Coordinated neuron-glia regeneration through Notch signaling in planarians.

Some animals can regenerate large missing regions of their nervous system, requiring mechanisms to restore the pattern, numbers, and wiring of diverse neuron classes. Because injuries are unpredictable, regeneration must be accomplished from an unlimited number of starting points. Coordinated regene...

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Main Authors: M Lucila Scimone, Bryanna Isela-Inez Canales, Patrick Aoude, Kutay D Atabay, Peter W Reddien
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-01-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1011577
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author M Lucila Scimone
Bryanna Isela-Inez Canales
Patrick Aoude
Kutay D Atabay
Peter W Reddien
author_facet M Lucila Scimone
Bryanna Isela-Inez Canales
Patrick Aoude
Kutay D Atabay
Peter W Reddien
author_sort M Lucila Scimone
collection DOAJ
description Some animals can regenerate large missing regions of their nervous system, requiring mechanisms to restore the pattern, numbers, and wiring of diverse neuron classes. Because injuries are unpredictable, regeneration must be accomplished from an unlimited number of starting points. Coordinated regeneration of neuron-glia architecture is thus a major challenge and remains poorly understood. In planarians, neurons and glia are regenerated from distinct progenitors. We found that planarians first regenerate neurons expressing a Delta-encoding gene, delta-2, at key positions in the central and peripheral nervous systems. Planarian glia are specified later from dispersed Notch-1-expressing mesoderm-like phagocytic progenitors. Inhibition of delta-2 or notch-1 severely reduced glia in planarians, but did not affect the specification of other phagocytic cell types. Loss of several delta-2-expressing neuron classes prevented differentiation of the glia associated with them, whereas transplantation of delta-2-expressing photoreceptor neurons was sufficient for glia formation at an ectopic location. Our results suggest a model in which patterned delta-2-expressing neurons instruct phagocytic progenitors to locally differentiate into glia, presenting a mechanism for coordinated regeneration of numbers and pattern of cell types.
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institution Kabale University
issn 1553-7390
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language English
publishDate 2025-01-01
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spelling doaj-art-af8890e9d084485b9976924f510c8ab12025-02-12T05:30:47ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042025-01-01211e101157710.1371/journal.pgen.1011577Coordinated neuron-glia regeneration through Notch signaling in planarians.M Lucila ScimoneBryanna Isela-Inez CanalesPatrick AoudeKutay D AtabayPeter W ReddienSome animals can regenerate large missing regions of their nervous system, requiring mechanisms to restore the pattern, numbers, and wiring of diverse neuron classes. Because injuries are unpredictable, regeneration must be accomplished from an unlimited number of starting points. Coordinated regeneration of neuron-glia architecture is thus a major challenge and remains poorly understood. In planarians, neurons and glia are regenerated from distinct progenitors. We found that planarians first regenerate neurons expressing a Delta-encoding gene, delta-2, at key positions in the central and peripheral nervous systems. Planarian glia are specified later from dispersed Notch-1-expressing mesoderm-like phagocytic progenitors. Inhibition of delta-2 or notch-1 severely reduced glia in planarians, but did not affect the specification of other phagocytic cell types. Loss of several delta-2-expressing neuron classes prevented differentiation of the glia associated with them, whereas transplantation of delta-2-expressing photoreceptor neurons was sufficient for glia formation at an ectopic location. Our results suggest a model in which patterned delta-2-expressing neurons instruct phagocytic progenitors to locally differentiate into glia, presenting a mechanism for coordinated regeneration of numbers and pattern of cell types.https://doi.org/10.1371/journal.pgen.1011577
spellingShingle M Lucila Scimone
Bryanna Isela-Inez Canales
Patrick Aoude
Kutay D Atabay
Peter W Reddien
Coordinated neuron-glia regeneration through Notch signaling in planarians.
PLoS Genetics
title Coordinated neuron-glia regeneration through Notch signaling in planarians.
title_full Coordinated neuron-glia regeneration through Notch signaling in planarians.
title_fullStr Coordinated neuron-glia regeneration through Notch signaling in planarians.
title_full_unstemmed Coordinated neuron-glia regeneration through Notch signaling in planarians.
title_short Coordinated neuron-glia regeneration through Notch signaling in planarians.
title_sort coordinated neuron glia regeneration through notch signaling in planarians
url https://doi.org/10.1371/journal.pgen.1011577
work_keys_str_mv AT mlucilascimone coordinatedneurongliaregenerationthroughnotchsignalinginplanarians
AT bryannaiselainezcanales coordinatedneurongliaregenerationthroughnotchsignalinginplanarians
AT patrickaoude coordinatedneurongliaregenerationthroughnotchsignalinginplanarians
AT kutaydatabay coordinatedneurongliaregenerationthroughnotchsignalinginplanarians
AT peterwreddien coordinatedneurongliaregenerationthroughnotchsignalinginplanarians