The transcription factor Jun is necessary for optic nerve regeneration in larval zebrafish.

Damage to the axons of the adult mammalian central nervous system (CNS) from traumatic injury or neurodegenerative diseases often results in permanent loss of function due to failure of axons to regenerate. Zebrafish, however, can express regeneration-associated genes to revert CNS neurons to a grow...

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Main Authors: Sarah C Sarich, Virinchipuram S Sreevidya, Ava J Udvadia, Kurt R Svoboda, Jennifer H Gutzman
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0313534
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author Sarah C Sarich
Virinchipuram S Sreevidya
Ava J Udvadia
Kurt R Svoboda
Jennifer H Gutzman
author_facet Sarah C Sarich
Virinchipuram S Sreevidya
Ava J Udvadia
Kurt R Svoboda
Jennifer H Gutzman
author_sort Sarah C Sarich
collection DOAJ
description Damage to the axons of the adult mammalian central nervous system (CNS) from traumatic injury or neurodegenerative diseases often results in permanent loss of function due to failure of axons to regenerate. Zebrafish, however, can express regeneration-associated genes to revert CNS neurons to a growth-competent state and regenerate damaged axons to functionality. An established model for CNS axon regeneration is optic nerve injury in zebrafish, where it was previously shown that thousands of genes are temporally expressed during the regeneration time course. It is likely that hubs of key transcription factors, rather than individual factors regulate the temporal clusters of expression after injury to facilitate cell survival, regrowth, and synaptic targeting in the brain. One transcription factor of interest in orchestrating CNS axon regeneration is jun. However, it remains unclear if CNS regeneration can progress without Jun. To test this, a transgenic zebrafish line was developed to express a heat-shock inducible dominant negative Jun. Induction of dominant negative Jun downregulated endogenous jun expression and larvae with functional jun knockdown demonstrated impaired retinal ganglion cell axon regeneration. Analysis of select putative Jun target genes, previously shown to be upregulated in adult zebrafish optic nerve regeneration, demonstrated that with functional Jun knockdown, atf3 and ascl1a were significantly downregulated, and sox11a was upregulated at distinct time points. These results position jun as a key regulator for successful optic nerve regeneration, further distinguish the regeneration program from development, and advance our knowledge for the formation of future therapies to treat CNS damage.
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spelling doaj-art-9363ecdefa1643dfb4e39c110fa784732025-08-20T03:47:28ZengPublic Library of Science (PLoS)PLoS ONE1932-62032025-01-01203e031353410.1371/journal.pone.0313534The transcription factor Jun is necessary for optic nerve regeneration in larval zebrafish.Sarah C SarichVirinchipuram S SreevidyaAva J UdvadiaKurt R SvobodaJennifer H GutzmanDamage to the axons of the adult mammalian central nervous system (CNS) from traumatic injury or neurodegenerative diseases often results in permanent loss of function due to failure of axons to regenerate. Zebrafish, however, can express regeneration-associated genes to revert CNS neurons to a growth-competent state and regenerate damaged axons to functionality. An established model for CNS axon regeneration is optic nerve injury in zebrafish, where it was previously shown that thousands of genes are temporally expressed during the regeneration time course. It is likely that hubs of key transcription factors, rather than individual factors regulate the temporal clusters of expression after injury to facilitate cell survival, regrowth, and synaptic targeting in the brain. One transcription factor of interest in orchestrating CNS axon regeneration is jun. However, it remains unclear if CNS regeneration can progress without Jun. To test this, a transgenic zebrafish line was developed to express a heat-shock inducible dominant negative Jun. Induction of dominant negative Jun downregulated endogenous jun expression and larvae with functional jun knockdown demonstrated impaired retinal ganglion cell axon regeneration. Analysis of select putative Jun target genes, previously shown to be upregulated in adult zebrafish optic nerve regeneration, demonstrated that with functional Jun knockdown, atf3 and ascl1a were significantly downregulated, and sox11a was upregulated at distinct time points. These results position jun as a key regulator for successful optic nerve regeneration, further distinguish the regeneration program from development, and advance our knowledge for the formation of future therapies to treat CNS damage.https://doi.org/10.1371/journal.pone.0313534
spellingShingle Sarah C Sarich
Virinchipuram S Sreevidya
Ava J Udvadia
Kurt R Svoboda
Jennifer H Gutzman
The transcription factor Jun is necessary for optic nerve regeneration in larval zebrafish.
PLoS ONE
title The transcription factor Jun is necessary for optic nerve regeneration in larval zebrafish.
title_full The transcription factor Jun is necessary for optic nerve regeneration in larval zebrafish.
title_fullStr The transcription factor Jun is necessary for optic nerve regeneration in larval zebrafish.
title_full_unstemmed The transcription factor Jun is necessary for optic nerve regeneration in larval zebrafish.
title_short The transcription factor Jun is necessary for optic nerve regeneration in larval zebrafish.
title_sort transcription factor jun is necessary for optic nerve regeneration in larval zebrafish
url https://doi.org/10.1371/journal.pone.0313534
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