Entrez search - placode development
Specification of sensory placode progenitors: signals and transcription factor networks
Int J Dev Biol. 2018;62(1-2-3):195-205. doi: 10.1387/ijdb.170298as.
Sensory placodes contribute to much of the sensory nervous system in the vertebrate head. They give rise to parts of the eye, ear and nose, as well as to the sensory ganglia that innervate the face, tongue, oesophagus and visceral tissues. Despite their diversity, during development placodes arise from a population of common progenitor cells, which are first specified at the border of the neural plate. The chick has been particularly instrumental in dissecting the timing of these events, and recent evidence has highlighted the close relationship of placode progenitors and precursors for neural crest cells and the central nervous system. This review focuses on the induction of placode progenitors by localised signalling events, and the transcriptional networks that lead to their specification.
Nasal and otic placode specific regulation of Sox2 involves both activation by Sox-Sall4 synergism and multiple repression mechanisms
Dev Biol. 2018 Jan 1;433(1):61-74. doi: 10.1016/j.ydbio.2017.11.005. Epub 2017 Nov 11.
Sugahara S1, Fujimoto T1, Kondoh H2, Uchikawa M3. Author information Abstract Transcription factor gene Sox2 is expressed throughout sensory development, but the enhancers that regulate the gene vary depending on the developmental stages and tissues. To gain new insights into the gene regulatory network in sensory placode specification, regulation of the nasal-otic bispecific NOP1 enhancer of Sox2 was investigated in chicken embryos. Deletion and mutational analyses using electroporation showed that transcriptional repression mechanisms in combination with activation mechanisms determine placodal specificity. Activation of the NOP1 enhancer involves synergistic action by Sall4 and SoxB1/SoxE factors that bind to the adjacent sites. Deletion of repressive elements resulted in widening of the tissue area for enhancer activity to a region where the expression of Sall4 and SoxB1/E overlaps, e.g., the CNS and neural crest. Among multiple repressive elements that contribute to the placodal confinement of the NOP1 enhancer activity, CACCT/CACCTG motifs bound by Zeb/Snail family repressors play important roles. Overexpression of δEF1 (Zeb1) or Snail2 (Slug) strongly inhibited NOP1 activity. These data indicate that both activation by Sall4-Sox synergism and multiple repression mechanisms involving Zeb/Snail factors are essential for Sox2 regulation to be confined to the nasal and otic placodes.
Copyright © 2017 Elsevier Inc. All rights reserved.
KEYWORDS: Nasal and otic placodes; Sall4; Sensory development; Sox factors; Sox2 NOP1 enhancer; Zeb and Snail factors PMID: 29137924 DOI: 10.1016/j.ydbio.2017.11.005 [Indexed for MEDLINE] Free full text
Nature. 2018 Aug;560(7717):228-232. doi: 10.1038/s41586-018-0385-7. Epub 2018 Aug 1. Horie R1, Hazbun A1,2, Chen K1, Cao C1, Levine M3,4, Horie T5,6.
Placodes and neural crests represent defining features of vertebrates, yet their relationship remains unclear despite extensive investigation1-3. Here we use a combination of lineage tracing, gene disruption and single-cell RNA-sequencing assays to explore the properties of the lateral plate ectoderm of the proto-vertebrate, Ciona intestinalis. There are notable parallels between the patterning of the lateral plate in Ciona and the compartmentalization of the neural plate ectoderm in vertebrates4. Both systems exhibit sequential patterns of Six1/2, Pax3/7 and Msxb expression that depend on a network of interlocking regulatory interactions4. In Ciona, this compartmentalization network produces distinct but related types of sensory cells that share similarities with derivatives of both cranial placodes and the neural crest in vertebrates. Simple genetic disruptions result in the conversion of one sensory cell type into another. We focused on bipolar tail neurons, because they arise from the tail regions of the lateral plate and possess properties of the dorsal root ganglia, a derivative of the neural crest in vertebrates5. Notably, bipolar tail neurons were readily transformed into palp sensory cells, a proto-placodal sensory cell type that arises from the anterior-most regions of the lateral plate in the Ciona tadpole6. Proof of transformation was confirmed by whole-embryo single-cell RNA-sequencing assays. These findings suggest that compartmentalization of the lateral plate ectoderm preceded the advent of vertebrates, and served as a common source for the evolution of both cranial placodes and neural crest3,4.
PMID: 30069052 PMCID: PMC6390964 DOI: 10.1038/s41586-018-0385-7
Lateral line placodes of aquatic vertebrates are evolutionarily conserved in mammals
Biol Open. 2018 Jun 19;7(6). pii: bio031815. doi: 10.1242/bio.031815.
Washausen S1, Knabe W2.
Placodes are focal thickenings of the surface ectoderm which, together with neural crest, generate the peripheral nervous system of the vertebrate head. Here we examine how, in embryonic mice, apoptosis contributes to the remodelling of the primordial posterior placodal area (PPA) into physically separated otic and epibranchial placodes. Using pharmacological inhibition of apoptosis-associated caspases, we find evidence that apoptosis eliminates hitherto undiscovered rudiments of the lateral line sensory system which, in fish and aquatic amphibia, serves to detect movements, pressure changes or electric fields in the surrounding water. Our results refute the evolutionary theory, valid for more than a century that the whole lateral line was completely lost in amniotes. Instead, those parts of the PPA which, under experimental conditions, escape apoptosis have retained the developmental potential to produce lateral line placodes and the primordia of neuromasts that represent the major functional units of the mechanosensory lateral line system.
© 2018. Published by The Company of Biologists Ltd.
KEYWORDS: Apoptosis; Lateral line; Mouse embryos; Neuromasts; Posterior placodal area; Vestigial placodes PMID: 29848488 PMCID: PMC6031350 DOI: 10.1242/bio.031815
Six1 and Irx1 have reciprocal interactions during cranial placode and otic vesicle formation
Dev Biol. 2018 Dec 6. pii: S0012-1606(18)30342-7. doi: 10.1016/j.ydbio.2018.12.003. [Epub ahead of print]
Sullivan CH1, Majumdar HD2, Neilson KM2, Moody SA3.
The specialized sensory organs of the vertebrate head are derived from thickened patches of cells in the ectoderm called cranial sensory placodes. The developmental program that generates these placodes and the genes that are expressed during the process have been studied extensively in a number of animals, yet very little is known about how these genes regulate one another. We previously found via a microarray screen that Six1, a known transcriptional regulator of cranial placode fate, up-regulates Irx1 in ectodermal explants. In this study, we investigated the transcriptional relationship between Six1 and Irx1 and found that they reciprocally regulate each other throughout cranial placode and otic vesicle formation. Although Irx1 expression precedes that of Six1 in the neural border zone, its continued and appropriately patterned expression in the pre-placodal region (PPR) and otic vesicle requires Six1. At early PPR stages, Six1 expands the Irx1 domain, but this activity subsides over time and changes to a predominantly repressive effect. Likewise, Irx1 initially expands Six1 expression in the PPR, but later represses it. We also found that Irx1 and Sox11, a known direct target of Six1, reciprocally affect each other. This work demonstrates that the interactions between Six1 and Irx1 are continuous during PPR and placode development and their transcriptional effects on one another change over developmental time.
KEYWORDS: Fgf; Pax2; Pre-placodal region; Sox11; Sox9 PMID: 30529252 DOI: 10.1016/j.ydbio.2018.12.003
The pre-vertebrate origins of neurogenic placodes
Nature. 2015 Aug 27;524(7566):462-5. doi: 10.1038/nature14657. Epub 2015 Aug 10.
Abitua PB1, Gainous TB1, Kaczmarczyk AN1, Winchell CJ1, Hudson C2, Kamata K3, Nakagawa M3, Tsuda M3, Kusakabe TG4, Levine M1.
Abstract The sudden appearance of the neural crest and neurogenic placodes in early branching vertebrates has puzzled biologists for over a century. These embryonic tissues contribute to the development of the cranium and associated sensory organs, which were crucial for the evolution of the vertebrate "new head". A previous study suggests that rudimentary neural crest cells existed in ancestral chordates. However, the evolutionary origins of neurogenic placodes have remained obscure owing to a paucity of embryonic data from tunicates, the closest living relatives to those early vertebrates. Here we show that the tunicate Ciona intestinalis exhibits a proto-placodal ectoderm (PPE) that requires inhibition of bone morphogenetic protein (BMP) and expresses the key regulatory determinant Six1/2 and its co-factor Eya, a developmental process conserved across vertebrates. The Ciona PPE is shown to produce ciliated neurons that express genes for gonadotropin-releasing hormone (GnRH), a G-protein-coupled receptor for relaxin-3 (RXFP3) and a functional cyclic nucleotide-gated channel (CNGA), which suggests dual chemosensory and neurosecretory activities. These observations provide evidence that Ciona has a neurogenic proto-placode, which forms neurons that appear to be related to those derived from the olfactory placode and hypothalamic neurons of vertebrates. We discuss the possibility that the PPE-derived GnRH neurons of Ciona resemble an ancestral cell type, a progenitor to the complex neuronal circuit that integrates sensory information and neuroendocrine functions in vertebrates.
Transcriptional regulation of cranial sensory placode development
Curr Top Dev Biol. 2015;111:301-50. doi: 10.1016/bs.ctdb.2014.11.009. Epub 2015 Jan 22.
Moody SA1, LaMantia AS2.
Cranial sensory placodes derive from discrete patches of the head ectoderm and give rise to numerous sensory structures. During gastrulation, a specialized "neural border zone" forms around the neural plate in response to interactions between the neural and nonneural ectoderm and signals from adjacent mesodermal and/or endodermal tissues. This zone subsequently gives rise to two distinct precursor populations of the peripheral nervous system: the neural crest and the preplacodal ectoderm (PPE). The PPE is a common field from which all cranial sensory placodes arise (adenohypophyseal, olfactory, lens, trigeminal, epibranchial, otic). Members of the Six family of transcription factors are major regulators of PPE specification, in partnership with cofactor proteins such as Eya. Six gene activity also maintains tissue boundaries between the PPE, neural crest, and epidermis by repressing genes that specify the fates of those adjacent ectodermally derived domains. As the embryo acquires anterior-posterior identity, the PPE becomes transcriptionally regionalized, and it subsequently becomes subdivided into specific placodes with distinct developmental fates in response to signaling from adjacent tissues. Each placode is characterized by a unique transcriptional program that leads to the differentiation of highly specialized cells, such as neurosecretory cells, sensory receptor cells, chemosensory neurons, peripheral glia, and supporting cells. In this review, we summarize the transcriptional and signaling factors that regulate key steps of placode development, influence subsequent sensory neuron specification, and discuss what is known about mutations in some of the essential PPE genes that underlie human congenital syndromes. © 2015 Elsevier Inc. All rights reserved. KEYWORDS: Branchio-otic syndrome; Branchio-otic-renal syndrome; Cranial sensory neurons; Epibranchial; Eya; Olfactory; Pax; Six1; Six4; Trigeminal
Early embryonic specification of vertebrate cranial placodes
Wiley Interdiscip Rev Dev Biol. 2014 Sep-Oct;3(5):349-63. doi: 10.1002/wdev.142. Epub 2014 Jul 2.
Cranial placodes contribute to many sensory organs and ganglia of the vertebrate head. The olfactory, otic, and lateral line placodes form the sensory receptor cells and neurons of the nose, ear, and lateral line system; the lens placode develops into the lens of the eye; epibranchial, profundal, and trigeminal placodes contribute sensory neurons to cranial nerve ganglia; and the adenohypophyseal placode gives rise to the anterior pituitary, a major endocrine control organ. Despite these differences in fate, all placodes are now known to originate from a common precursor, the preplacodal ectoderm (PPE). The latter is a horseshoe-shaped domain of ectoderm surrounding the anterior neural plate and neural crest and is defined by expression of transcription factor Six1, its cofactor Eya1, and other members of the Six and Eya families. Studies in zebrafish, Xenopus, and chick reveal that the PPE is specified together with other ectodermal territories (epidermis, neural crest, and neural plate) during early embryogenesis. During gastrulation, domains of ventrally (e.g., Dlx3/Dlx5, GATA2/GATA3, AP2, Msx1, FoxI1, and Vent1/Vent2) and dorsally (e.g., Zic1, Sox3, and Geminin) restricted transcription factors are established in response to a gradient of BMP and help to define non-neural and neural competence territories, respectively. At neural plate stages, the PPE is then induced in the non-neural competence territory by signals from the adjacent neural plate and mesoderm including FGF, BMP inhibitors, and Wnt inhibitors. Subsequently, signals from more localized signaling centers induce restricted expression domains of various transcription factors within the PPE, which specify multiplacodal areas and ultimately individual placodes. For further resources related to this article, please visit the WIREs website. CONFLICT OF INTEREST: The author has declared no conflicts of interest for this article. © 2014 Wiley Periodicals, Inc.
Sensational placodes: neurogenesis in the otic and olfactory systems
Dev Biol. 2014 May 1;389(1):50-67. doi: 10.1016/j.ydbio.2014.01.023. Epub 2014 Feb 6.
Maier EC1, Saxena A2, Alsina B3, Bronner ME4, Whitfield TT5.
For both the intricate morphogenetic layout of the sensory cells in the ear and the elegantly radial arrangement of the sensory neurons in the nose, numerous signaling molecules and genetic determinants are required in concert to generate these specialized neuronal populations that help connect us to our environment. In this review, we outline many of the proteins and pathways that play essential roles in the differentiation of otic and olfactory neurons and their integration into their non-neuronal support structures. In both cases, well-known signaling pathways together with region-specific factors transform thickened ectodermal placodes into complex sense organs containing numerous, diverse neuronal subtypes. Olfactory and otic placodes, in combination with migratory neural crest stem cells, generate highly specialized subtypes of neuronal cells that sense sound, position and movement in space, odors and pheromones throughout our lives. Copyright © 2014 The Authors. Published by Elsevier Inc. All rights reserved. KEYWORDS: Hair cell; Neurogenesis; Olfactory; Otic; Sensory neuron PMID 24508480
The evolutionary history of vertebrate cranial placodes--I: cell type evolution
Dev Biol. 2014 May 1;389(1):82-97. doi: 10.1016/j.ydbio.2014.01.017. Epub 2014 Feb 1.
Patthey C1, Schlosser G2, Shimeld SM3.
Vertebrate cranial placodes are crucial contributors to the vertebrate cranial sensory apparatus. Their evolutionary origin has attracted much attention from evolutionary and developmental biologists, yielding speculation and hypotheses concerning their putative homologues in other lineages and the developmental and genetic innovations that might have underlain their origin and diversification. In this article we first briefly review our current understanding of placode development and the cell types and structures they form. We next summarise previous hypotheses of placode evolution, discussing their strengths and caveats, before considering the evolutionary history of the various cell types that develop from placodes. In an accompanying review, we also further consider the evolution of ectodermal patterning. Drawing on data from vertebrates, tunicates, amphioxus, other bilaterians and cnidarians, we build these strands into a scenario of placode evolutionary history and of the genes, cells and developmental processes that underlie placode evolution and development. Copyright © 2014 Elsevier Inc. All rights reserved. KEYWORDS: Amphioxus; Cell type; Ciona; Development; Evolution; Neural crest; Placode
The evolutionary history of vertebrate cranial placodes II. Evolution of ectodermal patterning
Dev Biol. 2014 May 1;389(1):98-119. doi: 10.1016/j.ydbio.2014.01.019. Epub 2014 Feb 1.
Schlosser G1, Patthey C2, Shimeld SM2.
Cranial placodes are evolutionary innovations of vertebrates. However, they most likely evolved by redeployment, rewiring and diversification of preexisting cell types and patterning mechanisms. In the second part of this review we compare vertebrates with other animal groups to elucidate the evolutionary history of ectodermal patterning. We show that several transcription factors have ancient bilaterian roles in dorsoventral and anteroposterior regionalisation of the ectoderm. Evidence from amphioxus suggests that ancestral chordates then concentrated neurosecretory cells in the anteriormost non-neural ectoderm. This anterior proto-placodal domain subsequently gave rise to the oral siphon primordia in tunicates (with neurosecretory cells being lost) and anterior (adenohypophyseal, olfactory, and lens) placodes of vertebrates. Likewise, tunicate atrial siphon primordia and posterior (otic, lateral line, and epibranchial) placodes of vertebrates probably evolved from a posterior proto-placodal region in the tunicate-vertebrate ancestor. Since both siphon primordia in tunicates give rise to sparse populations of sensory cells, both proto-placodal domains probably also gave rise to some sensory receptors in the tunicate-vertebrate ancestor. However, proper cranial placodes, which give rise to high density arrays of specialised sensory receptors and neurons, evolved from these domains only in the vertebrate lineage. We propose that this may have involved rewiring of the regulatory network upstream and downstream of Six1/2 and Six4/5 transcription factors and their Eya family cofactors. These proteins, which play ancient roles in neuronal differentiation were first recruited to the dorsal non-neural ectoderm in the tunicate-vertebrate ancestor but subsequently probably acquired new target genes in the vertebrate lineage, allowing them to adopt new functions in regulating proliferation and patterning of neuronal progenitors. Copyright © 2014 Elsevier Inc. All rights reserved. KEYWORDS: Amphioxus; BMP; Ciona; Eya; Neural crest; Neural induction; Placodes; Preplacodal ectoderm; Six1; Wnt PMID 24491817
Setting appropriate boundaries: Fate, patterning and competence at the neural plate border
Dev Biol. 2013 Dec 7. pii: S0012-1606(13)00644-1. doi: 10.1016/j.ydbio.2013.11.027. [Epub ahead of print]
Groves AK1, Labonne C2. Author information
The neural crest and craniofacial placodes are two distinct progenitor populations that arise at the border of the vertebrate neural plate. This border region develops through a series of inductive interactions that begins before gastrulation and progressively divide embryonic ectoderm into neural and non-neural regions, followed by the emergence of neural crest and placodal progenitors. In this review, we describe how a limited repertoire of inductive signals-principally FGFs, Wnts and BMPs-set up domains of transcription factors in the border region which establish these progenitor territories by both cross-inhibitory and cross-autoregulatory interactions. The gradual assembly of different cohorts of transcription factors that results from these interactions is one mechanism to provide the competence to respond to inductive signals in different ways, ultimately generating the neural crest and cranial placodes. © 2013 Published by Elsevier Inc. KEYWORDS: Competence, Induction, Neural crest, Placode, Transcription factor
Graded levels of Pax2a and Pax8 regulate cell differentiation during sensory placode formation
Development. 2012 Aug;139(15):2740-50. Epub 2012 Jun 28.
McCarroll MN, Lewis ZR, Culbertson MD, Martin BL, Kimelman D, Nechiporuk AV. Source Department of Cell and Developmental Biology, Oregon Health & Science University, Portland, OR 97239, USA.
Pax gene haploinsufficiency causes a variety of congenital defects. Renal-coloboma syndrome, resulting from mutations in Pax2, is characterized by kidney hypoplasia, optic nerve malformation, and hearing loss. Although this underscores the importance of Pax gene dosage in normal development, how differential levels of these transcriptional regulators affect cell differentiation and tissue morphogenesis is still poorly understood. We show that differential levels of zebrafish Pax2a and Pax8 modulate commitment and behavior in cells that eventually contribute to the otic vesicle and epibranchial placodes. Initially, a subset of epibranchial placode precursors lie lateral to otic precursors within a single Pax2a/8-positive domain; these cells subsequently move to segregate into distinct placodes. Using lineage-tracing and ablation analyses, we show that cells in the Pax2a/8+ domain become biased towards certain fates at the beginning of somitogenesis. Experiments involving either Pax2a overexpression or partial, combinatorial Pax2a and Pax8 loss of function reveal that high levels of Pax favor otic differentiation whereas low levels increase cell numbers in epibranchial ganglia. In addition, the Fgf and Wnt signaling pathways control Pax2a expression: Fgf is necessary to induce Pax2a, whereas Wnt instructs the high levels of Pax2a that favor otic differentiation. Our studies reveal the importance of Pax levels during sensory placode formation and provide a mechanism by which these levels are controlled.
Mutual repression between Gbx2 and Otx2 in sensory placodes reveals a general mechanism for ectodermal patterning
Dev Biol. 2012 Jul 1;367(1):55-65. Epub 2012 Apr 28.
Steventon B, Mayor R, Streit A. Source Department of Craniofacial Development, King's College London, Guy's Campus, Tower Wing Floor 27, London SE1 9RT, UK. Abstract In the vertebrate head, central and peripheral components of the sensory nervous system have different embryonic origins, the neural plate and sensory placodes. This raises the question of how they develop in register to form functional sense organs and sensory circuits. Here we show that mutual repression between the homeobox transcription factors Gbx2 and Otx2 patterns the placode territory by influencing regional identity and by segregating inner ear and trigeminal progenitors. Activation of Otx2 targets is necessary for anterior olfactory, lens and trigeminal character, while Gbx2 function is required for the formation of the posterior otic placode. Thus, like in the neural plate antagonistic interaction between Otx2 and Gbx2 establishes positional information thus providing a general mechanism for rostro-caudal patterning of the ectoderm. Our findings support the idea that the Otx/Gbx boundary has an ancient evolutionary origin to which different modules were recruited to specify cells of different fates. Copyright © 2012 Elsevier Inc. All rights reserved.
An effective assay for high cellular resolution time-lapse imaging of sensory placode formation and morphogenesis
BMC Neurosci. 2011 May 9;12:37.
Shiau CE, Das RM, Storey KG. Source Neural Development Group, Division of Cell & Developmental Biology, College of Life Science, University of Dundee, Dundee DD1 5EH, Scotland, UK. email@example.com
BACKGROUND: The vertebrate peripheral nervous system contains sensory neurons that arise from ectodermal placodes. Placodal cells ingress to move inside the head to form sensory neurons of the cranial ganglia. To date, however, the process of placodal cell ingression and underlying cellular behavior are poorly understood as studies have relied upon static analyses on fixed tissues. Visualizing placodal cell behavior requires an ability to distinguish the surface ectoderm from the underlying mesenchyme. This necessitates high resolution imaging along the z-plane which is difficult to accomplish in whole embryos. To address this issue, we have developed an imaging system using cranial slices that allows direct visualization of placode formation.
RESULTS: We demonstrate an effective imaging assay for capturing placode development at single cell resolution using chick embryonic tissue ex vivo. This provides the first time-lapse imaging of mitoses in the trigeminal placodal ectoderm, ingression, and intercellular contacts of placodal cells. Cell divisions with varied orientations were found in the placodal ectoderm all along the apical-basal axis. Placodal cells initially have short cytoplasmic processes during ingression as young neurons and mature over time to elaborate long axonal processes in the mesenchyme. Interestingly, the time-lapse imaging data reveal that these delaminating placodal neurons begin ingression early on from within the ectoderm, where they start to move and continue on to exit as individual or strings of neurons through common openings on the basal side of the epithelium. Furthermore, dynamic intercellular contacts are abundant among the delaminating placodal neurons, between these and the already delaminated cells, as well as among cells in the forming ganglion.
CONCLUSIONS: This new imaging assay provides a powerful method to analyze directly development of placode-derived sensory neurons and subsequent ganglia formation for the first time in amniotes. Viewing placode development in a head cross-section provides a vantage point from which it is possible to study comprehensive events in placode formation, from differentiation, cell ingression to ganglion assembly. Understanding how placodal neurons form may reveal a new mechanism of neurogenesis distinct from that in the central nervous system and provide new insight into how cells acquire motility from a stationary epithelial cell type.
Includes videos of chick placodes
Making senses development of vertebrate cranial placodes
Int Rev Cell Mol Biol. 2010;283:129-234.
Schlosser G. Source Zoology, School of Natural Sciences & Martin Ryan Institute, National University of Ireland, Galway, Ireland.
Cranial placodes (which include the adenohypophyseal, olfactory, lens, otic, lateral line, profundal/trigeminal, and epibranchial placodes) give rise to many sense organs and ganglia of the vertebrate head. Recent evidence suggests that all cranial placodes may be developmentally related structures, which originate from a common panplacodal primordium at neural plate stages and use similar regulatory mechanisms to control developmental processes shared between different placodes such as neurogenesis and morphogenetic movements. After providing a brief overview of placodal diversity, the present review summarizes current evidence for the existence of a panplacodal primordium and discusses the central role of transcription factors Six1 and Eya1 in the regulation of processes shared between different placodes. Upstream signaling events and transcription factors involved in early embryonic induction and specification of the panplacodal primordium are discussed next. I then review how individual placodes arise from the panplacodal primordium and present a model of multistep placode induction. Finally, I briefly summarize recent advances concerning how placodal neurons and sensory cells are specified, and how morphogenesis of placodes (including delamination and migration of placode-derived cells and invagination) is controlled.
Copyright 2010 Elsevier Inc. All rights reserved.
The formation of the cranial ganglia by placodally-derived sensory neuronal precursors
Mol Cell Neurosci. 2010 Nov 26. Blentic A, Chambers D, Skinner A, Begbie J, Graham A.
MRC Centre for Developmental Neurobiology, King's College London, London SE1 1UL, UK. Abstract The generation of the sensory ganglia involves the migration of a precursor population to the site of ganglion formation and the differentiation of sensory neurons. There is, however, a significant difference between the ganglia of the head and trunk in that while all of the sensory neurons of the trunk are derived from the neural crest, the majority of cranial sensory neurons are generated by the neurogenic placodes. In this study, we have detailed the route through which the placodally-derived sensory neurons are generated, and we find a number of important differences between the head and trunk. Although, the neurogenic placodes release neuroblasts that migrate internally to the site of ganglion formation, we find that there are no placodally-derived progenitor cells within the forming ganglia. The cells released by the placodes differentiate during migration and contribute to the cranial ganglia as post-mitotic neurons. In the trunk, it has been shown that progenitor cells persist in the forming Dorsal Root Ganglia and that much of the process of sensory neuronal differentiation occurs within the ganglion. We also find that the period over which neuronal cells delaminate from the placodes is significantly longer than the time frame over which neural crest cells populate the DRGs. We further show that placodal sensory neuronal differentiation can occur in the absence of local cues. Finally, we find that, in contrast to neural crest cells, the different mature neurogenic placodes seem to lack plasticity. Nodose neuroblasts cannot be diverted to form trigeminal neurons and vice versa.
Copyright © 2010. Published by Elsevier Inc.
PMID: 21112397 http://www.ncbi.nlm.nih.gov/pubmed/20881354
Identification of early requirements for preplacodal ectoderm and sensory organ development
PLoS Genet. 2010 Sep 23;6(9). pii: e1001133.
Kwon HJ, Bhat N, Sweet EM, Cornell RA, Riley BB.
Biology Department, Texas A&M University, College Station, Texas, United States of America. Abstract Preplacodal ectoderm arises near the end of gastrulation as a narrow band of cells surrounding the anterior neural plate. This domain later resolves into discrete cranial placodes that, together with neural crest, produce paired sensory structures of the head. Unlike the better-characterized neural crest, little is known about early regulation of preplacodal development. Classical models of ectodermal patterning posit that preplacodal identity is specified by readout of a discrete level of Bmp signaling along a DV gradient. More recent studies indicate that Bmp-antagonists are critical for promoting preplacodal development. However, it is unclear whether Bmp-antagonists establish the proper level of Bmp signaling within a morphogen gradient or, alternatively, block Bmp altogether. To begin addressing these issues, we treated zebrafish embryos with a pharmacological inhibitor of Bmp, sometimes combined with heat shock-induction of Chordin and dominant-negative Bmp receptor, to fully block Bmp signaling at various developmental stages. We find that preplacodal development occurs in two phases with opposing Bmp requirements. Initially, Bmp is required before gastrulation to co-induce four transcription factors, Tfap2a, Tfap2c, Foxi1, and Gata3, which establish preplacodal competence throughout the nonneural ectoderm. Subsequently, Bmp must be fully blocked in late gastrulation by dorsally expressed Bmp-antagonists, together with dorsally expressed Fgf and Pdgf, to specify preplacodal identity within competent cells abutting the neural plate. Localized ventral misexpression of Fgf8 and Chordin can activate ectopic preplacodal development anywhere within the zone of competence, whereas dorsal misexpression of one or more competence factors can activate ectopic preplacodal development in the neural plate. Conversely, morpholino-knockdown of competence factors specifically ablates preplacodal development. Our work supports a relatively simple two-step model that traces regulation of preplacodal development to late blastula stage, resolves two distinct phases of Bmp dependence, and identifies the main factors required for preplacodal competence and specification.
Induction of the epibranchial placodes
- "The cranial sensory ganglia, in contrast to those of the trunk, have a dual embryonic origin arising from both neurogenic placodes and neural crest. Neurogenic placodes are focal thickenings of ectoderm, found exclusively in the head of vertebrate embryos. These structures can be split into two groups based on the positions that they occupy within the embryo, dorsolateral and epibranchial. The dorsolateral placodes develop alongside the central nervous system, while the epibranchial placodes are located close to the top of the clefts between the branchial arches. Importantly, previous studies have shown that the neurogenic placodes form under the influence of the surrounding cranial tissues. In this paper, we have analysed the nature of the inductive signal underlying the formation of the epibranchial placodes. We find that epibranchial placodes do not require neural crest for their induction, but rather that it is the pharyngeal endoderm that is the source of the inductive signal. We also find that, while cranial ectoderm is competent to respond to this inductive signal, trunk ectoderm is not. We have further identified the signalling molecule Bmp7 as the mediator of this inductive interaction. This molecule is expressed in a manner consistent with it playing such a role and, when added to ectoderm explants, it will promote the formation of epibranchial neuronal cells. Moreover, the Bmp7 antagonist follstatin will block the ability of pharyngeal endoderm to induce placodal neuronal cells, demonstrating that Bmp7 is required for this inductive interaction. This work answers the long standing question regarding the induction of the epibranchial placodes, and represents the first elucidation of an inductive mechanism, and a molecular effector, underlying the formation of any primary sensory neurons in higher vertebrates."
- dorsolateral placodes - develop alongside the central nervous system
- epibranchial placodes - located close to the top of the clefts between the branchial arches.
Induction of the epibranchial placodes
Development. 1999 Feb;126(5):895-902.
Begbie J1, Brunet JF, Rubenstein JL, Graham A. Author information Abstract The cranial sensory ganglia, in contrast to those of the trunk, have a dual embryonic origin arising from both neurogenic placodes and neural crest. Neurogenic placodes are focal thickenings of ectoderm, found exclusively in the head of vertebrate embryos. These structures can be split into two groups based on the positions that they occupy within the embryo, dorsolateral and epibranchial. The dorsolateral placodes develop alongside the central nervous system, while the epibranchial placodes are located close to the top of the clefts between the branchial arches. Importantly, previous studies have shown that the neurogenic placodes form under the influence of the surrounding cranial tissues. In this paper, we have analysed the nature of the inductive signal underlying the formation of the epibranchial placodes. We find that epibranchial placodes do not require neural crest for their induction, but rather that it is the pharyngeal endoderm that is the source of the inductive signal. We also find that, while cranial ectoderm is competent to respond to this inductive signal, trunk ectoderm is not. We have further identified the signalling molecule Bmp7 as the mediator of this inductive interaction. This molecule is expressed in a manner consistent with it playing such a role and, when added to ectoderm explants, it will promote the formation of epibranchial neuronal cells. Moreover, the Bmp7 antagonist follstatin will block the ability of pharyngeal endoderm to induce placodal neuronal cells, demonstrating that Bmp7 is required for this inductive interaction. This work answers the long standing question regarding the induction of the epibranchial placodes, and represents the first elucidation of an inductive mechanism, and a molecular effector, underlying the formation of any primary sensory neurons in higher vertebrates.