Early Fish Myoseptal Cells: Insights from the Trout and Relationships with Amniote Axial Tenocytes

Abstract

The trunk muscle in fish is organized as longitudinal series of myomeres which are separated by sheets of connective tissue called myoseptum to which myofibers attach. In this study we show in the trout that the myoseptum separating two somites is initially acellular and composed of matricial components such as fibronectin, laminin and collagen I. However, myoseptal cells forming a continuum with skeletogenic cells surrounding axial structures are observed between adjacent myotomes after the completion of somitogenesis. The myoseptal cells do not express myogenic markers such as Pax3, Pax7 and myogenin but express several tendon-associated collagens including col1a1, col5a2 and col12a1 and angiopoietin-like 7, which is a secreted molecule involved in matrix remodelling. Using col1a1 as a marker gene, we observed in developing trout embryo an initial labelling in disseminating cells ventral to the myotome. Later, labelled cells were found more dorsally encircling the notochord or invading the intermyotomal space. This opens the possibility that the sclerotome gives rise not only to skeletogenic mesenchymal cells, as previously reported, but also to myoseptal cells. We furthermore show that myoseptal cells differ from skeletogenic cells found around the notochord by the specific expression of Scleraxis, a distinctive marker of tendon cells in amniotes. In conclusion, the location, the molecular signature and the possible sclerotomal origin of the myoseptal cells suggest that the fish myoseptal cells are homologous to the axial tenocytes in amniotes.

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

“…It has been shown that the dermomyotome-like epithelium provides muscle progenitors necessary for myotome growth, (Hollway et al, 2007;Stellabotte et al, 2007;Steinbacher et al, 2008) and, in line with their myogenic commitment, cells of the dermomyotome-like epithelium express the myogenic markers Pax3 and Pax7 as shown in zebrafish (Groves et al, 2005;Devoto et al, 2006;Hammond et al, 2007) and trout (Dumont et al, 2008). Our observation that the dermomyotome-like epithelium expresses CILP1 in addition to collagen I, V and XII (Bricard et al, 2014) further supports the view that this epithelium not only is myogenic, but also has a major role in the formation of the acellular connective tissue between the myotome and the epidermis. Whether this epithelium, which notably expresses dermo-1, a marker of dermis differentiation (Dumont et al, 2008), actually gives rise to cells of the dermis is still debated (Hollway et al, 2007; Stellabote et al, 2007).…”

“…Skeletogenic cells surrounding the notochord have been shown to originate from the sclerotome compartment ventral to the myotome (Morin-Kensicki and Eisen, 1997). Although awaiting definitive evidence, it is likely that myoseptal/tendon cells originate from a sclerotome derivedcompartment similar to the syndetome of the amniotes (Bricard et al, 2014;Chen and Galloway, 2014;Subramanian and Schilling, 2014). Thus, although myoseptal and skeletogenic cells are likely to share a common sclerotomal origin, they rapidly differ not only by the expression of scleraxis and Osf2/periostin as previously reported (Bricard et al, 2014) but also by that of CILP1.…”

“…CILP1 expression was found to concentrate in myoseptal/tendon cells invading medio-laterally into the space separating adjacent myotomes (Fig.4 D and E). Myoseptal cells have been shown to express scleraxis, tenomodulin and tendon associated collagens and, as such, may be considered homologous to axial tenocytes in amniotes (Bricard et al, 2014;Chen and Galloway, 2014). Using combined fluorescence localization of CILP1 mRNA and osteoblastspecific factor 2 (Osf2)/periostin mRNA, we further observed that CILP1 labelling was excluded from the Osf2/periostin-expressing skeletogenic cells that surround the notochord and are abutted by the most medial CILP1 positive myoseptal cells (Fig.…”

“…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 originate from a somite-derived syndetome compartment (Bricard et al, 2014;Chen and Galloway, 2014;Subramanian and Schilling, 2014). Experimental ablation of the myogenic factors myoD and myf5 in zebrafish results in the loss of scleraxis expression in the myosepta, showing that developing muscle regulates the specification of the myoseptal cell progenitors (Chen and Galloway, 2014).…”

“…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). After somitogenesis, myoseptal cells become appar-ent in the intersomitic space (Charvet et al, 2011;Bricard et al, 2014;Chen and Galloway., 2014;Subramanian and Schilling., 2014).…”