Cell behaviors associated with somite segmentation and rotation in Xenopus laevis

Abstract

During vertebrate development the formation of somites is a critical step, as these structures will give rise to the vertebrae, muscle, and dermis. In Xenopus laevis, somitogenesis consists of the partitioning of the presomitic mesoderm into somites, which undergo a 90-degree rotation to become aligned parallel to the notochord. Using a membrane-targeted green fluorescent protein to visualize cell outlines, we examined the individual cell shape changes occurring during somitogenesis. We show that this process is the result of specific, coordinated cell behaviors beginning with the mediolateral elongation of cells in the anterior presomitic mesoderm and then the subsequent bending of these elongated cells to become oriented parallel with the notochord. By labeling a clonal population of paraxial mesoderm cells, we show that cells bend around their dorsoventral axis. Moreover, this cell bending correlates with an increase in the number of filopodial protrusions, which appear to be posteriorly directed toward the newly formed segmental boundary. By examining the formation of somites at various positions along the anteroposterior axis, we show that the general sequence of cell behaviors is the same; however, somite rotation in anterior somites is slower than in posterior somites. Lastly, this coordinated set of cell behaviors occurs in a dorsal-toventral progression within each somite such that cells in the dorsal aspect of the somite become aligned along the anteroposterior axis before cells in other regions of the same somite. Together, our data further define how these cell behaviors are temporally and spatially coordinated during somite segmentation and rotation. Developmental Dynamics 235:3268 -3279, 2006.

From segment to somite: Segmentation to epithelialization analyzed within quantitative frameworks

“…In Xenopus, a recent very detailed 3D confocal analysis of embryos confirms earlier explant observations (Wilson et al, 1989) that the expansion of short discrete fissures (Fig. 3B) acts to gently bisect the PSM to form a stable somite border (Afonin et al, 2006). Similarly, in zebrafish, cell rearrangements within a forming somite are minimal and a somite border forms when cells appear to gently detach from neighbors along a medio-to-lateral direction (Fig.…”

“…Interestingly, although Xenopus somites undergo a 90-degree rotation but do not epithelialize, time-lapse analyses showed that individual cells bend in a precise spatiotemporal manner that propagates in a dorsal-to-ventral direction (Afonin et al, 2006). In a similar manner, in analysis of histological sections from the chick PSM (Duband et al, 1987;Sato et al, 2002;Nakaya et al, 2004), the presumptive posterior border, including the dorsal, ventral, medial, and lateral sleeves of the new somite, appear epithelialized.…”

In vivo analyzes of dystroglycan function during somitogenesis in Xenopus laevis

“…Here, we show that the protein is detected from the onset of somitogenesis and is enriched at intersomitic junctions and at the notochord/somite boundaries. Somitogenesis requires the mediolateral elongation of presomitic cells, the formation of filopodia protrusions at the onset of rotation, the break of adhesive interactions with the ECM at the notochord/somite boundary, the bending of cells around the dorsoventral axis and finally the elongation and alignment of cells parallel to the notochord (Afonin et al, 2006). Dg is present during these events suggesting that Dg/ECM interactions might govern adhesive properties of cells during somitogenesis and muscle formation.…”

“…During gastrulation, presomitic cells of the paraxial mesoderm intercalate radially and mediolaterally, separate from the rest of the mesoderm, establish the notochord/somite boundary and finally form blocks of 7-9 cells width (Danker et al, 1992). In those blocks, cells change shape, lengthen along their mediolateral axis and narrow along their anteroposterior axis (Wilson et al, 1989;Afonin et al, 2006). At the onset of somitogenesis, the presomitic cells bend anteriorly and undergo a 90°rotation relative to the anteroposterior axis of the embryo to form mono-nucleate muscle cells that are aligned parallel to the notochord (Keller, 2000).…”

Coordinated Action of N-CAM, N-cadherin, EphA4, and ephrinB2 Translates Genetic Prepatterns into Structure during Somitogenesis in Chick

“…In Xenopus embryos, two short, discrete fissures start from both the medial and lateral edges of the PSM and expand gradually towards the middle of the PSM to form a stable somite-PSM border (Afonin et al, 2006). In zebrafish embryos, cell rearrangements within forming somites are minimal and the forming-somite-PSM border develops when cells in the forming somite gently detach from their PSM neighbors, forming a medial notch which spreads laterally (Wood and Thorogood, 1994;Henry et al, 2000;Jiang et al, 2000).…”