The Primary Cilium and Neuronal Migration

The primary cilium (PC) is a microtubule-based tiny sensory organelle emanating from the centrosome and protruding from the surface of most eukaryotic cells, including neurons. The extremely severe phenotypes of ciliopathies have suggested their paramount importance for multiple developmental events...

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Main Authors: Julie Stoufflet, Isabelle Caillé
Format: Article
Language:English
Published: MDPI AG 2022-10-01
Series:Cells
Subjects:
Online Access:https://www.mdpi.com/2073-4409/11/21/3384
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author Julie Stoufflet
Isabelle Caillé
author_facet Julie Stoufflet
Isabelle Caillé
author_sort Julie Stoufflet
collection DOAJ
description The primary cilium (PC) is a microtubule-based tiny sensory organelle emanating from the centrosome and protruding from the surface of most eukaryotic cells, including neurons. The extremely severe phenotypes of ciliopathies have suggested their paramount importance for multiple developmental events, including brain formation. Neuronal migration is an essential step of neural development, with all neurons traveling from their site of birth to their site of integration. Neurons perform a unique type of cellular migration called cyclic saltatory migration, where their soma periodically jumps along with the stereotyped movement of their centrosome. We will review here how the role of the PC on cell motility was first described in non-neuronal cells as a guide pointing to the direction of migration. We will see then how these findings are extended to neuronal migration. In neurons, the PC appears to regulate the rhythm of cyclic saltatory neuronal migration in multiple systems. Finally, we will review recent findings starting to elucidate how extracellular cues sensed by the PC could be intracellularly transduced to regulate the machinery of neuronal migration. The PC of migrating neurons was unexpectedly discovered to display a rhythmic extracellular emergence during each cycle of migration, with this transient exposure to the external environment associated with periodic transduction of cyclic adenosine monophosphate (cAMP) signaling at the centrosome. The PC in migrating neurons thus uniquely appears as a beat maker, regulating the tempo of cyclic saltatory migration.
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spelling doaj.art-3a5a975f957944f8b3a6bcc960aba0142023-11-24T04:07:47ZengMDPI AGCells2073-44092022-10-011121338410.3390/cells11213384The Primary Cilium and Neuronal MigrationJulie Stoufflet0Isabelle Caillé1Laboratory of Molecular Regulation of Neurogenesis, GIGA-Stem Cells and GIGA-Neurosciences, Interdisciplinary Cluster for Applied Genoproteomics (GIGA-R), University of Liège, CHU Sart Tilman, 4000 Liège, BelgiumInserm U1130, Institut de Biologie Paris Seine (IBPS), Neuroscience Paris Seine (NPS), Sorbonne University, CNRS UMR8246, 75005 Paris, FranceThe primary cilium (PC) is a microtubule-based tiny sensory organelle emanating from the centrosome and protruding from the surface of most eukaryotic cells, including neurons. The extremely severe phenotypes of ciliopathies have suggested their paramount importance for multiple developmental events, including brain formation. Neuronal migration is an essential step of neural development, with all neurons traveling from their site of birth to their site of integration. Neurons perform a unique type of cellular migration called cyclic saltatory migration, where their soma periodically jumps along with the stereotyped movement of their centrosome. We will review here how the role of the PC on cell motility was first described in non-neuronal cells as a guide pointing to the direction of migration. We will see then how these findings are extended to neuronal migration. In neurons, the PC appears to regulate the rhythm of cyclic saltatory neuronal migration in multiple systems. Finally, we will review recent findings starting to elucidate how extracellular cues sensed by the PC could be intracellularly transduced to regulate the machinery of neuronal migration. The PC of migrating neurons was unexpectedly discovered to display a rhythmic extracellular emergence during each cycle of migration, with this transient exposure to the external environment associated with periodic transduction of cyclic adenosine monophosphate (cAMP) signaling at the centrosome. The PC in migrating neurons thus uniquely appears as a beat maker, regulating the tempo of cyclic saltatory migration.https://www.mdpi.com/2073-4409/11/21/3384primary ciliumneuronal migration
spellingShingle Julie Stoufflet
Isabelle Caillé
The Primary Cilium and Neuronal Migration
Cells
primary cilium
neuronal migration
title The Primary Cilium and Neuronal Migration
title_full The Primary Cilium and Neuronal Migration
title_fullStr The Primary Cilium and Neuronal Migration
title_full_unstemmed The Primary Cilium and Neuronal Migration
title_short The Primary Cilium and Neuronal Migration
title_sort primary cilium and neuronal migration
topic primary cilium
neuronal migration
url https://www.mdpi.com/2073-4409/11/21/3384
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