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

ABSTRACT: 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.

SUBMITTER: Aguillon R

PROVIDER: S-EPMC5749950 | biostudies-literature | 2018 Jan

REPOSITORIES: biostudies-literature

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

Aguillon Raphaël R Batut Julie J Subramanian Arul A Madelaine Romain R Dufourcq Pascale P Schilling Thomas F TF Blader Patrick P

eLife 20180102

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. Unex ...[more]

PMID: 29292696

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Project description:BackgroundInsects detect a multitude of odors using a broad array of phenotypically distinct olfactory organs referred to as olfactory sensilla. Each sensillum contains one to several sensory neurons and at least three support cells; these cells arise from mitotic activities from one or a small group of defined precursor cells. Sensilla phenotypes are defined by distinct morphologies, and specificities to specific odors; these are the consequence of developmental programs expressed by associated neurons and support cells, and by selection and expression of subpopulations of olfactory genes encoding such proteins as odor receptors, odorant binding proteins, and odor degrading enzymes.Methodology/principal findingsWe are investigating development of the olfactory epithelium of adult M. sexta, identifying events which might establish sensilla phenotypes. In the present study, antennal tissue was examined during the first three days of an 18 day development, a period when sensory mitotic activity was previously reported to occur. Each antenna develops as a cylinder with an outward facing sensory epithelium divided into approximately 80 repeat units or annuli. Mitotic proliferation of sensory cells initiated about 20-24 hrs after pupation (a.p.), in pre-existing zones of high density cells lining the proximal and distal borders of each annulus. These high density zones were observed as early as two hr. a.p., and expanded with mitotic activity to fill the mid-annular regions by about 72 hrs a.p. Mitotic activity initiated at a low rate, increasing dramatically after 40-48 hrs a.p.; this activity was enhanced by ecdysteroids, but did not occur in animals entering pupal diapause (which is also ecdysteroid sensitive).Conclusions/significanceSensory proliferation initiates in narrow zones along the proximal and distal borders of each annulus; these zones rapidly expand to fill the mid-annular regions. These zones exist prior to any mitotic activity as regions of high density cells which form either at or prior to pupation. Mitotic sensitivity to ecdysteroids may be a regulatory mechanism coordinating olfactory development with the developmental choice of diapause entry.

Dataset Information

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

Publications

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

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