Role of MyoD in denervated, disused, and exercised muscle

Muscle and Nerve

Volumn 38, Issue 3, 2008, Pages 1087-1100

  Legerlotz, Kirsten ^a   Smith, Heather K ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Muscle plasticity; MyoD; Myosin heavy chain; Satellite cells; Spinal cord injury

Indexed keywords

MYOD PROTEIN;

ELECTROSTIMULATION; HUMAN; MECHANICAL STIMULATION; MUSCLE DENERVATION; MUSCLE EXCITATION; MUSCLE EXERCISE; MUSCLE GROWTH; MUSCLE STRETCHING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; REVIEW;

ANIMALS; EXERCISE; GENE EXPRESSION REGULATION; HUMANS; MUSCLE DENERVATION; MUSCLES; MUSCULAR DISORDERS, ATROPHIC; MYOD PROTEIN;

EID: 51349091038     PISSN: 0148639X     EISSN: 10974598     Source Type: Journal    
DOI: 10.1002/mus.21087     Document Type: Review

References (117)

1. Alway SE, Lowe DA, Chen KD. The effects of age and hindlimb suspension on the levels of expression of the myogenic regulatory factors MyoD and myogenin in rat fast and slow skeletal muscles. Exp Physiol 2001;86:509-517.
2. Andersen JL, Mohr T, Biering-Sorensen F, Galbo H, Kjaer M. Myosin heavy chain isoform transformation in single fibres from m. vastus lateralis in spinal cord injured individuals: effects of long-term functional electrical stimulation (FES). Pflugers Arch 1996;431:513-518.
3. Anderson JE. A role for nitric oxide in muscle repair: nitric oxide-mediated activation of muscle satellite cells. Mol Biol Cell 2000;11:1859-1874.
4. Bamman MM, Ragan RC, Kim JS, Cross JM, Hill VJ, Tuggle SC, et al. Myogenic protein expression before and after resistance loading in 26- and 64-yr-old men and women. J Appl Physiol 2004;97:1329-1337.
5. Bean C, Salamon M, Raffaello A, Campanaro S, Pallavicini A, Lanfranchi G. The Ankrd2, Cdkn1c and calcyclin genes are under the control of MyoD during myogenic differentiation. J Mol Biol 2005;349:349-366.
6. Benezra R, Davis RL, Lassar A, Tapscott S, Thayer M, Lockshon D, et al. Id: a negative regulator of helix-loop-helix DNA binding proteins. Control of terminal myogenic differentiation. Ann N Y Acad Sci 1990;599:1-11.
7. Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 1990;61:49-59.
8. Beylkin DH, Allen DL, Leinwand LA. MyoD, Myf5, and the calcineurin pathway activate the developmental myosin heavy chain genes. Dev Biol 2006;294:541-553.
9. Bickel CS, Slade J, Mahoney E, Haddad F, Dudley GA, Adams GR. Time course of molecular responses of human skeletal muscle to acute bouts of resistance exercise. J Appl Physiol 2005;98:482-488.
10. Blasi J, Chapman ER, Link E, Binz T, Yamasaki S, De Camilli P, et al. Botulinum neurotoxin A selectively cleaves the synaptic protein SNAP-25. Nature 1993;365:160-163.
11. Bornemann A, Schmalbruch H. Immunocytochemistry of M-cadherin in mature and regenerating rat muscle. Anat Rec 1994;239:119-125.
12. Brin MF. Botulinum toxin: chemistry, pharmacology, toxicity, and immunology. Muscle Nerve Suppl 1997;6:S146-168.
13. Caiozzo YJ, Wu YZ, Baker MJ, Crumley R. Effects of denervation on cell cycle control in laryngeal muscle. Arch Otolaryngol Head Neck Surg 2004;130:1056-1068.
14. Carlsen H, Gundersen K. Helix-loop-helix transcription factors in electrically active and inactive skeletal muscles. Muscle Nerve 2000;23:1374-1380.
15. Carson JA, Schwartz RJ, Booth FW. SRF and TEF-1 control of chicken skeletal alpha-actin gene during slow-muscle hypertrophy. Am J Physiol 1996;270:C1624-1633.
16. Carson JA, Booth FW. Myogenin mRNA is elevated during rapid, slow, and maintenance phases of stretch-induced hypertrophy in chicken slow-tonic muscle. Pflugers Arch 1998;435:850-858.
17. Cenciarelli C, De Santa F, Puri PL, Mattei E, Ricci L, Bucci F, et al. Critical role played by cyclin D3 in the MyoD-mediated arrest of cell cycle during myoblast differentiation. Mol Cell Biol 1999;19:5203-5217.
18. Charge SB, Rudnicki MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev 2004;84:209-238.
19. Chen CM, Stott NS, Smith HK. Effects of botulinum toxin A injection and exercise on the growth of juvenile rat gastrocnemius muscle. J Appl Physiol 2002;93:1437-1447.
20. Clowry GJ, Walker L, Davies P. The effects of botulinum neurotoxin A induced muscle paresis during a critical period upon muscle and spinal cord development in the rat. Exp Neurol 2006;202:456-469.
21. Cooper RN, Tajbakhsh S, Mouly V, Cossu G, Buckingham M, Butler-Browne GS. In vivo satellite cell activation via Myf5 and MyoD in regenerating mouse skeletal muscle. J Cell Sci 1999;112(Pt 17):2895-2901.
22. Costa A, Dalloul H, Hegyesi H, Apor P, Csende Z, Racz L, et al. Impact of repeated bouts of eccentric exercise on myogenic gene expression. Eur J Appl Physiol 2007;101:427-436.
23. Crameri RM, Aagaard P, Qvortrup K, Langberg H, Olesen J, Kjaer M. Myofibre damage in human skeletal muscle: effects of electrical stimulation versus voluntary contraction. J Physiol 2007;583:365-380.
24. Davis RL, Cheng PF, Lassar AB, Weintraub H. The MyoD DNA binding domain contains a recognition code for muscle-specific gene activation. Cell 1990;60:733-746.
25. Davis S, Aldrich TH, Valenzuela DM, Wong VV, Furth ME, Squinto SP, et al. The receptor for ciliary neurotrophic factor. Science 1991;253:59-63.
26. Davis S, Aldrich TH, Ip NY, Stahl N, Scherer S, Farruggella T, et al. Released form of CNTF receptor alpha component as a soluble mediator of CNTF responses. Science 1993;259:1736-1739.
27. de la Brousse FC, Emerson CP Jr. Localized expression of a myogenic regulatory gene, qmf1, in the somite dermatome of avian embryos. Genes Dev 1990;4:567-581.
28. Dedkov EI, Kostrominova TY, Borisov AB, Carlson BM. Reparative myogenesis in long-term denervated skeletal muscles of adult rats results in a reduction of the satellite cell population. Anat Rec 2001;263:139-154.
29. Dedkov EI, Kostrominova TY, Borisov AB, Carlson BM. MyoD and myogenin protein expression in skeletal muscles of senile rats. Cell Tissue Res 2003;311:401-416.
30. Delday MI, Maltin CA. Clenbuterol increases the expression of myogenin but not myoD in immobilized rat muscles. Am J Physiol 1997;272:E941-944.
31. Dodd SL, Selsby J, Payne A, Judge A, Dott C. Botulinum neurotoxin type A causes shifts in myosin heavy chain composition in muscle. Toxicon 2005;46:196-203.
32. Drachman DB, Stanley EF, Pestronk A, Griffin JW, Price DL. Neurotrophic regulation of two properties of skeletal muscle by impulse-dependent and spontaneous acetylcholine transmission. J Neurosci 1982;2:232-243.
33. Dupont-Versteegden EE, Houle JD, Gurley CM, Peterson CA. Early changes in muscle fiber size and gene expression in response to spinal cord transection and exercise. Am J Physiol 1998;275:C1124-1133.
34. Eftimie R, Brenner HR, Buonanno A. Myogenin and MyoD join a family of skeletal muscle genes regulated by electrical activity. Proc Natl Acad Sci U S A 1991;88:1349-1353.
35. Ekmark M, Rana ZA, Stewart G, Hardie DG, Gundersen K. De-phosphorylation of MyoD is linking nerve-evoked activity to fast myosin heavy chain expression in rodent adult skeletal muscle. J Physiol 2007;584:637-650.
36. Eppley ZA, Kim J, Russell B. A myogenic regulatory gene, qmf1, is expressed by adult myonuclei after injury. Am J Physiol 1993;265:C397-405.
37. Frick CG, Richtsfeld M, Sahani ND, Kaneki M, Blobner M, Martyn JA. Long-term effects of botulinum toxin on neuromuscular function. Anesthesiology 2007;106:1139-1146.
38. Gomes AR, Soares AG, Peviani S, Nascimento RB, Moriscot AS, Salvini TF. The effect of 30 minutes of passive stretch of the rat soleus muscle on the myogenic differentiation, myostatin, and atrogin-1 gene expressions. Arch Phys Med Rehabil 2006;87:241-246.
39. Grimby G, Broberg C, Krotkiewska I, Krotkiewski M. Muscle fiber composition in patients with traumatic cord lesion. Scand J Rehabil Med 1976;8:37-42.
40. Grossman EJ, Roy RR, Talmadge RJ, Zhong H, Edgerton VR. Effects of inactivity on myosin heavy chain composition and size of rat soleus fibers. Muscle Nerve 1998;21:375-389.
41. Grounds MD, Garrett KL, Lai MC, Wright WE, Beilharz MW. Identification of skeletal muscle precursor cells in vivo by use of MyoD1 and myogenin probes. Cell Tissue Res 1992;267:99-104.
42. Hawke TJ, Garry DJ. Myogenic satellite cells: physiology to molecular biology. J Appl Physiol. 2001;91:534-551.
43. Hentzen ER, Lahey M, Peters D, Mathew L, Barash IA, Friden J, et al. Stress-dependent and -independent expression of the myogenic regulatory factors and the MARP genes after eccentric contractions in rats. J Phvsiol 2006;570:157-167.
44. Hespel P, Op't Eijnde B, Van Leemputte M, Urso B, Greenhaff PL, Labarque V, et al. Oral creatine supplementation facilitates the rehabilitation of disuse atrophy and alters the expression of muscle myogenic factors in humans. J Physiol 2001;536:625-633.
45. Hill M, Goldspink G. Expression and splicing of the insulin-like growth factor gene in rodent muscle is associated with muscle satellite (stem) cell activation following local tissue damage. J Physiol 2003;549:409-418.
46. Holterman CE, Rudnicki MA. Molecular regulation of satellite cell function. Semin Cell Dev Biol 2005;16:575-584.
47. Huang S, Wang F, Hong G, Wan S, Kang H. Protective effects of ciliary neurotrophic factor on denervated skeletal muscle. J Huazhong Univ Sci Technolog Med Sci 2002;22:148-151.
48. Hughes SM, Taylor JM, Tapscott SJ, Gurley CM, Carter WJ, Peterson CA. Selective accumulation of MyoD and myogenin mRNAs in fast and slow adult skeletal muscle is controlled by innervation and hormones. Development 1993;118:1137-1147.
49. Hughes SM, Koishi K, Rudnicki M, Maggs AM. MyoD protein is differentially accumulated in fast and slow skeletal muscle fibres and required for normal fibre type balance in rodents. Mech Dev 1997;61:151-163.
50. Hwang DF, Noguchi T. Tetrodotoxin poisoning. Adv Food Nutr Res 2007;52:141-236.
51. Hyatt JP, Roy RR, Baldwin KM, Edgerton VR. Nerve activity-independent regulation of skeletal muscle atrophy: role of MyoD and myogenin in satellite cells and myonuclei. Am J Physiol Cell Physiol 2003;285:C1161-1173.
52. Hyatt JP, Roy RR, Baldwin KM, Wernig A, Edgerton VR. Activity-unrelated neural control of myogenic factors in a slow muscle. Muscle Nerve 2006;33:49-60.
53. Inagi K, Connor NP, Schultz E, Ford CN, Cook CH, Heisey DM. Muscle fiber-type changes induced by botulinum toxin injection in the rat larynx. Otolaryngol Head Neck Surg 1999;120:876-883.
54. Ip FC, Fu AK, Tsim KW, Ip NY. Differential expression of ciliary neurotrophic factor receptor in skeletal muscle of chick and rat after nerve injury. J Neurochem 1996;67:1607-1612.
55. Irintchev A, Zeschnigk M, Starzinski-Powitz A, Wernig A. Expression pattern of M-cadherin in normal, denervated, and regenerating mouse muscles. Dev Dyn 1994;199:326-337.
56. Ishido M, Kami K, Masuhara M. In vivo expression patterns of MyoD, p21, and Rb proteins in myonuclei and satellite cells of denervated rat skeletal muscle. Am J Physiol Cell Physiol 2004;287:C484-493.
57. Ishido M, Kami K, Masuhara M. Localization of MyoD, myogenin and cell cycle regulatory factors in hypertrophying rat skeletal muscles. Acta Physiol Scand 2004;180:281-289.
58. Jensky NE, Sims JK, Rice JC, Dreyer HC, Schroeder ET. The influence of eccentric exercise on mRNA expression of skeletal muscle regulators. Eur J Appl Physiol 2007;101:473-480.
59. Jones R, Vrbova G. Two factors responsible for the development of denervation hypersensitivity. J Physiol 1974;236:517-538.
60. Kadi F, Johansson F, Johansson R, Sjostrom M, Henriksson J. Effects of one bout of endurance exercise on the expression of myogenin in human quadriceps muscle. Histochem Cell Biol 2004;121:329-334.
61. Kadi F, Charifi N, Denis C, Lexell J, Andersen JL, Schjerling P, et al. The behaviour of satellite cells in response to exercise: what have we learned from human studies? Pflugers Arch 2005;451:319-327.
62. Kim JS, Kosek DJ, Petrella JK, Cross JM, Bamman MM. Resting and load-induced levels of myogenic gene transcripts differ between older adults with demonstrable sarcopenia and young men and women. J Appl Physiol 2005;99:2149-2158.
63. Koishi K, Zhang M, McLennan IS, Harris AJ. MyoD protein accumulates in satellite cells and is neurally regulated in regenerating myotubes and skeletal muscle fibers. Dev Dyn 1995;202:244-254.
64. Kong Y, Flick MJ, Kudla AJ, Konieczny SF. Muscle LIM protein promotes myogenesis by enhancing the activity of MyoD. Mol Cell Biol 1997;17:4750-4760.
65. Kosek DJ, Kim JS, Petrella JK, Cross JM, Bamman MM. Efficacy of 3 days/wk resistance training on myofiber hypertrophy and myogenic mechanisms in young vs. older adults. J Appl Physiol 2006;101:531-544.
66. Kranjc BS, Sketelj J, D'Albis A, Erzen I. Long-term changes in myosin heavy chain composition after botulinum toxin a injection into rat medial rectus muscle. Invest Ophthalmol Vis Sci 2001;42:3158-3164.
67. Lassar AB, Buskin JN, Lockshon D, Davis RL, Apone S, Hauschka SD, et al. MyoD is a sequence-specific DNA binding protein requiring a region of myc homology to bind to the muscle creatine kinase enhancer. Cell 1989;58:823-831.
68. Lehti TM, Silvennoinen M, Kivela R, Kainulainen H, Komulainen J. Effects of streptozotocin-induced diabetes and physical training on gene expression of titin-based stretch-sensing complexes in mouse striated muscle. Am J Physiol Endocrinol Metab 2007;292:E533-542.
69. Li H, Capetanaki Y. Regulation of the mouse desmin gene: transactivated by MyoD, myogenin, MRF4 and Myf5. Nucleic Acids Res 1993;21:335-343.
70. Lin H, Yutzey KE, Konieczny SF. Muscle-specific expression of the troponin I gene requires interactions between helix-loop-helix muscle regulatory factors and ubiquitous transcription factors. Mol Cell Biol 1991;11:267-280.
71. Loughna PT, Brownson C. Two myogenic regulatory factor transcripts exhibit muscle-specific responses to disuse and passive stretch in adult rats. FEBS Lett 1996;390:304-306.
72. Loughna PT, Morgan MJ. Passive stretch modulates denervation induced alterations in skeletal muscle myosin heavy chain mRNA levels. Pflugers Arch 1999;439:52-55.
73. Ma J, Shen J, Lee CA, Elsaidi GA, Smith TL, Walker FO, et al. Gene expression of nAChR, SNAP-25 and GAP-43 in skeletal muscles following botulinum toxin A injection: a study in rats. J Orthop Res 2005;23:302-309.
74. Ma J, Shen J, Garrett JP, Lee CA, Li Z, Elsaidi GA, et al. Gene expression of myogenic regulatory factors, nicotinic acetylcholine receptor subunits, and GAP-43 in skeletal muscle following denervation in a rat model. J Orthop Res 2007;25:1498-1505.
75. Maier A, Zhou Z, Bornemann A. The expression profile of myogenic transcription factors in satellite cells from denervated rat muscle. Brain Pathol 2002;12:170-177.
76. Martin TP, Stein RB, Hoeppner PH, Reid DC. Influence of electrical stimulation on the morphological and metabolic properties of paralyzed muscle. J Appl Physiol 1992;72:1401-1406.
77. McKinsey TA, Zhang CL, Olson EN. Signaling chromatin to make muscle. Curr Opin Cell Biol 2002;14:763-772.
78. McMahon CD, Popovic L, Oldham JM, Jeanplong F, Smith HK, Kambadur R, et al. Myostatin-deficient mice lose more skeletal muscle mass than wild-type controls during hindlimb suspension. Am J Physiol Endocrinol Metab 2003;285:E82-87.
79. Meissner JD, Umeda PK, Chang KC, Gros G, Scheibe RJ. Activation of the beta myosin heavy chain promoter by MEF-2D, MyoD, p300, and the calcineurin/NFATc1 pathway. J Cell Physiol 2007;211:138-148.
80. Mendelzon D, Changeux JP, Nghiem HO. Phosphorylation of myogenin in chick myotubes: regulation by electrical activity and by protein kinase C. Implications for acetylcholine receptor gene expression. Biochemistry 1994;33:2568-2575.
81. Michel RN, Parry DJ, Dunn SE. Regulation of myosin heavy chain expression in adult rat hindlimb muscles during short-term paralysis: comparison of denervation and tetrodotoxin-induced neural inactivation. FEBS Lett 1996;391:39-44.
82. Midrio M. The denervated muscle: facts and hypotheses. A historical review. Eur J Appl Physiol 2006;98:1-21.
83. Mozdziak PE, Greaser ML, Schultz E. Myogenin, MyoD, and myosin expression after pharmacologically and surgically induced hypertrophy. J Appl Physiol 1998;84:1359-1364.
84. Mozdziak PE, Greaser ML, Schultz E. Myogenin, MyoD, and myosin heavy chain isoform expression following hindlimb suspension. Aviat Space Environ Med 1999;70:511-516.
85. Murre C, McCaw PS, Baltimore D. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell 1989;56:777-783.
86. Peters D, Barash IA, Burdi M, Yuan PS, Mathew L, Friden J, et al. Asynchronous functional, cellular and transcriptional changes after a bout of eccentric exercise in the rat. J Physiol 2003;553:947-957.
87. Peviani SM, Gomes AR, Moreira RF, Moriscot AS, Salvini TF. Short bouts of stretching increase myo-D, myostatin and atrogin-1 in rat soleus muscle. Muscle Nerve 2007;35:363-370.
88. Piette J, Bessereau JL, Huchet M, Changeux JP. Two adjacent MyoD1-binding sites regulate expression of the acetylcholine receptor alpha-subunit gene. Nature 1990;345:353-355.
89. Raue U, Slivka D, Jemiolo B, Hollon C, Trappe S. Myogenic gene expression at rest and after a bout of resistance exercise in young (18-30 yr) and old (80-89 yr) women. J Appl Physiol 2006;101:53-59.
90. Rosenblatt JD, Yong D, Parry DJ. Satellite cell activity is required for hypertrophy of overloaded adult rat muscle. Muscle Nerve 1994;17:608-613.
91. Round JM, Barr FM, Moffat B, Jones DA. Fibre areas and histochemical fibre types in the quadriceps muscle of paraplegic subjects. J Neurol Sci 1993;116:207-211.
92. Roy RR, Zhong H, Khalili N, Kim SJ, Higuchi N, Monti RJ, et al. Is spinal cord isolation a good model of muscle disuse? Muscle Nerve 2007;35:312-321.
93. Russo TL, Peviani SM, Freria CM, Gigo-Benato D, Geuna S, Salvini TF. Electrical stimulation based on chronaxie reduces atrogin-1 and myoD gene expressions in denervated rat muscle. Muscle Nene 2007;35:87-97.
94. Sabourin LA, Rudnicki MA. The molecular regulation of myogenesis. Clin Genet 2000;57:16-25.
95. Sakuma K, Watanabe K, Sano M, Uramoto I, Sakamoto K, Totsuka T. The adaptive response of MyoD family proteins in overloaded, regenerating and denervated rat muscles. Biochim Biophys Acta 1999;1428:284-292.
96. Seward DJ, Haney JC, Rudnicki MA, Swoap SJ. bHLH transcription factor MyoD affects myosin heavy chain expression pattern in a muscle-specific fashion. Am J Physiol Cell Physiol 2001;280:C408-413.
97. Shen J, Ma J, Elsaidi GA, Lee CA, Smith TL, Tan KH, et al. Gene expression of myogenic regulatory factors following intramuscular injection of botulinum A toxin in juvenile rats. Neurosci Lett 2005;381:207-210.
98. Siu PM, Donley DA, Bryner RW, Alway SE. Myogenin and oxidative enzyme gene expression levels are elevated in rat soleus muscles after endurance training. J Appl Physiol 2004;97:277-285.
99. Spiller MP, Kambadur R, Jeanplong F, Thomas M, Martyn JK, Bass JJ, et al. The myostatin gene is a downstream target gene of basic helix-loop-helix transcription factor MyoD. Mol Cell Biol 2002;22:7066-7082.
100. Talmadge RJ, Roy RR, Edgerton VR. Prominence of myosin heavy chain hybrid fibers in soleus muscle of spinal cord-transected rats. J Appl Physiol 1995;78:1256-1265.
101. Talmadge RJ. Myosin heavy chain isoform expression following reduced neuromuscular activity: potential regulatory mechanisms. Muscle Nerve 2000;23:661-679.
102. Tamaki T, Uchiyama S, Uchiyama Y, Akatsuka A, Yoshimura S, Roy RR, et al. Limited myogenic response to a single bout of weight-lifting exercise in old rats. Am J Physiol Cell Physiol 2000;278:C1143-1152.
103. Tonami K, Kurihara Y, Aburatani H, Uchijima Y, Asano T, Kurihara H. Calpain 6 is involved in microtubule stabilization and cytoskeletal organization. Mol Cell Biol 2007;27:2548-2561.
104. Vissing K, Andersen JL, Harridge SD, Sandri C, Hartkopp A, Kjaer M, et al. Gene expression of myogenic factors and phenotype-specific markers in electrically stimulated muscle of paraplegics. J Appl Physiol 2005;99:164-172.
105. Vissing K, Andersen JL, Schjerling P. Are exercise-induced genes induced by exercise? FASEB J 2005;19:94-96.
106. Voytik SL, Przyborski M, Badylak SF, Konieczny SF. Differential expression of muscle regulatory factor genes in normal and denervated adult rat hindlimb muscles. Dev Dyn 1993;198:214-224.
107. Walters EH, Stickland NC, Loughna PT. The expression of the myogenic regulatory factors in denervated and normal muscles of different phenotypes. J Muscle Res Cell Motil 2000;21:647-653.
108. Wei Q, Paterson BM. Regulation of MyoD function in the dividing myoblast. FEBS Lett 2001;490:171-178.
109. Weinberg RA. The retinoblastoma protein and cell cycle control. Cell 1995;81:323-330.
110. Wentworth BM, Donoghue M, Engert JC, Berglund EB, Rosenthal N. Paired MyoD-binding sites regulate myosin light chain gene expression. Proc Natl Acad Sci U S A 1991;88:1242-1246.
111. Wheeler MT, Snyder EC, Patterson MN, Swoap SJ. An E-box within the MHC HB gene is bound by MyoD and is required for gene expression in fast muscle. Am J Physiol 1999;276:C1069-1078.
112. Witzemann V, Sakmann B. Differential regulation of MyoD and myogenin mRNA levels by nerve induced muscle activity. FEBS Lett 1991;282:259-264.
113. Wozniak AC, Kong J, Bock E, Pilipowicz O, Anderson JE. Signaling satellite-cell activation in skeletal muscle: markers, models, stretch, and potential alternate pathways. Muscle Nerve 2005;31:283-300.
114. Yang Y, Creer A, Jemiolo B, Trappe S. Time course of myogenic and metabolic gene expression in response to acute exercise in human skeletal muscle. J Appl Physiol 2005;98:1745-1752.
115. Zacksenhaus E, Jiang Z, Chung D, Marth JD, Phillips RA, Gallic BL. pRb controls proliferation, differentiation, and death of skeletal muscle cells and other lineages during embryogenesis. Genes Dev 1996;10:3051-3064.
116. Zador E, Dux L, Wuytack F. Prolonged passive stretch of rat soleus muscle provokes an increase in the mRNA levels of the muscle regulatory factors distributed along the entire length of the fibers. J Muscle Res Cell Motil 1999;20:395-402.
117. Zhao P, Iezzi S, Carver E, Dressman D, Gridley T, Sartorelli V, Hoffman EP. Slug is a novel downstream target of MyoD. Temporal profiling in muscle regeneration. J Biol Chem 2002;277:30091-30101.