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Differentiation of avian craniofacial muscles: I. Patterns of early regulatory gene expression and myosin heavy chain synthesis.
Dev Dyn. 1999 Oct; 216(2):96-112.DD

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 independent of origin (somitic vs. unsegmented paraxial vs. prechordal mesoderm), position (extraocular vs. branchial vs. subpharyngeal), and fiber type (fast vs. slow) and is shared among all muscles whose precursors interact with cephalic neural crest populations. Dev Dyn 1999;216:96-112.

Authors+Show Affiliations

Department of Biomedical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York 14853-6401, USA. dmn2@cornell.eduNo affiliation info availableNo affiliation info availableNo affiliation info available

Pub Type(s)

Journal Article
Research Support, U.S. Gov't, P.H.S.

Language

eng

PubMed ID

10536051

Citation

Noden, D M., et al. "Differentiation of Avian Craniofacial Muscles: I. Patterns of Early Regulatory Gene Expression and Myosin Heavy Chain Synthesis." Developmental Dynamics : an Official Publication of the American Association of Anatomists, vol. 216, no. 2, 1999, pp. 96-112.
Noden DM, Marcucio R, Borycki AG, et al. Differentiation of avian craniofacial muscles: I. Patterns of early regulatory gene expression and myosin heavy chain synthesis. Dev Dyn. 1999;216(2):96-112.
Noden, D. M., Marcucio, R., Borycki, A. G., & Emerson, C. P. (1999). Differentiation of avian craniofacial muscles: I. Patterns of early regulatory gene expression and myosin heavy chain synthesis. Developmental Dynamics : an Official Publication of the American Association of Anatomists, 216(2), 96-112.
Noden DM, et al. Differentiation of Avian Craniofacial Muscles: I. Patterns of Early Regulatory Gene Expression and Myosin Heavy Chain Synthesis. Dev Dyn. 1999;216(2):96-112. PubMed PMID: 10536051.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Differentiation of avian craniofacial muscles: I. Patterns of early regulatory gene expression and myosin heavy chain synthesis. AU - Noden,D M, AU - Marcucio,R, AU - Borycki,A G, AU - Emerson,C P,Jr PY - 1999/10/27/pubmed PY - 2001/3/28/medline PY - 1999/10/27/entrez SP - 96 EP - 112 JF - Developmental dynamics : an official publication of the American Association of Anatomists JO - Dev Dyn VL - 216 IS - 2 N2 - 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 independent of origin (somitic vs. unsegmented paraxial vs. prechordal mesoderm), position (extraocular vs. branchial vs. subpharyngeal), and fiber type (fast vs. slow) and is shared among all muscles whose precursors interact with cephalic neural crest populations. Dev Dyn 1999;216:96-112. SN - 1058-8388 UR - https://www.unboundmedicine.com/medline/citation/10536051/Differentiation_of_avian_craniofacial_muscles:_I__Patterns_of_early_regulatory_gene_expression_and_myosin_heavy_chain_synthesis_ L2 - https://doi.org/10.1002/(SICI)1097-0177(199910)216:2<96::AID-DVDY2>3.0.CO;2-6 DB - PRIME DP - Unbound Medicine ER -