Signaling satellite-cell activation in skeletal muscle: Markers, models, stretch, and potential alternate pathways

Muscle and Nerve

Volumn 31, Issue 3, 2005, Pages 283-300

  Wozniak, Ashley C ^a   Kong, Jiming ^a   Bock, Erika ^a   Pilipowicz, Orest ^a   Anderson, Judy E ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

Author keywords

c met; Hepatocyte growth factor; HGF; Nitric oxide; Regeneration; Single fiber

Indexed keywords

NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; SCATTER FACTOR;

CELL ACTIVATION; CELL ASSAY; CELL CYCLE; CELL DIFFERENTIATION; CELL GROWTH; CELL HETEROGENEITY; CELL POPULATION; CELL PROLIFERATION; CELL STIMULATION; HUMAN; MECHANICAL STIMULATION; MOLECULAR MODEL; MUSCLE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; SATELLITE CELL; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

ANIMALS; BIOLOGICAL MARKERS; HUMANS; MODELS, BIOLOGICAL; SATELLITE CELLS, SKELETAL MUSCLE; SIGNAL TRANSDUCTION; STRESS, MECHANICAL;

EID: 13844308294     PISSN: 0148639X     EISSN: None     Source Type: Journal    
DOI: 10.1002/mus.20263     Document Type: Review

References (165)

1. Abounader R, Ranganathan S, Kim BY, Nichols C, Laterra J. Signaling pathways in the induction of c-met receptor expression by its ligand scatter factor/hepatocyte growth factor in human glioblastoma. J Neurochem 2001;76:1497-1508.
2. Abu-Soud HM, Wang J, Rousseau DL, Stuehr DJ. Stopped-flow analysis of substrate binding to neuronal nitric oxide synthase. Biochemistry 1999;38:12446-12451.
3. Alderton WK, Cooper CE, Knowles RG. Nitric oxide synthases: structure, function and inhibition. Biochem J 2001;357:593-615.
4. Allen RE, Boxhorn LK. 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 1989;138:311-315.
5. Allen RE, Sheehan SM, Taylor RG, Kendall TL, Rice GM. Hepatocyte growth factor activates quiescent skeletal muscle satellite cells in vitro. J Cell Physiol 1995;165:307-312.
6. Anderson J, Pilipowicz O. Activation of muscle satellite cells in single-fiber cultures. Nitric Oxide 2002;7:36-41.
7. Anderson JE. Dystrophic changes in mdx muscle regenerating from denervation and devascularization. Muscle Nerve 1991;14:268-279.
8. Anderson JE, Murray L. Barr Award Lecture. Studies of the dynamics of skeletal muscle regeneration: the mouse came back! Biochem Cell Biol 1998;76:13-26.
9. 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.
10. Anderson JE, Garrett K, Moor A, McIntosh L, Penner K. Dystrophy and myogenesis in mdx diaphragm muscle. Muscle Nerve 1998;21:1153-1165.
11. Anderson JE, McIntosh LM, Moor AN, Yablonka-Reuveni Z. Levels of MyoD protein expression following injury of mdx and normal limb muscle are modified by thyroid hormone. J Histochem Cytochem 1998;46:59-67.
12. Anderson JE, Ovalle WK, Bressler BH. Electron microscopic and autoradiographic characterization of hindlimb muscle regeneration in the mdx mouse. Anat Rec 1987;219:243-257.
13. Anderson JE, Vargas C. Correlated NOS-Iμ and myf5 expression by satellite cells in mdx mouse muscle regeneration during NOS manipulation and deflazacort treatment. Neuromuscul Disord 2003;13:388-396.
14. Anderson JE, Weber M, Vargas C. Deflazacort increases laminin expression and myogenic repair, and induces early persistent functional gain in mdx mouse muscular dystrophy. Cell Transplant 2000;9:551-564.
15. Anderson JE, Wozniak AC. Satellite cell activation on fibers: modeling events in vivo - an invited review. Can J Physiol Pharmacol 2004;82:300-310.
16. Anderson LV, Davison K. Multiplex Western blotting system for the analysis of muscular dystrophy proteins. Am J Pathol 1999;154:1017-1022.
17. Aronson D, Dufresne SD, Goodyear LJ. Contractile activity stimulates the c-Jun NH2-terminal kinase pathway in rat skeletal muscle. J Biol Chem 1997;272:25636-25640.
18. Barani AE, Sabido O, Freyssenet D. Mitotic activity of rat muscle satellite cells in response to serum stimulation: relation with cellular metabolism. Exp Cell Res 2003;283:196-205.
19. Barton-Davis ER, Shoturma DI, Sweeney HL. Contribution of satellite cells to IGF-I induced hypertrophy of skeletal muscle. Acta Physiol Scand 1999;167:301-305.
20. Beauchamp JR, Heslop L, Yu DS, Tajbakhsh S, Kelly RG, Wernig A, Buckingham ME, Partridge TA, Zammit PS. Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J Cell Biol 2000;151:1221-1234.
21. Best TM, Hunter KD. Muscle injury and repair. Phys Med Rehabil Clin N Am 2000;11:251-266.
22. Bischoff R. A satellite cell mitogen from crushed adult muscle. Dev Biol 1986;115:140-147.
23. Bischoff R. Proliferation of muscle satellite cells on intact myofibers in culture. Dev Biol 1986;115:129-139.
24. Bischoff R. Interaction between satellite cells and skeletal muscle fibers. Development 1990;109:943-952.
25. Bischoff R, Heintz C. Enhancement of skeletal muscle regeneration. Dev Dyn 1994;201:41-54.
26. Bischoff R, Holtzer H. Mitosis and the processes of differentiation of myogenic cells in vitro. J Cell Biol 1969;41:188-200.
27. Boccaccio C, Gaudino G, Gambarotta G, Galimi F, Comoglio PM. Hepatocyte growth factor (HGF) receptor expression is inducible and is part of the delayed-early response to HGF. J Biol Chem 1994;269:12846-12851.
28. Bogdanovich S, Krag TO, Barton ER, Morris LD, Whittemore LA, Ahima RS, Khurana TS. Functional improvement of dystrophic muscle by myostatin blockade. Nature 2002;420:418-421.
29. Boppart MD, Hirshman MF, Sakamoto K, Fielding RA, Goodyear LJ. Static stretch increases c-Jun NH2-terminal kinase activity and p38 phosphorylation in rat skeletal muscle. Am J Physiol Cell Physiol 2001;280:C352-C358.
30. Bottaro DP, Rubin JS, Faletto DL, Chan AM, Kmiecik TE, Vande Woude GF, Aaronson SA. Identification of the hepatocyte growth factor receptor as the c-met proto-oncogene product. Science 1991;251:802-804.
31. Brzoska E, Grabowska I, Wrobel E, Moraczewski J. Syndecan-4 distribution during the differentiation of satellite cells isolated from soleus muscle treated by phorbol ester and calphostin C. Cell Mol Biol Lett 2003;8:269-278.
32. Cameron-Smith D. Exercise and skeletal muscle gene expression. Clin Exp Pharmacol Physiol 2002;29:209-213.
33. Cao B, Zheng B, Jankowski RJ, Kimura S, Ikezawa M, Deasy B, Cummins J, Epperly M, Qu-Petersen Z, Huard J. Muscle stem cells differentiate into haematopoietic lineages but retain myogenic potential. Nat Cell Biol 2003;5:640-646.
34. 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;112:2895-2901.
35. Cordelier P, Esteve JP, Rivard N, Marletta M, Vaysse N, Susini C, Buscail L. The activation of neuronal NO synthase is mediated by G-protein betagamma subunit and the tyrosine phosphatase SHP-2. FASEB J 1999;13:2037-2050.
36. Cornelison DD, Filla MS, Stanley HM, Rapraeger AC, Olwin BB. Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration. Dev Biol 2001;239:79-94.
37. -/-) satellite cells in single-fiber culture are differentiation defective and MRF4 deficient. Dev Biol 2000;224:122-137.
38. Cornelison DD, Wold BJ. Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol 1997;191:270-283.
39. Dahlqvist C, Blokzijl A, Chapman G, Falk A, Dannaeus K, Ibanez CF, Lendahl U. Functional Notch signaling is required for BMP4-induced inhibition of myogenic differentiation. Development 2003;130:6089-6099.
40. Deasy BM, Jankowski RJ, Huard J. Muscle-derived stem cells: characterization and potential for cell-mediated therapy. Blood Cells Mol Dis 2001;27:924-933.
41. Deasy BM, Jankowski RJ, Payne TR, Cao B, Goff JP, Greenberger JS, Huard J. Modeling stem cell population growth: incorporating terms for proliferative heterogeneity. Stem Cells 2003;21:536-545.
42. Derksen PW, de Gorter DJ, Meijer HP, Bende RJ, van Dijk M, Lokhorst HM, Bloem AC, Spaargaren M, Pals ST. The hepatocyte growth factor/Met pathway controls proliferation and apoptosis in multiple myeloma. Leukemia 2003;17:764-774.
43. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 1999;399:601-605.
44. Dreyfus PA, Chretien F, Chazaud B, Kirova Y, Caramelle P, Garcia L, Buder-Browne G, Gherardi RK. Adult bone marrow-derived stem cells in muscle connective tissue and satellite cell niches. Am J Pathol 2004;164:773-779.
45. Falcone G, Ciuffini L, Gauzzi MC, Provenzano C, Strano S, Gallo R, Castellani L, Alema S. v-Src inhibits myogenic differentiation by interfering with the regulatory network of muscle-specific transcriptional activators at multiple levels. Oncogene 2003;22:8302-8315.
46. Florini JR, Magri KA. Effects of growth factors on myogenic differentiation. Am J Physiol 1989;256:C701-C711.
47. Fluckey JD, Dupont-Versteegden EE, Montague DC, Knox M, Tesch P, Peterson CA, Gaddy-Kurten D. A rat resistance exercise regimen attenuates losses of musculoskeletal mass during hindlimb suspension. Acta Physiol Scand 2002;176:293-300.
48. Force T, Michael A, Kilter H, Haq S. Stretch-activated pathways and left ventricular remodeling. J Card Fail 2002;8:S351-S358.
49. Fulton D, Gratton JP, Sessa WC. Post-translational control of endothelial nitric oxide synthase: why isn't calcium/calmodulin enough? J Pharmacol Exp Ther 2001:299:818-824.
50. Furchgott RF. Studies on relaxation of rabbit aorta by sodium nitrite: the basis for the proposal that the acid-activatable inhibitory factor from retractor penis is inorganic nitrite and the endothelium-derived relaxing factor is nitric oxide. In: Vanhoutte PM, editor. Vasodilatation: vascular smooth muscle, peptides, autonomic nerves and endothelium. New York: Raven Press; 1988. p 401-414.
51. Furge KA, Zhang YW, Vande Woude GF. Met receptor tyrosine kinase: enhanced signaling through adapter proteins. Oncogene 2000;19:5582-5589.
52. Gandino L, Di Renzo MF, Giordano S, Bussolino F, Comoglio PM. Protein kinase-c activation inhibits tyrosine phosphorylation of the c-met protein. Oncogene 1990;5:721-725.
53. Garrett KL, Anderson JE. Colocalization of bFGF and the myogenic regulatory gene myogenin in dystrophic mdx muscle precursors and young myotubes in vivo. Dev Biol 1995;169:596-608.
54. Gohda E, Kataoka H, Tsubouchi H, Daikilara Y, Yamamoto I. Phorbol ester-induced secretion of human hepatocyte growth factor by human skin fibroblasts and its inhibition by dexamethasone. FEBS Lett 1992;301:107-110.
55. Goodell MA, Jackson KA, Majka SM, Mi T, Wang H, Pocius J, Hartley CJ, Majesky MW, Entman ML, Michael LH, Hirschi KK. Stem cell plasticity in muscle and bone marrow. Ann N Y Acad Sci 2001;938:208-218.
56. Grounds MD, Garrett KL, Beilharz MW. The transcription of MyoD1 and myogenin genes in thymic cells in vivo. Exp Cell Res 1992;198:357-361.
57. 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.
58. Grounds MD, McGeachie JK. A model of myogenesis in vivo, derived from detailed autoradiographic studies of regenerating skeletal muscle, challenges the concept of quantal mitosis. Cell Tissue Res 1987;250:563-569.
59. Grounds MD, McGeachie JK. A comparison of muscle precursor replication in crush-injured skeletal muscle of Swiss and BALBc mice. Cell Tissue Res 1989;255:385-391.
60. Grounds MD, McGeachie JK. Myogenic cells of regenerating adult chicken muscle can fuse into myotubes after a single cell division in vivo. Exp Cell Res 1989;180:429-439.
61. Grounds MD, Yablonka-Reuveni Z. Molecular and cell biology of skeletal muscle regeneration. Mol Cell Biol Hum Dis Ser 1993;3:210-256.
62. Gussoni E, Soneoka Y, Strickland CD, Buzney EA, Khan MK, Flint AF, Kunkel LM, Mulligan RC. Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 1999;401:390-394.
63. Gustafsson AB, Brunton LL. Attenuation of cAMP accumulation in adult rat cardiac fibroblasts by IL-1beta and NO: role of cGMP-stimulated PDE2. Am J Physiol Cell Physiol 2002;283:C463-C471.
64. Haddad F, Adams GR. Selected contribution: acute cellular and molecular responses to resistance exercise. J Appl Physiol 2002;93:394-403.
65. Hawke TJ, Garry DJ. Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 2001;91:534-551.
66. Heslop L, Morgan JE, Partridge TA. Evidence for a myogenic stem cell that is exhausted in dystrophic muscle. J Cell Sci 2000;113:2299-2308.
67. Hogg N. The biochemistry and physiology of S-nitrosothiols. Annu Rev Pharmacol Toxicol 2002;42:585-600.
68. Husmann I, Soulet L, Gautron J, Martelly I, Barritault D. Growth factors in skeletal muscle regeneration. Cytokine Growth Factor Rev 1996;7:249-258.
69. Ignarro LJ, Barry BK, Gruetter DY, Edwards JC, Ohlstein EH, Gruetter CA, Baricos WH. Guanylate cyclase activation of nitroprusside and nitrosoguanidine is related to formation of S-nitrosothiol intermediates. Biochem Biophys Res Commun 1980;94:93-100.
70. Ignarro LJ, Buga GM, Wood KS, Byrns RE, Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci U S A 1987; 84:9265-9269.
71. Ignarro LJ, Buga GM, Wood KS, Byrns RE, Chaudhuri G. Biochemical and pharmacological properties of endothelium-derived relaxing factor and its similarity to nitric oxide radical. In: Vanhoutte PM, editor. Vasodilatation: vascular smooth muscle, peptides, autonomie nerves and endothelium. New York: Raven Press; 1988. p 427-436.
72. Ignarro LJ, Byrns RE, Buga GM, Wood KS, Chaudhuri G. Pharmacological evidence that endothelium-derived relaxing factor is nitric oxide: use of pyrogallol and superoxide dismutase to study endothelium-dependent and nitric oxide-elicited vascular smooth muscle relaxation. J Pharmacol Exp Ther 1988;244:181-189.
73. Ikezawa M, Cao B, Qu Z, Peng H, Xiao X, Pruchnic R, Kimura S, Miike T, Huard J. Dystrophin delivery in dystrophin-deficient DMD mdx skeletal muscle by isogenic muscle-derived stem cell transplantation. Hum Gene Ther 2003;14:1535-1546.
74. 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.
75. Jackson KA, Mi T, Goodell MA. Hematopoietic potential of stem cells isolated from murine skeletal muscle. Proc Natl Acad Sci U S A 1999;96:14482-14486.
76. Jankowski RJ, Deasy BM, Cao B, Gates C, Huard J. The role of CD34 expression and cellular fusion in the regeneration capacity of myogenic progenitor cells. J Cell Sci 2002;115:4361-4374.
77. Jankowski RJ, Deasy BM, Huard J. Muscle-derived stem cells. Gene Ther 2002;9:642-647.
78. Jankowski RJ, Haluszczak C, Trucco M, Huard J. Flow cytometric characterization of myogenic cell populations obtained via the preplate technique: potential for rapid isolation of muscle-derived stem cells. Hum Gene Ther 2001;12:619-628.
79. Johnson SE, Allen RE. Proliferating cell nuclear antigen (PCNA) is expressed in activated rat skeletal muscle satellite cells. J Cell Physiol 1993;154:39-43.
80. Johnson SE, Allen RE. Activation of skeletal muscle satellite cells and the role of fibroblast growth factor receptors. Exp Cell Res 1995;219:449-453.
81. Jozsi AC, Dupont-Versteegden EE, Taylor-Jones JM, Evans WJ, Trappe TA, Campbell WW, Peterson CA. Molecular characteristics of aged muscle reflect an altered ability to respond to exercise. Int J Sport Nutr Exerc Metab 2001;11(Suppl):S9-S15.
82. Kablar B, Krastel K, Tajbakhsh S, Rudnicki MA. Myf5 and MyoD activation define independent myogenic compartments during embryonic development. Dev Biol 2003;258:307-318.
83. Kami K, Noguchi K, Senba E. Localization of myogenin, c-fos, c-jun, and muscle-specific gene mRNAs in regenerating rat skeletal muscle. Cell Tissue Res 1995;280:11-19.
84. Kirkendall DT, Garrett WE, Jr. Clinical perspectives regarding eccentric muscle injury. Clin Orthop 2002;S81-S89.
85. Klein C. Nitric oxide and the other cyclic nucleotide. Cell Signal 2002;14:493-498.
86. Kumar A, Chaudhry I, Reid MB, Boriek AM. Distinct signaling pathways are activated in response to mechanical stress applied axially and transversely to skeletal muscle fibers. J Biol Chem 2002;277:46493-46503.
87. Lane P, Gross SS. The autoinhibitory control element and calmodulin conspire to provide physiological modulation of endothelial and neuronal nitric oxide synthase activity. Acta Physiol Scand 2000;168:53-63.
88. Lee JY, Qu-Petersen Z, Cao B, Kimura S, Jankowski R, Cummins J, Usas A, Gates C, Robbins P, Wernig A, Huard J. Clonal isolation of muscle-derived cells capable of enhancing muscle regeneration and bone healing. J Cell Biol 2000;150:1085-1100.
89. Li C, Xu Q. Mechanical stress-initiated signal transductions in vascular smooth muscle cells. Cell Signal 2000;12:435-445.
90. Liou GI, Matragoon S, Samuel S, Behzadian MA, Tsai NT, Gu X, Roon P, Hunt DM, Hunt RC, Caldwell RB, Marcus DM. MAP kinase and beta-catenin signaling in HGF induced RPE migration. Mol Vis 2002;8:483-493.
91. Liu M, Post M. Invited review: mechanochemical signal transduction in the fetal lung. J Appl Physiol 2000;89:2078-2084.
92. Martineau LC, Gardiner PF. Insight into skeletal muscle mechanotransduction: MAPK activation is quantitatively related to tension. J Appl Physiol 2001;91:693-702.
93. Matsunaga T, Gohda E, Takebe T, Wu YL, Iwao M, Kataoka H, Yamamoto I. Expression of hepatocyte growth factor is up-regulated through activation of a cAMP-mediated pathway. Exp Cell Res 1994;210:326-335.
94. Maulik G, Shrikhande A, Kijima T, Ma PC, Morrison PT, Salgia R. Role of the hepatocyte growth factor receptor, c-Met, in oncogenesis and potential for therapeutic inhibition. Cytokine Growth Factor Rev 2002;13:41-59.
95. Mauro A. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 1961;9:493-495.
96. Mauro A, Shafiq SA, Milhorat AT. Regeneration of striated muscle, and myogenesis. Amsterdam: Excerpta Medica; 1970.
97. McCormick KM, Schultz E. Role of satellite cells in altering myosin expression during avian skeletal muscle hypertrophy. Dev Dyn 1994;199:52-63.
98. McCroskery S, Thomas M, Maxwell L, Sharma M, Kambadur R. Myostatin negatively regulates satellite cell activation and self-renewal. J Cell Biol 2003;162:1135-1147.
99. McIntosh LM, Garrett KL, Megeney L, Rudnicki MA, Anderson JE. Regeneration and myogenic cell proliferation correlate with taurine levels in dystrophin- and MyoD-deficient muscles. Anat Rec 1998;252:311-324.
100. McIntosh LM, Pernitsky AN, Anderson JE. The effects of altered metabolism (hypothyroidism) on muscle repair in the mdx dystrophic mouse. Muscle Nerve 1994;17:444-453.
101. McKinney-Freeman SL, Jackson KA, Camargo FD, Ferrari G, Mavilio F, Goodell MA. Muscle-derived hematopoietic stem cells are hematopoietic in origin. Proc Natl Acad Sci U S A 2002;99:1341-1346.
102. McLoon LK, Rowe J, Wirtschafter J, McCormick KM. Continuous myofiber remodeling in uninjured extraocular myofibers: myonuclear turnover and evidence for apoptosis. Muscle Nerve 2004;29:707-715.
103. McLoon LK, Wirtschafter J. Activated satellite cells are present in uninjured extraocular muscles of mature mice. Trans Am Ophthalmol Soc 2002;100:119-123.
104. McLoon LK, Wirtschafter J. Activated satellite cells in extraocular muscles of normal adult monkeys and humans. Invest Ophthalmol Vis Sci 2003;44:1927-1932.
105. McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 1997;387:83-90.
106. Milasincic DJ, Dhawan J, Farmer SR. Anchorage-dependent control of muscle-specific gene expression in C2C12 mouse myoblasts. In Vitro Cell Dev Biol Anim 1996;32:90-99.
107. Molnar G, Ho ML, Schroedl NA. Evidence for multiple satellite cell populations and a non-myogenic cell type that is regulated differently in regenerating and growing skeletal muscle. Tissue Cell 1996;28:547-556.
108. Moncada S, Higgs A. The L-arginine-nitric oxide pathway. N Engl J Med 1993;329:2002-2012.
109. Naldini L, Vigna E, Narsimhan RP, Gaudino G, Zarnegar R, Michalopoulos GK, Comoglio PM. Hepatocyte growth factor (HGF) stimulates the tyrosine kinase activity of the receptor encoded by the proto-oncogene c-MET. Oncogene 1991;6:501-504.
110. Norman TL, Bradley-Popovich G, Clovis N, Cutlip RG, Bryner RW. Aerobic exercise as a countermeasure for microgravity-induced bone loss and muscle atrophy in a rat hindlimb suspension model. Aviat Space Environ Med 2000;71:593-598.
111. Oldenhof AD, Shynlova OP, Liu M, Langille BL, Lye SJ. Mitogen-activated protein kinases mediate stretch-induced c-fos mRNA expression in myometrial smooth muscle cells. Am J Physiol Cell Physiol 2002;283:C1530-C1539.
112. Olwin BB, Arthur K, Hannon K, Hein P, McFall A, Riley B, Szebenyi G, Zhou Z, Zuber ME, Rapraeger AC. Role of FGFs in skeletal muscle and limb development. Mol Reprod Dev 1994;39:90-100.
113. Parr C, Jiang WG. Expression of hepatocyte growth factor/scatter factor, its activator, inhibitors and the c-Met receptor in human cancer cells. Int J Oncol 2001;19:857-863.
114. Parry DJ. Myosin heavy chain expression and plasticity: role of myoblast diversity. Exerc Sport Sci Rev 2001;29:175-179.
115. Pavlath GK, Thaloor D, Rando TA, Cheong M, English AW, Zheng B. Heterogeneity among muscle precursor cells in adult skeletal muscles with differing regenerative capacities. Dev Dyn 1998;212:495-508.
116. Pernitsky AN, McIntosh LM, Anderson JE. Hyperthyroidism impairs early repair in normal but not dystrophic mdx mouse tibialis anterior muscle. An in vivo study. Biochem Cell Biol 1996;74:315-324.
117. Ponzetto C, Bardelli A, Zhen Z, Maina F, dalla ZP, Giordano S, Graziani A, Panayotou G, Comoglio PM. A multifunctional docking site mediates signaling and transformation by the hepatocyte growth factor/scatter factor receptor family. Cell 1994;77:261-271.
118. Qu-Petersen Z, Deasy B, Jankowski R, Ikezawa M, Cummins J, Pruchnic R, Mytinger J, Cao B, Gates C, Wernig A, Huard J. Identification of a novel population of muscle stem cells in mice: potential for muscle regeneration. J Cell Biol 2002;157:851-864.
119. Rahimi N, Tremblay E, Elliott B. Phosphatidylinositol 3-kinase activity is required for hepatocyte growth factor-induced mitogenic signals in epithelial cells. J Biol Chem 1996;271:24850-24855.
120. Rantanen J, Hurme T, Lukka R, Heino J, Kalimo H. Satellite cell proliferation and the expression of myogenin and desmin in regenerating skeletal muscle: evidence for two different populations of satellite cells. Lab Invest 1995;72:341-347.
121. Reid MB. Role of nitric oxide in skeletal muscle: synthesis, distribution and functional importance. Acta Physiol Scand 1998;162:401-409.
122. Royer CL, Howell JC, Morrison PR, Srour EF, Yoder MC. Muscle-derived CD45-SCA-1+c-kit- progenitor cells give rise to skeletal muscle myotubes in vitro. In Vitro Cell Dev Biol Anim 2002;38:512-517.
123. Sabourin LA, Rudnicki MA. The molecular regulation of myogenesis. Clin Genet 2000;57:16-25.
124. Schalken JA, van Leenders G. Cellular and molecular biology of the prostate: stem cell biology. Urology 2003;62:11-20.
125. Schmidt K, Glaser G, Wernig A, Wegner M, Rosorius O. Sox8 is a specific marker for muscle satellite cells and inhibits myogenesis. J Biol Chem 2003;278:29769-29775.
126. Schoen JM, Wang HH, Minuk GY, Lautt WW. Shear stress-induced nitric oxide release triggers the liver regeneration cascade. Nitric Oxide 2001;5:453-464.
127. Schultz E. Fine structure of satellite cells in growing skeletal muscle. Am J Anat 1976;147:49-70.
128. Schultz E, Darr KC, Macius A. Acute effects of hindlimb unweighting on satellite cells of growing skeletal muscle. J Appl Physiol 1994;76:266-270.
129. Schultz E, Gibson MC, Champion T. Satellite cells are mitotically quiescent in mature mouse muscle: an EM and radioautographic study. J Exp Zool 1978;206:451-456.
130. Schultz E, Jaryszak DL. Effects of skeletal muscle regeneration on the proliferation potential of satellite cells. Mech Ageing Dev 1985;30:63-72.
131. Schultz E, Jaryszak DL, Valliere CR. Response of satellite cells to focal skeletal muscle injury. Muscle Nerve 1985;8:217-222.
132. Schultz E, McCormick KM. Skeletal muscle satellite cells. Rev Physiol Biochem Pharmacol 1994;123:213-257.
133. + stem cells from injured muscle. PLoS Biol 2004;2:E130.
134. Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Grass P, Rudnicki MA. Pax7 is required for the specification of myogenic satellite cells. Cell 2000;102:777-786.
135. Segalat L, Grisoni K, Archer JD, Vargas C, Bertrand A, Anderson JE. CAPON expression in skeletal muscle is regulated by position, repair, NOS activity and dystrophy. Exp Cell Res 2005;302:170-179.
136. Sheehan SM, Tatsumi R, Temm-Grove CJ, Allen RE. HGF is an autocrine growth factor for skeletal muscle satellite cells in vitro. Muscle Nerve 2000;23:239-245.
137. Sherwood DJ, Dufresne SD, Markuns JF, Cheatham B, Moller DE, Aronson D, Goodyear LJ. Differential regulation of MAP kinase, p70(S6K), and Akt by contraction and insulin in rat skeletal muscle. Am J Physiol 1999;276:E870-E878.
138. Sinanan AC, Hunt NP, Lewis MP. Human adult craniofacial muscle-derived cells; neural-cell adhesion-molecule (NCAM; CD56)-expressing cells appear to contain multipotential stem cells. Biotechnol Appl Biochem 2004;40:25-34.
139. Sinanan AC, Hunt NP, Lewis MP. Human adult craniofacial muscle-derived cells: neural-cell adhesion-molecule (NCAM; CD56)-expressing cells appear to contain multipotential stem cells. Biotechnol Appl Biochem 2004;40:25-34.
140. Smith CK, Janney MJ, Allen RE. Temporal expression of myogenic regulatory genes during activation, proliferation, and differentiation of rat skeletal muscle satellite cells. J Cell Physiol 1994;159:379-385.
141. Spangenburg EE, Chakravarthy MV, Booth FW. p27Kip1: a key regulator of skeletal muscle satellite cell proliferation. Clin Orthop 2002;S221-S227.
142. Tamaki T, Akatsuka A, Ando K, Nakamura Y, Matsuzawa H, Hotta T, Roy RR, Edgerton VR. Identification of myogenic-endothelial progenitor cells in the interstitial spaces of skeletal muscle. J Cell Biol 2002;157:571-577.
143. Tamaki T, Akatsuka A, Okada Y, Matsuzaki Y, Okano H, Kimura M. Growth and differentiation potential of main-and side-population cells derived from murine skeletal muscle. Exp Cell Res 2003;291:83-90.
144. Tamaki T, Akatsuka A, Yoshimura S, Roy RR, Edgerton VR. New fiber formation in the interstitial spaces of rat skeletal muscle during postnatal growth. J Histochem Cytochem 2002;50:1097-1111.
145. Tatsumi R, Anderson JE, Nevoret CJ, Halevy O, Allen RE. HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev Biol 1998;194:114-128.
146. Tatsumi R, Hattori A, Ikeuchi Y, Anderson JE, Allen RE. Release of hepatocyte growth factor from mechanically stretched skeletal muscle satellite cells and role of pH and nitric oxide. Mol Biol Cell 2002;13:2909-2918.
147. Tatsumi R, Sheehan SM, Iwasaki H, Hattori A, Allen RE. Mechanical stretch induces activation of skeletal muscle satellite cells in vitro. Exp Cell Res 2001;267:107-114.
148. Torrente Y, Camirand G, Pisati F, Belicchi M, Rossi B, Colombo F, El Fahime M, Caron NJ, Issekutz AC, Constantin G, Tremblay JP, Bresolin N. Identification of a putative pathway for the muscle homing of stem cells in a muscular dystrophy model. J Cell Biol 2003;162:511-520.
149. Vermeulen K, Berneman ZN, Van Bockstaele DR. Cell cycle and apoptosis. Cell Prolif 2003;36:165-175.
150. Wagner KR, McPherron AC, Winik N, Lee SJ. Loss of myostatin attenuates severity of muscular dystrophy in mdx mice. Ann Neurol 2002:52:832-836.
151. Wang HH, Lautt WW. Evidence of nitric oxide, a flow-dependent factor, being a trigger of liver regeneration in rats. Can J Physiol Pharmacol 1998;76:1072-1079.
152. Wedel B, Garbers D. The guanylyl cyclase family at Y2K. Annu Rev Physiol 2001;63:215-233.
153. Weintraub H. The MyoD family and myogenesis: redundancy, networks, and thresholds. Cell 1993;75:1241-1244.
154. Widegren U, Ryder JW, Zierath JR. Mitogen-activated protein kinase signal transduction in skeletal muscle: effects of exercise and muscle contraction. Acta Physiol Scand 2001;172:227-238.
155. Winn N, Paul A, Musaro A, Rosenthal N. Insulin-like growth factor isoforms in skeletal muscle aging, regeneration, and disease. Cold Spring Harb Symp Quant Biol 2002;67:507-518.
156. Wozniak AC, Pilipowicz O, Yablonka-Reuveni Z, Greenway S, Craven S, Scott E, Anderson JE. C-met expression and mechanical activation of satellite cells on cultured muscle fibers. J Histochem Cytochem 2003;51:1437-1445.
157. Yablonka-Reuveni Z. Isolation and characterization of stem cells from adult skeletal muscle. In: Lanza RP, Blau HM, Melton DA, Moore MAS, Thomas ED, Verfaillie CM, Weissman IL, West MD, editors. Handbook of stem cells. San Diego: Elsevier-Academic Press; 2004.
158. Yablonka-Reuveni Z. Isolation and characterization of stem cells from adult skeletal muscle. In: Lanza RP, Blau HM, Melton DA, Moore MAS, Thomas ED, Verfaillie CM, Weissman IL, West MD, editors. Handbook of stem cells. San Diego: Elsevier-Academic Press; 2004.
159. Yablonka-Reuveni Z. Patterns of proliferation and differentiation of adult myoblasts define a unique myogenic population. Prog Clin Biol Res 1993;383B:575-585.
160. Yablonka-Reuveni Z. Development and postnatal regulation of adult myoblasts. Microsc Res Tech 1995;30:366-380.
161. Yablonka-Reuveni Z, Rivera AJ. Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers. Dev Biol 1994;164:588-603.
162. Yablonka-Reuveni Z, Rivera AJ. Influence of PDGF-BB on proliferation and transition through the MyoD-myogenin-MEF2A expression program during myogenesis in mouse C2 myoblasts. Growth Factors 1997;15:1-27.
163. Yablonka-Reuveni Z, Rudnicki MA, Rivera AJ, Primig M, Anderson JE, Natanson P. The transition from proliferation to differentiation is delayed in satellite cells from mice lacking MyoD. Dev Biol 1999;210:440-455.
164. Yamamoto H, Teramoto H, Uetani K, Igawa K, Shimizu E. Stretch induces a growth factor in alveolar cells via protein kinase. Respir Physiol 2001;127:105-111.
165. Zacharias JM, Anderson JE. Muscle regeneration after imposed injury is better in younger than older mdx dystrophic mice. J Neurol Sci 1991;104:190-196.