4D‐analysis of early pelvic girdle development in the mouse (Mus musculus)

Abstract

The formation of limb girdles is a key-novelty in vertebrate evolution. Although the knowledge of pattern formation, genetic, and molecular analysis of limb development has prodigiously grown over the past four decades, the morphogenesis of the pelvic element, joining the appendicular with the axial skeleton has poorly been investigated. Because of their heterochrony in development and evolution, axial and appendicular skeletal elements have seldom been seen as a cojoined morphological complex. The present study examines the pelvis morphogenesis in the mouse (Mus musculus), with special focuses on the axio-appendicular linkage, the formation and number of elements, and the joint formation. Serial histological sections of specimens from Theiler stages (TH) 18-25 (Theiler, 1972) were examined using bright field microscopy. 3D-models of the growing pelvis were reconstructed from these serial sections. The generated 3D-models were subsequently integrated into a computer-animated 4D-visualization illustrating the complex developmental dynamics of the mammalian pelvis morphogenesis. The findings demonstrate that the pelvic element forms from a single mesenchymal condensation in close vicinity to the appendicular skeleton. From the early start of development the pelvic element is limb-associated, and quite lately connects to the axial skeleton. Additionally, the 4D-visualization of the entire developmental process reveals a yet unnoticed reorientation of the mouse pelvic element from an initial posteriorly oblique developmental position to a ventrally oblique definitive position.

Evolvability of the Primate Pelvic Girdle

“…to 25? in the mouse, Pomikal and Streicher 2010;Pomikal et al 2011), which suggests that ilium formation is not determined by growth of the vertebral column.…”

“…In addition to these genetic inputs, the ischium and pubis interact closely with the femur throughout the entirety of development (Pomikal and Streicher 2010), and when it is not present (e.g., in limb ablation experiments), the ischiopubis does not develop normally (Malashichev et al 2005).…”

“…The pelvic girdle develops from a single mesenchymal condensation of lateral plate mesoderm (Chevallier 1977;Malashichev et al 2008;Pomikal and Streicher 2010). The cartilaginous condensations of what will later be the ilium, ischium, and pubis arise from this common mesenchyme between 34 and 36 days in human embryos (Laurenson 1964;O'Rahilly and Gardner 1975).…”

Pbx homeodomain proteins: TALEnted regulators of limb patterning and outgrowth

“…In contrast, at the level of the hindlimb, only cells originating from the mesodermal somatopleure have been shown to give rise to the three main elements of each pelvic bone, i.e., a rostral oriented ilium, a ventral facing pubis, and a dorsal positioned ischium (Malashichev et al, 2008). These three elements fuse during development at the location of the hip joint, whereby each pelvic bone articulates with the proximal femur of the limb proper (Pomikal and Streicher, 2010). A number of genetic pathways are known to govern patterning of the bony elements of both pectoral and pelvic girdle during development, though knowledge of the genetic control of girdle development is still rudimentary in comparison to that of limb development (Kuijper et al, 2005; Huang et al, 2006).…”

Control of pelvic girdle development by genes of the Pbx family and Emx2

“…To date, research conducted mainly in the chick (Huang et al, 2006) but also in the mouse (Pomikal and Streicher, 2010; Valasek et al, 2010), has partially elucidated the tissue origins for each girdle. Notably, the scapula has been shown to develop from multiple tissues, such as the dermomyotome of the somites, the mesodermal portion of the somatopleure (a domain of the lateral plate mesoderm or LPM) and neural crest cell-derived mesenchyme (Huang et al, 2000; Matsuoka et al, 2005; Wang et al, 2005).…”