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Human Neural Cells Transiently Express Reelin during Olfactory Placode Development

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      Abstract

      Reelin, an extracellular glycoprotein is essential for migration and correct positioning of neurons during development. Since the olfactory system is known as a source of various migrating neuronal cells, we studied Reelin expression in the two chemosensory olfactory systems, main and accessory, during early developmental stages of human foetuses/embryos from Carnegie Stage (CS) 15 to gestational week (GW) 14. From CS 15 to CS 18, but not at later stages, a transient expression of Reelin was detected first in the presumptive olfactory and then in the presumptive vomeronasal epithelium. During the same period, Reelin-positive cells detach from the olfactory/vomeronasal epithelium and migrate through the mesenchyme beneath the telencephalon. Dab 1, an adaptor protein of the Reelin pathway, was simultaneously expressed in the migratory mass from CS16 to CS17 and, at later stages, in the presumptive olfactory ensheathing cells. Possible involvements of Reelin and Dab 1 in the peripheral migrating stream are discussed.

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      Most cited references 36

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      Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2.

      Layering of neurons in the cerebral cortex and cerebellum requires Reelin, an extracellular matrix protein, and mammalian Disabled (mDab1), a cytosolic protein that activates tyrosine kinases. Here, we report the requirement for two other proteins, cell surface receptors termed very low density lipoprotein receptor (VLDLR) and apolipoprotein E receptor 2 (ApoER2). Both receptors can bind mDab1 on their cytoplasmic tails and are expressed in cortical and cerebellar layers adjacent to layers that express Reelin. mDab1 expression is upregulated in knockout mice that lack both VLDLR and ApoER2. Inversion of cortical layers and absence of cerebellar foliation in these animals precisely mimic the phenotype of mice lacking Reelin or mDab1. These findings suggest that VLDLR and ApoER2 participate in transmitting the extracellular Reelin signal to intracellular signaling processes initiated by mDab1.
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        Reelin and brain development.

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          Origin of luteinizing hormone-releasing hormone neurons.

          Neurons expressing luteinizing hormone-releasing hormone (LHRH), found in the septal-preoptic nuclei and hypothalamus, control the release of gonadotropic hormones from the anterior pituitary gland and facilitate reproductive behaviour. LHRH-expressing neurons are also found in the nervus terminalis, a cranial nerve that is a part of the accessory olfactory system and which projects directly from the nose to the septal-preoptic nuclei in the brain. During development, LHRH-immunoreactivity is detected in the peripheral parts of the nervus terminalis before it is found in the brain. Using a combination of LHRH immunocytochemistry and tritiated thymidine autoradiography in fetal mice, we show that LHRH neurons originate in the medial olfactory placode of the developing nose, migrate across the nasal septum and enter the forebrain with the nervus terminalis, arching into the septal-preoptic area and hypothalamus. Clinically, this migratory route for LHRH-expressing neurons could explain the deficiency of gonadotropins seen in 'Kallmann's syndrome' (hypogonadotropic hypogonadism with anosmia).
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            Author and article information

            Affiliations
            [1 ]Institut d'Histologie, Faculté de Médecine, Université de Strasbourg, Strasbourg, France
            [2 ]Fédération de Médecine Translationnelle de Strasbourg, Strasbourg, France
            [3 ]Hôpitaux Universitaires de Strasbourg, Strasbourg, France
            [4 ]Laboratoire d’Imagerie et de Neurosciences Cognitives, CNRS, UMR 7237, Strasbourg, France
            [5 ]CNRS UMR 7357, Strasbourg, France
            Duke University, UNITED STATES
            Author notes

            Competing Interests: The authors have declared that no competing interests exist.

            Conceived and designed the experiments: NB. Performed the experiments: MCA BS MSG NB. Analyzed the data: NB. Contributed reagents/materials/analysis tools: MCA BS MSG NB. Wrote the paper: MCA BS MSG NB.

            Contributors
            Role: Editor
            Journal
            PLoS One
            PLoS ONE
            plos
            plosone
            PLoS ONE
            Public Library of Science (San Francisco, CA USA )
            1932-6203
            13 August 2015
            2015
            : 10
            : 8
            26270645 4535952 10.1371/journal.pone.0135710 PONE-D-15-16146

            This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

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            Figures: 7, Tables: 0, Pages: 14
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            Funding
            This study was supported in part by the Conseil Scientifique de la Faculté de Médecine de Strasbourg and by the Programme Hospitalier de Recherche Clinique, Hôpitaux Universitaires de Strasbourg. The funders had no role in study design, data collection and analysis, decision to publish, or preparetion of the manuscript.
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