Intertissue mechanical interactions shape the olfactory circuit in zebrafish

Monnot, Pauline; Baraban, Marion; Pottin, Karen; Cabrera, Mélody; Bonnet, Isabelle; Breau, Marie Anne

doi:10.15252/embr.202152963

Cited by 17 publications

(10 citation statements)

References 96 publications

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“…Consequently, when the optic cup does not form in eyeless rx3 mutant embryos, placode movements are reduced, and axons are shorter and less stretched. 69 Thus, pioneer axon elongation is mediated by mechanical forces but not by guidance or trophic molecules. While these findings have not been confirmed in other species, these movements could also explain pioneer olfactory axon formation in mammals and humans.…”

Section: Innervation Of the Olfactory Systemmentioning

confidence: 99%

Wiring the senses: Factors that regulate peripheral axon pathfinding in sensory systems

Nomdedeu‐Sancho

Alsina

2022

Developmental Dynamics

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Sensory neurons of the head are the ones that transmit the information about the external world to our brain for its processing. Axons from cranial sensory neurons sense different chemoattractant and chemorepulsive molecules during the journey and in the target tissue to establish the precise innervation with brain neurons and/or receptor cells. Here, we aim to unify and summarize the available information regarding molecular mechanisms guiding the different afferent sensory axons of the head. By putting the information together, we find the use of similar guidance cues in different sensory systems but in distinct combinations. In vertebrates, the number of genes in each family of guidance cues has suffered a great expansion in the genome, providing redundancy, and robustness. We also discuss recently published data involving the role of glia and mechanical forces in shaping the axon paths. Finally, we highlight the remaining questions to be addressed in the field.

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Section: Innervation Of the Olfactory Systemmentioning

confidence: 99%

Wiring the senses: Factors that regulate peripheral axon pathfinding in sensory systems

Nomdedeu‐Sancho

Alsina

2022

Developmental Dynamics

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“…To perturb the organisation of the rosette, we manipulated the early coalescence of the olfactory placodes, during which morphogenetic cell movements transform two elongated placodal cell fields lying on each side of the brain into spherical neuronal clusters (Breau et al, 2017; Aguillon et al, 2020; Monnot et al, 2022). We reasoned that perturbing the morphogenesis of the olfactory placode at these early stages (12-22 hpf) would likely result in abnormal rosette formation at our stages of interest (26-34 hpf).…”

Section: Resultsmentioning

confidence: 99%

Actomyosin contractility in olfactory placode neurons opens the skin epithelium to form the nostril

Baraban

Bonnet

et al. 2022

Preprint

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Despite their barrier function, epithelial layers can locally lose their integrity to create physiological openings during morphogenesis. The cellular and molecular mechanisms driving the formation of these epithelial breaks are only starting to be investigated. Here, we studied the formation of the zebrafish nostril (the olfactory orifice), which opens in the skin epithelium to expose the olfactory neurons to external odorant cues. Combining live imaging, drug treatments, laser ablation and tissue-specific functional perturbations, we demonstrate that the formation of the orifice is driven by a mechanical interplay between the olfactory placode neurons and the skin: the neurons pull on the overlying skin cells in an actomyosin-dependent manner, thus triggering the opening of the orifice. This work unravels an original mechanism to break an epithelial sheet, in which an adjacent group of cells instructs and mechanically assists the epithelium to induce its local rupture.

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“…Although there is related information, these questions have not been systematically addressed. A recent interesting study has shown that the extensive evagination and invagination movements of the zebrafish eye exert traction forces on the adjacent olfactory placode, influencing its development ( Monnot et al, 2022 ). Does the opposite hold true?…”

Section: Discussionmentioning

confidence: 99%

Optic cup morphogenesis across species and related inborn human eye defects

2023

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The vertebrate eye is shaped as a cup, a conformation that optimizes vision and is acquired early in development through a process known as optic cup morphogenesis. Imaging living, transparent teleost embryos and mammalian stem cell-derived organoids has provided insights into the rearrangements that eye progenitors undergo to adopt such a shape. Molecular and pharmacological interference with these rearrangements has further identified the underlying molecular machineries and the physical forces involved in this morphogenetic process. In this Review, we summarize the resulting scenarios and proposed models that include common and species-specific events. We further discuss how these studies and those in environmentally adapted blind species may shed light on human inborn eye malformations that result from failures in optic cup morphogenesis, including microphthalmia, anophthalmia and coloboma.

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Intertissue mechanical interactions shape the olfactory circuit in zebrafish

Cited by 17 publications

References 96 publications

Wiring the senses: Factors that regulate peripheral axon pathfinding in sensory systems

Wiring the senses: Factors that regulate peripheral axon pathfinding in sensory systems

Actomyosin contractility in olfactory placode neurons opens the skin epithelium to form the nostril

Optic cup morphogenesis across species and related inborn human eye defects

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