Abstract
Satellite cells, muscle-specific stem cells, are anatomically identified as the mononuclear cells residing external to the myofiber plasma membrane and beneath the basal lamina. Skeletal muscle has great regenerative potential, and the regeneration process depends absolutely on satellite cells. In uninjured muscle, satellite cells are maintained in a quiescent state, and some genes are expressed in a quiescent-specific manner. Here we show that Odz4/Ten-m4, a mouse homolog of the Drosophila pair-rule gene odd Oz (odz or Ten-m), is expressed in quiescent satellite cells on the protein level, but not in activated/proliferating myoblasts. Intriguingly, the timing of the reappearance of Odz4 and calcitonin receptor (another quiescence molecule) on Pax7-positive cells was different during the regeneration process. In addition, almost all neonatal satellite cells express Odz4, but only some of them express calcitonin receptor. These results indicate that Odz4 may be useful as a new marker of satellite cells and that quiescence molecules are differently expressed in regenerating and neonatal muscle.
Similar content being viewed by others
References
Bagutti C, Forro G, Ferralli J, Rubin B, Chiquet-Ehrismann R (2003) The intracellular domain of teneurin-2 has a nuclear function and represses zic-1-mediated transcription. J Cell Sci 116:2957–2966
Beauchamp JR, Heslop L, Yu DS, Tajbakhsh S, Kelly RG, Wernig A, Buckingham ME, Partridge TA, Zammit PS (2000) Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J Cell Biol 151:1221–1234
Charge SB, Rudnicki MA (2004) Cellular and molecular regulation of muscle regeneration. Physiol Rev 84:209–238
Cheung TH, Quach NL, Charville GW, Liu L, Park L, Edalati A, Yoo B, Hoang P, Rando TA (2012) Maintenance of muscle stem-cell quiescence by microRNA-489. Nature 482:524–528
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
Drabikowski K, Trzebiatowska A, Chiquet-Ehrismann R (2005) ten-1, an essential gene for germ cell development, epidermal morphogenesis, gonad migration, and neuronal pathfinding in Caenorhabditis elegans. Dev Biol 282:27–38
Fukada S, Higuchi S, Segawa M, Koda K, Yamamoto Y, Tsujikawa K, Kohama Y, Uezumi A, Imamura M, Miyagoe-Suzuki Y, Takeda S, Yamamoto H (2004) Purification and cell-surface marker characterization of quiescent satellite cells from murine skeletal muscle by a novel monoclonal antibody. Exp Cell Res 296:245–255
Fukada S, Uezumi A, Ikemoto M, Masuda S, Segawa M, Tanimura N, Yamamoto H, Miyagoe-Suzuki Y, Takeda S (2007) Molecular signature of quiescent satellite cells in adult skeletal muscle. Stem Cells 25:2448–2459
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
Kuang S, Rudnicki MA (2008) The emerging biology of satellite cells and their therapeutic potential. Trends Mol Med 14:82–91
Leamey CA, Glendining KA, Kreiman G, Kang ND, Wang KH, Fassler R, Sawatari A, Tonegawa S, Sur M (2008) Differential gene expression between sensory neocortical areas: potential roles for Ten_m3 and Bcl6 in patterning visual and somatosensory pathways. Cereb Cortex 18:53–66
Lepper C, Conway SJ, Fan CM (2009) Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature 460:627–631
Levine A, Bashan-Ahrend A, Budai-Hadrian O, Gartenberg D, Menasherow S, Wides R (1994) Odd Oz: a novel Drosophila pair rule gene. Cell 77:587–598
Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495
Oohashi T, Zhou XH, Feng K, Richter B, Morgelin M, Perez MT, Su WD, Chiquet-Ehrismann R, Rauch U, Fassler R (1999) Mouse ten-m/Odz is a new family of dimeric type II transmembrane proteins expressed in many tissues. J Cell Biol 145:563–577
Pallafacchina G, Francois S, Regnault B, Czarny B, Dive V, Cumano A, Montarras D, Buckingham M (2010) An adult tissue-specific stem cell in its niche: a gene profiling analysis of in vivo quiescent and activated muscle satellite cells. Stem Cell Res 4:77–91
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
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
Segawa M, Fukada S, Yamamoto Y, Yahagi H, Kanematsu M, Sato M, Ito T, Uezumi A, Hayashi S, Miyagoe-Suzuki Y, Takeda S, Tsujikawa K, Yamamoto H (2008) Suppression of macrophage functions impairs skeletal muscle regeneration with severe fibrosis. Exp Cell Res 314:3232–3244
Sherwood RI, Christensen JL, Conboy IM, Conboy MJ, Rando TA, Weissman IL, Wagers AJ (2004) Isolation of adult mouse myogenic progenitors: functional heterogeneity of cells within and engrafting skeletal muscle. Cell 119:543–554
Tatsumi R, Anderson JE, Nevoret CJ, Halevy O, Allen RE (1998) HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev Biol 194:114–128
Tucker RP, Chiquet-Ehrismann R (2006) Teneurins: a conserved family of transmembrane proteins involved in intercellular signaling during development. Dev Biol 290:237–245
Uezumi A, Ojima K, Fukada S, Ikemoto M, Masuda S, Miyagoe-Suzuki Y, Takeda S (2006) Functional heterogeneity of side population cells in skeletal muscle. Biochem Biophys Res Commun 341:864–873
Zhou XH, Brandau O, Feng K, Oohashi T, Ninomiya Y, Rauch U, Fassler R (2003) The murine Ten-m/Odz genes show distinct but overlapping expression patterns during development and in adult brain. Gene Expr Patterns 3:397–405
Acknowledgments
We thank Dr. Reinhard Faessler for anti-Odz4 antibody. We thank Katherine Ono for reading this manuscript. This work was supported by a JSPS KAKENHI grant (18800023 to S.F.), MEXT KAKENHI grants (20700358 to S.F), Intramural Research Grant (22-1 to S.F.) for Neurological and Psychiatric Disorders of NCNP, and the Nakatomi Foundation (to S.F.).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Yamaguchi, M., Ogawa, R., Watanabe, Y. et al. Calcitonin receptor and Odz4 are differently expressed in Pax7-positive cells during skeletal muscle regeneration. J Mol Hist 43, 581–587 (2012). https://doi.org/10.1007/s10735-012-9421-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10735-012-9421-3