Excitatory granule neuron precursors orchestrate laminar localization and differentiation of cerebellar inhibitory interneuron subtypes
Summary: GABAergic interneurons migrate long distances through stereotyped migration programs toward specific laminar positions. During their migration, GABAergic interneurons are morphologically alike but then differentiate into a rich array of interneuron subtypes critical for brain function. How...
Main Authors: | , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Elsevier
2021-03-01
|
Series: | Cell Reports |
Subjects: | |
Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124721002187 |
id |
doaj-54800aab6e3e4c21956104252f236149 |
---|---|
record_format |
Article |
spelling |
doaj-54800aab6e3e4c21956104252f2361492021-04-02T04:49:41ZengElsevierCell Reports2211-12472021-03-013413108904Excitatory granule neuron precursors orchestrate laminar localization and differentiation of cerebellar inhibitory interneuron subtypesChristelle Cadilhac0Isabelle Bachy1Antoine Forget2David J. Hodson3Céline Jahannault-Talignani4Andrew J. Furley5Olivier Ayrault6Patrice Mollard7Constantino Sotelo8Fabrice Ango9IGF, University Montpellier, CNRS, INSERM, Montpellier, FranceIGF, University Montpellier, CNRS, INSERM, Montpellier, FranceInstitut Curie, Université PSL, CNRS UMR3347, INSERM U1021, Signaling Radiobiology and Cancer, 91400 Orsay, France; Université Paris-Saclay, CNRS UMR3347, INSERM U1021, Signaling Radiobiology and Cancer, 91400 Orsay, FranceInstitute of Metabolism and Systems Research and Centre of Membrane Proteins and Receptors, University of Birmingham, Edgbaston B15 2TT, UKIGF, University Montpellier, CNRS, INSERM, Montpellier, FranceDepartment of Biomedical Science, University of Sheffield, Western Bank, Sheffield S10 2TN, UKInstitut Curie, Université PSL, CNRS UMR3347, INSERM U1021, Signaling Radiobiology and Cancer, 91400 Orsay, France; Université Paris-Saclay, CNRS UMR3347, INSERM U1021, Signaling Radiobiology and Cancer, 91400 Orsay, FranceIGF, University Montpellier, CNRS, INSERM, Montpellier, FranceInstitut de la Vision INSERM, UMRS_U968, Paris, FranceIGF, University Montpellier, CNRS, INSERM, Montpellier, France; INM, University Montpellier, INSERM, CNRS, Montpellier, France; Corresponding authorSummary: GABAergic interneurons migrate long distances through stereotyped migration programs toward specific laminar positions. During their migration, GABAergic interneurons are morphologically alike but then differentiate into a rich array of interneuron subtypes critical for brain function. How interneuron subtypes acquire their final phenotypic traits remains largely unknown. Here, we show that cerebellar molecular layer GABAergic interneurons, derived from the same progenitor pool, use separate migration paths to reach their laminar position and differentiate into distinct basket cell (BC) and stellate cell (SC) GABAergic interneuron subtypes. Using two-photon live imaging, we find that SC final laminar position requires an extra step of tangential migration supported by a subpopulation of glutamatergic granule cells (GCs). Conditional depletion of GCs affects SC differentiation but does not affect BCs. Our results reveal how timely feedforward control of inhibitory interneuron migration path regulates their terminal differentiation and, thus, establishment of the local inhibitory circuit assembly.http://www.sciencedirect.com/science/article/pii/S2211124721002187cerebelluminterneurontangential migrationGABAcell typestellate cell |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Christelle Cadilhac Isabelle Bachy Antoine Forget David J. Hodson Céline Jahannault-Talignani Andrew J. Furley Olivier Ayrault Patrice Mollard Constantino Sotelo Fabrice Ango |
spellingShingle |
Christelle Cadilhac Isabelle Bachy Antoine Forget David J. Hodson Céline Jahannault-Talignani Andrew J. Furley Olivier Ayrault Patrice Mollard Constantino Sotelo Fabrice Ango Excitatory granule neuron precursors orchestrate laminar localization and differentiation of cerebellar inhibitory interneuron subtypes Cell Reports cerebellum interneuron tangential migration GABA cell type stellate cell |
author_facet |
Christelle Cadilhac Isabelle Bachy Antoine Forget David J. Hodson Céline Jahannault-Talignani Andrew J. Furley Olivier Ayrault Patrice Mollard Constantino Sotelo Fabrice Ango |
author_sort |
Christelle Cadilhac |
title |
Excitatory granule neuron precursors orchestrate laminar localization and differentiation of cerebellar inhibitory interneuron subtypes |
title_short |
Excitatory granule neuron precursors orchestrate laminar localization and differentiation of cerebellar inhibitory interneuron subtypes |
title_full |
Excitatory granule neuron precursors orchestrate laminar localization and differentiation of cerebellar inhibitory interneuron subtypes |
title_fullStr |
Excitatory granule neuron precursors orchestrate laminar localization and differentiation of cerebellar inhibitory interneuron subtypes |
title_full_unstemmed |
Excitatory granule neuron precursors orchestrate laminar localization and differentiation of cerebellar inhibitory interneuron subtypes |
title_sort |
excitatory granule neuron precursors orchestrate laminar localization and differentiation of cerebellar inhibitory interneuron subtypes |
publisher |
Elsevier |
series |
Cell Reports |
issn |
2211-1247 |
publishDate |
2021-03-01 |
description |
Summary: GABAergic interneurons migrate long distances through stereotyped migration programs toward specific laminar positions. During their migration, GABAergic interneurons are morphologically alike but then differentiate into a rich array of interneuron subtypes critical for brain function. How interneuron subtypes acquire their final phenotypic traits remains largely unknown. Here, we show that cerebellar molecular layer GABAergic interneurons, derived from the same progenitor pool, use separate migration paths to reach their laminar position and differentiate into distinct basket cell (BC) and stellate cell (SC) GABAergic interneuron subtypes. Using two-photon live imaging, we find that SC final laminar position requires an extra step of tangential migration supported by a subpopulation of glutamatergic granule cells (GCs). Conditional depletion of GCs affects SC differentiation but does not affect BCs. Our results reveal how timely feedforward control of inhibitory interneuron migration path regulates their terminal differentiation and, thus, establishment of the local inhibitory circuit assembly. |
topic |
cerebellum interneuron tangential migration GABA cell type stellate cell |
url |
http://www.sciencedirect.com/science/article/pii/S2211124721002187 |
work_keys_str_mv |
AT christellecadilhac excitatorygranuleneuronprecursorsorchestratelaminarlocalizationanddifferentiationofcerebellarinhibitoryinterneuronsubtypes AT isabellebachy excitatorygranuleneuronprecursorsorchestratelaminarlocalizationanddifferentiationofcerebellarinhibitoryinterneuronsubtypes AT antoineforget excitatorygranuleneuronprecursorsorchestratelaminarlocalizationanddifferentiationofcerebellarinhibitoryinterneuronsubtypes AT davidjhodson excitatorygranuleneuronprecursorsorchestratelaminarlocalizationanddifferentiationofcerebellarinhibitoryinterneuronsubtypes AT celinejahannaulttalignani excitatorygranuleneuronprecursorsorchestratelaminarlocalizationanddifferentiationofcerebellarinhibitoryinterneuronsubtypes AT andrewjfurley excitatorygranuleneuronprecursorsorchestratelaminarlocalizationanddifferentiationofcerebellarinhibitoryinterneuronsubtypes AT olivierayrault excitatorygranuleneuronprecursorsorchestratelaminarlocalizationanddifferentiationofcerebellarinhibitoryinterneuronsubtypes AT patricemollard excitatorygranuleneuronprecursorsorchestratelaminarlocalizationanddifferentiationofcerebellarinhibitoryinterneuronsubtypes AT constantinosotelo excitatorygranuleneuronprecursorsorchestratelaminarlocalizationanddifferentiationofcerebellarinhibitoryinterneuronsubtypes AT fabriceango excitatorygranuleneuronprecursorsorchestratelaminarlocalizationanddifferentiationofcerebellarinhibitoryinterneuronsubtypes |
_version_ |
1724172932753653760 |