Abstract
The adult skeletal muscle stem cells, satellite cells, are responsible for skeletal muscle growth and regeneration. Satellite cells represent a heterogeneous cell population that differentially express cell surface markers. The membrane-associated heparan sulfate proteoglycans, syndecan-4, and glypican-1, are differentially expressed by satellite cells during the proliferation and differentiation stages of satellite cells. However, how the population of syndecan-4- or glypican-1-positive satellite cells changes during proliferation and differentiation, and how sex and muscle growth potential affect the expression of these genes is unknown. Differences in the amount of satellite cells positive for syndecan-4 or glypican-1 would affect the process of proliferation and differentiation which would impact both muscle mass accretion and the regeneration of muscle. In the current study, the percentage of satellite cells positive for syndecan-4 or glypican-1 from male and female turkeys from a Randombred Control Line 2 and a line (F) selected for increased 16-week body weight were measured during proliferation and differentiation. Growth selection altered the population of syndecan-4- and glypican-1-positive satellite cells and there were sex differences in the percentage of syndecan-4- and glypican-1-positive satellite cells. This study provides new information on dynamic changes in syndecan-4- and glypican-1-positive satellite cells showing that they are differentially expressed during myogenesis and growth selection and sex affects their expression.
Similar content being viewed by others
References
Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495
Moss FP, Leblond CP (1971) Satellite cells as the source of nuclei in muscles of growing rats. Anat Rec 170:421–435
Kuang S, Kuroda K, Le Grand F, Rudnicki MA (2007) Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129:999–1010
Schultz E, Gibson MC, Champion T (1978) Satellite cells are mitotically quiescent in mature mouse muscle: an EM and radioautographic study. J Exp Zool 206:451–456
Cornelison DD, Wold BJ (1997) Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol 191:270–283
Chargé SB, Rudnicki MA (2004) Cellular and molecular regulation of muscle regeneration. Physiol Rev 84:209–238
Dhawan J, Rando TA (2005) Stem cells in postnatal myogenesis: molecular mechanisms of satellite cell quiescence, activation and replenishment. Trends Cell Biol 15:666–673
Parker MH, Seale P, Rudnicki MA (2003) Looking back to the embryo: defining transcriptional networks in adult myogenesis. Nat Rev Genet 4:497–507
Armand O, Boutineau AM, Mauger A, Pautou MP, Kieny M (1983) Origin of satellite cells in avian skeletal muscles. Arch Anat Microsc Morphol Exp 72:163–181
Gros J, Manceau M, Thome V, Marcelle C (2005) A common somitic origin for embryonic muscle progenitors and satellite cells. Nature 435:954–958
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 19:1426–1431
Relaix F, Rocancourt D, Mansouri A, Buckingham M (2005) A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435:948–953
Harel I, Nathan E, Tirosh-Finkel L, Zigdon H, Guimarães-Camboa N, Evans SM, Tzahor E (2009) Distinct origins and genetic programs of head muscle satellite cells. Dev Cell 16:822–832
Sambasivan R, Gayraud-Morel B, Dumas G, Cimper C, Paisant S, Kelly RG, Tajbakhsh S (2009) Distinct regulatory cascades govern extraocular and pharyngeal arch muscle progenitor cell fates. Dev Cell 16:810–821
Biressi S, Rando TA (2010) Heterogeneity in the muscle satellite cell population. Semin Cell Dev Biol 21:845–854
Day K, Shefer G, Richardson JB, Enikolopov G, Yablonka-Reuveni Z (2007) Nestin-GFP reporter expression defines the quiescent state of skeletal muscle satellite cells. Dev Biol 304:246–259
Beauchamp JR, Heslop L, Yu DSW, Tajbakhsh S, Kelly RG, Wernig A (2000) Expression of Cd34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J Cell Biol 151:1221–1234
McFarland DC, Pesall JE, Gilkerson KK, Ye WV, Walker JS, Wellenreiter R (1995) Comparison of in vitro properties of satellite cells derived from the pectoralis major and biceps femoris muscles of growing turkeys. Basic Appl Myol 5:27–31
Yun Y, McFarland DC, Pesall JE, Gilkerson KK, Vander Wal LS, Ferrin NH (1997) Variation in response to growth factor stimuli in satellite cell populations. Comp Biochem Physiol 117A:463–470
Hawke TJ, Garry DJ (2001) Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91:534–551
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
Irintchev A, Zeschnigk M, Starzinski-Powitz A, Wernig A (1994) Expression pattern of M-cadherin in normal, denervated, and regenerating mouse muscles. Dev Dyn 199:326–337
Tajbakhsh S, Rocancourt D, Cossu G, Buckingham M (1997) Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 89:127–138
Shefer G, Van de Mark DP, Richardson JB, Yablonka-Reuveni Z (2006) Satellite-cell pool size does matter: defining the myogenic potency of aging skeletal muscle. Dev Biol 294:50–66
Cornelison DD, Filla MS, Stanley HM, Rapraeger AC, Olwin BB (2001) Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration. Dev Biol 239:79–94
Nagata Y, Kobayashi H, Umeda M, Ohta N, Kawashima S, Zammit P, Matsuda R (2006) Sphingomyelin levels in the plasma membrane correlate with the activation state of muscle satellite cells. J Histochem Cytochem 54:375–384
Volonte D, Liu Y, Galbiati F (2005) The modulation of caveolin-1 expression controls satellite cell activation during muscle repair. FASEB J 19:237–239
Füchtbauer EM, Westphal H (1992) MyoD and myogenin are coexpressed in regenerating skeletal muscle of the mouse. Dev Dyn 193:34–39
Grounds MD, Garrett KL, Lai MC, Wright WE, Beilharz MW (1992) Identification of skeletal muscle precursor cells in vivo by use of MyoD1 and myogenin probes. Cell Tissue Res 267:99–104
Yablonka-Reuveni Z, Rivera AJ (1994) Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers. Dev Biol 164:588–603
Smith TH, Block NE, Rhodes SJ, Konieczny SF, Miller JB (1993) A unique pattern of expression of the four muscle regulatory factor proteins distinguishes somitic from embryonic, fetal and newborn mouse myogenic cells. Development 117:1125–1133
Smith TH, Kachinsky AM, Miller JB (1994) Somite subdomains, muscle cell origins, and the four muscle regulatory factor proteins. J Cell Biol 127:95–105
Velleman SG, Liu C, Coy CS, McFarland DC (2006) Effects of glypican-1 on turkey skeletal muscle cell proliferation, differentiation and fibroblast growth factor 2 responsiveness. Dev Growth Differ 48:271–276
Zhang X, Liu C, Nestor KE, McFarland DC, Velleman SG (2007) The effect of glypican-1 glycosaminoglycan chains on turkey myogenic satellite cell proliferation, differentiation, and fibroblast growth factor 2 responsiveness. Poult Sci 86:2020–2028
Zhang X, Nestor KE, McFarland DC, Velleman SG (2008) The role of syndecan-4 and attached glycosaminoglycan chains on myogenic satellite cell growth. Matrix Biol 27:619–630
Song Y, McFarland DC, Velleman SG (2011) Role of syndecan-4 side chains in turkey satellite cell growth and development. Dev Growth Differ 53:97–109
Song Y, Nestor KE, McFarland DC, Velleman SG (2010) Effect of glypican-1 covalently attached chains on turkey myogenic satellite cell proliferation, differentiation, and fibroblast growth factor 2 responsiveness. Poult Sci 89:123–134
Shin J, McFarland DC, Velleman SG (2013) Migration of turkey muscle satellite cells is enhanced by the syndecan-4 cytoplasmic domain through the activation of RhoA. Mol Cell Biochem 375:115–130
Velleman SG, Song Y, Shin J, McFarland DC (2013) Modulation of turkey myogenic satellite cell differentiation through the shedding of glypican-1. Comp Biochem Physiol Pt A 164:36–43
Velleman SG, Liu X, Nestor KE, McFarland DC (2000) Heterogeneity in growth and differentiation characteristics in male and female satellite cells isolated from turkey lines with different growth rates. Comp Biochem Physiol A 125:503–509
Nestor KE (1977) The influence of a genetic change in egg production, body weight, fertility or response to cold stress on semen yield in the turkey. Poult Sci 56:421–425
Lilburn MS, Nestor KE (1991) Body weight and carcass development in different lines of turkeys. Poult Sci 70:2223–2231
Liu C, McFarland DC, Velleman SG (2005) Effect of genetic selection on MyoD and myogenin expression in turkeys with different growth rates. Poult Sci 84:376–384
Summers PJ, Medrano JF (1997) Delayed myogenesis associated with muscle fiber hyperplasia in high-growth mice. Proc Soc Exp Biol Med 214:380–385
Kuang S, Rudnicki MA (2008) The emerging biology of satellite cells and their therapeutic potential. Trends Mol Med 14:82–91
Liu C, McFarland DC, Nestor KE, Velleman SG (2006) Differential expression of membrane-associated heparan sulfate proteoglycans in the skeletal muscle of turkeys with different growth rates. Poult Sci 85:422–428
Gutiérrez J, Brandan E (2010) A novel mechanism of sequestering fibroblast growth factor 2 by glypican lipid rafts, allowing skeletal muscle differentiation. Mol Cell Biol 30:1634–1639
Volk R, Schwartz JJ, Li J, Rosenberg RD, Simons M (1999) The role of syndecan cytoplasmic domain in basic fibroblast growth factor-dependent signal transduction. J Biol Chem 274:24417–24424
Dollenmeier P, Turner DC, Eppenberger HM (1981) Proliferation and differentiation of chick skeletal muscle cells cultured in a chemically defined medium. Exp Cell Res 135:47–61
Liu X, McFarland DC, Nestor KE, Velleman SG (2003) Expression of fibroblast growth factor 2 and its receptor during skeletal muscle development from turkeys with different growth rates. Dom Anim Endocrinol 25:215–219
Steinfeld R, Van Den Berghe H, David G (1996) Stimulation of fibroblast growth factor receptor-1 occupancy and signaling by cell surface-associated syndecans and glypican. J Cell Biol 133:405–416
Manzano R, Toivonen JM, Calvo AC, Miana-Mena FJ, Zaragoza P, Muňoz MJ, Montarras D, Osta R (2011) Sex, fiber-type, and age dependent in vitro proliferation of mouse muscle satellite cells. J Cell Biochem 112:2825–2836
Acknowledgments
Salary and partial research support to S.G.V. provided by state and federal funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University, the National Institute of Food and Agriculture Multistate Project NC-1184 to S.G.V. and D.C.M., and the National Research Initiative Competitive Grant No. 2009-35503-05176 to S.G.V. from the USDA National Institute of Food and Agriculture are acknowledged.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Song, Y., McFarland, D.C. & Velleman, S.G. Growth and sex effects on the expression of syndecan-4 and glypican-1 in turkey myogenic satellite cell populations. Mol Cell Biochem 378, 65–72 (2013). https://doi.org/10.1007/s11010-013-1594-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11010-013-1594-x