NRP1-mediated Sema3A signals coordinate laminar formation in the developing chick optic tectum

The optic tectum comprises multiple layers, which are formed by radial and tangential migration during development. Here, we report that Neuropilin 1 (NRP1)-mediated Sema3A signals are involved in the process of tectal laminar formation, which is elaborated by tangential migration. In the developing...

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Published inDevelopment (Cambridge) Vol. 141; no. 18; pp. 3572 - 3582
Main Authors Watanabe, Yuji, Sakuma, Chie, Yaginuma, Hiroyuki
Format Journal Article
LanguageEnglish
Published England 01.09.2014
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Abstract The optic tectum comprises multiple layers, which are formed by radial and tangential migration during development. Here, we report that Neuropilin 1 (NRP1)-mediated Sema3A signals are involved in the process of tectal laminar formation, which is elaborated by tangential migration. In the developing chick tectum, NRP1, a receptor for Sema3A, is expressed in microtubule-associated protein 2 (MAP2)-positive intermediate layers IV and V. Sema3A itself is a diffusible guidance factor and is expressed in the overlying layer VI. Using stable fluorescent labeling of tectal cells, we show that MAP2-positive intermediate layers are formed by the neurons that have been dispersed by tangential migration along the tectal efferent axons. When Sema3A was mis-expressed during laminar formation, local Sema3A repelled the tangential migrants, thus eliminating MAP2-positive neurons that expressed NRP1. Furthermore, in the absence of the MAP2-positive neurons, tectal layers were disorganized into an undulated form, indicating that MAP2-positive intermediate layers are required for proper laminar formation. These results suggest that NRP1-mediated Sema3A signals provide repulsive signals for MAP2-positive neurons to segregate tectal layers, which is important in order to coordinate laminar organization of the optic tectum.
AbstractList The optic tectum comprises multiple layers, which are formed by radial and tangential migration during development. Here, we report that Neuropilin 1 (NRP1)-mediated Sema3A signals are involved in the process of tectal laminar formation, which is elaborated by tangential migration. In the developing chick tectum, NRP1, a receptor for Sema3A, is expressed in microtubule-associated protein 2 (MAP2)-positive intermediate layers IV and V. Sema3A itself is a diffusible guidance factor and is expressed in the overlying layer VI. Using stable fluorescent labeling of tectal cells, we show that MAP2-positive intermediate layers are formed by the neurons that have been dispersed by tangential migration along the tectal efferent axons. When Sema3A was mis-expressed during laminar formation, local Sema3A repelled the tangential migrants, thus eliminating MAP2-positive neurons that expressed NRP1. Furthermore, in the absence of the MAP2-positive neurons, tectal layers were disorganized into an undulated form, indicating that MAP2-positive intermediate layers are required for proper laminar formation. These results suggest that NRP1-mediated Sema3A signals provide repulsive signals for MAP2-positive neurons to segregate tectal layers, which is important in order to coordinate laminar organization of the optic tectum.
Author Yaginuma, Hiroyuki
Watanabe, Yuji
Sakuma, Chie
Author_xml – sequence: 1
  givenname: Yuji
  surname: Watanabe
  fullname: Watanabe, Yuji
  email: yuji-w@fmu.ac.jp
  organization: Department of Molecular Neurobiology, Graduate School of Life Sciences, Tohoku University, Aoba-ku, Sendai 980-8575, Japan Institute of Development, Aging & Cancer, Tohoku University, Sendai 980-8575, Japan Department of Neuroanatomy and Embryology, School of Medicine, Fukushima Medical University, Fukushima 960-1295, Japan yuji-w@fmu.ac.jp
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  givenname: Chie
  surname: Sakuma
  fullname: Sakuma, Chie
  organization: Department of Neuroanatomy and Embryology, School of Medicine, Fukushima Medical University, Fukushima 960-1295, Japan
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  givenname: Hiroyuki
  surname: Yaginuma
  fullname: Yaginuma, Hiroyuki
  organization: Department of Neuroanatomy and Embryology, School of Medicine, Fukushima Medical University, Fukushima 960-1295, Japan
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Keywords Sema3A
NRP1
Optic tectum
Laminar formation
Chick
Cell migration
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Snippet The optic tectum comprises multiple layers, which are formed by radial and tangential migration during development. Here, we report that Neuropilin 1...
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SubjectTerms Animals
Bromodeoxyuridine
Cell Movement - physiology
Chick Embryo
Electroporation
Fluorescence
In Situ Hybridization
Microscopy, Confocal
Microtubule-Associated Proteins - metabolism
Neuropilin-1 - metabolism
Organogenesis - physiology
Semaphorin-3A - metabolism
Signal Transduction - physiology
Superior Colliculi - embryology
Superior Colliculi - metabolism
Title NRP1-mediated Sema3A signals coordinate laminar formation in the developing chick optic tectum
URI https://www.ncbi.nlm.nih.gov/pubmed/25183873
https://search.proquest.com/docview/1560098136
https://search.proquest.com/docview/1808615013
Volume 141
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