Retroviral lineage analysis reveals dual contribution from ectodermal placodes and neural crest cells to avian olfactory sensory and GnRH neurons
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...
| Main Authors: | , , |
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| Format: | Article |
| Language: | English |
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Wiley-VCH
2022-07-01
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| Series: | Natural Sciences |
| Subjects: | |
| Online Access: | https://doi.org/10.1002/ntls.20210037 |
| _version_ | 1818532196210704384 |
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| author | Alison Koontz Hugo A. Urrutia Marianne E. Bronner |
| author_facet | Alison Koontz Hugo A. Urrutia Marianne E. Bronner |
| author_sort | Alison Koontz |
| collection | DOAJ |
| description | 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. Key Points Modified retroviruses were used to permanently label progenitor cells of the neural crest and olfactory placode for the long‐term lineage analysis of olfactory cells. Both neural crest cells and olfactory placode cells contribute to olfactory neurons and supporting cells of the olfactory epithelium. The gonadotropin‐releasing hormone neurons that arise in the nose and migrate toward the hypothalamus during development also receive contributions from both neural crest and placode cells. |
| first_indexed | 2024-12-11T17:42:20Z |
| format | Article |
| id | doaj.art-dcef0d2d0f854362bc97f5ebc0efaf7b |
| institution | Directory Open Access Journal |
| issn | 2698-6248 |
| language | English |
| last_indexed | 2024-12-11T17:42:20Z |
| publishDate | 2022-07-01 |
| publisher | Wiley-VCH |
| record_format | Article |
| series | Natural Sciences |
| spelling | doaj.art-dcef0d2d0f854362bc97f5ebc0efaf7b2022-12-22T00:56:29ZengWiley-VCHNatural Sciences2698-62482022-07-0123n/an/a10.1002/ntls.20210037Retroviral lineage analysis reveals dual contribution from ectodermal placodes and neural crest cells to avian olfactory sensory and GnRH neuronsAlison Koontz0Hugo A. Urrutia1Marianne E. Bronner2Division of Biology and Biological Engineering California Institute of Technology Pasadena California USADivision of Biology and Biological Engineering California Institute of Technology Pasadena California USADivision of Biology and Biological Engineering California Institute of Technology Pasadena California USAAbstract 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. Key Points Modified retroviruses were used to permanently label progenitor cells of the neural crest and olfactory placode for the long‐term lineage analysis of olfactory cells. Both neural crest cells and olfactory placode cells contribute to olfactory neurons and supporting cells of the olfactory epithelium. The gonadotropin‐releasing hormone neurons that arise in the nose and migrate toward the hypothalamus during development also receive contributions from both neural crest and placode cells.https://doi.org/10.1002/ntls.20210037cell lineage analysisgonadotropin‐releasing hormone neuronsneural crestolfactoryolfactory ensheathing cellsplacode |
| spellingShingle | Alison Koontz Hugo A. Urrutia Marianne E. Bronner Retroviral lineage analysis reveals dual contribution from ectodermal placodes and neural crest cells to avian olfactory sensory and GnRH neurons Natural Sciences cell lineage analysis gonadotropin‐releasing hormone neurons neural crest olfactory olfactory ensheathing cells placode |
| title | Retroviral lineage analysis reveals dual contribution from ectodermal placodes and neural crest cells to avian olfactory sensory and GnRH neurons |
| title_full | Retroviral lineage analysis reveals dual contribution from ectodermal placodes and neural crest cells to avian olfactory sensory and GnRH neurons |
| title_fullStr | Retroviral lineage analysis reveals dual contribution from ectodermal placodes and neural crest cells to avian olfactory sensory and GnRH neurons |
| title_full_unstemmed | Retroviral lineage analysis reveals dual contribution from ectodermal placodes and neural crest cells to avian olfactory sensory and GnRH neurons |
| title_short | Retroviral lineage analysis reveals dual contribution from ectodermal placodes and neural crest cells to avian olfactory sensory and GnRH neurons |
| title_sort | retroviral lineage analysis reveals dual contribution from ectodermal placodes and neural crest cells to avian olfactory sensory and gnrh neurons |
| topic | cell lineage analysis gonadotropin‐releasing hormone neurons neural crest olfactory olfactory ensheathing cells placode |
| url | https://doi.org/10.1002/ntls.20210037 |
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