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

American Journal of Physiology - Cell Physiology

Volumn 298, Issue 3, 2010, Pages

  Yamada, Michiko ^a   Tatsumi, Ryuichi ^a   Keitaro Yamanouchi, T ^b   Hosoyama, Ohru ^b   Shiratsuchi, Sei Ichi ^a   Sato, Akiko ^a   Mizunoya, Wataru ^a   Ikeuchi, Yoshihide ^a   Furuse, Mitsuhiro ^a   Allen, Ronald E ^c  

^a KYUSHU UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

Activation; Hepatocyte growth factor; Muscle regeneration; Myostatin; Quiescence; Satellite cells; Time lag

Indexed keywords

BROXURIDINE; CYCLIN DEPENDENT KINASE INHIBITOR 1A; MESSENGER RNA; MYOSTATIN; NEUTRALIZING ANTIBODY; SCATTER FACTOR;

ANIMAL EXPERIMENT; ARTICLE; CELL ACTIVATION; CELL CULTURE; CELL DIFFERENTIATION; CELL LYSATE; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL; MALE; MUSCLE INJURY; MUSCLE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SKELETAL MUSCLE SATELLITE CELL; SPLEEN CELL; UPREGULATION; WESTERN BLOTTING;

ANIMALS; ANTIBODIES; BLOTTING, WESTERN; CELL AGING; CELL PROLIFERATION; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DOSE-RESPONSE RELATIONSHIP, DRUG; FEEDBACK, PHYSIOLOGICAL; HEPATOCYTE GROWTH FACTOR; HUMANS; MALE; MUSCLE DEVELOPMENT; MYOSTATIN; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SATELLITE CELLS, SKELETAL MUSCLE; SIGNAL TRANSDUCTION; TIME FACTORS; UP-REGULATION;

EID: 77749292129     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00449.2009     Document Type: Article

References (107)

1. 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 138: 311-315, 1989.
2. Allen RE, Sheehan SM, Taylor RG, Kendall TL, Rice GM. Hepatocyte growth factor activates quiescent skeletal muscle satellite cells in vitro. J Cell Physiol 165: 307-312, 1995.
3. Allen RE, Temm-Grove CJ, Sheehan SM, Rice GM. Skeletal muscle satellite cell cultures. Methods Cell Biol 52: 155-176, 1997.
4. Allen RE, Goll DE. Cellular and developmental biology of skeletal muscle as related to muscle growth. In: Biology of Growth of Domestic Animals, edited by Scanes CG. Ames, IA: Iowa State Press, 2003, p. 148-169.
5. Amthor H, Otto A, Macharia R, McKinnell I, Patel K. Myostatin imposes reversible quiescence on embryonic muscle precursors. Dev Dyn 235: 672-680, 2006.
6. 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: 1057-1068, 1997.
7. Anderson JE. A role for nitric oxide in muscle repair: nitric oxidemediated activation of muscle satellite cells. Mol Biol Cell 11: 1859-1874, 2000.
8. Anderson JE, Pilipowicz O. Activation of muscle satellite cells in single-fiber cultures. Nitric Oxide 7: 36-41, 2002.
9. Anderson JE, Wozniak AC. Satellite cell activation on fibers: modeling events in vivo. Can J Physiol Pharmacol 82: 300-310, 2004.
10. Anderson JE. The satellite cell as a companion in skeletal muscle plasticity: currency, conveyance, clue, connector and colander. J Exp Biol 209: 2276-2292, 2006.
11. Anderson SB, Goldberg AL, Whitman M. Identification of a novel pool of extracellular pro-myostatin in skeletal muscle. J Biol Chem 283: 7027-7035, 2008.
12. Birchmeier C, Gherardi E. Developmental roles of HGF/SF and its receptor, the c-Met tyrosine kinase. Trends Cell Biol 8: 404-410, 1998.
13. Bischoff R. The satellite cell and muscle regeneration. In: Myology: Basic and Clinical (2nd ed.), edited by Engel AG and Franzini-Armstrong C. New York: McGraw-Hill, 1994, vol. 1, p. 97-118.
14. Bischoff R. Chemotaxis of skeletal muscle satellite cells. Dev Dyn 208: 505-515, 1997.
15. 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 251: 802-804, 1991.
16. Chan AM, Rubin JS, Bottaro DP, Hirschfield DW, Chedid M, Aaronson SA. Identification of a competitive HGF antagonist encoded by an alternative transcript. Science 254: 1382-1385, 1991.
17. Chiaverotti TA, Battula N, Monnat RJ Jr. Rat hypoxanthine phosphoribosyltransferase cDNA cloning and sequence analysis. Genomics 11: 1158-1160, 1991.
18. Clop A, Marcq F, Takeda H, Pirottin D, Tordoir X, Bibe B, Bouix J, Caiment F, Elsen JM, Eychenne F, Larzul C, Laville E, Meish F, Milenkovic D, Tobin J, Charlier C, Georges M. A mutation creating a potential illegitimate microRNA target site in the myostatin gene affects muscularity in sheep. Nat Genet 38: 813-818, 2006.
19. Collins CA. Satellite cell self-renewal. Curr Opin Pharmacol 6: 301-306, 2006.
20. Comoglio PM, Boccaccio C, Trusolino L. Interactions between growth factor receptors and adhesion molecules: breaking the rules. Curr Opin Cell Biol 15: 565-571, 2003.
21. Cornelison DDW, Wold BJ. Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol 191: 270-283, 1997.
22. Cromack DT, Sporn MB, Roberts AB, Merino MJ, Dart LL, Norton JA. Transforming growth factor-β levels in rat wound chambers. J Surg Res 42: 622-628, 1987.
23. Dhawan J, Rando TA. Stem cells in postnatal myogenesis: molecular mechanisms of satellite cell quiescence, activation and replenishment. Trends Cell Biol 15: 666-673, 2005.
24. 2/M-phase transition. Mol Cell Biol 18: 546-557, 1998.
25. Ellis LM. The role of neuropilins in cancer. Mol Cancer Ther 5: 1099-1107, 2006.
26. Gilson H, Schakman O, Kalista S, Lause P, Tsuchida K, Thissen JP. Follistatin induces muscle hypertrophy through satellite cell proliferation and inhibition of both myostatin and activin. Am J Physiol Endocrinol Metab 297: E157-E164, 2009.
27. Giordano S, Ponzetto C, Di Renzo MF, Cooper CS, Comoglio PM. Tyrosine kinase receptor indistinguishable from the c-met protein. Nature 339: 155-156, 1989.
28. Giordano S, Di Renzo MF, Narsimhan RP, Cooper CS, Rosa C, Comoglio PM. Biosynthesis of the protein encoded by the c-met protooncogene. Oncogene 4: 1383-1388, 1989.
29. Gonzatti-Haces M, Seth A, Park M, Copeland T, Oroszlan S, Vande Woude GF. Characterization of the TPR-MET oncogene p65 and the MET protooncogene p140 protein-tyrosine kinases. Proc Natl Acad Sci USA 85: 21-25, 1988.
30. Grobet L, Martin LJR, Poncelet D, Pirottin D, Brouwers B, Riquet J, Schoeberlein A, Dunner S, Menissier F, Massabanda J, Fries R, Hanset R, Georges M. A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle. Nat Genet 17: 71-74, 1997.
31. Halevy O, Cantley LC. Differential regulation of the phosphoinositide 3-kinase and MAP kinase pathways by hepatocyte growth factor vs. insulin-like growth factor-I in myogenic cells. Exp Cell Res 297: 224-234, 2004.
32. Hawke TJ, Garry DJ. Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91: 534-551, 2001.
33. Higuchi O, Nakamura T. Identification and change in the receptor for hepatocyte growth factor in rat liver after partial hepatectomy or induced hepatitis. Biochem Biophys Res Commun 176: 599-607, 1991.
34. Higuchi O, Mizuno K, VandeWoude GF, Nakamura T. Expression of c-met proto-oncogene in COS cells induces the signal transducing highaffinity receptor for hepatocyte growth factor. FEBS Lett 301: 282-286, 1992.
35. Igawa T, Kanda S, Kanetake H, Saitoh Y, Ichihara A, Tomita Y, Nakamura T. Hepatocyte growth factor is a potent mitogen for cultured rabbit renal tubular epithelial cells. Biochem Biophys Res Commun 174: 831-838, 1991.
36. Jennische E, Ekberg S, Matejka GL. Expression of hepatocyte growth factor in growing regenerating rat skeletal muscle. Am J Physiol Cell Physiol 265: C122-C128, 1993.
37. Kambadur R, Sharma M, Smith TP, Bass JJ. Mutations in myostatin (GDF8) in double-muscled Belgian Blue and Piedmontese cattle. Genome Res 7: 910-916, 1997.
38. Kontaridis MI, Eminaga S, Fornaro M, Zito CI, Sordella R, Settleman J, Bennett AM. SHP-2 positively regulates myogenesis by coupling to the Rho GTPase signaling pathway. Mol Cell Biol 24: 5340-5352, 2004.
39. Kuang S, Rudnicki MA. The emerging biology of satellite cells and their therapeutic potential. Trends Mol Med 14: 82-91, 2008.
40. Langley B, Thomas M, Bishop A, Sharma M, Glimour S, Kambadur R. Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. J Biol Chem 277: 49831-49840, 2002.
41. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 277: 680-685, 1970.
42. Lee SJ, McPherron AC. Regulation of myostatin activity and muscle growth. Proc Natl Acad Sci USA 98: 9306-9311, 2001.
43. Lee SJ. Regulation of muscle mass by myostatin. Annu Rev Cell Dev Biol 20: 61-86, 2004.
44. Li J, Reed SA, Johnson SE. Hepatocyte growth factor (HGF) signals through SHP2 to regulate primary mouse myoblast proliferation. Exp Cell Res 315: 2284-2292, 2009.
45. Lokker NA, Godowski PJ. Generation and characterization of a competitive antagonist of human hepatocyte growth factor, HGF/NK1. J Biol Chem 268: 17145-17150, 1993.
46. Massague J, Wotton D. Transcriptional control by the TGF-beta/Smad signaling system. EMBO J 19: 1745-1754, 2000.
47. McCormick KM, Schultz E. Mechanisms of nascent fiber formation during avian skeletal-muscle hypertrophy. Dev Biol 150: 319-334, 1992.
48. McCroskery S, Thomas M, Maxwell L, Sharma M, Kambadur R. Myostatin negatively regulates satellite cell activation and self renewal. J Cell Biol 162: 1135-1147, 2003.
49. McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-β superfamily member. Nature 387: 83-90, 1997.
50. McPherron AC, Lee SJ. Double muscling in cattle due to mutations in the myostatin gene. Proc Natl Acad Sci USA 94: 12457-12461, 1997.
51. Miller KJ, Thaloor D, Matteson S, Pavlath GK. Hepatocyte growth factor affects satellite cell activation and differentiation in regenerating skeletal muscle. Am J Physiol Cell Physiol 278: C174-C181, 2000.
52. Miyazawa K, Kitamura A, Naka D, Kitamura N. An alternatively processed mRNA generated from human hepatocyte growth factor gene. Eur J Biochem 197: 15-22, 1991.
53. Mohi MG, Neel BG. The role of SHP2 (PTPN11) in cancer. Curr Opin Genet Dev 17: 23-30, 2007.
54. Nakano N, Moriguchi A, Morishita R, Kida I, Tomita N, Natsyniti K, Nakamura T, Higaki J, Ogihara T. Role of angiotensin II in the regulation of novel vascular modulator, hepatocyte growth factor (HGF), in experimental hypertensive rats. Hypertension 30: 1448-1454, 1997.
55. Naldini L, Vigna E, Narshimhan RP, Gaudino G, Zarnegar R, Michalopoulos GK, Comoglio PM. Hepatocyte growth factor (HGF) stimulates the tyrosine kinase activity of the receptor encoded by the protooncogene c-met. Oncogene 6: 501-504, 1991.
56. Neel BG, Gu H, Pao L. The 'Shp'ing news: SH2 domain-containing tyrosine phosphatases in cell signaling. Trends Biochem Sci 28: 284-293, 2003.
57. Olguin HC, Olwin BB. Pax-7 up-regulation inhibits myogenesis and cell cycle progression in satellite cells: a potential mechanism for selfrenewal. Dev Biol 275: 375-388, 2004.
58. Rabbapragada A, Benchabane H, Wrana JL, Celeste AJ, Attisano L. Myostatin signals through a transforming growth factor beta-like signaling pathway to block adipogenesis. Mol Cell Biol 23: 7230-7242, 2003.
59. Reuveny M, Heller H, Bengal E. RhoA controls myoblast survival by inducing the phosphatidylinositol 3-kinase-Akt signaling pathway. FEBS Lett 569: 129-134, 2004.
60. Ridley AJ, Comoglio PM, Hall A. Regulation of Scatter factor/Hepatocyte growth factor responses by Ras, Rac, and Rho in MDCK cells. Mol Cell Biol 15: 1110-1122, 1995.
61. Rios R, Carneiro I, Arce VM, Devesa J. Myostatin regulates cell survival during C2C12 myogenesis. Biochem Biophys Res Commun 280: 561-566, 2001.
62. Rios R, Fernandez-Nocelos S, Carneiro I, Arce VM, Devesa JS. Differential response to exogenous and endogenous myostatin in myoblasts suggests that myostatin acts as an autocrine factor in vivo. Endocrinology 145: 2795-2803, 2004.
63. Rodino-Klapac LR, Haidet AM, Kota J, Handy C, Kaspar BK, Mendell JR. Inhibition of myostatin with emphasis on follistatin as a therapy for muscle disease. Muscle Nerve 39: 283-296, 2009.
64. Rosario M, Birchmeier W. How to make tubes: signaling by the Met receptor tyrosine kinase. Trends Cell Biol 13: 328-335, 2003.
65. Sakata T, Tatsumi R, Yamada M, Shiratsuchi S, Okamoto S, Mizunoya W, Hattori A, Ikeuchi Y. Preliminary experiments on mechanical stretch-induced activation of skeletal muscle satellite cells in vivo. Anim Sci J 77: 518-525, 2006.
66. Schaeper U, Gehring NH, Fuchs KP, Sachs M, Kempkes B, Birchmeier W. Coupling of Gab1 to c-Met, Grb2, and Shp2 mediates biological responses. J Cell Biol 149: 1419-1432, 2000.
67. Schuelke M, Wagner KR, Stolz LE, Hübner C, Riebel T, Kömen W, Braun T, Tobin JF, Lee SJ. Myostatin mutation associated with gross muscle hypertrophy in a child. N Engl J Med 350: 2682-2688, 2004.
68. Schultz E. Satellite cell proliferative compartments in growing skeletal muscles. Dev Biol 175: 84-94, 1996.
69. Schwall RH, Chang LY, Godowski PJ, Kahn DW, Hillan KJ, Bauer KD, Zioncheck TF. Heparin induces dimerization and confers proliferative activity onto the hepatocyte growth factor antagonists NK1 and NK2. J Cell Biol 133: 709-718, 1996.
70. Seale P, Rudnicki MA. A new look at the origin, function, and "Stem-Cell" status of muscle satellite cells. Dev Biol 218: 115-124, 2000.
71. Serini G, Valdembri D, Zanivan S, Morterra G, Burkhardt C, Caccavari F, Zammataro L, Primo L, Tamagnone L, Logan M, Tessier-Lavigne M, Taniguchi M, Püschel AW, Bussolino F. Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature 424: 391-397, 2003.
72. Sharma M, Kambadur R, Matthews KG, Somers WG, Devlin GP, Conaglen JV, Fowke PJ, Bass JJ. Myostatin, a transforming growth factor-β superfamily member, is expressed in heart muscle and is upregulated in cardiomyocytes after infarct. J Cell Physiol 180: 1-9, 1999.
73. Sheehan SM, Tatsumi R, Temm-Grove CJ, Allen RE. HGF is an autocrine growth factor for skeletal muscle satellite cells in vitro. Muscle Nerve 23: 239-245, 2000.
74. Sherr CJ, Roberts JM. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 13: 1501-1512, 1999.
75. Smith HK, Maxwell L, Rodgers CD, Mckee NH, Plyley MJ. Exerciseenhanced satellite cell proliferation and new myonuclear accretion in rat skeletal muscle. J Appl Physiol 90: 1407-1414, 2001.
76. Suzuki S, Yamanouchi K, Soeta C, Katakai Y, Harada R, Naito K, Tojo H. Skeletal muscle injury induces hepatocyte growth factor expression in spleen. Biochem Biophys Res Commun 292: 709-714, 2002.
77. Swierczynski J, Korczynska J, Goyke E, Adrych K, Raczynska S, Sledzinski Z. Serum hepatocyte growth factor concentration in obese women decreases after vertical banded gastroplasty. Obes Surg 15: 803-808, 2005.
78. Tamagnone L, Comoglio PM. Signalling by semaphorin receptors: cell guidance and beyond. Trends Cell Biol 10: 377-383, 2000.
79. Tanaka S, Tachino K, Kawahara E, Tanaka J, Funakoshi H, Nakamura T. Hepatocyte growth factor in mouse soleus muscle increases with reloading after unloading. J Phys Ther Sci 18: 33-41, 2006.
80. 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 194: 114-128, 1998.
81. Tatsumi R, Sheehan SM, Iwasaki H, Hattori A, Allen RE. Mechanical stretch induces activation of skeletal muscle satellite cells in vitro. Exp Cell Res 267: 107-114, 2001.
82. Tatsumi R, Hattori A, Allen RE, Ikeuchi Y, Ito T. Mechanical stretch-induced activation of skeletal muscle satellite cells is dependent on nitric oxide production in vitro. Anim Sci J 73: 235-239, 2002.
83. Tatsumi R, Hattori A, Ikeuchi Y, Anderson JE, Allen RE. Release of hepatocyte growth factor from mechanical stretched skeletal muscle satellite cells and the role of pH and nitric oxide. Mol Biol Cell 13: 2909-2918, 2002.
84. Tatsumi R, Allen RE. Active hepatocyte growth factor is present in skeletal muscle extracellular matrix. Muscle Nerve 30: 654-658, 2004.
85. Tatsumi R, Liu X, Pulido A, Morales M, Sakata T, Dial S, Hattori A, Ikeuchi Y, Allen RE. Satellite cell activation in stretched skeletal muscle and the role of nitric oxide and hepatocyte growth factor. Am J Physiol Cell Physiol 290: C1487-C1494, 2006.
86. Tatsumi R, Yamada M, Katsuki Y, Okamoto S, Ishizaki J, Mizunoya W, Ikeuchi Y, Hattori A, Shimokawa H, Allen RE. Low-pH preparation of skeletal muscle satellite cells can be used to study activation in vitro. Int J Biochem Cell Biol 38: 1678-1685, 2006.
87. Tatsumi R, Allen RE. Mechano-biology of resident myogenic stem cells: molecular mechanism of stretch-induced activation of satellite cells. Anim Sci J 79: 279-290, 2008.
88. Tatsumi R, Wuollet AL, Tabata K, Nishimura S, Tabata S, Mizunoya W, Ikeuchi Y, Allen RE. A role for calcium-calmodulin in regulating nitric oxide production during skeletal muscle satellite cell activation. Am J Physiol Cell Physiol 296: C922-C929, 2009.
89. Tatsumi R, Sankoda Y, Anderson JE, Sato Y, Mizunoya W, Shimizu N, Suzuki T, Yamada M, Rhoads RP Jr, Ikeuchi Y, Allen RE. Possible implication of satellite cells in regenerative motoneuritogenesis: HGF up-regulates neural chemorepellent Sema3A during myogenic differentiation. Am J Physiol Cell Physiol 297: C238-C252, 2009.
90. Tatsumi R. Mechano-biology of skeletal muscle hypertrophy and regeneration: possible mechanism of stretch-induced activation of resident myogenic stem cells. Anim Sci J. In press.
91. Tatsumi R, Yamanouchi K, Hosoyama T, Shiratsuchi SI, Yamada M, Mizunoya W, Ikeuchi Y, Allen RE. A possible mechanism for muscle satellite cell quiescence: HGF induces myostatin expression and secretion (Abstract). FASEB Summer Research Conference on Skeletal Muscle and Stem Cells, Tucson, AZ, June 11-16, 2005.
92. Thomas M, Langley B, Berry C, Sharma M, Kirk S, Bass J, Kambadur R. Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. J Biol Chem 275: 40235-40243, 2000.
93. Trusolino L, Comoglio PM. Scatter-factor and semaphorin receptors: cell signaling for invasive growth. Nat Rev 2: 289-300, 2002.
94. Tsukada Y, Tanaka T, Miyazawa K, Kitamura N. Involvement of down-regulation of Cdk2 activity in hepatocyte growth factor-induced cell cycle arrest at G1 in the human hepatocellular carcinoma cell line HepG2. J Biochem (Tokyo) 186: 701-709, 2004.
95. Wagers AJ, Conboy IM. Cellular and molecular signatures of muscle regeneration: current concepts and controversies in adult myogenesis. Cell 122: 659-667, 2005.
96. Wagner KR, Liu X, Chang X, Allen RE. Muscle regeneration in the prolonged absence of myostatin. Proc Natl Acad Sci USA 102: 2519-2524, 2005.
97. Winchester PK, Davis ME, Alway SE, Gonyea WJ. Satellite cell activation in the stretch-enlarged anterior latissimus-dorsi muscle of the adult quail. Am J Physiol Cell Physiol 260: C206-C212, 1991.
98. Wolfman NM, Mcpherron AC, Pappano WN, Davies MV, Song K, Tomkinson KN, Wright JF, Zhao L, Sebald SM, Greenspspan DS, Leet SI. Activation of latent myostatin by the BMP-1/tolloid family of metalloproteinases. Proc Natl Acad Sci USA 100: 15842-15846, 2003.
99. 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 51: 1-9, 2003.
100. Wozniak AC, Anderson JE. Single-fiber isolation and maintenance of satellite cell quiescence. Biochem Cell Biol 83: 674-676, 2005.
101. Wozniak AC, Kong JM, Bock E, Pilipowicz O, Anderson JE. Signaling satellite-cell activation in skeletal muscle: markers, models, stretch, and potential alternate pathways. Muscle Nerve 31: 283-300, 2005.
102. Wozniak AC, Anderson JE. Nitric oxide-dependence of satellite stem cell activation and quiescence on normal skeletal muscle fibers. Dev Dyn 236: 240-250, 2007.
103. Wozniak AC, Anderson JE. The dynamics of the nitric oxide release-transient from stretched muscle cells. Int J Biochem Cell Biol 41: 625-631, 2009.
104. Yamada M, Tatsumi R, Kikuiri T, Okamoto S, Nonoshita S, Mizunoya W, Ikeuchi Y, Shimokawa H, Sunagawa K, Allen RE. Matrix metalloproteinases are involved in mechanical stretch-induced activation of skeletal muscle satellite cells. Muscle Nerve 34: 313-319, 2006.
105. Yamada M, Sankoda Y, Tatsumi R, Mizunoya W, Ikeuchi Y, Sunagawa K, Allen RE. Matrix metalloproteinase-2 mediates stretchinduced activation of skeletal muscle satellite cells in a nitric oxide dependent manner. Int J Biochem Cell Biol 40: 2183-2191, 2008.
106. Yoshida N, Yoshida S, Koishi K, Masuda K, Nabeshima Y. Cell heterogeneity upon differentiation: down-regulation of MyoD and Myf-5 generates 'reserve cells'. J Cell Sci 111: 769-779, 1998.
107. Zammit PS, Golding JP, Nagata Y, Hudon V, Partridge TA, Beauchamp JR. Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J Cell Biol 166: 347-357, 2004.