GPR37 Signaling Modulates Migration of Olfactory Ensheathing Cells and Gonadotropin Releasing Hormone Cells in Mice
Gonadotropin releasing hormone (GnRH) neurons, part of the hypothalamic-pituitary-gonadal axis, regulate reproduction. Prenatally, GnRH neurons migrate into the brain from the nasal placode along terminal nerve fibers, intermixed with olfactory sensory axons and olfactory ensheathing cells (OECs). A...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-05-01
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| Series: | Frontiers in Cellular Neuroscience |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fncel.2019.00200/full |
| _version_ | 1811202825303097344 |
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| author | Hassan Saadi Yufei Shan Daniela Marazziti Susan Wray |
| author_facet | Hassan Saadi Yufei Shan Daniela Marazziti Susan Wray |
| author_sort | Hassan Saadi |
| collection | DOAJ |
| description | Gonadotropin releasing hormone (GnRH) neurons, part of the hypothalamic-pituitary-gonadal axis, regulate reproduction. Prenatally, GnRH neurons migrate into the brain from the nasal placode along terminal nerve fibers, intermixed with olfactory sensory axons and olfactory ensheathing cells (OECs). An expression analysis from embryonic GnRH neurons identified the G protein-coupled receptor 37 (GPR37 or PAEL-r). GPR37 has been linked to (1) juvenile Parkinson’s disease in humans, (2) oligodendrocyte differentiation, and (3) Wnt/β-catenin signaling during neurogenesis. In this study, the role of GPR37 was investigated in the developing GnRH/olfactory system. PCR and immunocytochemistry confirmed expression of GPR37 in migrating GnRH neurons as well as in OECs. Inhibition of GPR37 signaling in nasal explants attenuated GnRH neuronal migration and OEC movement. Examination of GPR37 deficient mice revealed a decrease in the olfactory bulb nerve layer and attenuated/delayed maturation and migration of GnRH neurons into the brain. These data demonstrate a developmental role for GPR37 signaling in neural migration.Significance StatementReproduction is controlled by gonadotrophin releasing hormone (GnRH) neurons located in the central nervous system. Embryonically, GnRH neurons originate in the nasal/olfactory placode and migrate into the brain on axonal tracks from cells in the vomeronasal organ, intermixed with olfactory sensory axons and olfactory ensheathing cells (OECs). An expression analysis from embryonic GnRH neurons identified the G protein-coupled receptor 37. Here we show that inhibition of GPR37 signaling in nasal explants and mutant mice attenuated GnRH neuronal migration. Signaling via GPR37 also perturbed OEC movement, resulting in a decrease in the olfactory bulb nerve layer in vivo. Together, these results identify a new role for GPR37 signaling during development – modulating cell migration. |
| first_indexed | 2024-04-12T02:45:09Z |
| format | Article |
| id | doaj.art-3e48c2b1f8134ca6991628bb9d381345 |
| institution | Directory Open Access Journal |
| issn | 1662-5102 |
| language | English |
| last_indexed | 2024-04-12T02:45:09Z |
| publishDate | 2019-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cellular Neuroscience |
| spelling | doaj.art-3e48c2b1f8134ca6991628bb9d3813452022-12-22T03:51:11ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022019-05-011310.3389/fncel.2019.00200451907GPR37 Signaling Modulates Migration of Olfactory Ensheathing Cells and Gonadotropin Releasing Hormone Cells in MiceHassan Saadi0Yufei Shan1Daniela Marazziti2Susan Wray3Cellular and Developmental Neurobiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, United StatesCellular and Developmental Neurobiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, United StatesConsiglio Nazionale delle Ricerche, Emma-Infrafrontier-Impc, Istituto di Biologia Cellulare e Neurobiologia, Monterotondo Scalo, Rome, ItalyCellular and Developmental Neurobiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, United StatesGonadotropin releasing hormone (GnRH) neurons, part of the hypothalamic-pituitary-gonadal axis, regulate reproduction. Prenatally, GnRH neurons migrate into the brain from the nasal placode along terminal nerve fibers, intermixed with olfactory sensory axons and olfactory ensheathing cells (OECs). An expression analysis from embryonic GnRH neurons identified the G protein-coupled receptor 37 (GPR37 or PAEL-r). GPR37 has been linked to (1) juvenile Parkinson’s disease in humans, (2) oligodendrocyte differentiation, and (3) Wnt/β-catenin signaling during neurogenesis. In this study, the role of GPR37 was investigated in the developing GnRH/olfactory system. PCR and immunocytochemistry confirmed expression of GPR37 in migrating GnRH neurons as well as in OECs. Inhibition of GPR37 signaling in nasal explants attenuated GnRH neuronal migration and OEC movement. Examination of GPR37 deficient mice revealed a decrease in the olfactory bulb nerve layer and attenuated/delayed maturation and migration of GnRH neurons into the brain. These data demonstrate a developmental role for GPR37 signaling in neural migration.Significance StatementReproduction is controlled by gonadotrophin releasing hormone (GnRH) neurons located in the central nervous system. Embryonically, GnRH neurons originate in the nasal/olfactory placode and migrate into the brain on axonal tracks from cells in the vomeronasal organ, intermixed with olfactory sensory axons and olfactory ensheathing cells (OECs). An expression analysis from embryonic GnRH neurons identified the G protein-coupled receptor 37. Here we show that inhibition of GPR37 signaling in nasal explants and mutant mice attenuated GnRH neuronal migration. Signaling via GPR37 also perturbed OEC movement, resulting in a decrease in the olfactory bulb nerve layer in vivo. Together, these results identify a new role for GPR37 signaling during development – modulating cell migration.https://www.frontiersin.org/article/10.3389/fncel.2019.00200/fullGPR37GnRHolfactory ensheathing cellsmigrationolfactory system |
| spellingShingle | Hassan Saadi Yufei Shan Daniela Marazziti Susan Wray GPR37 Signaling Modulates Migration of Olfactory Ensheathing Cells and Gonadotropin Releasing Hormone Cells in Mice Frontiers in Cellular Neuroscience GPR37 GnRH olfactory ensheathing cells migration olfactory system |
| title | GPR37 Signaling Modulates Migration of Olfactory Ensheathing Cells and Gonadotropin Releasing Hormone Cells in Mice |
| title_full | GPR37 Signaling Modulates Migration of Olfactory Ensheathing Cells and Gonadotropin Releasing Hormone Cells in Mice |
| title_fullStr | GPR37 Signaling Modulates Migration of Olfactory Ensheathing Cells and Gonadotropin Releasing Hormone Cells in Mice |
| title_full_unstemmed | GPR37 Signaling Modulates Migration of Olfactory Ensheathing Cells and Gonadotropin Releasing Hormone Cells in Mice |
| title_short | GPR37 Signaling Modulates Migration of Olfactory Ensheathing Cells and Gonadotropin Releasing Hormone Cells in Mice |
| title_sort | gpr37 signaling modulates migration of olfactory ensheathing cells and gonadotropin releasing hormone cells in mice |
| topic | GPR37 GnRH olfactory ensheathing cells migration olfactory system |
| url | https://www.frontiersin.org/article/10.3389/fncel.2019.00200/full |
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