CILP1 is dynamically expressed in the developing musculoskeletal system of the trout

Abstract

An in situ screen for genes expressed in the skeletal muscle of eyed-stage trout embryos led to the identification of a transcript encoding a polypeptide related to CILP1, a secreted glycoprotein present in the extracellular matrix. In situ hybridisation in developing trout embryos revealed that CILP1 expression was initially detected in fast muscle progenitors of the early somite. Later, CILP1 expression was down-regulated medio-laterally in differentiating fast muscle cells, to become finally restricted to the undifferentiated muscle progenitors forming the dermomyotomelike epithelium at the surface of the embryonic myotome. At the completion of somitogenesis, CILP1 expression was concentrated in the myoseptal/tendon cells that develop between adjacent myotomes but was excluded from the skeletogenic cells of the vertebral axis to which the most medial myoseptal/tendon cells attach. Overall, our work shows that muscle cells and myoseptal/ tendon cells contribute dynamically and cooperatively to the production of CILP1 during ontogeny of the trout musculoskeletal system. KEY WORDS: CILP1, somite, myotome, dermomyotome, myoseptal cell, teleostIn fish, the musculoskeletal system is a multicomponent system composed of W-shaped myomeres, myosepta and the axial skeleton. Myomeres arise from somites that are generated repeatedly from the presomitic mesoderm in an anterior to posterior progression. Two main muscle fibre types differentiate within somites: the superficial slow muscle fibres and the deep fast muscle fibres. Embryonic slow muscle fibres originate from adaxial cells, initially deep in the somite, that migrate radially to reach the lateral surface of the developing myotome, while embryonic fast muscle fibres derive from myogenic muscle cell precursors located in the posterior somitic compartment (for review see Bryson-Richardson and Currie, 2008). Cells of the anterior somitic compartment form a superficial dermomyotome-like epithelium surrounding the slow muscle fibres. This epithelium provides the myogenic precursor cells necessary for the growth of the embryonic myotome (Hollway et al., 2007;Stellabotte et al., 2007, Steinbacher et al., 2008. The fish myosepta that separate adjacent myomeres are medially inserted on the bony axial skeleton and are laterally connected to the collagenous dermis. Like tendons in amniotes, fish myosepta serve as transmitters of muscle contractility to bones. In the developing fish embryo, the myosepta are initially acellular and composed of matricial compounds such as fibronectin, laminin and collagens (Henry et al., 2005;Charvet et al., 2011;Bricard et al., 2014 ent in the intersomitic space (Charvet et al., 2011;Bricard et al., 2014;Chen and Galloway., 2014;Subramanian and Schilling., 2014). These myoseptal cells are considered homologous to axial tenocytes in amniotes: they express scleraxis, tenomodulin and tendon associated collagens (Bricard et al., 2014;Chen and Galloway, 2014) and, like axial tenocytes in amniotes (Brent et al., 2003), they probably originat...

Single cell dynamics of embryonic muscle progenitor cells in zebrafish

“…Second, we found that embryonic MPCs in the dermomyotome express a number of ECM genes, including col1a2, col5a1 and cilp. Similarly, col1a1 and cilp are expressed in what is described as a dermomyotome-like domain in trout embryos (Ralliere et al, 2015;Rescan et al, 2005). Moreover, we found that the expression of these ECM genes is dynamically induced during muscle regeneration.…”

Origin and diversification of fibroblasts from the sclerotome in zebrafish

“…We and others have previously shown that tenocytes are located along the myotendinous junction (MTJ), extending long cellular processes into the intersomitic space (Fig 2A) (Ma et al, 2018; Subramanian et al, 2018). Marker analysis revealed that nkx3.1 NTR-mCherry -positive cells along the MTJ were specifically labeled by known tendon markers such as scxa, cilp , and tnmd (Chen and Galloway, 2014; Ralliere et al, 2015) (Fig 2C). By contrast, interstitial fibroblasts were scattered throughout the interstitial space and displayed varied morphologies (Fig 1C and 2A).…”

Formation of intramuscular connective tissue network in fish: first insight from the rainbow trout (Oncorhynchus mykiss)

“…Myoseptal cells become apparent between adjacent myomeres only after the completion of somitogenesis (Bricard et al, 2014;Charvet et al, 2011;Chen & Galloway, 2014). These myoseptal cells that express scleraxis and tendon associated collagens are considered homologous to axial tenocytes in amniotes (Bricard et al, 2014;Chen & Galloway, 2014;Ralliere et al, 2015;Subramanian & Schilling, 2014). Similar to the axial tenocytes in amniotes (Brent et al, 2003), myoseptal cells are likely to originate from a syndetome compartment that derives from a subdomain of the early fish sclerotome.…”