Cell-type heterogeneity in the early zebrafish olfactory epithelium is generated from progenitors within preplacodal ectoderm

The zebrafish olfactory epithelium comprises a variety of neuronal populations, which are thought to have distinct embryonic origins. For instance, while ciliated sensory neurons arise from preplacodal ectoderm (PPE), previous lineage tracing studies suggest that both Gonadotropin releasing hormone...

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Main Authors: Raphaël Aguillon, Julie Batut, Arul Subramanian, Romain Madelaine, Pascale Dufourcq, Thomas F Schilling, Patrick Blader
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2018-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/32041
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author Raphaël Aguillon
Julie Batut
Arul Subramanian
Romain Madelaine
Pascale Dufourcq
Thomas F Schilling
Patrick Blader
author_facet Raphaël Aguillon
Julie Batut
Arul Subramanian
Romain Madelaine
Pascale Dufourcq
Thomas F Schilling
Patrick Blader
author_sort Raphaël Aguillon
collection DOAJ
description The zebrafish olfactory epithelium comprises a variety of neuronal populations, which are thought to have distinct embryonic origins. For instance, while ciliated sensory neurons arise from preplacodal ectoderm (PPE), previous lineage tracing studies suggest that both Gonadotropin releasing hormone 3 (Gnrh3) and microvillous sensory neurons derive from cranial neural crest (CNC). We find that the expression of Islet1/2 is restricted to Gnrh3 neurons associated with the olfactory epithelium. Unexpectedly, however, we find no change in Islet1/2+ cell numbers in sox10 mutant embryos, calling into question their CNC origin. Lineage reconstruction based on backtracking in time-lapse confocal datasets, and confirmed by photoconversion experiments, reveals that Gnrh3 neurons derive from the anterior PPE. Similarly, all of the microvillous sensory neurons we have traced arise from preplacodal progenitors. Our results suggest that rather than originating from separate ectodermal populations, cell-type heterogeneity is generated from overlapping pools of progenitors within the preplacodal ectoderm.
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spelling doaj.art-9342fd89a923408f816c8c7ed53c63352022-12-22T02:05:00ZengeLife Sciences Publications LtdeLife2050-084X2018-01-01710.7554/eLife.32041Cell-type heterogeneity in the early zebrafish olfactory epithelium is generated from progenitors within preplacodal ectodermRaphaël Aguillon0Julie Batut1https://orcid.org/0000-0002-1984-2094Arul Subramanian2https://orcid.org/0000-0001-8455-6804Romain Madelaine3Pascale Dufourcq4Thomas F Schilling5https://orcid.org/0000-0003-1798-8695Patrick Blader6https://orcid.org/0000-0003-3299-6108Centre de Biologie du Développement (CBD, UMR5547), Centre de Biologie Intégrative (CBI, FR3743), Université de Toulouse, Toulouse, FranceCentre de Biologie du Développement (CBD, UMR5547), Centre de Biologie Intégrative (CBI, FR3743), Université de Toulouse, Toulouse, FranceDepartment of Developmental and Cell Biology, University of California, Irvine, United StatesCentre de Biologie du Développement (CBD, UMR5547), Centre de Biologie Intégrative (CBI, FR3743), Université de Toulouse, Toulouse, FranceCentre de Biologie du Développement (CBD, UMR5547), Centre de Biologie Intégrative (CBI, FR3743), Université de Toulouse, Toulouse, FranceDepartment of Developmental and Cell Biology, University of California, Irvine, United StatesCentre de Biologie du Développement (CBD, UMR5547), Centre de Biologie Intégrative (CBI, FR3743), Université de Toulouse, Toulouse, FranceThe zebrafish olfactory epithelium comprises a variety of neuronal populations, which are thought to have distinct embryonic origins. For instance, while ciliated sensory neurons arise from preplacodal ectoderm (PPE), previous lineage tracing studies suggest that both Gonadotropin releasing hormone 3 (Gnrh3) and microvillous sensory neurons derive from cranial neural crest (CNC). We find that the expression of Islet1/2 is restricted to Gnrh3 neurons associated with the olfactory epithelium. Unexpectedly, however, we find no change in Islet1/2+ cell numbers in sox10 mutant embryos, calling into question their CNC origin. Lineage reconstruction based on backtracking in time-lapse confocal datasets, and confirmed by photoconversion experiments, reveals that Gnrh3 neurons derive from the anterior PPE. Similarly, all of the microvillous sensory neurons we have traced arise from preplacodal progenitors. Our results suggest that rather than originating from separate ectodermal populations, cell-type heterogeneity is generated from overlapping pools of progenitors within the preplacodal ectoderm.https://elifesciences.org/articles/32041olfactory placodeneuronal subtypelineage origin
spellingShingle Raphaël Aguillon
Julie Batut
Arul Subramanian
Romain Madelaine
Pascale Dufourcq
Thomas F Schilling
Patrick Blader
Cell-type heterogeneity in the early zebrafish olfactory epithelium is generated from progenitors within preplacodal ectoderm
eLife
olfactory placode
neuronal subtype
lineage origin
title Cell-type heterogeneity in the early zebrafish olfactory epithelium is generated from progenitors within preplacodal ectoderm
title_full Cell-type heterogeneity in the early zebrafish olfactory epithelium is generated from progenitors within preplacodal ectoderm
title_fullStr Cell-type heterogeneity in the early zebrafish olfactory epithelium is generated from progenitors within preplacodal ectoderm
title_full_unstemmed Cell-type heterogeneity in the early zebrafish olfactory epithelium is generated from progenitors within preplacodal ectoderm
title_short Cell-type heterogeneity in the early zebrafish olfactory epithelium is generated from progenitors within preplacodal ectoderm
title_sort cell type heterogeneity in the early zebrafish olfactory epithelium is generated from progenitors within preplacodal ectoderm
topic olfactory placode
neuronal subtype
lineage origin
url https://elifesciences.org/articles/32041
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