NGF-induced cell differentiation and gene activation is mediated by integrative nuclear FGFR1 signaling (INFS)
Nerve growth factor (NGF) is the founding member of the polypeptide neurotrophin family responsible for neuronal differentiation. To determine whether the effects of NGF rely upon novel Integrative Nuclear FGF Receptor-1 (FGFR1) Signaling (INFS) we utilized the PC12 clonal cell line, a long-standing...
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| description | Nerve growth factor (NGF) is the founding member of the polypeptide neurotrophin family responsible for neuronal differentiation. To determine whether the effects of NGF rely upon novel Integrative Nuclear FGF Receptor-1 (FGFR1) Signaling (INFS) we utilized the PC12 clonal cell line, a long-standing benchmark model of sympathetic neuronal differentiation. We demonstrate that NGF increases expression of the fgfr1 gene and promotes trafficking of FGFR1 protein from cytoplasm to nucleus by inhibiting FGFR1 nuclear export. Nuclear-targeted dominant negative FGFR1 antagonizes NGF-induced neurite outgrowth, doublecortin (dcx) expression and activation of the tyrosine hydroxylase (th) gene promoter, while active constitutive nuclear FGFR1 mimics the effects of NGF. NGF increases the expression of dcx, th, βIII tubulin, nurr1 and nur77, fgfr1and fibroblast growth factor-2 (fgf-2) genes, while enhancing binding of FGFR1and Nur77/Nurr1 to those genes. NGF activates transcription from isolated NurRE and NBRE motifs. Nuclear FGFR1 transduces NGF activation of the Nur dimer and raises basal activity of the Nur monomer. Cooperation of nuclear FGFR1 with Nur77/Nurr1 in NGF signaling expands the integrative functions of INFS to include NGF, the first discovered pluripotent neurotrophic factor. |
| doi_str_mv | 10.1371/journal.pone.0068931 |
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To determine whether the effects of NGF rely upon novel Integrative Nuclear FGF Receptor-1 (FGFR1) Signaling (INFS) we utilized the PC12 clonal cell line, a long-standing benchmark model of sympathetic neuronal differentiation. We demonstrate that NGF increases expression of the fgfr1 gene and promotes trafficking of FGFR1 protein from cytoplasm to nucleus by inhibiting FGFR1 nuclear export. Nuclear-targeted dominant negative FGFR1 antagonizes NGF-induced neurite outgrowth, doublecortin (dcx) expression and activation of the tyrosine hydroxylase (th) gene promoter, while active constitutive nuclear FGFR1 mimics the effects of NGF. NGF increases the expression of dcx, th, βIII tubulin, nurr1 and nur77, fgfr1and fibroblast growth factor-2 (fgf-2) genes, while enhancing binding of FGFR1and Nur77/Nurr1 to those genes. NGF activates transcription from isolated NurRE and NBRE motifs. Nuclear FGFR1 transduces NGF activation of the Nur dimer and raises basal activity of the Nur monomer. Cooperation of nuclear FGFR1 with Nur77/Nurr1 in NGF signaling expands the integrative functions of INFS to include NGF, the first discovered pluripotent neurotrophic factor.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0068931</identifier><identifier>PMID: 23874817</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Active Transport, Cell Nucleus - drug effects ; Active Transport, Cell Nucleus - genetics ; Animals ; Axonogenesis ; Biology ; Cell activation ; Cell differentiation ; Cell Differentiation - drug effects ; Cell Nucleus - drug effects ; Cell Nucleus - metabolism ; Cells, Cultured ; Cytoplasm ; Deoxyribonucleic acid ; Differentiation (biology) ; DNA ; Doublecortin protein ; Fibroblast growth factor 2 ; Fibroblast growth factor receptor 1 ; Fibroblast growth factors ; Fibroblasts ; Gene expression ; Genes ; Genetic transcription ; Growth factors ; Humans ; Hydroxylase ; Kinases ; Ligands ; Morphology ; Nanoparticles ; Nerve growth factor ; Nerve Growth Factor - pharmacology ; Nerve Growth Factor - physiology ; Nervous system ; Neurites - drug effects ; Neurites - physiology ; Neurosciences ; Neurotrophic factors ; Nuclear receptors ; Nuclear transport ; Nur77 protein ; Nurr1 protein ; Pathology ; PC12 Cells ; Pluripotency ; Protein Transport ; Proteins ; Rats ; Receptor, Fibroblast Growth Factor, Type 1 - physiology ; Signal transduction ; Signal Transduction - drug effects ; Signal Transduction - physiology ; Signaling ; Stem cells ; Studies ; Transcription ; Transcription factors ; Transcriptional Activation - drug effects ; Tubulin ; Tyrosine ; Tyrosine 3-monooxygenase</subject><ispartof>PloS one, 2013-07, Vol.8 (7), p.e68931</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Lee et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2013 Lee et al 2013 Lee et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-393e354c89aa0c4138d1b693f529e618727f5b02db16548a08390f84198cea313</citedby><cites>FETCH-LOGICAL-c692t-393e354c89aa0c4138d1b693f529e618727f5b02db16548a08390f84198cea313</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3707895/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3707895/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23874817$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>van Wijnen, Andre</contributor><creatorcontrib>Lee, Yu-Wei</creatorcontrib><creatorcontrib>Stachowiak, Ewa K</creatorcontrib><creatorcontrib>Birkaya, Barbara</creatorcontrib><creatorcontrib>Terranova, Christopher</creatorcontrib><creatorcontrib>Capacchietti, Mariolina</creatorcontrib><creatorcontrib>Claus, Peter</creatorcontrib><creatorcontrib>Aletta, John M</creatorcontrib><creatorcontrib>Stachowiak, Michal K</creatorcontrib><title>NGF-induced cell differentiation and gene activation is mediated by integrative nuclear FGFR1 signaling (INFS)</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Nerve growth factor (NGF) is the founding member of the polypeptide neurotrophin family responsible for neuronal differentiation. To determine whether the effects of NGF rely upon novel Integrative Nuclear FGF Receptor-1 (FGFR1) Signaling (INFS) we utilized the PC12 clonal cell line, a long-standing benchmark model of sympathetic neuronal differentiation. We demonstrate that NGF increases expression of the fgfr1 gene and promotes trafficking of FGFR1 protein from cytoplasm to nucleus by inhibiting FGFR1 nuclear export. Nuclear-targeted dominant negative FGFR1 antagonizes NGF-induced neurite outgrowth, doublecortin (dcx) expression and activation of the tyrosine hydroxylase (th) gene promoter, while active constitutive nuclear FGFR1 mimics the effects of NGF. NGF increases the expression of dcx, th, βIII tubulin, nurr1 and nur77, fgfr1and fibroblast growth factor-2 (fgf-2) genes, while enhancing binding of FGFR1and Nur77/Nurr1 to those genes. NGF activates transcription from isolated NurRE and NBRE motifs. Nuclear FGFR1 transduces NGF activation of the Nur dimer and raises basal activity of the Nur monomer. Cooperation of nuclear FGFR1 with Nur77/Nurr1 in NGF signaling expands the integrative functions of INFS to include NGF, the first discovered pluripotent neurotrophic factor.</description><subject>Active Transport, Cell Nucleus - drug effects</subject><subject>Active Transport, Cell Nucleus - genetics</subject><subject>Animals</subject><subject>Axonogenesis</subject><subject>Biology</subject><subject>Cell activation</subject><subject>Cell differentiation</subject><subject>Cell Differentiation - drug effects</subject><subject>Cell Nucleus - drug effects</subject><subject>Cell Nucleus - metabolism</subject><subject>Cells, Cultured</subject><subject>Cytoplasm</subject><subject>Deoxyribonucleic acid</subject><subject>Differentiation (biology)</subject><subject>DNA</subject><subject>Doublecortin protein</subject><subject>Fibroblast growth factor 2</subject><subject>Fibroblast growth factor receptor 1</subject><subject>Fibroblast growth factors</subject><subject>Fibroblasts</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genetic transcription</subject><subject>Growth factors</subject><subject>Humans</subject><subject>Hydroxylase</subject><subject>Kinases</subject><subject>Ligands</subject><subject>Morphology</subject><subject>Nanoparticles</subject><subject>Nerve growth factor</subject><subject>Nerve Growth Factor - pharmacology</subject><subject>Nerve Growth Factor - physiology</subject><subject>Nervous system</subject><subject>Neurites - drug effects</subject><subject>Neurites - physiology</subject><subject>Neurosciences</subject><subject>Neurotrophic factors</subject><subject>Nuclear receptors</subject><subject>Nuclear transport</subject><subject>Nur77 protein</subject><subject>Nurr1 protein</subject><subject>Pathology</subject><subject>PC12 Cells</subject><subject>Pluripotency</subject><subject>Protein Transport</subject><subject>Proteins</subject><subject>Rats</subject><subject>Receptor, Fibroblast Growth Factor, Type 1 - physiology</subject><subject>Signal transduction</subject><subject>Signal Transduction - drug effects</subject><subject>Signal Transduction - physiology</subject><subject>Signaling</subject><subject>Stem cells</subject><subject>Studies</subject><subject>Transcription</subject><subject>Transcription factors</subject><subject>Transcriptional Activation - drug effects</subject><subject>Tubulin</subject><subject>Tyrosine</subject><subject>Tyrosine 3-monooxygenase</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNklFr2zAUhc3YWLtu_2BshsFYH5JJli1LL4NSlixQWmi3vQpZunIUHCmV7LD--ymLWxLYYPjB5uo7R9eHk2VvMZpiUuPPKz8EJ7vpxjuYIkQZJ_hZdoo5KSa0QOT5wfdJ9irGFUIVYZS-zE4KwuqS4fo0c9fz2cQ6PSjQuYKuy7U1BgK43sreepdLp_MWHORS9Xa7n9mYr0EnIImah9y6HtqQjraQu0F1IEM-m89ucR5tm3a0rs0_La5nd-evsxdGdhHejO-z7Mfs6_fLb5Orm_ni8uJqoigv-gnhBEhVKsalRKrEhGncUE5MVXCgmNVFbaoGFbrBtCqZRIxwZFiJOVMgCSZn2fu976bzUYxRRYEJ5wWvUF0lYrEntJcrsQl2LcOD8NKKPwMfWiFDb9PPiIpiqaUhUhtaGk2bQlaSFg00JaC6huT1ZbxtaFIuKoUXZHdkenzi7FK0fitIjWrGd8t8GA2Cvx8g9v9YeaRambayzvhkptY2KnFR1oyUhBU0UdO_UOnRsLYqlcXYND8SnB8JEtPDr76VQ4xicXf7_-zNz2P24wG7BNn1y-i7YdegeAyWe1AFH2MA85QcRmLX9cc0xK7rYux6kr07TP1J9Fhu8htcxfjf</recordid><startdate>20130710</startdate><enddate>20130710</enddate><creator>Lee, Yu-Wei</creator><creator>Stachowiak, Ewa K</creator><creator>Birkaya, Barbara</creator><creator>Terranova, Christopher</creator><creator>Capacchietti, Mariolina</creator><creator>Claus, Peter</creator><creator>Aletta, John M</creator><creator>Stachowiak, Michal K</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20130710</creationdate><title>NGF-induced cell differentiation and gene activation is mediated by integrative nuclear FGFR1 signaling (INFS)</title><author>Lee, Yu-Wei ; Stachowiak, Ewa K ; Birkaya, Barbara ; Terranova, Christopher ; Capacchietti, Mariolina ; Claus, Peter ; Aletta, John M ; Stachowiak, Michal K</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-393e354c89aa0c4138d1b693f529e618727f5b02db16548a08390f84198cea313</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Active Transport, Cell Nucleus - drug effects</topic><topic>Active Transport, Cell Nucleus - genetics</topic><topic>Animals</topic><topic>Axonogenesis</topic><topic>Biology</topic><topic>Cell activation</topic><topic>Cell differentiation</topic><topic>Cell Differentiation - drug effects</topic><topic>Cell Nucleus - drug effects</topic><topic>Cell Nucleus - metabolism</topic><topic>Cells, Cultured</topic><topic>Cytoplasm</topic><topic>Deoxyribonucleic acid</topic><topic>Differentiation (biology)</topic><topic>DNA</topic><topic>Doublecortin protein</topic><topic>Fibroblast growth factor 2</topic><topic>Fibroblast growth factor receptor 1</topic><topic>Fibroblast growth factors</topic><topic>Fibroblasts</topic><topic>Gene expression</topic><topic>Genes</topic><topic>Genetic transcription</topic><topic>Growth factors</topic><topic>Humans</topic><topic>Hydroxylase</topic><topic>Kinases</topic><topic>Ligands</topic><topic>Morphology</topic><topic>Nanoparticles</topic><topic>Nerve growth factor</topic><topic>Nerve Growth Factor - 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To determine whether the effects of NGF rely upon novel Integrative Nuclear FGF Receptor-1 (FGFR1) Signaling (INFS) we utilized the PC12 clonal cell line, a long-standing benchmark model of sympathetic neuronal differentiation. We demonstrate that NGF increases expression of the fgfr1 gene and promotes trafficking of FGFR1 protein from cytoplasm to nucleus by inhibiting FGFR1 nuclear export. Nuclear-targeted dominant negative FGFR1 antagonizes NGF-induced neurite outgrowth, doublecortin (dcx) expression and activation of the tyrosine hydroxylase (th) gene promoter, while active constitutive nuclear FGFR1 mimics the effects of NGF. NGF increases the expression of dcx, th, βIII tubulin, nurr1 and nur77, fgfr1and fibroblast growth factor-2 (fgf-2) genes, while enhancing binding of FGFR1and Nur77/Nurr1 to those genes. NGF activates transcription from isolated NurRE and NBRE motifs. Nuclear FGFR1 transduces NGF activation of the Nur dimer and raises basal activity of the Nur monomer. Cooperation of nuclear FGFR1 with Nur77/Nurr1 in NGF signaling expands the integrative functions of INFS to include NGF, the first discovered pluripotent neurotrophic factor.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23874817</pmid><doi>10.1371/journal.pone.0068931</doi><tpages>e68931</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | PloS one, 2013-07, Vol.8 (7), p.e68931 |
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| source | PLoS; MEDLINE; DOAJ Directory of Open Access Journals; Free E-Journal (出版社公開部分のみ）; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Active Transport, Cell Nucleus - drug effects Active Transport, Cell Nucleus - genetics Animals Axonogenesis Biology Cell activation Cell differentiation Cell Differentiation - drug effects Cell Nucleus - drug effects Cell Nucleus - metabolism Cells, Cultured Cytoplasm Deoxyribonucleic acid Differentiation (biology) DNA Doublecortin protein Fibroblast growth factor 2 Fibroblast growth factor receptor 1 Fibroblast growth factors Fibroblasts Gene expression Genes Genetic transcription Growth factors Humans Hydroxylase Kinases Ligands Morphology Nanoparticles Nerve growth factor Nerve Growth Factor - pharmacology Nerve Growth Factor - physiology Nervous system Neurites - drug effects Neurites - physiology Neurosciences Neurotrophic factors Nuclear receptors Nuclear transport Nur77 protein Nurr1 protein Pathology PC12 Cells Pluripotency Protein Transport Proteins Rats Receptor, Fibroblast Growth Factor, Type 1 - physiology Signal transduction Signal Transduction - drug effects Signal Transduction - physiology Signaling Stem cells Studies Transcription Transcription factors Transcriptional Activation - drug effects Tubulin Tyrosine Tyrosine 3-monooxygenase |
| title | NGF-induced cell differentiation and gene activation is mediated by integrative nuclear FGFR1 signaling (INFS) |
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