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Protracted neuronal maturation in a long-lived, highly social rodent

Naked mole-rats are a long-lived rodent species (current lifespan >37 years) and an increasingly popular biomedical model. Naked mole-rats exhibit neuroplasticity across their long lifespan. Previous studies have begun to investigate their neurogenic patterns. Here, we test the hypothesis that ne...

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Autores principales: Faykoo-Martinez, Mariela, Collins, Troy, Peragine, Diana, Malik, Manahil, Javed, Fiza, Kolisnyk, Matthew, Ziolkowski, Justine, Jeewa, Imaan, Cheng, Arthur H., Lowden, Christopher, Mascarenhas, Brittany, Cheng, Hai-Ying Mary, Holmes, Melissa M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9477366/
https://www.ncbi.nlm.nih.gov/pubmed/36107951
http://dx.doi.org/10.1371/journal.pone.0273098
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author Faykoo-Martinez, Mariela
Collins, Troy
Peragine, Diana
Malik, Manahil
Javed, Fiza
Kolisnyk, Matthew
Ziolkowski, Justine
Jeewa, Imaan
Cheng, Arthur H.
Lowden, Christopher
Mascarenhas, Brittany
Cheng, Hai-Ying Mary
Holmes, Melissa M.
author_facet Faykoo-Martinez, Mariela
Collins, Troy
Peragine, Diana
Malik, Manahil
Javed, Fiza
Kolisnyk, Matthew
Ziolkowski, Justine
Jeewa, Imaan
Cheng, Arthur H.
Lowden, Christopher
Mascarenhas, Brittany
Cheng, Hai-Ying Mary
Holmes, Melissa M.
author_sort Faykoo-Martinez, Mariela
collection PubMed
description Naked mole-rats are a long-lived rodent species (current lifespan >37 years) and an increasingly popular biomedical model. Naked mole-rats exhibit neuroplasticity across their long lifespan. Previous studies have begun to investigate their neurogenic patterns. Here, we test the hypothesis that neuronal maturation is extended in this long-lived rodent. We characterize cell proliferation and neuronal maturation in established rodent neurogenic regions over 12 months following seven days of consecutive BrdU injection. Given that naked mole-rats are eusocial (high reproductive skew where only a few socially-dominant individuals reproduce), we also looked at proliferation in brain regions relevant to the social-decision making network. Finally, we measured co-expression of EdU (newly-born cells), DCX (immature neuron marker), and NeuN (mature neuron marker) to assess the timeline of neuronal maturation in adult naked mole-rats. This work reaffirms the subventricular zone as the main source of adult cell proliferation and suggests conservation of the rostral migratory stream in this species. Our profiling of socially-relevant brain regions suggests that future work which manipulates environmental context can unveil how newly-born cells integrate into circuitry and facilitate adult neuroplasticity. We also find naked mole-rat neuronal maturation sits at the intersection of rodents and long-lived, non-rodent species: while neurons can mature by 3 weeks (rodent-like), most neurons mature at 5 months and hippocampal neurogenic levels are low (like long-lived species). These data establish a timeline for future investigations of longevity- and socially-related manipulations of naked mole-rat adult neurogenesis.
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spelling pubmed-94773662022-09-16 Protracted neuronal maturation in a long-lived, highly social rodent Faykoo-Martinez, Mariela Collins, Troy Peragine, Diana Malik, Manahil Javed, Fiza Kolisnyk, Matthew Ziolkowski, Justine Jeewa, Imaan Cheng, Arthur H. Lowden, Christopher Mascarenhas, Brittany Cheng, Hai-Ying Mary Holmes, Melissa M. PLoS One Research Article Naked mole-rats are a long-lived rodent species (current lifespan >37 years) and an increasingly popular biomedical model. Naked mole-rats exhibit neuroplasticity across their long lifespan. Previous studies have begun to investigate their neurogenic patterns. Here, we test the hypothesis that neuronal maturation is extended in this long-lived rodent. We characterize cell proliferation and neuronal maturation in established rodent neurogenic regions over 12 months following seven days of consecutive BrdU injection. Given that naked mole-rats are eusocial (high reproductive skew where only a few socially-dominant individuals reproduce), we also looked at proliferation in brain regions relevant to the social-decision making network. Finally, we measured co-expression of EdU (newly-born cells), DCX (immature neuron marker), and NeuN (mature neuron marker) to assess the timeline of neuronal maturation in adult naked mole-rats. This work reaffirms the subventricular zone as the main source of adult cell proliferation and suggests conservation of the rostral migratory stream in this species. Our profiling of socially-relevant brain regions suggests that future work which manipulates environmental context can unveil how newly-born cells integrate into circuitry and facilitate adult neuroplasticity. We also find naked mole-rat neuronal maturation sits at the intersection of rodents and long-lived, non-rodent species: while neurons can mature by 3 weeks (rodent-like), most neurons mature at 5 months and hippocampal neurogenic levels are low (like long-lived species). These data establish a timeline for future investigations of longevity- and socially-related manipulations of naked mole-rat adult neurogenesis. Public Library of Science 2022-09-15 /pmc/articles/PMC9477366/ /pubmed/36107951 http://dx.doi.org/10.1371/journal.pone.0273098 Text en © 2022 Faykoo-Martinez et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Faykoo-Martinez, Mariela
Collins, Troy
Peragine, Diana
Malik, Manahil
Javed, Fiza
Kolisnyk, Matthew
Ziolkowski, Justine
Jeewa, Imaan
Cheng, Arthur H.
Lowden, Christopher
Mascarenhas, Brittany
Cheng, Hai-Ying Mary
Holmes, Melissa M.
Protracted neuronal maturation in a long-lived, highly social rodent
title Protracted neuronal maturation in a long-lived, highly social rodent
title_full Protracted neuronal maturation in a long-lived, highly social rodent
title_fullStr Protracted neuronal maturation in a long-lived, highly social rodent
title_full_unstemmed Protracted neuronal maturation in a long-lived, highly social rodent
title_short Protracted neuronal maturation in a long-lived, highly social rodent
title_sort protracted neuronal maturation in a long-lived, highly social rodent
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9477366/
https://www.ncbi.nlm.nih.gov/pubmed/36107951
http://dx.doi.org/10.1371/journal.pone.0273098
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