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Retroviral lineage analysis reveals dual contribution from ectodermal placodes and neural crest cells to avian olfactory sensory and GnRH neurons

Koontz, Alison and Urrutia, Hugo A. and Bronner, Marianne E. (2022) Retroviral lineage analysis reveals dual contribution from ectodermal placodes and neural crest cells to avian olfactory sensory and GnRH neurons. Natural Sciences, 2 (3). Art. No. e20210037. ISSN 2698-6248. doi:10.1002/ntls.20210037. https://resolver.caltech.edu/CaltechAUTHORS:20220526-391453000

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Abstract

The origin of the neurons and glia in the olfactory system of vertebrates has been controversial, with different cell types attributed to being of ectodermal placode versus neural crest lineage, depending upon the species. Here, we use replication incompetent avian retroviruses to perform a prospective cell lineage analysis of either presumptive olfactory placode or neural crest cells during early development of the chick embryo. Surprisingly, the results reveal a dual contribution from both the olfactory placode and neural crest cells to sensory neurons in the nose and gonadotropin-releasing hormone neurons migrating to the olfactory bulb. We also confirm that olfactory ensheathing glia cells are solely derived from the neural crest. Finally, our results show that neural crest cells and olfactory placode cells contribute to p63 positive cells, likely to be basal stem cells of the olfactory epithelium. Taken together, these finding provide evidence for previously unknown contributions of neural crest cells to some cell types in the chick olfactory system and help resolve previous discrepancies in the literature.


Item Type:Article
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URLURL TypeDescription
https://doi.org/10.1002/ntls.20210037DOIArticle
https://onlinelibrary.wiley.com/action/downloadSupplement?doi=10.1002%2Fntls.20210037&file=ntls20210037-sup-0001-FigureS1.tiffPublisherSupporting Information
https://publons.com/publon/10.1002/ntls.20210037Related ItemPeer Review History
ORCID:
AuthorORCID
Koontz, Alison0000-0001-7779-4839
Urrutia, Hugo A.0000-0002-2970-6918
Bronner, Marianne E.0000-0003-4274-1862
Additional Information:© 2022 The Authors. Natural Sciences published by Wiley-VCH GmbH. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. Issue Online: 13 July 2022. Version of Record online: 25 May 2022. Manuscript accepted: 19 April 2022. Manuscript revised: 11 April 2022. Manuscript received: 07 July 2021. Alison Koontz and, Hugo A. Urrutia, and Marianne E. Bronner contributed equally to this work. This work was supported by NIH (NIH 5F31DE027583, NIH 5F31DE031154 and NIH R01DE027568). Graphical Abstract was made using a Biorender platform. AUTHOR CONTRIBUTIONS. AK, HAU, and MEB contributed to the conceptualization, experimentation, and the writing and editing of this paper. AK and HAU performed data collection and analysis, validation, and produced the figures. The authors confirm that they have followed the ethical policies of the journal. CONFLICT OF INTEREST. MEB is a coauthor of the manuscript and an editor of Natural Sciences and was not involved at the handling of the peer-review process of this submission.
Funders:
Funding AgencyGrant Number
NIH Predoctoral Fellowship5F31DE027583
NIHNIH Predoctoral Fellowship5F31DE031154
NIHR01DE027568
Subject Keywords:cell lineage analysis; gonadotropin-releasing hormone neurons; neural crest; olfactory; olfactory ensheathing cells; placode; viral labeling
Issue or Number:3
DOI:10.1002/ntls.20210037
Record Number:CaltechAUTHORS:20220526-391453000
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20220526-391453000
Official Citation:Koontz, A, Urrutia, HA, Bronner, ME. Retroviral lineage analysis reveals dual contribution from ectodermal placodes and neural crest cells to avian olfactory sensory and GnRH neurons. Nat Sci. 2022; 2:e20210037. https://doi.org/10.1002/ntls.20210037
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:114951
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:31 May 2022 22:18
Last Modified:12 Aug 2022 17:41

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