Differential regulation of avian pelvic girdle development by the limb field ectoderm

Abstract

Although limb development has been a subject of intense research over the last decades, development of the girdles has been poorly investigated. Particularly, a detailed analysis of pelvic girdle development including functional data is not available to date. Here, we describe the early steps of the formation of mesenchymal and cartilaginous anlagen of the pelvic elements using alcian blue staining in whole mount embryos and serial histological sections, and the expression pattern of several marker genes to provide an operative basis for further research in pelvis development. Moreover, we describe pelvis development after unilateral hindlimb bud amputation and somatopleural ectoderm extirpation. We show for the first time, that ectodermal signals at pre-limb bud stages are required for pelvis formation. We present evidence suggesting that the regulation of ilium development is different from the development of ischium and pubis.

Avian pelvis originates from lateral plate mesoderm and its development requires signals from both ectoderm and paraxial mesoderm

“…the ilium, pubis, and ischium, whose structure and morphological development have been previously described (Mehnert 1887;Johnson 1893;Baumel et al 1979;Malashichev et al 2005). In the avian embryo, the ilium is the first visible skeletal element of the pelvic girdle and can be detected as early as HH-stage 26 (Hamburger and Hamilton 1951) as a local mesenchymal condensation at the position of the prospective acetabulum.…”

“…Some data are available concerning the developmental (Chevallier 1977;Huang et al 2000;Matsuoka et al 2005) and evolutionary (Burke 1991a,b;Vickaryous and Hall 2006) origin of the shoulder girdle and the genes controlling its development (Selleri et al 2001;Pröls et al 2004;Kuijper et al 2005). However, our knowledge of the development of the pelvic girdle, especially the ilium, remains controversial (Chevallier 1977;Malashichev et al 2005).…”

“…Chevallier (1977) has suggested that the pelvic girdle is entirely of somatopleural origin but has not shown this explicitly. Evidence is now accumulating that the scapular blade and the ilium are subjected to control mechanisms that differ from those of the rest of the girdle elements and/ or are derived from somitic material (Malashichev et al 2005). Two knockout mice, Emx2 −/− (Pellegrini et al 2001) and Fgf10 −/− mice (Sekine et al 1999), with ablated scapular blade and ilium or preserved clavicula, anterior scapula blade and rudimentary ilium, respectively, suggest that proximal bones in both shoulder and pelvic girdles share a common developmental mechanism.…”

“…It later chondrifies and expands rapidly in a caudal and then in a cranial direction. At HH-stage 36, the ilium stretches along 12 synsacral vertebrae (Malashichev et al 2005). Its dorsal pre-and postacetabular wings (Alae prae-and postacetabulares ilii) form the ilio-synsacral joint, connecting the appendicular with the axial skeleton.…”

BMP signals control limb bud interdigital programmed cell death by regulating FGF signaling

“…A preAER signal is required for normal hip girdle formation Surgical removal of chick ectoderm prior to limb bud formation prevents normal pelvic bone development, suggesting that a preAER factor signals to the lateral flank mesoderm for pelvic girdle development (Malashichev et al, 2005). Also, certain mouse mutations that prevent hindlimb AER induction also affect pelvic bone development, including defects in p63 (Trp63 -Mouse Genome Informatics), Wnt3 or ␤-catenin (Barrow et al, 2003;Mills et al, 1999;Yang et al, 1999).…”