Nuclear Organization in the Spinal Cord Depends on Motor Neuron Lamination Orchestrated by Catenin and Afadin Function

Summary: Motor neurons in the spinal cord are found grouped in nuclear structures termed pools, whose position is precisely orchestrated during development. Despite the emerging role of pool organization in the assembly of spinal circuits, little is known about the morphogenetic programs underlying...

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Main Authors: Carola Dewitz, Sofia Pimpinella, Patrick Hackel, Altuna Akalin, Thomas M. Jessell, Niccolò Zampieri
Format: Article
Language:English
Published: Elsevier 2018-02-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124718301086
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spelling doaj-c24457a3fa174e2e9da86db68b0691672020-11-25T03:07:14ZengElsevierCell Reports2211-12472018-02-012271681169410.1016/j.celrep.2018.01.059Nuclear Organization in the Spinal Cord Depends on Motor Neuron Lamination Orchestrated by Catenin and Afadin FunctionCarola Dewitz0Sofia Pimpinella1Patrick Hackel2Altuna Akalin3Thomas M. Jessell4Niccolò Zampieri5Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), 13125 Berlin, Germany; Cluster of Excellence NeuroCure, Neuroscience Research Center, Charité Universitätsmedizin Berlin, Charitéplatz 1, 10117 Berlin, GermanyMax Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), 13125 Berlin, Germany; Cluster of Excellence NeuroCure, Neuroscience Research Center, Charité Universitätsmedizin Berlin, Charitéplatz 1, 10117 Berlin, GermanyMax Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), 13125 Berlin, Germany; Cluster of Excellence NeuroCure, Neuroscience Research Center, Charité Universitätsmedizin Berlin, Charitéplatz 1, 10117 Berlin, GermanyCluster of Excellence NeuroCure, Neuroscience Research Center, Charité Universitätsmedizin Berlin, Charitéplatz 1, 10117 Berlin, Germany; Berlin Institute for Medical Systems Biology, 13125 Berlin, GermanyDepartment of Neuroscience , Columbia University, New York, NY 10032, USA; Department of Biochemistry , Columbia University, New York, NY 10032, USA; Department of Molecular Biophysics, Columbia University, New York, NY 10032, USA; Howard Hughes Medical Institute , Columbia University, New York, NY 10032, USA; Kavli Institute for Brain Science, Columbia University, New York, NY 10032, USAMax Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), 13125 Berlin, Germany; Cluster of Excellence NeuroCure, Neuroscience Research Center, Charité Universitätsmedizin Berlin, Charitéplatz 1, 10117 Berlin, Germany; Corresponding authorSummary: Motor neurons in the spinal cord are found grouped in nuclear structures termed pools, whose position is precisely orchestrated during development. Despite the emerging role of pool organization in the assembly of spinal circuits, little is known about the morphogenetic programs underlying the patterning of motor neuron subtypes. We applied three-dimensional analysis of motor neuron position to reveal the roles and contributions of cell adhesive function by inactivating N-cadherin, catenin, and afadin signaling. Our findings reveal that nuclear organization of motor neurons is dependent on inside-out positioning, orchestrated by N-cadherin, catenin, and afadin activities, controlling cell body layering on the medio-lateral axis. In addition to this lamination-like program, motor neurons undergo a secondary, independent phase of organization. This process results in segregation of motor neurons along the dorso-ventral axis of the spinal cord, does not require N-cadherin or afadin activity, and can proceed even when medio-lateral positioning is perturbed.http://www.sciencedirect.com/science/article/pii/S2211124718301086afadinnectinsN-cadherinβ-cateninmotor poolmigration
collection DOAJ
language English
format Article
sources DOAJ
author Carola Dewitz
Sofia Pimpinella
Patrick Hackel
Altuna Akalin
Thomas M. Jessell
Niccolò Zampieri
spellingShingle Carola Dewitz
Sofia Pimpinella
Patrick Hackel
Altuna Akalin
Thomas M. Jessell
Niccolò Zampieri
Nuclear Organization in the Spinal Cord Depends on Motor Neuron Lamination Orchestrated by Catenin and Afadin Function
Cell Reports
afadin
nectins
N-cadherin
β-catenin
motor pool
migration
author_facet Carola Dewitz
Sofia Pimpinella
Patrick Hackel
Altuna Akalin
Thomas M. Jessell
Niccolò Zampieri
author_sort Carola Dewitz
title Nuclear Organization in the Spinal Cord Depends on Motor Neuron Lamination Orchestrated by Catenin and Afadin Function
title_short Nuclear Organization in the Spinal Cord Depends on Motor Neuron Lamination Orchestrated by Catenin and Afadin Function
title_full Nuclear Organization in the Spinal Cord Depends on Motor Neuron Lamination Orchestrated by Catenin and Afadin Function
title_fullStr Nuclear Organization in the Spinal Cord Depends on Motor Neuron Lamination Orchestrated by Catenin and Afadin Function
title_full_unstemmed Nuclear Organization in the Spinal Cord Depends on Motor Neuron Lamination Orchestrated by Catenin and Afadin Function
title_sort nuclear organization in the spinal cord depends on motor neuron lamination orchestrated by catenin and afadin function
publisher Elsevier
series Cell Reports
issn 2211-1247
publishDate 2018-02-01
description Summary: Motor neurons in the spinal cord are found grouped in nuclear structures termed pools, whose position is precisely orchestrated during development. Despite the emerging role of pool organization in the assembly of spinal circuits, little is known about the morphogenetic programs underlying the patterning of motor neuron subtypes. We applied three-dimensional analysis of motor neuron position to reveal the roles and contributions of cell adhesive function by inactivating N-cadherin, catenin, and afadin signaling. Our findings reveal that nuclear organization of motor neurons is dependent on inside-out positioning, orchestrated by N-cadherin, catenin, and afadin activities, controlling cell body layering on the medio-lateral axis. In addition to this lamination-like program, motor neurons undergo a secondary, independent phase of organization. This process results in segregation of motor neurons along the dorso-ventral axis of the spinal cord, does not require N-cadherin or afadin activity, and can proceed even when medio-lateral positioning is perturbed.
topic afadin
nectins
N-cadherin
β-catenin
motor pool
migration
url http://www.sciencedirect.com/science/article/pii/S2211124718301086
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AT sofiapimpinella nuclearorganizationinthespinalcorddependsonmotorneuronlaminationorchestratedbycateninandafadinfunction
AT patrickhackel nuclearorganizationinthespinalcorddependsonmotorneuronlaminationorchestratedbycateninandafadinfunction
AT altunaakalin nuclearorganizationinthespinalcorddependsonmotorneuronlaminationorchestratedbycateninandafadinfunction
AT thomasmjessell nuclearorganizationinthespinalcorddependsonmotorneuronlaminationorchestratedbycateninandafadinfunction
AT niccolozampieri nuclearorganizationinthespinalcorddependsonmotorneuronlaminationorchestratedbycateninandafadinfunction
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