The transcription factors Tfeb and Tfe3 are required for survival and embryonic development of pancreas and liver in zebrafish.

The transcription factors TFEB and TFE3 modulate expression of lysosomal, autophagic, and metabolic genes to restore energy and cellular homeostasis in response to a variety of stress conditions. Since their role during vertebrate development is less characterized, we used CRISPR/Cas9 to deplete tfe...

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Main Authors: Alberto Rissone, Martina La Spina, Erica Bresciani, Zulfeqhar A Syed, Christian A Combs, Martha Kirby, Abdel Elkahloun, Vicky Chen, Raman Sood, Shawn M Burgess, Rosa Puertollano
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-06-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1011754
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author Alberto Rissone
Martina La Spina
Erica Bresciani
Zulfeqhar A Syed
Christian A Combs
Martha Kirby
Abdel Elkahloun
Vicky Chen
Raman Sood
Shawn M Burgess
Rosa Puertollano
author_facet Alberto Rissone
Martina La Spina
Erica Bresciani
Zulfeqhar A Syed
Christian A Combs
Martha Kirby
Abdel Elkahloun
Vicky Chen
Raman Sood
Shawn M Burgess
Rosa Puertollano
author_sort Alberto Rissone
collection DOAJ
description The transcription factors TFEB and TFE3 modulate expression of lysosomal, autophagic, and metabolic genes to restore energy and cellular homeostasis in response to a variety of stress conditions. Since their role during vertebrate development is less characterized, we used CRISPR/Cas9 to deplete tfeb, tfe3a, and tfe3b in zebrafish. The simultaneous lack of these genes compromised embryo survival during early development, with an almost complete lethality of the larvae by 8-10 dpf. The knockout animals showed apoptosis in brain and retina and alterations in pancreas, liver, and gut. Exocrine pancreas presented the most severe defects, with accumulation of abnormal zymogen granules leading to acinar atrophy in embryos and pancreatitis-like phenotypes in adults; likely due to a block of the autophagy machinery implicated in removal of damaged granules. Knockout animals displayed increased susceptibility to oxidative and heat-shock stress. Our work reveals an essential role of Tfeb and Tfe3 in maintaining cellular and tissue homeostasis during development.
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institution Kabale University
issn 1553-7390
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publishDate 2025-06-01
publisher Public Library of Science (PLoS)
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series PLoS Genetics
spelling doaj-art-8fb95e79e6444f94beffa09e115828532025-08-20T03:28:51ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042025-06-01216e101175410.1371/journal.pgen.1011754The transcription factors Tfeb and Tfe3 are required for survival and embryonic development of pancreas and liver in zebrafish.Alberto RissoneMartina La SpinaErica BrescianiZulfeqhar A SyedChristian A CombsMartha KirbyAbdel ElkahlounVicky ChenRaman SoodShawn M BurgessRosa PuertollanoThe transcription factors TFEB and TFE3 modulate expression of lysosomal, autophagic, and metabolic genes to restore energy and cellular homeostasis in response to a variety of stress conditions. Since their role during vertebrate development is less characterized, we used CRISPR/Cas9 to deplete tfeb, tfe3a, and tfe3b in zebrafish. The simultaneous lack of these genes compromised embryo survival during early development, with an almost complete lethality of the larvae by 8-10 dpf. The knockout animals showed apoptosis in brain and retina and alterations in pancreas, liver, and gut. Exocrine pancreas presented the most severe defects, with accumulation of abnormal zymogen granules leading to acinar atrophy in embryos and pancreatitis-like phenotypes in adults; likely due to a block of the autophagy machinery implicated in removal of damaged granules. Knockout animals displayed increased susceptibility to oxidative and heat-shock stress. Our work reveals an essential role of Tfeb and Tfe3 in maintaining cellular and tissue homeostasis during development.https://doi.org/10.1371/journal.pgen.1011754
spellingShingle Alberto Rissone
Martina La Spina
Erica Bresciani
Zulfeqhar A Syed
Christian A Combs
Martha Kirby
Abdel Elkahloun
Vicky Chen
Raman Sood
Shawn M Burgess
Rosa Puertollano
The transcription factors Tfeb and Tfe3 are required for survival and embryonic development of pancreas and liver in zebrafish.
PLoS Genetics
title The transcription factors Tfeb and Tfe3 are required for survival and embryonic development of pancreas and liver in zebrafish.
title_full The transcription factors Tfeb and Tfe3 are required for survival and embryonic development of pancreas and liver in zebrafish.
title_fullStr The transcription factors Tfeb and Tfe3 are required for survival and embryonic development of pancreas and liver in zebrafish.
title_full_unstemmed The transcription factors Tfeb and Tfe3 are required for survival and embryonic development of pancreas and liver in zebrafish.
title_short The transcription factors Tfeb and Tfe3 are required for survival and embryonic development of pancreas and liver in zebrafish.
title_sort transcription factors tfeb and tfe3 are required for survival and embryonic development of pancreas and liver in zebrafish
url https://doi.org/10.1371/journal.pgen.1011754
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