Impact of ATF6 deletion on the embryonic brain development

Summary: Although the unfolded protein response (UPR) is activated during brain development, its roles remain unclear. Here, we report that deletion of activating transcription factor 6 (ATF6), consisting of ATF6α and ATF6β, in the developing brain caused microcephaly and neonatal death in mice. Ana...

Full description

Saved in:
Bibliographic Details
Main Authors: Loc Dinh Nguyen, Ly Huong Nguyen, Dat Xuan Dao, Tsuyoshi Hattori, Mika Takarada-Iemata, Hiroshi Ishii, Takashi Tamatani, Hiroshi Kawasaki, Yohei Shinmyo, Kenta Onoue, Shigenobu Yonemura, Jun Zhang, Masato Miyake, Seiichi Oyadomari, Kazutoshi Mori, Osamu Hori
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:iScience
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2589004225008302
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849725294553858048
author Loc Dinh Nguyen
Ly Huong Nguyen
Dat Xuan Dao
Tsuyoshi Hattori
Mika Takarada-Iemata
Hiroshi Ishii
Takashi Tamatani
Hiroshi Kawasaki
Yohei Shinmyo
Kenta Onoue
Shigenobu Yonemura
Jun Zhang
Masato Miyake
Seiichi Oyadomari
Kazutoshi Mori
Osamu Hori
author_facet Loc Dinh Nguyen
Ly Huong Nguyen
Dat Xuan Dao
Tsuyoshi Hattori
Mika Takarada-Iemata
Hiroshi Ishii
Takashi Tamatani
Hiroshi Kawasaki
Yohei Shinmyo
Kenta Onoue
Shigenobu Yonemura
Jun Zhang
Masato Miyake
Seiichi Oyadomari
Kazutoshi Mori
Osamu Hori
author_sort Loc Dinh Nguyen
collection DOAJ
description Summary: Although the unfolded protein response (UPR) is activated during brain development, its roles remain unclear. Here, we report that deletion of activating transcription factor 6 (ATF6), consisting of ATF6α and ATF6β, in the developing brain caused microcephaly and neonatal death in mice. Analysis of Atf6a/Atf6b double conditional knockout (dcKO) brains revealed diverse neuronal phenotypes, such as reduced neurogenesis, increased cell death, impaired cortical layer formation, and axon projection defects. Furthermore, hypervasculature, glial defects, and neuroinflammation were observed in dcKO brains. Notably, hypervasculature was detected at E14.5, when endoplasmic reticulum (ER) stress was morphologically unclear, but the UPR was activated to a greater extent in dcKO brains. Expression profiles revealed reduced levels of molecular chaperones in the ER and enhanced levels of PERK- and IRE1-downstream molecules, including VEGFA, in dcKO brains. Administration of a chemical chaperone 4-phenylbutyric acid partially rescued dcKO mice, suggesting roles of ATF6 for improving proteostasis and for coordinating the UPR.
format Article
id doaj-art-9549806bfcc84fc08019eedac825fa39
institution DOAJ
issn 2589-0042
language English
publishDate 2025-06-01
publisher Elsevier
record_format Article
series iScience
spelling doaj-art-9549806bfcc84fc08019eedac825fa392025-08-20T03:10:31ZengElsevieriScience2589-00422025-06-0128611256910.1016/j.isci.2025.112569Impact of ATF6 deletion on the embryonic brain developmentLoc Dinh Nguyen0Ly Huong Nguyen1Dat Xuan Dao2Tsuyoshi Hattori3Mika Takarada-Iemata4Hiroshi Ishii5Takashi Tamatani6Hiroshi Kawasaki7Yohei Shinmyo8Kenta Onoue9Shigenobu Yonemura10Jun Zhang11Masato Miyake12Seiichi Oyadomari13Kazutoshi Mori14Osamu Hori15Department of Neuroanatomy, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Ishikawa, JapanDepartment of Neuroanatomy, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Ishikawa, JapanDepartment of Neuroanatomy, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Ishikawa, JapanDepartment of Neuroanatomy, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Ishikawa, JapanDepartment of Neuroanatomy, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Ishikawa, JapanDepartment of Neuroanatomy, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Ishikawa, JapanDepartment of Neuroanatomy, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Ishikawa, JapanDepartment of Medical Neuroscience, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Ishikawa, JapanDepartment of Neurophysiology, Hamamatsu University School of Medicine, Hamamatsu, Shizuoka, JapanLaboratory for Ultrastructural Research, RIKEN Center for Biosystems Dynamics Research, Kobe, Hyogo, JapanLaboratory for Ultrastructural Research, RIKEN Center for Biosystems Dynamics Research, Kobe, Hyogo, Japan; Department of Cell Biology, Tokushima University Graduate School of Medicine, Tokushima, JapanDivision of Molecular Biology, Institute of Advanced Medical Sciences, Tokushima University, Tokushima, JapanDivision of Molecular Biology, Institute of Advanced Medical Sciences, Tokushima University, Tokushima, JapanDivision of Molecular Biology, Institute of Advanced Medical Sciences, Tokushima University, Tokushima, JapanKyoto University Institute for Advanced Study, Kyoto, JapanDepartment of Neuroanatomy, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Ishikawa, Japan; Corresponding authorSummary: Although the unfolded protein response (UPR) is activated during brain development, its roles remain unclear. Here, we report that deletion of activating transcription factor 6 (ATF6), consisting of ATF6α and ATF6β, in the developing brain caused microcephaly and neonatal death in mice. Analysis of Atf6a/Atf6b double conditional knockout (dcKO) brains revealed diverse neuronal phenotypes, such as reduced neurogenesis, increased cell death, impaired cortical layer formation, and axon projection defects. Furthermore, hypervasculature, glial defects, and neuroinflammation were observed in dcKO brains. Notably, hypervasculature was detected at E14.5, when endoplasmic reticulum (ER) stress was morphologically unclear, but the UPR was activated to a greater extent in dcKO brains. Expression profiles revealed reduced levels of molecular chaperones in the ER and enhanced levels of PERK- and IRE1-downstream molecules, including VEGFA, in dcKO brains. Administration of a chemical chaperone 4-phenylbutyric acid partially rescued dcKO mice, suggesting roles of ATF6 for improving proteostasis and for coordinating the UPR.http://www.sciencedirect.com/science/article/pii/S2589004225008302NeuroscienceCell biologyDevelopmental biology
spellingShingle Loc Dinh Nguyen
Ly Huong Nguyen
Dat Xuan Dao
Tsuyoshi Hattori
Mika Takarada-Iemata
Hiroshi Ishii
Takashi Tamatani
Hiroshi Kawasaki
Yohei Shinmyo
Kenta Onoue
Shigenobu Yonemura
Jun Zhang
Masato Miyake
Seiichi Oyadomari
Kazutoshi Mori
Osamu Hori
Impact of ATF6 deletion on the embryonic brain development
iScience
Neuroscience
Cell biology
Developmental biology
title Impact of ATF6 deletion on the embryonic brain development
title_full Impact of ATF6 deletion on the embryonic brain development
title_fullStr Impact of ATF6 deletion on the embryonic brain development
title_full_unstemmed Impact of ATF6 deletion on the embryonic brain development
title_short Impact of ATF6 deletion on the embryonic brain development
title_sort impact of atf6 deletion on the embryonic brain development
topic Neuroscience
Cell biology
Developmental biology
url http://www.sciencedirect.com/science/article/pii/S2589004225008302
work_keys_str_mv AT locdinhnguyen impactofatf6deletionontheembryonicbraindevelopment
AT lyhuongnguyen impactofatf6deletionontheembryonicbraindevelopment
AT datxuandao impactofatf6deletionontheembryonicbraindevelopment
AT tsuyoshihattori impactofatf6deletionontheembryonicbraindevelopment
AT mikatakaradaiemata impactofatf6deletionontheembryonicbraindevelopment
AT hiroshiishii impactofatf6deletionontheembryonicbraindevelopment
AT takashitamatani impactofatf6deletionontheembryonicbraindevelopment
AT hiroshikawasaki impactofatf6deletionontheembryonicbraindevelopment
AT yoheishinmyo impactofatf6deletionontheembryonicbraindevelopment
AT kentaonoue impactofatf6deletionontheembryonicbraindevelopment
AT shigenobuyonemura impactofatf6deletionontheembryonicbraindevelopment
AT junzhang impactofatf6deletionontheembryonicbraindevelopment
AT masatomiyake impactofatf6deletionontheembryonicbraindevelopment
AT seiichioyadomari impactofatf6deletionontheembryonicbraindevelopment
AT kazutoshimori impactofatf6deletionontheembryonicbraindevelopment
AT osamuhori impactofatf6deletionontheembryonicbraindevelopment