Development of ribs and intercostal muscles in the chicken embryo

Abstract

In the thorax of higher vertebrates, ribs and intercostal muscles play a decisive role in stability and respiratory movements of the body wall. They are derivatives of the somites, the ribs originating in the sclerotome and the intercostal muscles originating in the myotome. During thorax development, ribs and intercostal muscles extend into the lateral plate mesoderm and eventually contact the sternum during ventral closure. Here, we give a detailed description of the morphogenesis of ribs and thoracic muscles in the chicken embryo ( Gallus gallus ). Using Alcian blue staining as well as Sox9 and Desmin whole‐mount immunohistochemistry, we monitor synchronously the development of rib cartilage and intercostal muscle anlagen. We show that the muscle anlagen precede the rib anlagen during ventrolateral extension, which is in line with the inductive role of the myotome in rib differentiation. Our studies furthermore reveal the temporary formation of a previously unknown eighth rib in the chicken embryonic thorax.

Building a vertebra: Development of the amniote sclerotome

“…The decisive role of the myotome-derived intercostal muscle anlagen to promote both early and late stages of rib development has been shown by experimental inhibition of muscle formation, which leads to disruption of rib development (Wood et al, 2020). In agreement with this, detailed analysis of rib and intercostal muscle growth has shown that intercostal muscle extension into the somatopleura slightly precedes the growing rib anlagen (Khabyuk et al, 2022).…”

Pudgy mouse rib deformities emanate from abnormal paravertebral longitudinal cartilage/bone accumulations

“…The orderly embryonic structural formation of ribs, the vertebral column and the costo-vertebral region has been illustrated, with variable degrees of detail, in: garden snake (reptile) ( von Ebner, 1888 ); mouse ( Dawes, 1930 ; von Bochmann, 1937 ; Dalgleish, 1985 ; Theiler, 1988 ); chick ( Remak, 1855 ; Lillie, 1919 ; Shapiro, 1992 ; Christ and Ordahl, 1995 ; Stockdale et al, 2000 ; Christ et al, 2000 , 2004 , 2007 ); gull ( Piiper, 1928 ); sheep (also mouse, human and other vertebrates) ( Verbout, 1985 ); and human ( Sensenig, 1949 ; Töndury, 1953 ; O'Rahilly and Meyer, 1979 ; Drews, 1994 ). Regarding rib development: hox genes control regulation and development of the vertebrae and ribs along the proximo-distal (cranio-caudal) axis with Hox group 6 genes playing a major role in thoracic vertebral and posterior rib development ( McIntyre et al, 2007 ; Vinagre et al, 2010 ; Scaal, 2021 ; Khabyuk et al, 2022 ). All parts of the ribs originate from the thoracic somites initially and subsequently from the sclerotome; further assessments of proximal rib formation then show compartmentalization into the central, medial and ventral/caudal half of the somites/sclerotomes in particular ( Verbout, 1985 ; Huang et al, 1996 , 2000 ; Evans, 2003 ; Christ et al, 2007 ; Scaal, 2016 , 2021 ).…”

“…Some studies suggested that only the proximal ribs originate from sclerotomes with the distal components from the dermomyotomes ( Kato and Aoyama, 1998 ) but other studies, using the same model, confirmed only sclerotomal origin for the entire rib ( Huang et al, 2000 ). Recently, chick embryo rib development study has assigned specific parts of the rib to specific regions and quadrants within the sclerotome ( Scaal, 2021 ; Khabyuk et al, 2022 ). Vertebrate ribs have three anatomic regions: proximal (vertebral) involving the head (capitulum), neck and tubercle (tuberculum); middle (intermediate) involving the shaft; and distal (sternal) involving the bone/cartilage region that is either independent or directly attached to the anterior sternum ( Gray, 1973 ; Platzer, 2015 ).…”

“…Molecular localization assessments for normal vertebral and rib formation at somite and sclerotome stages have been invaluable ( Christ et al, 2007 ; Scaal, 2016 ; Scaal, 2021 ; Khabyuk et al, 2022 ). In addition, overviews at the molecular level tracing how irregularities amongst segmentation clock signaling genes lead to axial abnormalities (referred to as spondylocostal dysostoses or congenital scoliosis) have been outlined ( Pourquié and Kusumi, 2001 ; Schnell et al, 2002 ; Kusumi and Turnpenny, 2007 ; Turnpenny et al, 2007 ; Pourquié, 2011 ; Makino et al, 2013 ; Nóbrega et al, 2021 ).…”

A Spatio-Temporal-Dependent Requirement of Sonic Hedgehog in the Early Development of Sclerotome-Derived Vertebrae and Ribs

“…A compelling illustration of this principle is provided by the development of the rib cage and its associated structures. Here, the interactions among developing muscles, connective tissue, ribs, and tendons orchestrate the creation of a scaffold crucial for the normal morphogenesis and function of the body wall [ 1 , 2 , 3 ]. The rib cage plays a vital role in providing postural support, safeguarding internal organs, and facilitating adequate ventilation.…”