Sabillo A et al. (2016), Making muscle: Morphogenetic movements and mole...

XB-ART-51853

Semin Cell Dev Biol 2016 Mar 01;51:80-91. doi: 10.1016/j.semcdb.2016.02.006.

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Making muscle: Morphogenetic movements and molecular mechanisms of myogenesis in Xenopus laevis.

Sabillo A , Ramirez J , Domingo CR .

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Xenopus laevis offers unprecedented access to the intricacies of muscle development. The large, robust embryos make it ideal for manipulations at both the tissue and molecular level. In particular, this model system can be used to fate map early muscle progenitors, visualize cell behaviors associated with somitogenesis, and examine the role of signaling pathways that underlie induction, specification, and differentiation of muscle. Several characteristics that are unique to X. laevis include myogenic waves with distinct gene expression profiles and the late formation of dermomyotome and sclerotome. Furthermore, myogenesis in the metamorphosing frog is biphasic, facilitating regeneration studies. In this review, we describe the morphogenetic movements that shape the somites and discuss signaling and transcriptional regulation during muscle development and regeneration. With recent advances in gene editing tools, X. laevis remains a premier model organism for dissecting the complex mechanisms underlying the specification, cell behaviors, and formation of the musculature system.

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Species referenced: Xenopus laevis
Genes referenced: bmp4 dag1 fn1 myf5 myf6 myod1 myog shh wnt1 wnt11 wnt3 wnt4 wnt6 wnt7a

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	Fig. 1. A schematic representation of somite morphogenesis in X. laevis. A dorsal view of a step-wise process of somite morphogenesis that begins in the PSM (posterior end) and ends with the formation of aligned myotome fibers (anterior end). The process begins with cells in the PSM that become progressively more elongated in the mediolateral direction as they near the transition zone where somite formation will begin (Step 1). Somite formation begins with the formation of the intersomitic boundary which first appears from the lateral edge and moves medially toward the notochord. This early intersomitic boundary is comprised of fibronectin (red arrow). As this intersomitic boundary begins to form at the lateral edge of the paraxial mesoderm, somite cells increase their filopodial activity. These cells also express integrin β1 (Step 2). This is followed by a 90° rotation such that each elongated cell individually bends around the anterior to posterior axis (Step 3). At the same time, these cells begin to express β-dystroglycan, which plays an important role in crosslinking laminin (blue) to the intersomitic ECM. The last step involves the stable attachment of myotome fibers to the intersomitic boundary, thereby establishing an elongated and aligned morphology (Step 4). Adapted from Refs. [17,21].
	Fig. 2. Muscle fate maps of the gastrula and tadpole. Cells positioned in the upper lateral lip region (A; light green) will undergo a significant amount of convergence and extension to give rise to both the anterior-most somites as well as myotome fibers positioned in the central region of somites along the entire anterior to posterior axis. Cells positioned in the lateral circumblastoporal region (B; red) will intercalate with cells from region A to give rise to myotome fibers found throughout the dorsal and ventral extent of the trunk somites. Cells positioned in the lower lip region (C; blue) are found in the dorsal and ventral-most domain of somites located in the trunk and tail regions of the tadpole. Scanning electron micrographs of cross sections of embryos from stages 13 to 24 reveal the distribution of mesoderm cells from gastrula regions A, B, and C. Cells from region A are positioned medially adjacent to the notochord, while cells from region B will lie lateral to region A although a subset of B cells will intercalate among A cells and end up residing more medially. Cells from region C will lie lateral to region B (stage 13). As the embryo matures there is considerable dorsal convergence and expansion of the two-layered PSM (stages 16–24). These movements displace cells from the lateral region to the dorsal and ventral aspects of the somite. Cells from region B will undergo a significant amount of convergence and will mix with cells from regions A and C of the gastrula. Cells from region C of the gastrula will lie at the lateral edge of the PSM and will eventually contribute to the formation of the most dorsal and ventral cells of the somite. Around stage 19 we begin to see a thin epithelial layer consisting of cuboidal cells that lie on the surface of the paraxial mesoderm. This tissue is likely the dermomyotome (shown in white). Anterior is to the left for images of the tadpole musculature. Adapted from Ref. [27].
	Fig. 3. Signals that pattern the vertebrate somite. A simplified diagram of a cross-sectioned amniote (I) and X. laevis (II) embryo illustrating proteins secreted by adjacent tissues that pattern the somite. In the amniote somite, Wnts from the dorsal neural tube (tan) and the epidermal ectoderm (black), along with Bmp4 from the lateral plate (violet) maintain the dermomyotome (dark red) in an undifferentiated state. Hedgehog from the notochord and neural tube floor plate (dark blue) specify the sclerotome (light blue). Once the sclerotome segregates, the prospective epaxial (orange) and hypaxial (yellow) myotome differentiate from the dermomyotome. In X. laevis, Wnt1 from the dorsal neural tube (tan) and Wnt11 from the somite instruct myotome (green) proliferation and differentiation. Medium levels of Bmp4 from the lateral plate (violet) specify the dermomyotome (dark red) and muscle satellite cells. Hedgehog from the notochord and neural tube floorplate (dark blue) induces sclerotome (light blue) and slow-twitch myotome (green) in the tail. Hedgehog, along with Wnt7a from the epidermal ectoderm, regulates the differentiation of epaxial (orange) and hypaxial (yellow) myotome from the dermomyotome. Adapted from Ref. [30].
	Fig. 4. Expression patterns of Myogenic regulatory factors (MRFs) throughout the three myogenic waves. During the first wave, myoD and myf5 are expressed in the PSM. As somitogenesis progresses, myoD and myf5 become restricted to the caudal PSM and early somites, while mrf4 and myogenin become expressed in differentiating myotome. During the second wave, all MRFs are expressed in the epaxial (dorsal) region of the dermomyotome. By the third wave, myf5 is expressed as puncta in the anterior and posterior region of each somite, whereas mrf4 is expressed in the center of each myotome and myogenin is most highly expressed in the hypaxial myotome. Gastrulae are viewed from the vegetal perspective; neurulae are viewed from the dorsal perspective with anterior to the left; tadpoles are from the lateral perspective with anterior to the left. Dark green indicates high levels of expression, yellow indicates lower levels. Adapted from Ref. [31].

References [+] :

Abou-Elhamd, Klhl31 attenuates β-catenin dependent Wnt signaling and regulates embryo myogenesis. 2015, Pubmed, Xenbase