Differentiation of avian craniofacial muscles: I. Patterns of early regulatory gene expression and myosin heavy chain synthesis

Abstract

Myogenic populations of the avian head arise within both epithelial (somitic) and mesenchymal (unsegmented) mesodermal populations. The former, which gives rise to neck, tongue, laryngeal, and diaphragmatic muscles, show many similarities to trunk axial, body wall, and appendicular muscles. However, muscle progenitors originating within unsegmented head mesoderm exhibit several distinct features, including multiple ancestries, the absence of several somite lineage-determining regulatory gene products, diverse locations relative to neuraxial and pharyngeal tissues, and a prolonged and necessary interaction with neural crest cells. The object of this study has been to characterize the spatial and temporal patterns of early muscle regulatory gene expression and subsequent myosin heavy chain isoform appearance in avian mesenchyme-derived extraocular and branchial muscles, and compare these with expression patterns in myotome-derived neck and tongue muscles. Myf5 and myoD transcripts are detected in the dorsomedial (epaxial) region of the occipital somites before stage 12, but are not evident in the ventrolateral domain until stage 14. Within unsegmented head mesoderm, myf5 expression begins at stage 13.5 in the second branchial arch, followed within a few hours in the lateral rectus and first branchial arch myoblasts, then other eye and branchial arch muscles. Expression of myoD is detected initially in the first branchial arch beginning at stage 14.5, followed quickly by its appearance in other arches and eye muscles. Multiple foci of myoblasts expressing these transcripts are evident during the early stages of myogenesis in the first and third branchial arches and the lateral rectus-pyramidalis/quadratus complex, suggesting an early patterned segregation of muscle precursors within head mesoderm. Myf5-positive myoblasts forming the hypoglossal cord emerge from the lateral borders of somites 4 and 5 by stage 15 and move ventrally as a cohort. Myosin heavy chain (MyHC) is first immunologically detectable in several eye and branchial arch myofibers between stages 21 and 22, although many tongue and laryngeal muscles do not initiate myosin production until stage 24 or later. Detectable synthesis of the MyHC-S3 isoform, which characterizes myofibers as having "slow" contraction properties, occurs within 1-2 stages of the onset of MyHC synthesis in most head muscles, with tongue and laryngeal muscles being substantially delayed. Such a prolonged, 2- to 3-day period of regulatory gene expression preceding the onset of myosin production contrasts with the interval seen in muscles developing in axial (approximately 18 hr) and wing (approximately 1-1.5 days) locations, and is unique to head muscles. This finding suggests that ongoing interactions between head myoblasts and their surroundings, most likely neural crest cells, delay myoblast withdrawal from the mitotic pool. These descriptions define a spatiotemporal pattern of muscle regulatory gene and myosin heavy chain expression unique to head muscles. This pattern is inde...

Spatial relations between avian craniofacial neural crest and paraxial mesoderm cells

“…The locations of extraocular and branchial muscle precursors identified in this study correlate well with the sites of activation of muscle-specific transcription factors, e.g., Myf5 and MyoD (Hacker and Guthrie, 1998;Noden et al, 1999;Mootoosamy and Dietrich, 2002). They are concordant with transplantation-based maps by Noden (1983b) and add finer definition to the boundaries of individual myogenic foci.…”

“…Previous mapping and gene expression studies have shown that skeletal muscle progenitors form aggregates at or close to their sites of origin within paraxial mesoderm (Noden, 1983b;McClearn and Noden, 1988;Noden et al, 1999). Retroviral injections confirm that progenitors of extraocular muscles first condense, then move as cohorts toward the mesoderm:crest interface, and subsequently enter the crest-derived periocular environment.…”

“…Information on the other lineages is based on the earliest appearance of known lineage-specific transcription factors. The earliest signs of muscle commitment are evident at stage 13.5 (Noden et al, 1999), and most head muscles initiate aggregation and molecular differentiation close to the sites of their stage 9 progenitors. Craniofacial cartilage and bone do not show molecular evidence of lineage commitment, e.g., expression of Sox9 and Runx, until day 5 of incubation (Eames and Helms, 2004;also Jaskoll et al, 1981), which is coincidental with the onset of precartilage mesenchymal condensation.…”

Tbx1 regulation of myogenic differentiation in the limb and cranial mesoderm

“…The coexpression of MyoD and MyoR in the developing head may explain why terminal differentiation in the head is delayed relative to the axial muscles (see Fig. 2; Noden et al, 1999). Therefore, one simple hypothesis is that loss of Tbx1 function results in the increase of a factor (MyoR) that represses myogenesis-hence, the hypoplasia of the branchial arch muscles.…”

Many routes to the same destination: lessons from skeletal muscle development

“…1). Somites are found throughout the chordates and are the source of all the skeletal muscle of the trunk and limbs as well as some head muscles, such as the tongue muscles (Noden et al 1999, Brent & Tabin 2002, Christ et al 2007. Somites begin forming at the anterior of the embryo and are added posteriorly as the embryo extends.…”