Low-Threshold Mechanoreceptor Subtypes Selectively Express MafA and Are Specified by Ret Signaling
Low-threshold mechanoreceptor neurons (LTMs) of the dorsal root ganglia (DRG) are essential for touch sensation. They form highly specialized terminations in the skin and display stereotyped projections in the spinal cord. Functionally defined LTMs depend on neurotrophin signaling for their postnata...
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| Veröffentlicht in: | Neuron (Cambridge, Mass.) Mass.), 2009-12, Vol.64 (6), p.857-870 |
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| creator | Bourane, Steeve Garces, Alain Venteo, Stephanie Pattyn, Alexandre Hubert, Thomas Fichard, Agnes Puech, Sylvie Boukhaddaoui, Hassan Baudet, Christel Takahashi, Satoru Valmier, Jean Carroll, Patrick |
| description | Low-threshold mechanoreceptor neurons (LTMs) of the dorsal root ganglia (DRG) are essential for touch sensation. They form highly specialized terminations in the skin and display stereotyped projections in the spinal cord. Functionally defined LTMs depend on neurotrophin signaling for their postnatal survival and functioning, but how these neurons arise during development is unknown. Here, we show that specific types of LTMs can be identified shortly after DRG genesis by unique expression of the MafA transcription factor, the Ret receptor and coreceptor GFRα2, and find that their specification is Ngn2 dependent. In mice lacking Ret, these LTMs display early differentiation defects, as revealed by reduced MafA expression, and at later stages their central and peripheral projections are compromised. Moreover, in MafA mutants, a discrete subset of LTMs display altered expression of neurotrophic factor receptors. Our results provide evidence that genetic interactions involving Ret and MafA progressively promote the differentiation and diversification of LTMs. |
| doi_str_mv | 10.1016/j.neuron.2009.12.004 |
| format | Article |
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They form highly specialized terminations in the skin and display stereotyped projections in the spinal cord. Functionally defined LTMs depend on neurotrophin signaling for their postnatal survival and functioning, but how these neurons arise during development is unknown. Here, we show that specific types of LTMs can be identified shortly after DRG genesis by unique expression of the MafA transcription factor, the Ret receptor and coreceptor GFRα2, and find that their specification is Ngn2 dependent. In mice lacking Ret, these LTMs display early differentiation defects, as revealed by reduced MafA expression, and at later stages their central and peripheral projections are compromised. Moreover, in MafA mutants, a discrete subset of LTMs display altered expression of neurotrophic factor receptors. Our results provide evidence that genetic interactions involving Ret and MafA progressively promote the differentiation and diversification of LTMs.</description><identifier>ISSN: 0896-6273</identifier><identifier>EISSN: 1097-4199</identifier><identifier>DOI: 10.1016/j.neuron.2009.12.004</identifier><identifier>PMID: 20064392</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Afferent Pathways - cytology ; Afferent Pathways - embryology ; Afferent Pathways - metabolism ; Animals ; Cell Differentiation - genetics ; CELLBIO ; DEVBIO ; Ganglia, Spinal - cytology ; Ganglia, Spinal - embryology ; Ganglia, Spinal - metabolism ; Gene expression ; Gene Expression Regulation, Developmental - genetics ; Glial Cell Line-Derived Neurotrophic Factor Receptors - genetics ; Glial Cell Line-Derived Neurotrophic Factor Receptors - metabolism ; Kinases ; Life Sciences ; Ligands ; Maf Transcription Factors, Large - genetics ; Maf Transcription Factors, Large - metabolism ; Mechanoreceptors - cytology ; Mechanoreceptors - metabolism ; Mice ; Mice, Knockout ; Mice, Transgenic ; MOLNEURO ; Mutation - genetics ; Nerve Growth Factors - genetics ; Nerve Growth Factors - metabolism ; Neurogenesis - genetics ; Neurons ; Population ; Proteins ; Proto-Oncogene Proteins c-ret - genetics ; Proto-Oncogene Proteins c-ret - metabolism ; Sensory Receptor Cells - cytology ; Sensory Receptor Cells - metabolism ; Sensory Thresholds - physiology ; Signal Transduction - genetics ; Skin ; Spinal cord ; Touch - physiology ; Transcription factors</subject><ispartof>Neuron (Cambridge, Mass.), 2009-12, Vol.64 (6), p.857-870</ispartof><rights>2009 Elsevier Inc.</rights><rights>2009 Elsevier Inc. All rights reserved.</rights><rights>Copyright Elsevier Limited Dec 24, 2009</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c566t-a4f1fb7b567e6dd11a55cdcaef3e8c4f5dcc57e9c8c0d61bdcffafef71a765323</citedby><cites>FETCH-LOGICAL-c566t-a4f1fb7b567e6dd11a55cdcaef3e8c4f5dcc57e9c8c0d61bdcffafef71a765323</cites><orcidid>0000-0001-6252-9995</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0896627309009817$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3537,27903,27904,65309</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20064392$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04891297$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Bourane, Steeve</creatorcontrib><creatorcontrib>Garces, Alain</creatorcontrib><creatorcontrib>Venteo, Stephanie</creatorcontrib><creatorcontrib>Pattyn, Alexandre</creatorcontrib><creatorcontrib>Hubert, Thomas</creatorcontrib><creatorcontrib>Fichard, Agnes</creatorcontrib><creatorcontrib>Puech, Sylvie</creatorcontrib><creatorcontrib>Boukhaddaoui, Hassan</creatorcontrib><creatorcontrib>Baudet, Christel</creatorcontrib><creatorcontrib>Takahashi, Satoru</creatorcontrib><creatorcontrib>Valmier, Jean</creatorcontrib><creatorcontrib>Carroll, Patrick</creatorcontrib><title>Low-Threshold Mechanoreceptor Subtypes Selectively Express MafA and Are Specified by Ret Signaling</title><title>Neuron (Cambridge, Mass.)</title><addtitle>Neuron</addtitle><description>Low-threshold mechanoreceptor neurons (LTMs) of the dorsal root ganglia (DRG) are essential for touch sensation. They form highly specialized terminations in the skin and display stereotyped projections in the spinal cord. Functionally defined LTMs depend on neurotrophin signaling for their postnatal survival and functioning, but how these neurons arise during development is unknown. Here, we show that specific types of LTMs can be identified shortly after DRG genesis by unique expression of the MafA transcription factor, the Ret receptor and coreceptor GFRα2, and find that their specification is Ngn2 dependent. In mice lacking Ret, these LTMs display early differentiation defects, as revealed by reduced MafA expression, and at later stages their central and peripheral projections are compromised. Moreover, in MafA mutants, a discrete subset of LTMs display altered expression of neurotrophic factor receptors. Our results provide evidence that genetic interactions involving Ret and MafA progressively promote the differentiation and diversification of LTMs.</description><subject>Afferent Pathways - cytology</subject><subject>Afferent Pathways - embryology</subject><subject>Afferent Pathways - metabolism</subject><subject>Animals</subject><subject>Cell Differentiation - genetics</subject><subject>CELLBIO</subject><subject>DEVBIO</subject><subject>Ganglia, Spinal - cytology</subject><subject>Ganglia, Spinal - embryology</subject><subject>Ganglia, Spinal - metabolism</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Developmental - genetics</subject><subject>Glial Cell Line-Derived Neurotrophic Factor Receptors - genetics</subject><subject>Glial Cell Line-Derived Neurotrophic Factor Receptors - metabolism</subject><subject>Kinases</subject><subject>Life Sciences</subject><subject>Ligands</subject><subject>Maf Transcription Factors, Large - genetics</subject><subject>Maf Transcription Factors, Large - metabolism</subject><subject>Mechanoreceptors - cytology</subject><subject>Mechanoreceptors - metabolism</subject><subject>Mice</subject><subject>Mice, Knockout</subject><subject>Mice, Transgenic</subject><subject>MOLNEURO</subject><subject>Mutation - genetics</subject><subject>Nerve Growth Factors - genetics</subject><subject>Nerve Growth Factors - metabolism</subject><subject>Neurogenesis - genetics</subject><subject>Neurons</subject><subject>Population</subject><subject>Proteins</subject><subject>Proto-Oncogene Proteins c-ret - genetics</subject><subject>Proto-Oncogene Proteins c-ret - metabolism</subject><subject>Sensory Receptor Cells - cytology</subject><subject>Sensory Receptor Cells - metabolism</subject><subject>Sensory Thresholds - physiology</subject><subject>Signal Transduction - genetics</subject><subject>Skin</subject><subject>Spinal cord</subject><subject>Touch - physiology</subject><subject>Transcription factors</subject><issn>0896-6273</issn><issn>1097-4199</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2009</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kV1rFDEUhgdR7Lb6D0QCguLFrDnzkUxuCkupVtgiuPU6ZJKTbpbZyZjMrO6_b5apvfCiV4HD854c3ifL3gFdAgX2ZbfscQq-XxaUiiUUS0qrF9kCqOB5BUK8zBa0ESxnBS_PsvMYd5RCVQt4nZ2lCKtKUSyydu3_5HfbgHHrO0NuUW9V7wNqHEYfyGZqx-OAkWywQz26A3ZHcv13SHwkt8quiOoNWQUkmwG1sw4NaY_kJ45k4-571bn-_k32yqou4tvH9yL79fX67uomX__49v1qtc51zdiYq8qCbXlbM47MGABV19pohbbERle2NlrXHIVuNDUMWqOtVRYtB8VZXRblRfZ53rtVnRyC26twlF45ebNay9OMVo2AQvADJPbTzA7B_54wjnLvosauUz36KUpelqw49ZXIj8-SBZQAlPEEfvgP3PkppAqihJqWvKGFOB1ZzZQOPsaA9ulSoPLkVe7k7FWevEooZPKaYu8fl0_tHs1T6J_IBFzOAKaGDw6DjNphr9G4JHOUxrvnf3gAzIe2Kw</recordid><startdate>20091224</startdate><enddate>20091224</enddate><creator>Bourane, Steeve</creator><creator>Garces, Alain</creator><creator>Venteo, Stephanie</creator><creator>Pattyn, Alexandre</creator><creator>Hubert, Thomas</creator><creator>Fichard, Agnes</creator><creator>Puech, Sylvie</creator><creator>Boukhaddaoui, Hassan</creator><creator>Baudet, Christel</creator><creator>Takahashi, Satoru</creator><creator>Valmier, Jean</creator><creator>Carroll, Patrick</creator><general>Elsevier Inc</general><general>Elsevier Limited</general><general>Elsevier</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>NAPCQ</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0001-6252-9995</orcidid></search><sort><creationdate>20091224</creationdate><title>Low-Threshold Mechanoreceptor Subtypes Selectively Express MafA and Are Specified by Ret Signaling</title><author>Bourane, Steeve ; 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They form highly specialized terminations in the skin and display stereotyped projections in the spinal cord. Functionally defined LTMs depend on neurotrophin signaling for their postnatal survival and functioning, but how these neurons arise during development is unknown. Here, we show that specific types of LTMs can be identified shortly after DRG genesis by unique expression of the MafA transcription factor, the Ret receptor and coreceptor GFRα2, and find that their specification is Ngn2 dependent. In mice lacking Ret, these LTMs display early differentiation defects, as revealed by reduced MafA expression, and at later stages their central and peripheral projections are compromised. Moreover, in MafA mutants, a discrete subset of LTMs display altered expression of neurotrophic factor receptors. 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| source | MEDLINE; Cell Press Free Archives; Elsevier ScienceDirect Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals |
| subjects | Afferent Pathways - cytology Afferent Pathways - embryology Afferent Pathways - metabolism Animals Cell Differentiation - genetics CELLBIO DEVBIO Ganglia, Spinal - cytology Ganglia, Spinal - embryology Ganglia, Spinal - metabolism Gene expression Gene Expression Regulation, Developmental - genetics Glial Cell Line-Derived Neurotrophic Factor Receptors - genetics Glial Cell Line-Derived Neurotrophic Factor Receptors - metabolism Kinases Life Sciences Ligands Maf Transcription Factors, Large - genetics Maf Transcription Factors, Large - metabolism Mechanoreceptors - cytology Mechanoreceptors - metabolism Mice Mice, Knockout Mice, Transgenic MOLNEURO Mutation - genetics Nerve Growth Factors - genetics Nerve Growth Factors - metabolism Neurogenesis - genetics Neurons Population Proteins Proto-Oncogene Proteins c-ret - genetics Proto-Oncogene Proteins c-ret - metabolism Sensory Receptor Cells - cytology Sensory Receptor Cells - metabolism Sensory Thresholds - physiology Signal Transduction - genetics Skin Spinal cord Touch - physiology Transcription factors |
| title | Low-Threshold Mechanoreceptor Subtypes Selectively Express MafA and Are Specified by Ret Signaling |
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