Hedgehog regulation of superficial slow muscle fibres inXenopusand the evolution of tetrapod trunk myogenesis

Abstract

In tetrapod phylogeny, the dramatic modifications of the trunk have received less attention than the more obvious evolution of limbs. In somites,several waves of muscle precursors are induced by signals from nearby tissues. In both amniotes and fish, the earliest myogenesis requires secreted signals from the ventral midline carried by Hedgehog (Hh) proteins. To determine if this similarity represents evolutionary homology, we have examined myogenesis in Xenopus laevis, the major species from which insight into vertebrate mesoderm patterning has been derived. Xenopus embryos form two distinct kinds of muscle cells analogous to the superficial slow and medial fast muscle fibres of zebrafish. As in zebrafish, Hh signalling is required for XMyf5 expression and generation of a first wave of early superficial slow muscle fibres in tail somites. Thus, Hh-dependent adaxial myogenesis is the likely ancestral condition of teleosts, amphibia and amniotes. Our evidence suggests that midline-derived cells migrate to the lateral somite surface and generate superficial slow muscle. This cell re-orientation contributes to the apparent rotation of Xenopussomites. Xenopus myogenesis in the trunk differs from that in the tail. In the trunk, the first wave of superficial slow fibres is missing,suggesting that significant adaptation of the ancestral myogenic programme occurred during tetrapod trunk evolution. Although notochord is required for early medial XMyf5 expression, Hh signalling fails to drive these cells to slow myogenesis. Later, both trunk and tail somites develop a second wave of Hh-independent slow fibres. These fibres probably derive from an outer cell layer expressing the myogenic determination genes XMyf5, XMyoD and Pax3 in a pattern reminiscent of amniote dermomyotome. Thus, Xenopus somites have characteristics in common with both fish and amniotes that shed light on the evolution of somite differentiation. We propose a model for the evolutionary adaptation of myogenesis in the transition from fish to tetrapod trunk.

Stabilization of Speckle-type POZ Protein (Spop) by Daz Interacting Protein 1 (Dzip1) Is Essential for Gli Turnover and the Proper Output of Hedgehog Signaling

“…In Xenopus and zebrafish embryos, superficial slow fibers (SSF) arise at the lateral border of the somite. Specification of SSF depends on low levels of Hh signals from the notochord (53)(54)(55). Ectopic Hh signaling in Xenopus embryos results in a mis-positioning and an increased incidence of SSF within more medial positions of the posterior somite (55).…”

“…Specification of SSF depends on low levels of Hh signals from the notochord (53)(54)(55). Ectopic Hh signaling in Xenopus embryos results in a mis-positioning and an increased incidence of SSF within more medial positions of the posterior somite (55). To determine how partial Dzip1 depletion affected somitic mesoderm development, we examined total muscle fiber and SSF formation in posterior trunk sections of DMO-injected embryos.…”

Cell behaviors associated with somite segmentation and rotation in Xenopus laevis

“…A recent study examining the expression pattern of slow myosin heavy chain (MyHC) during the formation of myotome fibers in X. laevis, led to another model for somite rotation (Grimaldi et al, 2004). This model proposes that PSM cells fated to form slow muscle fibers are initially positioned adjacent to the notochord.…”

Muscle stem cells and model systems for their investigation

“…The external Pax7-positive cells as well as those located deeper in the myotome, on the surface of differentiating fibers were also detected in the sturgeon (Devoto et al, 2006). Of interest, in amphibians, external cells also are the source of myogenic precursors (Grimaldi et al, 2004).…”

“…They have been found in diverse teleosts, including the sea bass (Veggetti et al, 1990), herring (Johnston, 1993), and gilthead sea bream (Ramirez-Zarzoza et al, 1995), as well as in the amphibians Xenopus laevis (Hamilton, 1969) and European common frog (Maurer, 1906). In Xenopus laevis, this layer is MyHC-negative and expresses Pax3, Col1a1, and in specific zones XMyf-5 and XMyoD genes (Grimaldi et al, 2004).…”