Myogenic Regulator Genes Responsible For Muscle Development in Farm Animals

Year 2024, Volume: 7 Issue: 4, 418 - 428, 15.07.2024

Godswill Arinzechukwu Iwuchukwu , Dilek Gökçek , Zeynep Özdemir

https://doi.org/10.47115/bsagriculture.1480033

Abstract

Breeding farm animals, especially poultry, helps meet global meat demand and boosts meat production efficiency. To meet high-quality meat demand, muscle growth and development must improve. Fetal skeletal muscle formation involves myogenesis, fibrogenesis, and adipogenesis. Kinase-encoding genes and myogenic regulatory factor genes regulate a complex network of intrinsic and extrinsic components in two or three stages. MYF5, MYOD, myogenin, and MRF4 are helix-loop-helix transcription factors that govern skeletal muscle cell specification and differentiation throughout embryogenesis and postnatal myogenesis. The transcription factors MYF5, MYOD, Myogenin, and MRF4 have been discovered to determine the skeletal muscle lineage and regulate myogenic differentiation during development. These factors also determine the muscle satellite cell lineage that becomes the adult skeletal muscle stem cell compartment. MYF5, MYOD, Myogenin, and MRF4 serve small functions in adult muscle, but they again direct satellite cell activity to regenerate skeletal muscle, linking genetic regulation of development and regeneration myogenesis. Understanding and identifying these genes helps increase meat yield and quality. This detailed review examines myogenic regulatory variables in satellite cell specification, maturation, and skeletal muscle regeneration.

Keywords

Meat, Myogenesis, Satellite cell, Myogenic differentiation, Regeneration, Skeletal muscle

References

• Amthor H, Nicholas G, McKinnell I, Kemp CF, Sharma M, Kambadur R, Patel K 2004. Follistatin complexes myostatin and antagonises myostatin-mediated inhibition of myogenesis. Devel Biol, 270: 19-30.
• Anderson C, Williams VC, Moyon B, Daubas P, Tajbakhsh S, Buckingham ME, 2012. Sonic hedgehog acts cell-autonomously on muscle precursor cells to generate limb muscle diversity, Genes Dev, 26(18): 2103–2117.
• Arnold HH, Winter B, 1998. Muscle differentiation: More complexity to the network of myogenic regulators. Curr. Opin. Genet. Giant, 8: 539-544.
• Arnold SJ, Robertson EJ, 2009. Making a commitment: Cell lineage allocation and axis patterning in the early mouse embryo. Nature Reviews Molecular Cell Biology, 10(2): 91–103.
• Ayuso M, Fernández A, Núñez Y, Benítez R, Isabel B, Fernández AI, Rey AI, González-Bulnes A, Medrano JF, Cánovas A, et al. 2016. Developmental stage, muscle and genetic type modify muscle transcriptome in pigs: Effects on gene expression and regulatory factors involved in growth and metabolism. PLoS ONE 11: e0167858.
• Bandow K, Ohnishi T, Tamura M, Semba I, Daikuhara Y 2004. Hepatocyte growth factor/scatter factor stimulates migration of muscle precursors in developing mouse tongue. J. Cell Physiol. 201:236–243.
• Beermann DH, Cassens RG, Hausman GJ 1978. A second look at fiber type differentiation in porcine skeletal muscle. J.Anim. Sci., 46: 125–132.
• Bentzinger CF, Wang YX, Rudnicki MA. Building muscle: Molecular regulation of myogenesis cold spring war. Perspect. Biol. February 2 2012, 4: a008342.
• Berri C, Godet E, Haj Hattab N, Duclos MJ 2006. Growth and differentiation of the chicken Pectoralis major muscle: Effect of genotype and early nutrition. Arch. Anim. Breed, 49:31–32.
• Bhat NR, Zhang P, Mohanty SB 2007, p38 MAP kinase regulation of oligodendrocyte differentiation with CREB as a potential target. Neurochem. Pic., 32: 293– 302.
• Biressi S, Molinaro M, Cossu G, 2007. Cellular heterogeneity during vertebrate skeletal muscle development. Giant. Biol. 308: 281-293.
• Braun T, Bober E, Winter B, Rosenthal N, Arnold HH 1990. Myf-6, a new member of the human gene family of myogenic factors determination: Evidence for a gene cluster on chromosome 12. EMBO J 9: 821–831
• Braun T, Buschhausen-Denker G, Bober E, Tannich E, Arnold HH 1989. A novel human muscle factor related to but distinct from MYOD1 induces myogenic conversion in 10T1/2 fibroblasts. EMBO J 8: 701– 709.
• Brunetti A, Goldfine ID, 1990. Role of myogenin in myoblast differentiation and its regulation by fibroblast growth factor. J. Biol. Chem, 265: 5960–5963.
• Bryson-Richardson RJ, Currie PD, The genetics of vertebrate myogenesis, Nat. Rev. Genet. 9 August 8 2008: 632–646.
• Buckingham M, Rigby PWJ, Gene regulatory networks and transcriptional mechanisms that control myogenesis, Dev. Cell 28 February 3 2014: 225–238.
• Buckingham M 1992. Making muscles in mammals. Trends Genet 8: 144–148.
• Buckingham M 2001. Skeletal muscle formation in vertebrates. Curr. Opin. Genet. Giant, 11: 440–448.
• Bulfield G, Siller WG, Wight PA, et al. 1984. X chromosome-linked muscular dystrophy (mdx) in the mouse, Proc. Natl. Acad. Sci. USA 81: 1189–1192.
• Chen AE, Ginty DD 2005, Fan CM. Protein kinase A signaling via CREB controls myogenesis induced by Wnt proteins. Nature, 433: 317–322.
• Coles CA, Wadeson J, Leyton CP, Siddell JP, Greenwood PL, White JD, McDonagh MB 2015. Proliferation rates of bovine primary muscle cells relate to live weight and carcase weight in cattle. PLoS ONE, 10: e0124468.
• Comai G, Tajbakhsh S 2014. Molecular and cellular regulation of skeletal myogenesis, Curr. Ball. Giant. Biol. 110:1–73.
• Cornelison DDW, Wold BJ, 1997. Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Giant. Biol. 191: 270-283.
• Crist CG, Montarras D, Buckingham M 2012. Muscle satellite cells are primed for myogenesis but maintain quiescence with sequestration of MYF5 mrna targeted by microrna-31 in mrnp granules, Cell Stem Cell 11 July 1: 118–126.
• Currie PD, Ingham PW, 1998. The generation and interpretation of positional information within the vertebrate myotome. Mech. Giant. 73, 321.
• Deato MDE, Marr MT, Sottero T, Inouye C, Hu P, Tjian R, 2008. MYOD targets TAF3/TRF3 to activate myogenin transcription, Mol. Cell 32 October 1: 96– 105.
• DeFronzo RA, Jacot E, Jequier E, Maeder E, Wahren J, Felber JP 1981. The effect of insulin on the disposal of intravenous glucose. Results from indirect calorimetry and hepatic and femoral venous catheterization. Diabetes, 30: 1000–1007.
• Du M, Tong J, Zhao J, Underwood KR, Zhu M, Ford SP, Nathanielsz PW 2010. Fetal programming of skeletal muscle development in ruminant animals. J.Anim. Sci, 88: E51–E60.
• Dumont NA, Bentzinger CF, Sincennes MC, et al., 2015. Satellite cells and skeletal muscle regeneration, Compr. Physiol. 5 2015b:1027–1059.
• Dumont NA, Wang YX, Rudnicki MA 2015. Intrinsic and extrinsic mechanisms regulating satellite cell function, Development 142 2015a: 1572–1581.
• Edmondson DG, Olson EN 1989. A gene with homology to the myc similarity region of MYOD1 is expressed during myogenesis and is sufficient to activate the muscle differentiation program. Genes Dev 3: 628–640.
• Edmonson DG, Olson EN, 1993. Helixloophelix proteins as regulators of muscle-specific transcription J. Biol. Chem. 268, 755758
• Fahey AJ, Brameld JM, Parr T, Buttery PJ 2005. Ontogeny of factors associated with proliferation and differentiation of muscle in the ovine fetus. J.Anim. Sci., 83: 2330–2338.
• Florini JR, Ewton DZ, Roof SL 1991. Mol. Endo. 5: 718-724.
• Fuchtbauer EM, Westphal H, 1992. MYOD and myogenin are coexpressed in regenerating skeletal muscle of the mouse, Dev. Dyn,193: 34–39.
• Fujisawa-Sehara A, Nabeshima Y, Komiya T, Uetsuki T, Asakura, A, Nabeshima Y 1992. J. Biol. Chem. 267: 10031-10038.
• Fukada S 2018. The roles of muscle stem cells in muscle injury, atrophy and hypertrophy. J. Biochem, 163: 353–358.
• Gerrard DE, Grant AL, 1994. Insulin-like growth factor-II expression in developing skeletal Muscle of double muscled and normal cattle. home Anim. Endocrinol, 11: 339–347.
• Grifone R, Demignon J, Houbron C, Souil E, Niro C, Seller MJ, et al. 2005. Six1 and six4 homeoproteins are required for PAX3 and mrf expression during myogenesis in the mouse embryo, Development 132, May 9 2005:2235–2249.
• Grounds MD, Garrett KL, Lai MC, et al., 1992. Identification of skeletal muscle precursor cells in vivo by use of MYOD1 and myogenin probes, Cell Tissue Res. 267: 99– 104.
• Gu W, Schneider JW, Condorelli G, Kaushal S, Mahdavi V, Nadal-Ginard B 1993. Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation. Cell 1993, 72: 309–324.
• Hardy D, Besnard A, Latil M, et al., 2016. Comparative study of injury models for studying muscle regeneration in mice, PLoS One 11: e0147198.
• Hasty P, Bradley A, Morris JH, et al., 1993. Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364: 501–506.
• Heino J, Massague J 1990. J. Biol. Chem. 265: 10181-10184.
• Hinck AP 2012. Structural studies of the tgfs and their receptors–insights into evolution of the tgf-superfamily, FEBS Lett. 586 July 14 2012: 1860–1870.
• Hinterberger TJ, Sassoon DA, Rhodes SJ, Konieczny SF, 1991. Expression of the muscle regulatory factor MRF4 during somite and skeletal myofiber development. Dev. Biol, 147 September 1 1991: 144–156.
• Hirsinger E, Duprez D, Jouve C, Malapert P, Cooke J, Pourquié O, 1997. Noggin acts downstream of wnt and sonic hedgehog to antagonize BMP4 in avian somite patterning. Development 124, November 22 1997: 4605–4614.
• Hirsinger E, Malapert P, Dubrulle J, Delfini MC, Duprez D, Henrique D, et al., 2001. Notch signaling acts in postmitotic avian myogenic cells to control MYOD activation, Development 128, January 1 2001: 107–116.
• Horst D, Ustanina S, Sergi C, Mikuz G, Juergens H, Braun T, Vorobyov E, 2006. Comparative expression analysis of PAX3 and PAX7 during mouse myogenesis. Int. J. Dev. Biol. 50, 47-54.
• Hu P, Geles KG, Paik JH, DePinho RA, Tjian R 2008. Codependent activators direct myoblast-specific MYOD transcription, Dev. Cell 15 October 4 2008: 534–546.
• Hughes SM, Taylor JM, Tapscott SJ, et al., 1993. Selective accumulation of MYOD and myogenin mRNAs in fast and slow adult skeletal muscle is controlled by innervation and hormones, Development 118:1137–1147.
• Hutcheson DA, Zhao J, Merrell A, Haldar M, Kardon G 2009. Embryonic and fetal limb myogenic cells are derived from developmentally distinct progenitors and have different requirements for beta-catenin. Genes Dev. 23: 997-1013.
• Kamanga-Sollo E, Pampusch MS, White ME, Dayton WR 2003. Role of insulin-like growth factor binding protein (IGFBP)-3 in TGF β-and GDF 8 (myostatin)-induced suppression of proliferation in porcine embryonic myogenic cell cultures. J. Cell Physiol, 197: 225–231.
• Kanisicak O, Mendez JJ, Yamamoto S, Yamamoto M, Goldhamer DJ 2009. Progenitors of skeletal muscle satellite cells express the muscle determination gene, MYOD, Dev. Biol. August 1 2009, 332:131–141.
• Kassar-Duchossoy L, Gayraud-Morel B, Gomes D, et al. 2004. MRF4 determines skeletal muscle identity in MYF5: MYOD double-mutant mice, Nature 431:466–471.
• Kassar-Duchossoy L, Giacone E, Gayraud-Morel B, Jory A, Gomès D, Tajbakhsh S 2005. PAX3/PAX7 mark a novel population of primitive myogenic cells during development, Genes Dev. June 12 2005, 19:1426–1431.
• Knight JDR, Kothary R 2011. The myogenic kinome: Protein kinases critical to mammalian skeletal myogenesis. Skeletal Muscle, 1: 29.
• Koishi K, Zhang M, McLennan IS, et al. 1995. MYOD protein accumulates in satellite cells and is neurally regulated in regenerating myotubes and skeletal muscle fibers, Dev. Dyn. 202: 244–254.
• Krüger M, Mennerich D, Fees S, Schäfer R, Mundlos S, Braun T 2001. Sonic hedgehog is a survival factor for hypaxial muscles during mouse development, Development March 5 2001 128: 743–752.
• Lapin MR, Gonzalez JM, Johnson SE 2013. Substrate elasticity affects bovine satellite cell activation kinetics in vitro. J.Anim. Sci. 91: 2083–2090.
• Leatherland JF 1994. Reflections on the thyroidology of fishes: From molecules to human kind Guelph. Ichthyol. Rev, 2:1–67.
• Lee SJ, McPherron AC 2001. Regulation of myostatin activity and muscle growth. Proceedings of the National Academy of Sciences of the United States of America 98: 9306–9311.
• Liu QC, Zha XH, Faralli H, Yin H, Louis-Jeune C, Perdiguero E, et al., 2012. Comparative expression profiling identifies differential roles for myogenin and p38 MAPK signaling in myogenesis, J. Mol. Cell Biol. 4 December 6 2012 :386– 397.
• Liu M, Peng J, Xu D, Zheng R, Li F, Li J, Zuo B, Lei M, Xiong Y, Deng C, et al. 2008. Association of MYF5 and MYOD1 gene polymorphisms and meat quality traits in Large White × Meishan F2 pig populations. Biochem. Genet, 46: 720–732.
• Luo H, Lv W, Tong Q, Jin J, Xu Z, Zuo B 2021. Functional non-coding rna during embryonic myogenesis and postnatal muscle development and disease. Front. Cell Dev. Biol. 9:628339. doi: 10.3389/fcell.2021.628339
• Marcelle C, Stark MR, Bronner-Fraser M 1997. Coordinate actions of bmps, wnts, shh and noggin mediate patterning of the dorsal somite, Development October 20 1997, 124: 3955–3963.
• McKinnell IW, Ishibashi J, Le Grand F, Punch VGJ, Addicks GC, Greenblatt JF, et al., 2008. PAX7 activates myogenic genes by recruitment of a histone methyltransferase complex, Nat. Cell Biol. January 1 2008, 10: 77–84.
• McPherron AC, Lee SJ 1997. Double muscling in cattle due to mutations in the myostatin gene. Proceedings of the National Academy of Sciences of the United States of America 94: 12457–12461.
• Meadows E, Cho JH, Flynn JM, Klein WH 2008. Myogenin regulates a distinct genetic program in adult muscle stem cells. Giant. Biol, 322: 406–414.
• Mifflin MD, St Jeor ST, Hill LA, Scott BJ, Daugherty SA, Koh YO 1990. A new predictive equation for resting energy expenditure in healthy individuals. Am. J. Clin. Nutr., 51:241–247.
• Miner JH, Wold B 1990. Herculin, a fourth member of the MYOD family of myogenic regulatory genes Proc Natl Acad Sci 87: 1089–1093.
• Morooka T, Nishida E, 1998. Requirement of p38 mitogen-activated protein kinase for neuronal differentiation in PC12 cells. J. Biol. Chem. 273: 24285–24288.
• Münsterberg AE, Kitajewski J, Bumcrot DA, McMahon AP, Lassar AB 1995. Combinatorial signaling by sonic hedgehog and wnt family members induces myogenic bhlh gene expression in the somite, Genes Dev. December 23 1995, 9:2911–2922.
• Murphy M, Kardon G 2011. Origin of vertebrate limb muscle: the role of progenitor and myoblast populations. Curr. Ball. Giant. Biol. 96: 1-32.
• Nabeshima Y, Hanaoka K, Hayasaka M, Esumi E, Li S, Nonaka I, Nabeshima YI 1993. Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 364: 532–535.
• Nagata Y, Takahashi N, Davis RJ, Todokoro K 1998. Activation of p38 MAP kinase and JNK but not ERK is required for erythropoietin-induced erythroid differentiation. Blood, 92: 1859–1869.
• Nelson KM, Weinsier RL, Long CL, Schutz Y 1992. Prediction of resting energy expenditure from fat-free mass and fat mass. Am. J. Clin. Nutr, 56: 848– 856.
• Noll M 1993. Evolution and role of Pax genesis. Curr Opin Genet Dev 3: 595–605.
• Obinata T, Kawashima M, Kinani S, Saitoh O, Masaki T, Bader DM, Fischman, DA 1986. Molecular Biology of Muscle Development. Emerson C, Fischman DA, Nadal-Ginard B, Siddiquis AQ, eds. p293 -307.
• Obinata T, Saitoh O, Takano-Ohmuro H 1984. J. Biochem. 95: 585 -588.
• Ott MO, Bober E, Lyons G, Arnold H, Buckingham 1991. Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo. Development 111: 1097-1107.
• Otto A, Schmidt C, Patel K 2006. PAX3 and PAX7 expression and regulation in the avian embryo. Anat. Embryol. 211: 293-310.
• Parakati R, DiMario JX 2013. Repression of myoblast proliferation and fibroblast growth factor receptor 1 promoter activity by KLF10 protein. J. Biol. Chem, 288: 13876–13884.
• Pavlath GK, Dominov JA, Kegley KM, et al., 2003. Regeneration of transgenic skeletal muscles with altered timing of expression of the basic helix-loop-helix muscle regulatory factor MRF4, Am. J. Pathol. 162:1685–1691.
• Pownall ME, Emerson CP 1992. Sequential activation of three myogenic regulatory genes during somite morphogenesis in quail embryos. Giant. Biol, 151: 67–79.
• Rantanen J, Hurme T, Lukka R, et al., 1995. Satellite cell proliferation and the expression of myogenin and desmin in regenerating skeletal muscle: evidence for two different populations of satellite cells, Lab. Invest. 72:341–347.
• Rehfeldt C, Te Pas MFW, Wimmers K, Brameld JM, Nissen PM, Berri C, Valente LMP, Power DM, Picard B, Stickland NC, et al. 2011. Advances in research on the prenatal development of skeletal muscle in animals in relation to the quality of muscle-based food. Animal 2011, 5:703–717.
• Relaix F, Zammit PS 2012. Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage. Development, 139: 3845-56
• Relaix F, Rocancourt D, Mansouri A, Buckingham M 2004. Divergent functions of murine PAX3 and PAX7 in limb muscle development, Genes Dev. May 9 2004, 18: 1088–1105.
• Rhodes SJ, Konieczny SF 1989. Identification of MRF4: A new member of the muscle regulatory factor gene family. Genes Dev, 3: 2050–2061.
• Ridgeway AG, Skerjanc IS 2001. PAX3 is essential for skeletal myogenesis and the expression of Six1 and Eya2. J. Biol. Chem, 276: 19033–19039.
• Rudnicki MA, Jaenisch R 1995. The MYOD family of transcription factors and skeletal myogenesis Bioessays, 17:203–209
• Rudnicki MA, Schnegelsberg PN, Stead RH, et al., 1993. MYOD or Myf-5 is required for the formation of skeletal muscle, Cell 75: 1351–1359.
• Rudnicki MA, Williams BO, Wnt signaling in bone and muscle, Bone November 2015, 80: 60–66.
• Schuster-Gossler K, Cordes R, Gossler A 2007. Premature myogenic differentiation and depletion of progenitor cells causes severe muscle hypotrophy in delta1 mutants, Proc. Natl. Acad. Sci. USA January 2 2007, 104: 537–542.
• 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 102:777–786.
• Shahjahan MD 2015. Skeletal muscle development in vertebrate animals. Asian J. Med. Biol. Pic, 1: 139–148.
• Shi X, Garry DJ 2006. Muscle stem cells in development, regeneration, and disease. Genes Giant, 20: 1692–1708.
• Skapek SX, Rhee J, Kim PS, Novitch BG, Lassar AB 1996. Cyclin-mediated inhibition of muscle gene expression via a mechanism that is independent of pRB hyperphosphorylation. Mole. Cell. Biol., 16: 7043–7053.
• Smith CK, Janney MJ, Allen RE 1994. Temporal expression of myogenic regulation genesis during activation, proliferation, and differentiation of rat skeletal muscle satellite cells. J. Cell Physiol. 159: 379-385.
• Soleimani VD, Punch VG, Kawabe YI, Jones AE, Palidwor GA, Porter CJ, et al., 2012. Transcriptional dominance of PAX7 in adult myogenesis is due to high-affinity recognition of homeodomain motifs, Dev. Cell, June 6 2012, 22: 1208–1220.
• Stockdale FE 1992. Myogenic cell lineages. Giant. Biol. 154: 284-298.
• Taguchi M, Ishikawa-Takata K, Tatsuta W, Katsuragi C, Usui C, Sakamoto S, Higuchi M 2011. Resting energy expenditure can be assessed by fat-free mass in female athletes regardless of body size. J. Nutr. Sci. Vitaminol, 57: 22–29.
• Tapscott SJ 2005. The circuitry of a master switch: MYOD and the regulation of skeletal muscle gene transcription, Development, June 12 2005 132:2685–2695.
• Theil PK, Sørensen IL, Nissen PM, Oksbjerg N 2006. Temporal expression of growth factor genesis of primary porcine satellite cells during myogenesis. Anim. Sci. J., 77: 330–337.
• Trukhachev V, Stavropol State Agrarian University, Skripkin V, Kvochko A, Kulichenko A, Kovalev D, Pisarenko S, Volynkina A, Selionova M, Aybazov M, et al., 2016. Correlation between gene expression profiles in muscle and live weight in Dzhalginsky Merino sheep. RCCP, 29: 188–198.
• Ujan JA, Zan LS, Ujan SA, Adoligbe C, Wang HB 2011. Back fat thickness and meat tenderness are associated with a 526 T →Amutation in the exon 1 promoter region of the MyF-5 gene in Chinese Bos taurus. Genet. Mole. Pic, 10: 3070–3079.
• Vaidya TB, Rhodes SJ, Taparowsky EJ, Konieczny SF 1989. Mol. Cell. Biol. 9: 3576-3579.
• Velleman SG 2007. Muscle development in the embryo and hatchling. Poult. Sci, 86: 1050–1054.
• Venuti JM, Morris JH, Vivian JL, et al. 1995. Myogenin is required for late but not early aspects of myogenesis during mouse development, J. Cell Biol. 128: 563- 576
• Voytik SL, Przyborski M, Badylak SF, et al. 1993. Differential expression of muscle regulatory factor genes in normal and denervated adult rat hindlimb muscles, Dev. Dyn. 198: 214–224.
• Weintraub H, Davis R, Tapscott S, Thayer M, Krause M, Benezra R, Blackwell TK, Turner D, Rupp R, Hollenberg S, et al. 1991. The MYOD gene family: Nodal point during specification of the muscle cell lineage. Science 251: 761–766.
• White RB, Biérinx AS, Gnocchi VF, Zammit PS 2010. Dynamics of muscle fiber growth during postnatal mouse development. BMC Dev. Biol. 10: 21.
• Wolfe RR 2006. The underappreciated role of muscle in health and disease. Am. J. Clin. Nutr, 84: 475–482.
• Wu G, Siegel PB, Gilbert ER, Yang N, Wong EA 2011. Expression profiles of somatotropic axis genes in lines of chickens divergently selected for 56-day body weight. Anim. Biotechnol, 22: 100–110.
• Yablonka-Reuveni Z, Rivera A, 1994. Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers. Giant. Biol. 164: 588-603.
• Yao J, Fetter RD, Hu P, Betzig E, Tjian R 2011. Subnuclear segregation of genes and core promoter factors in myogenesis, Genes Dev, March 6 2011, 25: 569–580.
• Yin H, Zhang S, Gilbert ER, Siegel PB, Zhu Q, Wong EA 2014. Expression profiles of muscle genesis in postnatal skeletal muscle in lines of chickens divergently selected for high and low body weight. Poult. Sci, 93: 147–154.
• Zammit PS, Golding JP, Nagata Y, Hudon V, Partridge TA, Beauchamp JR 2004. Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? The Journal of Cell Biology 166: 347–357.
• Zhao L, Huang Y, Du M 2019. Farm animals for studying muscle development and metabolism: Dual purposes for animal production and human health. Anim. Front, 9: 21–27.
• Zhou Z, Bornemann A 2001. MRF4 protein expression in regenerating rat muscle, J. Muscle Pic. Cell Motil. 22: 311–316.