Analysis of β‐Catenin Signalling Activity Suggests Differential Regulation of Ontogenetically Distinct Dentate Granule Neuron Populations

ABSTRACT In mammals, the dentate gyrus of the hippocampus is one of the few regions where neurogenesis continues throughout life. As a result, the dentate gyrus harbours neurons of ontogenetically different origin. Notably, ontogenetically different dentate granule neurons (DGNs) are morphologically...

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Published inInternational journal of developmental neuroscience Vol. 85; no. 1; pp. e70009 - n/a
Main Authors Billmann, Charlotte, Schäffner, Iris, Heppt, Jana, Lie, D. Chichung
Format Journal Article
LanguageEnglish
Published United States John Wiley and Sons Inc 01.02.2025
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ISSN0736-5748
1873-474X
1873-474X
DOI10.1002/jdn.70009

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Abstract ABSTRACT In mammals, the dentate gyrus of the hippocampus is one of the few regions where neurogenesis continues throughout life. As a result, the dentate gyrus harbours neurons of ontogenetically different origin. Notably, ontogenetically different dentate granule neurons (DGNs) are morphologically distinct and fulfil specialized functions in hippocampal information processing and plasticity. Development of adult‐born DGNs is tightly controlled by signals released by the complex cellular environment of the adult dentate gyrus. In mice, an adult‐like cytoarchitecture of the dentate gyrus is observed only after postnatal Week 2. The question therefore arises when the signalling environment controlling adult neurogenesis is established and whether development of ontogenetically distinct DGNs is subject to the same regulatory pathways. Here, we analyse BATGAL reporter mice to determine the temporal development of β‐catenin‐signalling activity in the murine DGN lineage. We show that the β‐catenin‐signalling pattern, which is essential for precise dendritogenesis and neuronal maturation in adulthood, emerges only around 2 weeks after birth and continues to be refined over the next weeks. These results indicate that the signalling environment controlling adult neurogenesis is only gradually established and suggest that the development of ontogenetically distinct DGNs is controlled by different mechanisms. Wnt/β‐catenin signalling controls neurogenesis in the dentate gyrus of adult mice. This study describes that the adult pattern of Wnt/β‐catenin signalling in the hippocampal neurogenic lineage is progressively established over the first postnatal weeks.
AbstractList In mammals, the dentate gyrus of the hippocampus is one of the few regions where neurogenesis continues throughout life. As a result, the dentate gyrus harbours neurons of ontogenetically different origin. Notably, ontogenetically different dentate granule neurons (DGNs) are morphologically distinct and fulfil specialized functions in hippocampal information processing and plasticity. Development of adult‐born DGNs is tightly controlled by signals released by the complex cellular environment of the adult dentate gyrus. In mice, an adult‐like cytoarchitecture of the dentate gyrus is observed only after postnatal Week 2. The question therefore arises when the signalling environment controlling adult neurogenesis is established and whether development of ontogenetically distinct DGNs is subject to the same regulatory pathways. Here, we analyse BATGAL reporter mice to determine the temporal development of β‐catenin‐signalling activity in the murine DGN lineage. We show that the β‐catenin‐signalling pattern, which is essential for precise dendritogenesis and neuronal maturation in adulthood, emerges only around 2 weeks after birth and continues to be refined over the next weeks. These results indicate that the signalling environment controlling adult neurogenesis is only gradually established and suggest that the development of ontogenetically distinct DGNs is controlled by different mechanisms. Wnt/β‐catenin signalling controls neurogenesis in the dentate gyrus of adult mice. This study describes that the adult pattern of Wnt/β‐catenin signalling in the hippocampal neurogenic lineage is progressively established over the first postnatal weeks.
ABSTRACT In mammals, the dentate gyrus of the hippocampus is one of the few regions where neurogenesis continues throughout life. As a result, the dentate gyrus harbours neurons of ontogenetically different origin. Notably, ontogenetically different dentate granule neurons (DGNs) are morphologically distinct and fulfil specialized functions in hippocampal information processing and plasticity. Development of adult‐born DGNs is tightly controlled by signals released by the complex cellular environment of the adult dentate gyrus. In mice, an adult‐like cytoarchitecture of the dentate gyrus is observed only after postnatal Week 2. The question therefore arises when the signalling environment controlling adult neurogenesis is established and whether development of ontogenetically distinct DGNs is subject to the same regulatory pathways. Here, we analyse BATGAL reporter mice to determine the temporal development of β‐catenin‐signalling activity in the murine DGN lineage. We show that the β‐catenin‐signalling pattern, which is essential for precise dendritogenesis and neuronal maturation in adulthood, emerges only around 2 weeks after birth and continues to be refined over the next weeks. These results indicate that the signalling environment controlling adult neurogenesis is only gradually established and suggest that the development of ontogenetically distinct DGNs is controlled by different mechanisms. Wnt/β‐catenin signalling controls neurogenesis in the dentate gyrus of adult mice. This study describes that the adult pattern of Wnt/β‐catenin signalling in the hippocampal neurogenic lineage is progressively established over the first postnatal weeks.
In mammals, the dentate gyrus of the hippocampus is one of the few regions where neurogenesis continues throughout life. As a result, the dentate gyrus harbours neurons of ontogenetically different origin. Notably, ontogenetically different dentate granule neurons (DGNs) are morphologically distinct and fulfil specialized functions in hippocampal information processing and plasticity. Development of adult-born DGNs is tightly controlled by signals released by the complex cellular environment of the adult dentate gyrus. In mice, an adult-like cytoarchitecture of the dentate gyrus is observed only after postnatal Week 2. The question therefore arises when the signalling environment controlling adult neurogenesis is established and whether development of ontogenetically distinct DGNs is subject to the same regulatory pathways. Here, we analyse BATGAL reporter mice to determine the temporal development of β-catenin-signalling activity in the murine DGN lineage. We show that the β-catenin-signalling pattern, which is essential for precise dendritogenesis and neuronal maturation in adulthood, emerges only around 2 weeks after birth and continues to be refined over the next weeks. These results indicate that the signalling environment controlling adult neurogenesis is only gradually established and suggest that the development of ontogenetically distinct DGNs is controlled by different mechanisms.In mammals, the dentate gyrus of the hippocampus is one of the few regions where neurogenesis continues throughout life. As a result, the dentate gyrus harbours neurons of ontogenetically different origin. Notably, ontogenetically different dentate granule neurons (DGNs) are morphologically distinct and fulfil specialized functions in hippocampal information processing and plasticity. Development of adult-born DGNs is tightly controlled by signals released by the complex cellular environment of the adult dentate gyrus. In mice, an adult-like cytoarchitecture of the dentate gyrus is observed only after postnatal Week 2. The question therefore arises when the signalling environment controlling adult neurogenesis is established and whether development of ontogenetically distinct DGNs is subject to the same regulatory pathways. Here, we analyse BATGAL reporter mice to determine the temporal development of β-catenin-signalling activity in the murine DGN lineage. We show that the β-catenin-signalling pattern, which is essential for precise dendritogenesis and neuronal maturation in adulthood, emerges only around 2 weeks after birth and continues to be refined over the next weeks. These results indicate that the signalling environment controlling adult neurogenesis is only gradually established and suggest that the development of ontogenetically distinct DGNs is controlled by different mechanisms.
In mammals, the dentate gyrus of the hippocampus is one of the few regions where neurogenesis continues throughout life. As a result, the dentate gyrus harbours neurons of ontogenetically different origin. Notably, ontogenetically different dentate granule neurons (DGNs) are morphologically distinct and fulfil specialized functions in hippocampal information processing and plasticity. Development of adult‐born DGNs is tightly controlled by signals released by the complex cellular environment of the adult dentate gyrus. In mice, an adult‐like cytoarchitecture of the dentate gyrus is observed only after postnatal Week 2. The question therefore arises when the signalling environment controlling adult neurogenesis is established and whether development of ontogenetically distinct DGNs is subject to the same regulatory pathways. Here, we analyse BATGAL reporter mice to determine the temporal development of β‐catenin‐signalling activity in the murine DGN lineage. We show that the β‐catenin‐signalling pattern, which is essential for precise dendritogenesis and neuronal maturation in adulthood, emerges only around 2 weeks after birth and continues to be refined over the next weeks. These results indicate that the signalling environment controlling adult neurogenesis is only gradually established and suggest that the development of ontogenetically distinct DGNs is controlled by different mechanisms.
Author Schäffner, Iris
Lie, D. Chichung
Heppt, Jana
Billmann, Charlotte
AuthorAffiliation 1 Institute for Anatomy Friedrich‐Alexander Universität Erlangen‐Nürnberg Erlangen Germany
2 Institute for Biochemistry Friedrich‐Alexander Universität Erlangen‐Nürnberg Erlangen Germany
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Issue 1
Keywords neurogenesis
dentate gyrus
niche
β‐catenin signalling
Language English
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2025 The Author(s). International Journal of Developmental Neuroscience published by Wiley Periodicals LLC on behalf of International Society for Developmental Neuroscience.
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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Notes This work was supported by the Deutsche Forschungsgemeinschaft (LI 858/9‐2, LI 858/11‐1 and 270949263/DFG GRK2162/1).
Charlotte Billmann and Iris Schäffner contributed equally.
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Funding: This work was supported by the Deutsche Forschungsgemeinschaft (LI 858/9‐2, LI 858/11‐1 and 270949263/DFG GRK2162/1).
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Snippet ABSTRACT In mammals, the dentate gyrus of the hippocampus is one of the few regions where neurogenesis continues throughout life. As a result, the dentate...
In mammals, the dentate gyrus of the hippocampus is one of the few regions where neurogenesis continues throughout life. As a result, the dentate gyrus...
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StartPage e70009
SubjectTerms Animals
Animals, Newborn
beta Catenin - genetics
beta Catenin - metabolism
dentate gyrus
Dentate Gyrus - cytology
Dentate Gyrus - growth & development
Dentate Gyrus - metabolism
Gene Expression Regulation, Developmental - genetics
Gene Expression Regulation, Developmental - physiology
Mice
Mice, Inbred C57BL
Mice, Transgenic
neurogenesis
Neurogenesis - physiology
Neurons - classification
Neurons - cytology
Neurons - metabolism
Neurons - physiology
niche
Signal Transduction - physiology
β‐catenin signalling
Title Analysis of β‐Catenin Signalling Activity Suggests Differential Regulation of Ontogenetically Distinct Dentate Granule Neuron Populations
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fjdn.70009
https://www.ncbi.nlm.nih.gov/pubmed/39964247
https://www.proquest.com/docview/3168025350
https://pubmed.ncbi.nlm.nih.gov/PMC11834944
Volume 85
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