Title: Variations in Tissue Interactions During Head Muscle Development
For decades it has been established that head muscle development differs from trunk muscle development. Similarly known, even though not in such detail, is that different subgroups of head muscles develop dependent on different underlying gene regulatory networks. Even less well studied are the tissue interactions during the developmental processes. Muscles derived from pharyngeal arch mesoderm depend on interactions with endoderm and neural crest cells, and, to a minor extent, ectodermal cues. Extraocular eye muscles respond to a mix of signals from surrounding mesoderm, but also neural crest cells; however, they are independent of endodermal cues. Head muscles derived from occipital paraxial mesoderm depend on tissue interactions similar to pharyngeal arch muscles but have a different migration trajectory. While the pharyngeal arch mesodermal cells and neural crest cells largely migrate from dorsal to ventral, the occipital paraxial mesodermal cells migrate from dorsal to ventral and from posterior to anterior. During the migration these cells proliferate and even start to differentiate, while pharyngeal mesodermal cells begin the differentiation process after reaching their respective pharyngeal arches. Here we present an overview of tissue interactions during the development of different head muscle populations, highlighting general concepts and main differences. Topic Category: Neural Crest, Placodes and Craniofacial Development Keywords: Craniofacial muscles, Myogenesis Funding or Support Information: NSF #2000005 to JMZC more »« less
Sagarin, Kathleen A.; Redgrave, Anna C.; Mosimann, Christian; Burke, Ann C.; Devoto, Stephen H.
(, Developmental dynamics)
null
(Ed.)
Background: Skeletal muscle in the trunk derives from the somites, paired segments of paraxial mesoderm. Whereas axial musculature develops within the somite, appendicular muscle develops following migration of muscle precursors into lateral plate mesoderm. The development of muscles bridging axial and appendicular systems appears mixed. Results: We examine development of three migratory muscle precursor-derived muscles in zebrafish: the sternohyoideus (SH), pectoral fin (PF), and posterior hypaxial (PHM) muscles. We show there is an anterior to posterior gradient to the developmental gene expression and maturation of these three muscles. SH muscle precursors exhibit a long delay between migration and differentiation, PF muscle precursors exhibit a moderate delay in differentiation, and PHM muscle precursors show virtually no delay between migration and differentiation. Using lineage tracing, we show that lateral plate contribution to the PHM muscle is minor, unlike its known extensive contribution to the PF muscle and absence in the ventral extension of axial musculature. Conclusions: We propose that PHM development is intermediate between a migratory muscle mode and an axial muscle mode of development, wherein the PHM differentiates after a very short migration of its precursors and becomes more anterior primarily by elongation of differentiated muscle fibers.
Sharma, Praveer P.; MacLean, Adam L.; Meinecke, Lina; Clouthier, David E.; Nie, Qing; Schilling, Thomas F.
(, genesis)
Summary The mandibular or first pharyngeal arch forms the upper and lower jaws in all gnathostomes. A gene regulatory network that defines ventral, intermediate, and dorsal domains along the dorsal–ventral (D–V) axis of the arch has emerged from studies in zebrafish and mice, but the temporal dynamics of this process remain unclear. To define cell fate trajectories in the arches we have performed quantitative gene expression analyses of D–V patterning genes in pharyngeal arch primordia in zebrafish and mice. Using NanoString technology to measure transcript numbers per cell directly we show that, in many cases, genes expressed in similar D–V domains and induced by similar signals vary dramatically in their temporal profiles. This suggests that cellular responses to D‐V patterning signals are likely shaped by the baseline kinetics of target gene expression. Furthermore, similarities in the temporal dynamics of genes that occupy distinct pathways suggest novel shared modes of regulation. Incorporating these gene expression kinetics into our computational models for the mandibular arch improves the accuracy of patterning, and facilitates temporal comparisons between species. These data suggest that the magnitude and timing of target gene expression help diversify responses to patterning signals during craniofacial development.
Ziermann, Janine M; Johnson, Nicholas R; Correa-Alfonzo, Paola; Aquino_Colon, Andres; Waters, Samuel T
(, Developmental Dynamics)
A key player in brain and neural crest development is the gastrulation-brain-homeobox (Gbx) transcription factor family member, Gbx2. During the early stages of gastrulation, Gbx2 RNA is broadly expressed in the prospective hindbrain and posterior region of the embryo. Later it becomes restricted to a sharp transverse band at the interface between the prospective midbrain and hindbrain, and is maintained in the anterior hindbrain in the developing neuroaxis (Bouillet et al. 1995; Li & Joyner 2001; Martinez-Barbera et al. 2001). Gbx2 regulates diverse developmental processes, including anteroposterior patterning within the mid-/hindbrain boundary and anterior hindbrain (Burroughs-Garcia et al. 2011). Expression of Gbx2 is required for the correct formation of rhombomeres r1-r3 (Wassarman et al. 1997). Loss of Gbx2 function in mouse embryos (Gbx2-/-), results in aberrant neural crest cell patterning leading to defects in neural crest derivatives and to abnormalities in the central nervous system, craniofacial, and cardiovascular components (Byrd & Meyers 2005). Li et al. (2009) demonstrated that Gbx2 is a direct target of the neural crest inducer Wnt, and is essential for neural crest induction. Together, these studies show that Gbx2 resides upstream in the genetic cascade controlling neural crest development and directly regulates the expression of key molecules involved in the migration and survival of neural crest cells that differentiate into neural and other components (e.g., connective tissue) of the head and heart. It was shown that Gbx2neo/neo mouse embryos, in which wild-type levels of Gbx2 expression is reduced to 6-10% of normal, are useful to further elucidate the complexity concerning the role of Gbx2 in anterior hindbrain development (Waters & Lewandoski 2006). Among other malformations, in Gbx2neo/neo embryos the mandibular branch of the trigeminal nerve (CNV3) is absent. CNV3 innervates the muscles of mastication (e.g., pterygoids, masseter, temporalis). However these muscles are needed to suckle and neonate (P0) Gbx2neo/neo mice are not able to suckle and die perinatally (Langenbach & van Eijden 2001). Here we describe the anatomy of the trigeminal ganglion and the trigeminal nerves in neonate Gbx2neo/neo mice and evaluate if there are differences in the muscles of mastication in these mice as compared to wildtype specimens. We expected that we find clear abnormalities in the thickness of the masseter, temporalis, and other muscles innervated by CNV3. However, this is not the case, indicating that the innervation of a muscle is not, as previously thought, needed for the differentiation of the muscles. Histological analyses will give insights into the muscle cell structure and if this is altered in the Gbx2neo/neo mice, which could be related to the loss of motor innervation. The research was funded by NSF EiR HBUC 18-522 awarded to JMZ (#2000005) and STW (#1956450). Bouillet et al. (1995). Dev Dyn, 204: 372-82. Burroughs-Garcia et al. (2011). Dev Dyn, 240: 828-38. Byrd & Meyers (2005). Dev Biol, 284: 233-45. Langenbach & van Eijden(2001). Am Zool, 41: 1338-51. Li et al. (2009). Development, 136: 3267-78. Li & Joyner (2001). Development, 128: 4979-91. Martinez-Barbera et al. (2001). Development, 128: 4789-800. Wassarman et al. (1997). Development, 124: 2923-34. Waters & Lewandoski (2006) Development, 133: 1991-2000. Funding or Support Information: The research was funded by NSF EiR HBUC 18-522 awarded to JMZ (#2000005) and STW(#1956450).
DeLorenzo, Leah; Powder, Kara E.
(, Evolution & Development)
Abstract A central question in biology is the molecular origins of phenotypic diversity. While genetic changes are key to the genotype–phenotype relationship, alterations to chromatin structure and the physical packaging of histone proteins may also be important drivers of vertebrate divergence. We investigate the impact of such an epigenetic mechanism, histone acetylation, within a textbook example of an adaptive radiation. Cichlids of Lake Malawi have adapted diverse craniofacial structures, and here we investigate how histone acetylation influences morphological variation in these fishes. Specifically, we assessed the effect of inhibiting histone deacetylation using the drug trichostatin A (TSA) on developing facial structures. We examined this during three critical developmental windows in two cichlid species with alternate adult morphologies. Exposure to TSA during neural crest cell (NCC) migration and as postmigratory NCCs proliferate in the pharyngeal arches resulted in significant changes in lateral and ventral shape inMaylandia, but not inTropheops. This included an overall shortening of the head, widening of the lower jaw, and steeper craniofacial profile, all of which are paedomorphic morphologies. In contrast, treatment with TSA during early chondrogenesis did not result in significant morphological changes in either species. Together, these data suggest a sensitivity to epigenetic alterations that are both time‐ and species‐dependent. We find that morphologies are due to nonautonomous or potentially indirect effects on NCC development, including in part a global developmental delay. Our research bolsters the understanding that proper histone acetylation is essential for early craniofacial development and identifies a species‐specific robustness to developmental change. Overall, this study demonstrates how epigenetic regulation may play an important role in both generating and buffering morphological variation.
McFann, Sarah; Dutta, Sayantan; Toettcher, Jared E.; Shvartsman, Stanislav Y.
(, Proceedings of the National Academy of Sciences)
Markers for the endoderm and mesoderm germ layers are commonly expressed together in the early embryo, potentially reflecting cells’ ability to explore potential fates before fully committing. It remains unclear when commitment to a single-germ layer is reached and how it is impacted by external signals. Here, we address this important question in Drosophila , a convenient model system in which mesodermal and endodermal fates are associated with distinct cellular movements during gastrulation. Systematically applying endoderm-inducing extracellular signal-regulated kinase (ERK) signals to the ventral medial embryo—which normally only receives a mesoderm-inducing cue—reveals a critical time window during which mesodermal cell movements and gene expression are suppressed by proendoderm signaling. We identify the ERK target gene huckebein ( hkb ) as the main cause of the ventral furrow suppression and use computational modeling to show that Hkb repression of the mesoderm-associated gene snail is sufficient to account for a broad range of transcriptional and morphogenetic effects. Our approach, pairing precise signaling perturbations with observation of transcriptional dynamics and cell movements, provides a general framework for dissecting the complexities of combinatorial tissue patterning.
Ziermann-Canabarro, Janine M, and Correa-Alfonzo, Paola. Variations in Tissue Interactions During Head Muscle Development. Retrieved from https://par.nsf.gov/biblio/10616887. The Anatomical Record 307.S1 Web. doi:10.1002/ar.25522.
Ziermann-Canabarro, Janine M, & Correa-Alfonzo, Paola. Variations in Tissue Interactions During Head Muscle Development. The Anatomical Record, 307 (S1). Retrieved from https://par.nsf.gov/biblio/10616887. https://doi.org/10.1002/ar.25522
Ziermann-Canabarro, Janine M, and Correa-Alfonzo, Paola.
"Variations in Tissue Interactions During Head Muscle Development". The Anatomical Record 307 (S1). Country unknown/Code not available: Anatomical Record. https://doi.org/10.1002/ar.25522.https://par.nsf.gov/biblio/10616887.
@article{osti_10616887,
place = {Country unknown/Code not available},
title = {Variations in Tissue Interactions During Head Muscle Development},
url = {https://par.nsf.gov/biblio/10616887},
DOI = {10.1002/ar.25522},
abstractNote = {For decades it has been established that head muscle development differs from trunk muscle development. Similarly known, even though not in such detail, is that different subgroups of head muscles develop dependent on different underlying gene regulatory networks. Even less well studied are the tissue interactions during the developmental processes. Muscles derived from pharyngeal arch mesoderm depend on interactions with endoderm and neural crest cells, and, to a minor extent, ectodermal cues. Extraocular eye muscles respond to a mix of signals from surrounding mesoderm, but also neural crest cells; however, they are independent of endodermal cues. Head muscles derived from occipital paraxial mesoderm depend on tissue interactions similar to pharyngeal arch muscles but have a different migration trajectory. While the pharyngeal arch mesodermal cells and neural crest cells largely migrate from dorsal to ventral, the occipital paraxial mesodermal cells migrate from dorsal to ventral and from posterior to anterior. During the migration these cells proliferate and even start to differentiate, while pharyngeal mesodermal cells begin the differentiation process after reaching their respective pharyngeal arches. Here we present an overview of tissue interactions during the development of different head muscle populations, highlighting general concepts and main differences. Topic Category: Neural Crest, Placodes and Craniofacial Development Keywords: Craniofacial muscles, Myogenesis Funding or Support Information: NSF #2000005 to JMZC},
journal = {The Anatomical Record},
volume = {307},
number = {S1},
publisher = {Anatomical Record},
author = {Ziermann-Canabarro, Janine M and Correa-Alfonzo, Paola},
}
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