Development of the sensory nervous system in the vertebrate head: the importance of being on time

Lleras-Forero, Laura; Streit, Andrea

doi:10.1016/j.gde.2012.05.003

Cited by 33 publications

(30 citation statements)

References 65 publications

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“…The data obtained from studies in model organisms on the roles of signaling systems in sensory placode development are sometimes contradictory (reviewed by Saint-Jeannet and Moody, 2014), perhaps owing to the fact that activation of similar combinations of signaling molecules at different time points can result in strikingly different outcomes (Lleras-Forero and Streit, 2012;Sjödal et al, 2007). Here, we studied three signaling systems in two morphs of a single species, and investigated their effects on the specification of regional placodal identity and sensory fate at the end of gastrulation/neural plate stage (Fig.…”

Section: General Considerations Of Sensory Development and Evolutionmentioning

confidence: 99%

Sensory evolution in blind cavefish is driven by early embryonic events during gastrulation and neurulation

et al. 2016

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Natural variations in sensory systems constitute adaptive responses to the environment. Here, we compared sensory placode development in the blind cave-adapted morph and the eyed riverdwelling morph of Astyanax mexicanus. Focusing on the lens and olfactory placodes, we found a trade-off between these two sensory components in the two morphs: from neural plate stage onwards, cavefish have larger olfactory placodes and smaller lens placodes. In a search for developmental mechanisms underlying cavefish sensory evolution, we analyzed the roles of Shh, Fgf8 and Bmp4 signaling, which are known to be fundamental in patterning the vertebrate head and are subtly modulated in space and time during cavefish embryogenesis. Modulating these signaling systems at the end of gastrulation shifted the balance toward a larger olfactory derivative. Olfactory tests to assess potential behavioral outcomes of such developmental evolution revealed that Astyanax cavefish are able to respond to a 10 5 -fold lower concentration of amino acids than their surface-dwelling counterparts. We suggest that similar evolutionary developmental mechanisms may be used throughout vertebrates to drive adaptive sensory specializations according to lifestyle and habitat.

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Section: General Considerations Of Sensory Development and Evolutionmentioning

confidence: 99%

Sensory evolution in blind cavefish is driven by early embryonic events during gastrulation and neurulation

et al. 2016

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“…3 I-L) (12). Anterior neural plate (neural ectoderm) and NNE develop in close proximity during the transitional period of late gastrulation and early neurulation (2). NNE markers MSX2, TFAP2A, and GATA3 were among the genes that contributed most to separation of the pNNE cell population from the neural ectoderm group that was defined by expression of LHX2, RAX, and PAX6 ( Fig.…”

Section: -I)mentioning

confidence: 94%

Single-cell analysis delineates a trajectory toward the human early otic lineage

Ealy

Ellwanger

Kosaric

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Efficient pluripotent stem cell guidance protocols for the production of human posterior cranial placodes such as the otic placode that gives rise to the inner ear do not exist. Here we use a systematic approach including defined monolayer culture, signaling modulation, and single-cell gene expression analysis to delineate a developmental trajectory for human otic lineage specification in vitro. We found that modulation of bone morphogenetic protein (BMP) and WNT signaling combined with FGF and retinoic acid treatments over the course of 18 days generates cell populations that develop chronological expression of marker genes of non-neural ectoderm, preplacodal ectoderm, and early otic lineage. Gene expression along this differentiation path is distinct from other lineages such as endoderm, mesendoderm, and neural ectoderm. Single-cell analysis exposed the heterogeneity of differentiating cells and allowed discrimination of non-neural ectoderm and otic lineage cells from off-target populations. Pseudotemporal ordering of human embryonic stem cell and induced pluripotent stem cell-derived single-cell gene expression profiles revealed an initially synchronous guidance toward non-neural ectoderm, followed by comparatively asynchronous occurrences of preplacodal and otic marker genes. Positive correlation of marker gene expression between both cell lines and resemblance to mouse embryonic day 10.5 otocyst cells implied reasonable robustness of the guidance protocol. Singlecell trajectory analysis further revealed that otic progenitor cell types are induced in monolayer cultures, but further development appears impeded, likely because of lack of a lineage-stabilizing microenvironment. Our results provide a framework for future exploration of stabilizing microenvironments for efficient differentiation of stem cell-generated human otic cell types.posterior placode | ectoderm | gene expression analysis | inner ear | pluripotent stem cells V ertebrate cranial placodes arise from a region of non-neural ectoderm (NNE) lateral to the rostral neural crest progenitor region and the neural plate (reviewed in refs. 1 and 2). In humans, the cranial placodes form during the first month of gestation, restricting our insight to experiments using pluripotent stem cell-based models. Generation of human NNE and derivation of anterior placodal cells (i.e., pituitary, lens, and trigeminal neurons) from human embryonic stem cells (hESCs) has previously been achieved (3, 4). Production of posterior human placodal fates such as the otic placode and epibranchial ganglia neurons remains elusive, despite indications that immature sensory hair cell-like cells might arise in hESC-derived aggregates via manipulation of TGFβ, WNT, and FGF signaling, albeit with low efficiency (5-7).We used adherently grown hESCs and human induced pluripotent stem cells (iPSCs) to systematically test conditions for stepwise induction of NNE to posterior placode fates; specifically, the otic lineage. A challenge of in vitro guidance is the transient state of presump...

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“…These studies showed that sensory placodes arise from a crescent-shaped ectodermal territory surrounding the anterior neural plate at late gastrulation/ early neurulation stages. This contiguous region coincides with the expression domain of transcription factors such as Eya1, Six1/2 and Six4/5, which are crucial for placode formation and are thought to establish a placodal bias in this domain (Lleras-Forero and Streit, 2012;Pieper et al, 2011;Schlosser, 2010). These observations, together with unique properties shared by cells within this territory Martin and Grooves, 2006), argue that it represents the common domain of origin for all placodes, the so-called pan-placodal or pre-placodal region (PPR) Schlosser, 2010;Streit, 2008).…”

Section: Introductionmentioning

confidence: 90%

Mechanisms of cranial placode assembly

Breau¹,

Schneider‐Maunoury²

2014

Int. J. Dev. Biol.

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Cranial placodes are transient ectodermal structures contributing to the paired sensory organs and ganglia of the vertebrate head. Placode progenitors are initially spread and intermixed within a continuous embryonic territory surrounding the anterior neural plate, the so-called panplacodal region, which progressively breaks into distinct and compact placodal structures. The mechanisms driving the formation of these discrete placodes from the initial scattered distribution of their progenitors are poorly understood, and the implication of cell fate changes, local sorting out or massive cell movements is still a matter of debate. Here, we discuss different models that could account for placode assembly and review recent studies unraveling novel cellular and molecular aspects of this key event in the construction of the vertebrate head.

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Development of the sensory nervous system in the vertebrate head: the importance of being on time

Cited by 33 publications

References 65 publications

Sensory evolution in blind cavefish is driven by early embryonic events during gastrulation and neurulation

Sensory evolution in blind cavefish is driven by early embryonic events during gastrulation and neurulation

Single-cell analysis delineates a trajectory toward the human early otic lineage

Mechanisms of cranial placode assembly

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