar
  8. Biressi S.; Molinaro M.; Cossu G. Cellular heterogeneity during vertebrate skeletal muscle development. Dev. Biol. 308(2): 281–293; 2007.PubMedCrossRefGoogle Scholar
  9. Biressi S.; Rando T. A. Heterogeneity in the muscle satellite cell population. Semin. Cell Dev. Biol. 21(8): 845–854; 2010.PubMedCrossRefGoogle Scholar
  10. Bosnakovski D.; Xu Z.; Li W.; Thet S.; Cleaver O.; Perlingeiro R. C.; Kyba M. Prospective isolation of skeletal muscle stem cells with a Pax7 reporter. 3204 12: 3194; 2008.Google Scholar
  11. Boutet S. C.; Cheung T. H.; Quach N. L.; Liu L.; Prescott S. L.; Edalati A.; Iori K.; Rando T. A. Alternative polyadenylation mediates microRNA regulation of muscle stem cell function. Cell Stem Cell 10(3): 327–336; 2012.PubMedCrossRefGoogle Scholar
  12. Bower N. I.; Johnston I. A. Paralogs of Atlantic salmon myoblast determination factor genes are distinctly regulated in proliferating and differentiating myogenic cells. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298(6): R1615–1626; 2010.PubMedCrossRefGoogle Scholar
  13. Buckingham M.; Vincent S. D. Distinct and dynamic myogenic populations in the vertebrate embryo. Curr. Opin. Genet. Dev. 19(5): 444–453; 2009.PubMedCrossRefGoogle Scholar
  14. Cao Y.; Kumar R. M.; Penn B. H.; Berkes C. A.; Kooperberg C.; Boyer L. A.; Young R. A.; Tapscott S. J. Global and gene-specific analyses show distinct roles for Myod and Myog at a common set of promoters. EMBO J. 25(3): 502–511; 2006.PubMedCrossRefGoogle Scholar
  15. Charbonnier F.; Gaspera B. D.; Armand A. S.; Van der Laarse W. J.; Launay T.; Becker C.; Gallien C. L.; Chanoine C. Two myogenin-related genes are differentially expressed in Xenopus laevis myogenesis and differ in their ability to transactivate muscle structural genes. J. Biol. Chem. 277(2): 1139–1147; 2002.PubMedCrossRefGoogle Scholar
  16. Charge S. B.; Rudnicki M. A. Cellular and molecular regulation of muscle regeneration. Physiol. Rev. 84(1): 209–238; 2004.PubMedCrossRefGoogle Scholar
  17. Codina M.; Garcia dela serrana D.; Sanchez-Gurmaches J.; Montserrat N.; Chistyakova O.; Navarro I.; Gutierrez J. Metabolic and mitogenic effects of IGF-II in rainbow trout (Oncorhynchus mykiss) myocytes in culture and the role of IGF-II in the PI3K/Akt and MAPK signalling pathways. Gen. Comp. Endocrinol. 157(2): 116–124; 2008.PubMedCrossRefGoogle Scholar
  18. Collins C. A.; Olsen I.; Zammit P. S.; Heslop L.; Petrie A.; Partridge T. A.; Morgan J. E. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 122(2): 289–301; 2005.PubMedCrossRefGoogle Scholar
  19. Conboy I. M.; Rando T. A. The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev. Cell 3(3): 397–409; 2002.PubMedCrossRefGoogle Scholar
  20. Cornelison D. D.; Filla M. S.; Stanley H. M.; Rapraeger A. C.; Olwin B. B. 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; 2001.PubMedCrossRefGoogle Scholar
  21. Cornelison D. D.; Wilcox-Adelman S. A.; Goetinck P. F.; Rauvala H.; Rapraeger A. C.; Olwin B. B. Essential and separable roles for Syndecan-3 and Syndecan-4 in skeletal muscle development and regeneration. Genes Dev. 18(18): 2231–2236; 2004.PubMedCrossRefGoogle Scholar
  22. Cornelison D. D.; Wold B. J. Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev. Biol. 191(2): 270–283; 1997.PubMedCrossRefGoogle Scholar
  23. Cossu G.; Biressi S. Satellite cells, myoblasts and other occasional myogenic progenitors: possible origin, phenotypic features and role in muscle regeneration. Semin. Cell Dev. Biol. 16(4–5): 623–631; 2005.PubMedGoogle Scholar
  24. Coutelle O.; Blagden C. S.; Hampson R.; Halai C.; Rigby P. W.; Hughes S. M. Hedgehog signalling is required for maintenance of myf5 and myoD expression and timely terminal differentiation in zebrafish adaxial myogenesis. Dev. Biol. 236(1): 136–150; 2001.PubMedCrossRefGoogle Scholar
  25. Day K.; Paterson B.; Yablonka-Reuveni Z. A distinct profile of myogenic regulatory factor detection within Pax7+ cells at S phase supports a unique role of Myf5 during posthatch chicken myogenesis. Dev. Dyn. 238(4): 1001–1009; 2009.PubMedCrossRefGoogle Scholar
  26. Fauconneau B.; Paboeuf G. Effect of fasting and refeeding on in vitro muscle cell proliferation in rainbow trout (Oncorhynchus mykiss). Cell Tissue Res. 301(3): 459–463; 2000.PubMedCrossRefGoogle Scholar
  27. Funkenstein B.; Balas V.; Skopal T.; Radaelli G.; Rowlerson A. Long-term culture of muscle explants from Sparus aurata. Tissue Cell 38(6): 399–415; 2006.PubMedCrossRefGoogle Scholar
  28. Gayraud-Morel B.; Chretien F.; Jory A.; Sambasivan R.; Negroni E.; Flamant P.; Soubigou G.; Coppee J. Y.; Di Santo J.; Cumano A.; Mouly V.; Tajbakhsh S. Myf5 haploinsufficiency reveals distinct cell fate potentials for adult skeletal muscle stem cells. J. Cell Sci. 125(Pt 7): 1738–1749; 2012.PubMedCrossRefGoogle Scholar
  29. Greenlee A.; Dodson M.; Yablonka-Reuveni Z.; Kersten C.; Cloud J. In vitro differentiation of myoblast from skeletal muscle of rainbow trout. J. Fish Biol. 46: 731–747; 1995.Google Scholar
  30. Halevy O.; Piestun Y.; Allouh M. Z.; Rosser B. W.; Rinkevich Y.; Reshef R.; Rozenboim I.; Wleklinski-Lee M.; Yablonka-Reuveni Z. Pattern of Pax7 expression during myogenesis in the posthatch chicken establishes a model for satellite cell differentiation and renewal. Dev. Dyn. 231(3): 489–502; 2004.PubMedCrossRefGoogle Scholar
  31. Hawke T. J.; Garry D. J. Myogenic satellite cells: physiology to molecular biology. J. Appl. Physiol. 91(2): 534–551; 2001.PubMedGoogle Scholar
  32. Hightower L. E.; Renfro J. L. Recent applications of fish cell culture to biomedical research. J. Exp. Zool. 248(3): 290–302; 1988.PubMedCrossRefGoogle Scholar
  33. Hinits Y.; Osborn D. P.; Hughes S. M. Differential requirements for myogenic regulatory factors distinguish medial and lateral somitic, cranial and fin muscle fibre populations. Development 136(3): 403–414; 2009.PubMedCrossRefGoogle Scholar
  34. Johnston I. A.; Manthri S.; Smart A.; Campbell P.; Nickell D.; Alderson R. Plasticity of muscle fibre number in seawater stages of Atlantic salmon in response to photoperiod manipulation. J. Exp. Biol. 206(Pt 19): 3425–3435; 2003.PubMedCrossRefGoogle Scholar
  35. Johnston I. A.; McLay H. A.; Abercromby M.; Robins D. Phenotypic plasticity of early myogenesis and satellite cell numbers in Atlantic salmon spawning in upland and lowland tributaries of a river system. J. Exp. Biol. 203(Pt 17): 2539–2552; 2000.PubMedGoogle Scholar
  36. Kirkpatrick L. J.; Yablonka-Reuveni Z.; Rosser B. W. Retention of Pax3 expression in satellite cells of muscle spindles. J. Histochem. Cytochem. 58(4): 317–327; 2010.PubMedCrossRefGoogle Scholar
  37. Kishioka Y.; Thomas M.; Wakamatsu J.; Hattori A.; Sharma M.; Kambadur R.; Nishimura T. Decorin enhances the proliferation and differentiation of myogenic cells through suppressing myostatin activity. J. Cell. Physiol. 215(3): 856–867; 2008.PubMedCrossRefGoogle Scholar
  38. Knudsen B. S.; Zhao P.; Resau J.; Cottingham S.; Gherardi E.; Xu E.; Berghuis B.; Daugherty J.; Grabinski T.; Toro J.; Giambernardi T.; Skinner R. S.; Gross M.; Hudson E.; Kort E.; Lengyel E.; Ventura A.; West R. A.; Xie Q.; Hay R.; Woude G. V.; Cao B. A novel multipurpose monoclonal antibody for evaluating human c-Met expression in preclinical and clinical settings. Appl. Immunohistochem. Mol. Morphol. 17(1): 57–67; 2009.PubMedCrossRefGoogle Scholar
  39. Koumans J. T. M.; Akster H.; Dulos G.; Osse J. W. M. Myosatellite cells of Cyprinid carpio (Teleosti) in vitro: isolation, recognition, and differentiation. Cell Tissue Res. 261: 173–181; 1990.CrossRefGoogle Scholar
  40. Kuang S.; Kuroda K.; Le Grand F.; Rudnicki M. A. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129(5): 999–1010; 2007.PubMedCrossRefGoogle Scholar
  41. Le Grand F.; Rudnicki M. A. Skeletal muscle satellite cells and adult myogenesis. Curr. Opin. Cell Biol. 19(6): 628–633; 2007.PubMedCrossRefGoogle Scholar
  42. Lemischka I. The power of stem cells reconsidered? Proc. Natl. Acad. Sci. U. S. A. 96(25): 14193–14195; 1999.PubMedCrossRefGoogle Scholar
  43. Lepper C.; Conway S. J.; Fan C. M. Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature 460(7255): 627–631; 2009.PubMedCrossRefGoogle Scholar
  44. Levesque H. M.; Shears M. A.; Fletcher G. L.; Moon T. W. Myogenesis and muscle metabolism in juvenile Atlantic salmon (Salmo salar) made transgenic for growth hormone. J. Exp. Biol. 211(Pt 1): 128–137; 2008.PubMedCrossRefGoogle Scholar
  45. Macqueen D. J.; Johnston I. A. An update on MyoD evolution in teleosts and a proposed consensus nomenclature to accommodate the tetraploidization of different vertebrate genomes. PLoS One 3(2): e1567; 2008.PubMedCrossRefGoogle Scholar
  46. Matschak T. W.; Stickland N. C. The growth of Atlantic salmon (Salmo salar L.) myosatellite cells in culture at two different temperatures. Experientia 51(3): 260–266; 1995.PubMedCrossRefGoogle Scholar
  47. McCroskery S.; Thomas M.; Maxwell L.; Sharma M.; Kambadur R. Myostatin negatively regulates satellite cell activation and self-renewal. J. Cell Biol. 162(6): 1135–1147; 2003.PubMedCrossRefGoogle Scholar
  48. McFarlane C.; Hennebry A.; Thomas M.; Plummer E.; Ling N.; Sharma M.; Kambadur R. Myostatin signals through Pax7 to regulate satellite cell self-renewal. Exp. Cell Res. 314(2): 317–329; 2008.PubMedCrossRefGoogle Scholar
  49. McFarland D. C.; Velleman S. G.; Pesall J. E.; Liu C. Effect of myostatin on turkey myogenic satellite cells and embryonic myoblasts. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 144(4): 501–508; 2006.PubMedCrossRefGoogle Scholar
  50. McPherron A. C.; Lawler A. M.; Lee S. J. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387(6628): 83–90; 1997.PubMedCrossRefGoogle Scholar
  51. Meyer A.; Biermann C. H.; Orti G. The phylogenetic position of the zebrafish (Danio rerio), a model system in developmental biology: an invitation to the comparative method. Proc. Biol. Sci. 252(1335): 231–236; 1993.PubMedCrossRefGoogle Scholar
  52. Miura T.; Kishioka Y.; Wakamatsu J.; Hattori A.; Hennebry A.; Berry C. J.; Sharma M.; Kambadur R.; Nishimura T. Decorin binds myostatin and modulates its activity to muscle cells. Biochem. Biophys. Res. Commun. 340(2): 675–680; 2006.PubMedCrossRefGoogle Scholar
  53. Mommsen T. P. Paradigms of growth in fish. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 129(2–3): 207–219; 2001.PubMedCrossRefGoogle Scholar
  54. Moss F. P.; Leblond C. P. Satellite cells as the source of nuclei in muscles of growing rats. Anat. Rec. 170(4): 421–435; 1971.PubMedCrossRefGoogle Scholar
  55. Mulvaney D. R.; Cyrino J. E. P. Establishment of channel catfish satellite cell cultures. Basic Appl. Myol. 5(1): 65–70; 1995.Google Scholar
  56. Nabeshima Y.; Hanaoka K.; Hayasaka M.; Esumi E.; Li S.; Nonaka I. Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 6437: 532–535; 1993.CrossRefGoogle Scholar
  57. Nishimura T.; Oyama K.; Kishioka Y.; Wakamatsu J.; Hattori A. Spatiotemporal expression of decorin and myostatin during rat skeletal muscle development. Biochem. Biophys. Res. Commun. 361(4): 896–902; 2007.PubMedCrossRefGoogle Scholar
  58. Nyholm M. K.; Wu S. F.; Dorsky R. I.; Grinblat Y. The zebrafish zic2a–zic5 gene pair acts downstream of canonical Wnt signaling to control cell proliferation in the developing tectum. Development 134(4): 735–746; 2007.PubMedCrossRefGoogle Scholar
  59. Olguin H. C.; Olwin B. B. Pax-7 up-regulation inhibits myogenesis and cell cycle progression in satellite cells: a potential mechanism for self-renewal. Dev. Biol. 275(2): 375–388; 2004.PubMedCrossRefGoogle Scholar
  60. Ostbye T. K.; Bardal T.; Vegusdal A.; Frang O. T.; Kjorsvik E.; Andersen O. Molecular cloning of the Atlantic salmon activin receptor IIB cDNA—localization of the receptor and myostatin in vivo and in vitro in muscle cells. Comp. Biochem. Physiol. Part D Genomics Proteomics 2(2): 101–111; 2007.PubMedCrossRefGoogle Scholar
  61. Oustanina S.; Hause G.; Braun T. Pax7 directs postnatal renewal and propagation of myogenic satellite cells but not their specification. EMBO J. 23(16): 3430–3439; 2004.PubMedCrossRefGoogle Scholar
  62. Patterson S. E.; Mook L. B.; Devoto S. H. Growth in the larval zebrafish pectoral fin and trunk musculature. Dev. Dyn. 237(2): 307–315; 2008.PubMedCrossRefGoogle Scholar
  63. Relaix F.; Montarras D.; Zaffran S.; Gayraud-Morel B.; Rocancourt D.; Tajbakhsh S.; Mansouri A.; Cumano A.; Buckingham M. Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. J. Cell Biol. 172(1): 91–102; 2006.PubMedCrossRefGoogle Scholar
  64. Relaix F.; Rocancourt D.; Mansouri A.; Buckingham M. Divergent functions of murine Pax3 and Pax7 in limb muscle development. Genes Dev. 18(9): 1088–1105; 2004.PubMedCrossRefGoogle Scholar
  65. Relaix F.; Rocancourt D.; Mansouri A.; Buckingham M. A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435(7044): 948–953; 2005.PubMedCrossRefGoogle Scholar
  66. Rescan P. Y. Muscle growth patterns and regulation during fish ontogeny. Gen. Comp. Endocrinol. 142(1–2): 111–116; 2005.PubMedCrossRefGoogle Scholar
  67. Rescan P. Y.; Gauvry L.; Paboeuf G. A gene with homology to myogenin is expressed in developing myotomal musculature of the rainbow trout and in vitro during the conversion of myosatellite cells to myotubes. FEBS Lett. 362(1): 89–92; 1995.PubMedCrossRefGoogle Scholar
  68. Roberts S. B.; Goetz F. W. Myostatin protein and RNA transcript levels in adult and developing brook trout. Mol. Cell. Endocrinol. 210(1–2): 9–20; 2003.PubMedCrossRefGoogle Scholar
  69. Sabourin L. A.; Girgis-Gabardo A.; Seale P.; Asakura A.; Rudnicki M. A. Reduced differentiation potential of primary MyoD−/− myogenic cells derived from adult skeletal muscle. J. Cell Biol. 144(4): 631–643; 1999.PubMedCrossRefGoogle Scholar
  70. Scaal M.; Wiegreffe C. Somite compartments in anamniotes. Anat. Embryol. (Berl) 211 Suppl 1: 9–19; 2006.Google Scholar
  71. Scrable H. J.; Johnson D. K.; Rinchik E. M.; Cavenee W. K. Rhabdomyosarcoma-associated locus and MYOD1 are syntenic but separate loci on the short arm of human chromosome 11. Proc. Natl. Acad. Sci. U. S. A. 87(6): 2182–2186; 1990.PubMedCrossRefGoogle Scholar
  72. Seale P.; Ishibashi J.; Scime A.; Rudnicki M. A. Pax7 is necessary and sufficient for the myogenic specification of CD45+:Sca1+ stem cells from injured muscle. PLoS Biol. 2(5): E130; 2004.PubMedCrossRefGoogle Scholar
  73. Seale P.; Rudnicki M. A. A new look at the origin, function, and "stem-cell" status of muscle satellite cells. Dev. Biol. 218(2): 115–124; 2000.PubMedCrossRefGoogle Scholar
  74. Seale P.; Sabourin L. A.; Girgis-Gabardo A.; Mansouri A.; Gruss P.; Rudnicki M. A. Pax7 is required for the specification of myogenic satellite cells. Cell 102(6): 777–786; 2000.PubMedCrossRefGoogle Scholar
  75. Seger C.; Hargrave M.; Wang X.; Chai R. J.; Elworthy S.; Ingham P. W. Analysis of Pax7 expressing myogenic cells in zebrafish muscle development, injury, and models of disease. Dev. Dyn. 240(11): 2440–2451; 2011.PubMedCrossRefGoogle Scholar
  76. Seo H. C.; Saetre B. O.; Havik B.; Ellingsen S.; Fjose A. The zebrafish Pax3 and Pax7 homologues are highly conserved, encode multiple isoforms and show dynamic segment-like expression in the developing brain. Mech. Dev. 70(1–2): 49–63; 1998.PubMedCrossRefGoogle Scholar
  77. Sepich D. S.; Ho R. K.; Westerfield M. Autonomous expression of the nic1 acetylcholine receptor mutation in zebrafish muscle cells. Dev. Biol. 161(1): 84–90; 1994.PubMedCrossRefGoogle Scholar
  78. Shefer G.; Van de Mark D. P.; Richardson J. B.; Yablonka-Reuveni Z. Satellite-cell pool size does matter: defining the myogenic potency of aging skeletal muscle. Dev. Biol. 294(1): 50–66; 2006.PubMedCrossRefGoogle Scholar
  79. Sparrow J.; Hughes S. M.; Segalat L. Other model organisms for sarcomeric muscle diseases. Adv. Exp. Med. Biol. 642: 192–206; 2008.PubMedCrossRefGoogle Scholar
  80. Stellabotte F.; Devoto S. H. The teleost dermomyotome. Dev. Dyn. 236(9): 2432–2443; 2007.PubMedCrossRefGoogle Scholar
  81. Stellabotte F.; Dobbs-McAuliffe B.; Fernandez D. A.; Feng X.; Devoto S. H. Dynamic somite cell rearrangements lead to distinct waves of myotome growth. Development 134(7): 1253–1257; 2007.PubMedCrossRefGoogle Scholar
  82. Stockdale F. E. Myogenic cell lineages. Dev. Biol. 154(2): 284–298; 1992.PubMedCrossRefGoogle Scholar
  83. Tanaka K. K.; Hall J. K.; Troy A. A.; Cornelison D. D.; Majka S. M.; Olwin B. B. Syndecan-4-expressing muscle progenitor cells in the SP engraft as satellite cells during muscle regeneration. Cell Stem Cell 4(3): 217–225; 2009.PubMedCrossRefGoogle Scholar
  84. Tang K. L.; Agnew M. K.; Hirt M. V.; Sado T.; Schneider L. M.; Freyhof J.; Sulaiman Z.; Swartz E.; Vidthayanon C.; Miya M.; Saitoh K.; Simons A. M.; Wood R. M.; Mayden R. L. Systematics of the subfamily Danioninae (Teleostei: Cypriniformes: Cyprinidae). Mol. Phylogenet. Evol. 57(1): 189–214; 2010.PubMedCrossRefGoogle Scholar
  85. Tatsumi R.; Anderson J. E.; Nevoret C. J.; Halevy O.; Allen R. E. HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev. Biol. 194(1): 114–128; 1998.PubMedCrossRefGoogle Scholar
  86. van Raamsdonk W.; van’t Veer L.; Veeken K.; te Kronnie T.; de Jager S. Fiber type differentiation in fish. Mol. Physiol. 2: 31–47; 1982.Google Scholar
  87. Vivien C.; Scerbo P.; Girardot F.; Le Blay K.; Demeneix B. A.; Coen L. Non-viral expression of mouse Oct4, Sox2, and Klf4 transcription factors efficiently reprograms tadpole muscle fibers in vivo. J. Biol. Chem. 287(10): 7427–7435; 2012.PubMedCrossRefGoogle Scholar
  88. Wei Q.; Rong Y.; Paterson B. M. Stereotypic founder cell patterning and embryonic muscle formation in Drosophila require nautilus (MyoD) gene function. Proc. Natl. Acad. Sci. U. S. A. 104(13): 5461–5466; 2007.PubMedCrossRefGoogle Scholar
  89. Yablonka-Reuveni Z.; Anderson J. E. Satellite cells from dystrophic (mdx) mice display accelerated differentiation in primary cultures and in isolated myofibers. Dev. Dyn. 235(1): 203–212; 2006.PubMedCrossRefGoogle Scholar
  90. Yamada M.; Tatsumi R.; Yamanouchi K.; Hosoyama T.; Shiratsuchi S.; Sato A.; Mizunoya W.; Ikeuchi Y.; Furuse M.; Allen R. E. 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): C465–476; 2010.PubMedCrossRefGoogle Scholar
  91. Young A. P.; Wagers A. J. Pax3 induces differentiation of juvenile skeletal muscle stem cells without transcriptional upregulation of canonical myogenic regulatory factors. J. Cell Sci. 123(Pt 15): 2632–2639; 2010.PubMedCrossRefGoogle Scholar
  92. Zammit P. S.; Partridge T. A.; Yablonka-Reuveni Z. The skeletal muscle satellite cell: the stem cell that came in from the cold. J. Histochem. Cytochem. 54(11): 1177–1191; 2006a.PubMedCrossRefGoogle Scholar
  93. Zammit P. S.; Relaix F.; Nagata Y.; Ruiz A. P.; Collins C. A.; Partridge T. A.; Beauchamp J. R. Pax7 and myogenic progression in skeletal muscle satellite cells. J. Cell Sci. 119(Pt 9): 1824–1832; 2006b.PubMedCrossRefGoogle Scholar
  94. Zhu J.; Li Y.; Shen W.; Qiao C.; Ambrosio F.; Lavasani M.; Nozaki M.; Branca M. F.; Huard J. Relationships between transforming growth factor-beta1, myostatin, and decorin: implications for skeletal muscle fibrosis. J. Biol. Chem. 282(35): 25852–25863; 2007.PubMedCrossRefGoogle Scholar

Copyright information

© The Society for In Vitro Biology 2013

Authors and Affiliations

  • Jacob Michael Froehlich
    • 1
  • Nicholas J. Galt
    • 1
  • Matthew J. Charging
    • 2
  • Ben M. Meyer
    • 2
  • Peggy R. Biga
    • 1
    Email author
  1. 1.Department of BiologyUniversity of Alabama at BirminghamBirminghamUSA
  2. 2.Department of Biological SciencesNorth Dakota State UniversityFargoUSA

Personalised recommendations