The occipital lateral plate mesoderm is a novel source for vertebrate neck musculature

Abstract

SUMMARYIn vertebrates, body musculature originates from somites, whereas head muscles originate from the cranial mesoderm. Neck muscles are located in the transition between these regions. We show that the chick occipital lateral plate mesoderm has myogenic capacity and gives rise to large muscles located in the neck and thorax. We present molecular and genetic evidence to show that these muscles not only have a unique origin, but additionally display a distinct temporal development, forming later than any other muscle group described to date. We further report that these muscles, found in the body of the animal, develop like head musculature rather than deploying the programme used by the trunk muscles. Using mouse genetics we reveal that these muscles are formed in trunk muscle mutants but are absent in head muscle mutants. In concordance with this conclusion, their connective tissue is neural crest in origin. Finally, we provide evidence that the mechanism by which these neck muscles develop is conserved in vertebrates.

Clonal analysis reveals a common origin between nonsomite-derived neck muscles and heart myocardium

“…Furthermore, these muscles are absent in Tbx1 null embryos at fetal stages (10,19). We confirm this result at E14.5 in a cross with the Mlc3f-nlacZ-2E transgene, expressed in differentiated skeletal muscle cells, (Fig.…”

“…1 A and B), indicating that they originate from somites. However, the trapezius and sternocleidomastoid muscles are negative with only residual labeling, which is due to connective tissue, as previously reported (19). With the Mesp1 Cre/+ line, which is activated in cardiac progenitors in the primitive streak (20), the heart and some neck muscles, including the trapezius and sternocleidomastoid muscles, are labeled ( Fig.…”

“…Despite evolutionary changes in cranial somites, this is also the case for the progenitors of the trapezius and sternocleidomastoid muscles in the mouse (19), where progenitors were also shown to have expressed Islet1. Furthermore the trapezius muscle is missing in Tbx1 mutants (10,19), consistent with an origin in cranial mesoderm rather than somites, in the mouse embryo.…”

“…Recent analysis of gene expression and genetic tracing supports this view. The cucullaris muscle in birds and turtles derives from cells in adjacent lateral mesoderm that do not express Pax3 but express Tbx1 (19). Despite evolutionary changes in cranial somites, this is also the case for the progenitors of the trapezius and sternocleidomastoid muscles in the mouse (19), where progenitors were also shown to have expressed Islet1.…”

The developmental basis of bat wing muscle

“…In vertebrates, skeletal muscles which form in the head, trunk and limbs are patterned by extrinsic cues from surrounding tissues to adopt specific arrangements of muscle fibres in the adult form [23][24][25][26][27][28][29][30][31] . For example, somite-derived limb muscle precursor cells migrate into the limb bud which is filled with lateral platederived connective tissue.…”