M Cabrera

Author response: Basement membranes are crucial for proper olfactory placode shape, position and boundary with the brain, and for olfactory axon development

P Tignard Karen Pottin Audrey Geeverding Mohamed Doulazmi M Cabrera

Position (finance)

10.7554/elife.92004.3.sa4

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Basement membranes are crucial for proper olfactory placode shape, position and boundary with the brain, and for olfactory axon development

eLife (2024)

P Tignard Karen Pottin Audrey Geeverding Mohamed Doulazmi M Cabrera

Despite recent progress, the complex roles played by the extracellular matrix in development and disease are still far from being fully understood. Here, we took advantage of the zebrafish sly mutation which affects Laminin γ1, a major component of basement membranes, to explore its role in the development of the olfactory system. Following a detailed characterisation of Laminin distribution in the developing olfactory circuit, we analysed basement membrane integrity, olfactory placode and brain morphogenesis, and olfactory axon development in sly mutants, using a combination of immunochemistry, electron microscopy and quantitative live imaging of cell movements and axon behaviours. Our results point to an original and dual contribution of Laminin γ1-dependent basement membranes in organising the border between the olfactory placode and the adjacent brain: they maintain placode shape and position in the face of major brain morphogenetic movements, they establish a robust physical barrier between the two tissues while at the same time allowing the local entry of the sensory axons into the brain and their navigation towards the olfactory bulb. This work thus identifies key roles of Laminin γ1-dependent basement membranes in neuronal tissue morphogenesis and axon development in vivo.

10.7554/elife.92004.3

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Intertissue mechanical interactions shape the olfactory circuit in zebrafish

bioRxiv (Cold Spring Harbor Laboratory) (2021)

Pauline Monnot Girisaran Gangatharan Marion Baraban Karen Pottin M Cabrera

Abstract While the chemical signals guiding neuronal migration and axon elongation have been extensively studied, the influence of mechanical cues on these processes remains poorly studied in vivo . Here, we investigate how mechanical forces exerted by surrounding tissues steer neuronal movements and axon extension during the morphogenesis of the olfactory placode in zebrafish. We mainly focus on the mechanical contribution of the adjacent eye tissue, which develops underneath the placode through extensive evagination and invagination movements. Using quantitative analysis of cell movements and biomechanical manipulations, we show that the developing eye exerts lateral traction forces on the olfactory placode through extracellular matrix, mediating proper morphogenetic movements and axon extension within the placode. Our data shed new light on the key participation of intertissue mechanical interactions in the sculpting of neuronal circuits.

Convergent extension

10.1101/2021.03.15.435408

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Laminin γ1-dependent basement membranes are instrumental to ensure proper olfactory placode shape, position and boundary with the brain, as well as olfactory axon development

eLife (2023)

P Tignard Karen Pottin Audrey Geeverding Mohamed Doulazmi M Cabrera

Despite recent progress, the complex roles played by the extracellular matrix in development and disease are still far from being fully understood. Here, we took advantage of the zebrafish sly mutation which affects Laminin γ1, a major component of basement membranes, to explore its role in the development of the olfactory system. Following a detailed characterisation of Laminin distribution in the developing olfactory circuit, we analysed basement membrane integrity, olfactory placode and brain morphogenesis, and olfactory axon development in sly mutants, using a combination of immunochemistry, electron microscopy and quantitative live imaging of cell movements and axon behaviours. Our results point to an original and dual contribution of Laminin γ1-dependent basement membranes in organising the border between the olfactory placode and the adjacent brain: they maintain placode shape and position in the face of major brain morphogenetic movements, they establish a robust physical barrier between the two tissues while at the same time allowing the local entry of the sensory axons into the brain and their navigation towards the olfactory bulb. This work thus identifies key roles of Laminin γ1-dependent basement membranes in neuronal tissue morphogenesis and axon development in vivo.

Olfactory nerve

10.7554/elife.92004

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Reviewer #1 (Public Review): Laminin γ1-dependent basement membranes are instrumental to ensure proper olfactory placode shape, position and boundary with the brain, as well as olfactory axon development

P Tignard Karen Pottin Audrey Geeverding Mohamed Doulazmi M Cabrera

Despite recent progress, the complex roles played by the extracellular matrix in development and disease are still far from being fully understood. Here, we took advantage of the zebrafish sly mutation which affects Laminin γ1, a major component of basement membranes, to explore its role in the development of the olfactory system. Following a detailed characterisation of Laminin distribution in the developing olfactory circuit, we analysed basement membrane integrity, olfactory placode and brain morphogenesis, and olfactory axon development in sly mutants, using a combination of immunochemistry, electron microscopy and quantitative live imaging of cell movements and axon behaviours. Our results point to an original and dual contribution of Laminin γ1-dependent basement membranes in organising the border between the olfactory placode and the adjacent brain: they maintain placode shape and position in the face of major brain morphogenetic movements, they establish a robust physical barrier between the two tissues while at the same time allowing the local entry of the sensory axons into the brain and their navigation towards the olfactory bulb. This work thus identifies key roles of Laminin γ1-dependent basement membranes in neuronal tissue morphogenesis and axon development in vivo.

10.7554/elife.92004.1.sa2

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Laminin γ1-dependent basement membranes are instrumental to ensure proper olfactory placode shape, position and boundary with the brain, as well as olfactory axon development

bioRxiv (Cold Spring Harbor Laboratory) (2023)

P Tignard Karen Pottin Audrey Geeverding Mohamed Doulazmi M Cabrera

Despite recent progress, the complex roles played by the extracellular matrix in development and disease are still far from being fully understood. Here, we took advantage of the zebrafish

Position (finance)

10.1101/2023.06.29.547040

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Laminin γ1-dependent basement membranes are instrumental to ensure proper olfactory placode shape, position and boundary with the brain, as well as olfactory axon development

P Tignard Karen Pottin Audrey Geeverding Mohamed Doulazmi M Cabrera

Despite recent progress, the complex roles played by the extracellular matrix in development and disease are still far from being fully understood. Here, we took advantage of the zebrafish sly mutation which affects Laminin γ1, a major component of basement membranes, to explore its role in the development of the olfactory system. Following a detailed characterisation of Laminin distribution in the developing olfactory circuit, we analysed basement membrane integrity, olfactory placode and brain morphogenesis, and olfactory axon development in sly mutants, using a combination of immunochemistry, electron microscopy and quantitative live imaging of cell movements and axon behaviours. Our results point to an original and dual contribution of Laminin γ1-dependent basement membranes in organising the border between the olfactory placode and the adjacent brain: they maintain placode shape and position in the face of major brain morphogenetic movements, they establish a robust physical barrier between the two tissues while at the same time allowing the local entry of the sensory axons into the brain and their navigation towards the olfactory bulb. This work thus identifies key roles of Laminin γ1-dependent basement membranes in neuronal tissue morphogenesis and axon development in vivo .

Position (finance)

10.7554/elife.92004.1

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Reviewer #3 (Public Review): Laminin γ1-dependent basement membranes are instrumental to ensure proper olfactory placode shape, position and boundary with the brain, as well as olfactory axon development

P Tignard Karen Pottin Audrey Geeverding Mohamed Doulazmi M Cabrera

Despite recent progress, the complex roles played by the extracellular matrix in development and disease are still far from being fully understood. Here, we took advantage of the zebrafish sly mutation which affects Laminin γ1, a major component of basement membranes, to explore its role in the development of the olfactory system. Following a detailed characterisation of Laminin distribution in the developing olfactory circuit, we analysed basement membrane integrity, olfactory placode and brain morphogenesis, and olfactory axon development in sly mutants, using a combination of immunochemistry, electron microscopy and quantitative live imaging of cell movements and axon behaviours. Our results point to an original and dual contribution of Laminin γ1-dependent basement membranes in organising the border between the olfactory placode and the adjacent brain: they maintain placode shape and position in the face of major brain morphogenetic movements, they establish a robust physical barrier between the two tissues while at the same time allowing the local entry of the sensory axons into the brain and their navigation towards the olfactory bulb. This work thus identifies key roles of Laminin γ1-dependent basement membranes in neuronal tissue morphogenesis and axon development in vivo.

10.7554/elife.92004.1.sa0

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

bioRxiv (Cold Spring Harbor Laboratory) (2022)

Marion Baraban Clara Gordillo Pi Isabelle Bonnet Jean-François Gilles Camille Lejeune

Summary 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.

Nostril

10.1101/2022.07.15.500210

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Intertissue mechanical interactions shape the olfactory circuit in zebrafish

EMBO Reports (2021)

Pauline Monnot Girisaran Gangatharan Marion Baraban Karen Pottin M Cabrera

Convergent extension

10.15252/embr.202152963

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Citations (20)