Inductive Signals from the Somatopleure Mediated by Bone Morphogenetic Proteins Are Essential for the Formation of the Sternal Component of Avian Ribs

Abstract

The posterior five pairs of avian ribs are composed of vertebral and sternal components, both derived from the somitic mesoderm. For the patterning of the rib cartilage, inductive signals from neighboring tissues on the somitic mesoderm have been suggested to play critical roles. The notochord and surface ectoderm overlying the somitic mesoderm are essentially required for the development of proximal and distal regions of the ribs, respectively. Involvement of the somatopleure in rib development has already been suggested but is less understood than those of the notochord and surface ectoderm. In this study, we reinvestigated the role of the somatopleure during rib development. We first identified the chicken homologue of the mouse Mesenchymal forkhead-1 (cMfh-1) gene based on sequence similarities. cMfh-1 was observed to be expressed in the nonaxial mesoderm, including the somitic mesoderm, and, subsequently, in cartilage forming the ribs, vertebrae, and appendicular skeletal system. In the interlimb region, corresponding to somites 21-25 (or 26), cMfh-1-positive somitic mesoderm was seen penetrating the somatopleure of E4 embryos, and cMfh-1 was used as a molecular marker demarcating prospective rib cartilage. A series of experiments affecting the penetration of the somitic mesoderm into the somatopleure was performed in the present study, resulting in defects in sternal rib formation. The inductive signals emanating from the somatopleure mediated by BMP family proteins were observed to be essentially involved in the ingrowth of the somitic mesoderm. BMP4 alone, however, could not completely replace inductive signals from the somatopleure, suggesting the involvement of additional signals for rib formation.

Three developmental compartments involved in rib formation

“…When the insert covered only part of the somite and lateral plate for the first 24 hours, the ratio of embryos lacking the distal ribs to total operated number were 6/ 21 (29%) ( Table 1, Table 1, case 5), except for only the loss of the sternal rib in three cases, as has been reported previously (Sudo, et al, 2001). In the case when the insert covered both the somite and the neural tube partially, 21% (4/19) of the operated embryos lacked their distal ribs (Table 1, case 6).…”

“…We have reported that blocking the interaction between the somite and the somatopleure caused deficiency in the sternal rib (Sudo et al, 2001). However, the vertebral ribs were intact.…”

“…When the interaction between the somite and the axial tissues was interrupted by inserting a piece of nonpermeable film between the tissues in 2-day chick embryos, the proximal rib did not develop, while the interruption between the surface ectoderm and the somite caused loss of the distal rib. We previously showed that the lateral plate was essential for the development of sternal ribs, more specifically of the distal part of the distal rib in avian embryos (Sudo et al, 2001). Here we report that the three parts of the rib, proximal, distal and sternal, are developmentally different compartments.…”

“…Ablation of the surface ectoderm has been reported to cause various types of rib malformations (Huang et al, 2000b;Sudo et al, 2001). Ribs were missing, shortened or misshapen when the surface ectoderm overlying the thoracic segmental plate was removed (Huang et al, 2000b).…”

Ventral abdominal wall dysmorphogenesis of Msx1/Msx2 double‐mutant mice

“…In fact, orchestration of regulatory genes involved in Bmp signaling has been reported for organogenesis such as tooth, palate, and heart development (Chen et al, 1996;Bei and Maas, 1998;Zhang et al, 2002;Brugger et al, 2004). Bmp genes are expressed in developing body wall and they are required for normal body wall development (Suzuki et al, 1996;Funayama et al, 1999;Sudo et al, 2001). Hence, we analyzed the spatial and temporal expression pattern of Msx1 and Msx2 during abdominal body formation and performed histological studies on abdominal body walls of Msx1/Msx2 double-mutant embryos.…”