Making a head: Neural crest and ectodermal placodes in cranial sensory development

Koontz, Alison; Urrutia, Hugo A.; Bronner, Marianne E.

doi:10.1016/j.semcdb.2022.06.009

Cited by 16 publications

(10 citation statements)

References 270 publications

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“…Some inconsistencies between the results and other studies were evident. In the present study, the zygomatic arch was included in the anterior cranial module, while other studies reported that this was included in the posterior cranial module ( 20 ). This could be attributed to the overlapping nature of the anterior and posterior modules or its role as a bridging structure between the anterior and posterior skull.…”

Section: Discussionmentioning

confidence: 77%

“…Sensory placodes and neural crest cells are among the key cell populations that have facilitated the evolution of vertebrates. Shared molecular mechanisms underlie these processes before the establishment of definitive lineages, and anterior–posterior patterning forms the basis of sensory placode identity ( 20 ). The AnNA modules identified in the present study correspond to such anterior and posterior patterning of the placodes.…”

Section: Discussionmentioning

confidence: 99%

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Anatomical network modules of the human central nervous-craniofacial skeleton system

et al. 2023

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Anatomical network analysis (AnNA) is a systems biological framework based on network theory that enables anatomical structural analysis by incorporating modularity to model structural complexity. The human brain and facial structures exhibit close structural and functional relationships, suggestive of a co-evolved anatomical network. The present study aimed to analyze the human head as a modular entity that comprises the central nervous system, including the brain, spinal cord, and craniofacial skeleton. An AnNA model was built using 39 anatomical nodes from the brain, spinal cord, and craniofacial skeleton. The linkages were identified using peripheral nerve supply and direct contact between structures. The Spinglass algorithm in the igraph software was applied to construct a network and identify the modules of the central nervous system-craniofacial skeleton anatomical network. Two modules were identified. These comprised an anterior module, which included the forebrain, anterior cranial base, and upper-middle face, and a posterior module, which included the midbrain, hindbrain, mandible, and posterior cranium. These findings may reflect the genetic and signaling networks that drive the mosaic central nervous system and craniofacial development and offer important systems biology perspectives for developmental disorders of craniofacial structures.

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Section: Discussionmentioning

confidence: 77%

Section: Discussionmentioning

confidence: 99%

Anatomical network modules of the human central nervous-craniofacial skeleton system

et al. 2023

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“…In the trigeminal ganglion at E12.5 fate-mapped NCCs (tdTomato + cells) represent a mix of both neurons and glia (Schwan cells), as both populations arise from the neural crest (Koontz et al 2023, Le Douarin & Smith 1988, Mendez-Maldonado et al 2020). We observed a reduction in NCC-derived Sox10 + , but not placodal (Isl1/2 + ), upon Wnt1 Cre2/+ -mediated Mllt11 ablation.…”

Section: Discussionmentioning

confidence: 99%

“…The peripheral nervous system is composed of the cranial and spinal nerves, which function in relaying sensory and motor signals between the central nervous system and somatic tissues. The peripheral nerves are derived from the neural crest cells (NCCs) and cells from specialized regional thickenings of the cranial ectoderm called placodes (D’Amico-Martel & Noden 1983, Hamburger 1961, Koontz et al 2023, Trainor 2014). During peripheral nerve neurogenesis, both neural crest cells and ectodermal placode cells delaminate from their respective epithelia, interact and ultimately lead to the formation of the peripheral nerves (Hamburger 1961, Kurosaka et al 2015).…”

Section: Introductionmentioning

confidence: 99%

Innervation of cranial muscles requires Mllt11/Af1q/Tcf7c function during trigeminal ganglion development

Zinck,

Stanton-Turcotte,

Witt

et al. 2024

Preprint

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The development of cranial nerves, including the trigeminal nerve, and the formation of neuromuscular junctions (NMJs) are crucial processes for craniofacial motor function. Mllt11/Af1q/Tcf7c (henceforth Mllt11), a novel type of cytoskeletal-interacting protein, has been implicated in neuronal migration and neuritogenesis during central nervous system development. However, its role in peripheral nerve development and NMJ formation remains poorly understood. This study investigates the function of Mllt11 during trigeminal ganglion development and its impact on motor innervation of the masseter muscle. We report Mllt11 expression in the developing trigeminal ganglia, suggesting a potential role in cranial nerve development. Using a conditional knockout mouse model to delete Mllt11 in Wnt1-expressing neural crest cells, we assessed trigeminal ganglion development and innervation of the masseter muscle in the jaw. Surprisingly, we find that Mllt11 loss does not affect the initial formation of the trigeminal ganglion but disrupts its cellular composition, with a reduction in the ratio of neural crest-derived Sox10+ cells relative to placode-derived Isl1/2+ cells. Furthermore, our study demonstrates that conditional Mllt11 knockout leads to reduction of neurofilament density and NMJs within the masseter muscle, indicating altered trigeminal motor innervation. Our findings show that Mllt11 regulates the cellular composition of the trigeminal ganglion and is essential for proper trigeminal motor innervation in the masseter muscle.

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“…Reciprocal interactions between neural crest cells and trigeminal placode cells are required to form the cranial trigeminal ganglion [1][2][3], which is involved in the perception of many sensations in the head and face, including touch, pressure, temperature, and pain [25].While this dual cellular origin of the trigeminal ganglion has been known for decades [1], the molecules mediating this process remain obscure. Neurogs belong to the bHLH transcription factor family and are known to play a crucial role in the development of placode-derived cranial sensory neurons.…”

Section: Discussionmentioning

confidence: 99%

Neurogenin 2 and Neuronal Differentiation 1 control proper development of the chick trigeminal ganglion and its nerve branches

Bina

Taneyhill

2022

Preprint

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The trigeminal ganglion contains the cell bodies of sensory neurons comprising cranial nerve V, which relays information related to pain, touch, and temperature from the face and head to the brain. Like other cranial ganglia, the trigeminal ganglion is composed of neuronal derivatives of two critical embryonic cell types, neural crest and placode cells. Neurogenesis within the cranial ganglia is promoted by Neurogenin 2 (Neurog2), which is expressed in trigeminal placode cells and their neuronal derivatives and transcriptionally activates neuronal differentiation genes like Neuronal Differentiation 1 (NeuroD1). Little is known, however, about the role of Neurog2 and NeuroD1 during chick trigeminal gangliogenesis. To address this, we depleted Neurog2 and NeuroD1 from trigeminal placode cells with morpholinos and demonstrated that Neurog2 and NeuroD1 influence trigeminal ganglion development. While knockdown of both Neurog2 and NeuroD1 affected innervation of the eye, Neurog2 and NeuroD1 had opposite effects on ophthalmic nerve branch organization. Taken together, our results highlight, for the first time, functional roles for Neurog2 and NeuroD1 during chick trigeminal gangliogenesis. These studies shed new light on the molecular mechanisms underlying trigeminal ganglion formation and may also provide insight into general cranial gangliogenesis and diseases of the peripheral nervous system.

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Making a head: Neural crest and ectodermal placodes in cranial sensory development

Cited by 16 publications

References 270 publications

Anatomical network modules of the human central nervous-craniofacial skeleton system

Anatomical network modules of the human central nervous-craniofacial skeleton system

Innervation of cranial muscles requires Mllt11/Af1q/Tcf7c function during trigeminal ganglion development

Neurogenin 2 and Neuronal Differentiation 1 control proper development of the chick trigeminal ganglion and its nerve branches

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