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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Main Authors: Mariela Faykoo-Martinez, Troy Collins, Diana Peragine, Manahil Malik, Fiza Javed, Matthew Kolisnyk, Justine Ziolkowski, Imaan Jeewa, Arthur H Cheng, Christopher Lowden, Brittany Mascarenhas, Hai-Ying Mary Cheng, Melissa M Holmes
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2022-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0273098
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author Mariela Faykoo-Martinez
Troy Collins
Diana Peragine
Manahil Malik
Fiza Javed
Matthew Kolisnyk
Justine Ziolkowski
Imaan Jeewa
Arthur H Cheng
Christopher Lowden
Brittany Mascarenhas
Hai-Ying Mary Cheng
Melissa M Holmes
author_facet Mariela Faykoo-Martinez
Troy Collins
Diana Peragine
Manahil Malik
Fiza Javed
Matthew Kolisnyk
Justine Ziolkowski
Imaan Jeewa
Arthur H Cheng
Christopher Lowden
Brittany Mascarenhas
Hai-Ying Mary Cheng
Melissa M Holmes
author_sort Mariela Faykoo-Martinez
collection DOAJ
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 doaj.art-058917493d0d43b69d09e6f8e86fef002022-12-22T04:25:50ZengPublic Library of Science (PLoS)PLoS ONE1932-62032022-01-01179e027309810.1371/journal.pone.0273098Protracted neuronal maturation in a long-lived, highly social rodent.Mariela Faykoo-MartinezTroy CollinsDiana PeragineManahil MalikFiza JavedMatthew KolisnykJustine ZiolkowskiImaan JeewaArthur H ChengChristopher LowdenBrittany MascarenhasHai-Ying Mary ChengMelissa M HolmesNaked 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.https://doi.org/10.1371/journal.pone.0273098
spellingShingle Mariela Faykoo-Martinez
Troy Collins
Diana Peragine
Manahil Malik
Fiza Javed
Matthew Kolisnyk
Justine Ziolkowski
Imaan Jeewa
Arthur H Cheng
Christopher Lowden
Brittany Mascarenhas
Hai-Ying Mary Cheng
Melissa M Holmes
Protracted neuronal maturation in a long-lived, highly social rodent.
PLoS ONE
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
url https://doi.org/10.1371/journal.pone.0273098
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