Abstract
Muscle regeneration supports muscle function in aging, and plays a role in the functional impairment caused by progressive neuromuscular diseases. Major substances controlling this process are growth factors and the extracellular matrix (ECM). Thus, follistatin is known to antagonize the function of several members of the TGF-β family of secreted signaling factors, including myostatin—the most powerful inhibitor of muscle growth characterized to date. Decorin—a small leucine-rich proteoglycan—traps myostatin and modulates its activity towards myogenic cells in the ECM. In addition, there are few reports concerning the regenerative muscle process of masseter muscles, which are of branchial arch origin, in mdx mice. Thus, in order to clarify the muscle regenerative process of masseter muscle, gene and protein expression of myostatin, follistatin and decorin were examined using the tibialis anterior (TA)muscle as a positive control. In both muscles, a gradual increase in mRNA myostatin, follistatin and decorin expression was detected, with the increase being greater in TA muscle than in masseter muscle. At 2 weeks, both muscles exhibited normal skeletal muscle cells. At 3 weeks, masseter muscle demonstrated scant areas of necrosis, whereas large necrotic zones were seen in TA muscle. At 4 weeks, the formation of necrotic tissue and presence of follistatin protein was observed clearly in masseter muscle. This result indicates that follistatin production is stimulated in the presence of necrosis. Interestingly, both muscles showed the same process of muscular formation, but with different time frames, which could be related to muscle origin.
Similar content being viewed by others
References
Abe S, Soejima M, Iwanuma O et al (2009a) Expression of myostatin and follistatin in Mdx mice, an animal model for muscular dystrophy. Zool Sci 26:315–320
Abe S, Hirose D, Kado S et al (2009b) Increased expression of decorin during the regeneration stage of mdx mouse. Anat Sci Int 84:305–311
Allen RE, Rankin LL (1990) Regulation of satellite cells during skeletal muscle growth and development. Proc Soc Exp Biol Med 194:81–86
Amthor H, Connolly D, Patel K et al (1996) The expression and regulation of follistatin and a follistatin-like gene during avian somite compartmentalization and myogenesis. Dev Biol 178:343–362
Amthor H, Christ B, Rashid-Doubell F, Kemp CF, Lang E, Patel K (2002) Follistatin regulates bone morphogenetic protein-7 (BMP-7) activity to stimulate embryonic muscle growth. Dev Biol 243:115–127
Amthor H, Nicholas G, McKinnell I et al (2004) Follistatin complexes myostatin and antagonises myostatin-mediated inhibition of myogenesis. Dev Biol 270:19–30
Armand AS, Della Gaspera B, Launay T, Charbonnier F, Gallien CL, Chanoine C (2003) Expression and neural control of follistatin versus myostatin genes during regeneration of mouse soleus. Dev Dyn 227:256–265
Brandan E, Fuentes ME, Andrade W (1991) The proteoglycan decorin is synthesized and secreted by differentiated myotubes. Eur J Cell Biol 55:209–216
Bulfield G, Siller WG, Wight PA, Moore KJ (1984) X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 81:1189–1192
Dangain J, Vrbova G (1984) Muscle development in mdx mutant mice. Muscle Nerve 7:700–704
DiMario JX, Uzman A, Strohman RC (1991) Fiber regeneration is not persistent in dystrophic (MDX) mouse skeletal muscle. Dev Biol 148:314–321
Florini JR, Ewton DZ, Magri KA (1991) Hormones, growth factors, and myogenic differentiation. Annu Rev Physiol 53:201–216
Florini JR, Ewton DZ, Coolican SA (1996) Growth hormone and the insulin-like growth factor system in myogenesis. Endocr Rev 17:481–517
Floss T, Arnold HH, Braun T (1997) A role for FGF-6 in skeletal muscle regeneration. Genes Dev 11:2040–2051
Gillis JM (1996) Membrane abnormalities and Ca homeostasis in muscles of the mdx mouse, an animal model of the Duchenne muscular dystrophy: a review. Acta Physiol Scand 156:397–406
Hawke TJ, Garry DJ (2001) Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91:534–551
Hill JJ, Davies MV, Pearson AA et al (2002) The myostatin propeptide and the follistatin-related gene are inhibitory binding proteins of myostatin in normal serum. J Biol Chem 277:40735–40741
Hoffman EP, Brown RH Jr, Kunkel LM (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51:919–928
Hosoyama T, Kawada S, Oshiumi R et al (2002) Molecular cloning of equine (thoroughbred) myostatin cDNA and detection of myostatin precursor proteins in the serum. J Reprod Dev 48:335–342
Kirk S, Oldham J, Kambadur R, Sharma M, Dobbie P, Bass J (2000) Myostatin regulation during skeletal muscle regeneration. J.Cell Physiol 184:356–363
Kishioka Y, Thomas M, Wakamatsu J et al (2008) Decorin enhances the proliferation and differentiation of myogenic cells through suppressing myostatin activity. J Cell Physiol 215:856–867
Lee SJ, McPherron AC (2001) Regulation of myostatin activity and muscle growth. Proc Natl Acad Sci USA 98:9306–9311
Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495
McCroskery S, Thomas M, Platt A et al (2005) Improved muscle healing through enhanced regeneration and reduced fibrosis in myostatin-null mice. J Cell Sci 118:3531–3541
McPherron AC, Lawler AM, Lee SJ (1997) Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387:83–90
Miller KJ, Thaloor D, Matteson S, Pavlath GK (2000) Hepatocyte growth factor affects satellite cell activation and differentiation in regenerating skeletal muscle. Am J Physiol Cell Physiol 278:C174–C181
Miura T, Kishioka Y, Wakamatsu J et al (2006) Decorin binds myostatin and modulates its activity to muscle cells. Biochem Biophys Res Commun 340:675–680
Muller J, Vayssiere N, Royuela M et al (2001) Comparative evolution of muscular dystrophy in diaphragm, gastrocnemius and masseter muscles from old male mdx mice. J Muscle Res Cell Motil 22:133–139
Nishimura T, Oyama K, Kishioka Y, Wakamatsu J, Hattori A (2007) Spatiotemporal expression of decorin and myostatin during rat skeletal muscle development. Biochem Biophys Res Commun 361:896–902
Ríos R, Carneiro I, Arce VM, Devesa J (2002) Myostatin is an inhibitor of myogenic differentiation. Am J Physiol Cell Physiol 282:C993–C999
Schultz E, Jaryszak DL, Valliere CR (1985) Response of satellite cells to focal skeletal muscle injury. Muscle Nerve 8:217–222
Sidis Y, Mukherjee A, Keutmann H, Delbaere A, Sadatsuki M, Schneyer A (2006) Biological activity of follistatin isoforms and follistatin-like-3 is dependent on differential cell surface binding and specificity for activin, myostatin, and bone morphogenetic proteins. Endocrinology 147:3586–3597
Thomas M, Langley B, Berry C et al (2000) Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. J Biol Chem 275:40235–40243
Torres LF, Duchen LW (1987) The mutant mdx: inherited myopathy in the mouse. Morphological studies of nerves, muscles and end-plates. Brain 110(Pt 2):269–299
Whittemore LA, Song K, Li X et al (2003) Inhibition of myostatin in adult mice increases skeletal muscle mass and strength. Biochem Biophys Res Commun 300:965–971
Zhu J, Li Y, Shen W et al (2007) Relationships between transforming growth factor-beta1, myostatin, and decorin: implications for skeletal muscle fibrosis. J Biol Chem 282:25852–25863
Acknowledgments
This research was supported by Oral Health Science Center Grant hrc8 (S.A.) from Tokyo Dental College, and by a Project for Private Universities: matching fund subsidy from MEXT (Ministry of Education, Culture, Sports, Science and Technology) of Japan, 2010–2012.
Author information
Authors and Affiliations
Corresponding author
Additional information
E. Hiroki and S. Abe contributed equally to this work.
Rights and permissions
About this article
Cite this article
Hiroki, E., Abe, S., Iwanuma, O. et al. A comparative study of myostatin, follistatin and decorin expression in muscle of different origin. Anat Sci Int 86, 151–159 (2011). https://doi.org/10.1007/s12565-011-0103-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12565-011-0103-0