Prdm5 regulates collagen gene transcription by association with RNA polymerase II in developing bone
PRDM family members are transcriptional regulators involved in tissue specific differentiation. PRDM5 has been reported to predominantly repress transcription, but a characterization of its molecular functions in a relevant biological context is lacking. We demonstrate here that Prdm5 is highly expr...
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| Veröffentlicht in: | PLoS genetics 2012-05, Vol.8 (5), p.e1002711 |
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| creator | Galli, Giorgio Giacomo Honnens de Lichtenberg, Kristian Carrara, Matteo Hans, Wolfgang Wuelling, Manuela Mentz, Bettina Multhaupt, Hinke Arnolda Fog, Cathrine Kolster Jensen, Klaus Thorleif Rappsilber, Juri Vortkamp, Andrea Coulton, Les Fuchs, Helmut Gailus-Durner, Valérie Hrabě de Angelis, Martin Calogero, Raffaele Adolfo Couchman, John Robert Lund, Anders Henrik |
| description | PRDM family members are transcriptional regulators involved in tissue specific differentiation. PRDM5 has been reported to predominantly repress transcription, but a characterization of its molecular functions in a relevant biological context is lacking. We demonstrate here that Prdm5 is highly expressed in developing bones; and, by genome-wide mapping of Prdm5 occupancy in pre-osteoblastic cells, we uncover a novel and unique role for Prdm5 in targeting all mouse collagen genes as well as several SLRP proteoglycan genes. In particular, we show that Prdm5 controls both Collagen I transcription and fibrillogenesis by binding inside the Col1a1 gene body and maintaining RNA polymerase II occupancy. In vivo, Prdm5 loss results in delayed ossification involving a pronounced impairment in the assembly of fibrillar collagens. Collectively, our results define a novel role for Prdm5 in sustaining the transcriptional program necessary to the proper assembly of osteoblastic extracellular matrix. |
| doi_str_mv | 10.1371/journal.pgen.1002711 |
| format | Article |
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PRDM5 has been reported to predominantly repress transcription, but a characterization of its molecular functions in a relevant biological context is lacking. We demonstrate here that Prdm5 is highly expressed in developing bones; and, by genome-wide mapping of Prdm5 occupancy in pre-osteoblastic cells, we uncover a novel and unique role for Prdm5 in targeting all mouse collagen genes as well as several SLRP proteoglycan genes. In particular, we show that Prdm5 controls both Collagen I transcription and fibrillogenesis by binding inside the Col1a1 gene body and maintaining RNA polymerase II occupancy. In vivo, Prdm5 loss results in delayed ossification involving a pronounced impairment in the assembly of fibrillar collagens. Collectively, our results define a novel role for Prdm5 in sustaining the transcriptional program necessary to the proper assembly of osteoblastic extracellular matrix.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1002711</identifier><identifier>PMID: 22589746</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>3T3 Cells ; Animals ; Bars ; Biology ; Bone density ; Bone Development - genetics ; Bones ; Cell Differentiation - genetics ; Collagen ; Collagen Type I - genetics ; Collagen Type I - metabolism ; Collagen Type I, alpha 1 Chain ; Decorin - genetics ; Decorin - metabolism ; Defects ; DNA-Binding Proteins - genetics ; DNA-Binding Proteins - metabolism ; Embryonic Development - genetics ; Embryos ; Enhancer Elements, Genetic ; Extracellular Matrix - genetics ; Extracellular Matrix - metabolism ; Fibrillar Collagens ; Gene Expression Regulation, Developmental ; Genes ; Genetic aspects ; Genetic regulation ; Genome ; Genomes ; Grants ; Growth ; Mice ; Organ Specificity ; Osteoblasts - cytology ; Osteoblasts - metabolism ; Physiological aspects ; Promoter Regions, Genetic ; Proteins ; Proteoglycans - genetics ; Proteoglycans - metabolism ; RNA Polymerase II - genetics ; RNA polymerases ; Scholarships & fellowships ; Transcription Factors - genetics ; Transcription Factors - metabolism ; Transcription, Genetic</subject><ispartof>PLoS genetics, 2012-05, Vol.8 (5), p.e1002711</ispartof><rights>COPYRIGHT 2012 Public Library of Science</rights><rights>2012 Galli et al. 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: Galli GG, Honnens de Lichtenberg K, Carrara M, Hans W, Wuelling M, et al. (2012) Prdm5 Regulates Collagen Gene Transcription by Association with RNA Polymerase II in Developing Bone. PLoS Genet 8(5): e1002711. doi:10.1371/journal.pgen.1002711</rights><rights>Galli et al. 2012</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c726t-b26b9427751412d2dc05cebf4f6486bff4b4c403200e3334286f74b5b6d1c8ef3</citedby><cites>FETCH-LOGICAL-c726t-b26b9427751412d2dc05cebf4f6486bff4b4c403200e3334286f74b5b6d1c8ef3</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/PMC3349747/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3349747/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22589746$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Galli, Giorgio Giacomo</creatorcontrib><creatorcontrib>Honnens de Lichtenberg, Kristian</creatorcontrib><creatorcontrib>Carrara, Matteo</creatorcontrib><creatorcontrib>Hans, Wolfgang</creatorcontrib><creatorcontrib>Wuelling, Manuela</creatorcontrib><creatorcontrib>Mentz, Bettina</creatorcontrib><creatorcontrib>Multhaupt, Hinke Arnolda</creatorcontrib><creatorcontrib>Fog, Cathrine Kolster</creatorcontrib><creatorcontrib>Jensen, Klaus Thorleif</creatorcontrib><creatorcontrib>Rappsilber, Juri</creatorcontrib><creatorcontrib>Vortkamp, Andrea</creatorcontrib><creatorcontrib>Coulton, Les</creatorcontrib><creatorcontrib>Fuchs, Helmut</creatorcontrib><creatorcontrib>Gailus-Durner, Valérie</creatorcontrib><creatorcontrib>Hrabě de Angelis, Martin</creatorcontrib><creatorcontrib>Calogero, Raffaele Adolfo</creatorcontrib><creatorcontrib>Couchman, John Robert</creatorcontrib><creatorcontrib>Lund, Anders Henrik</creatorcontrib><title>Prdm5 regulates collagen gene transcription by association with RNA polymerase II in developing bone</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>PRDM family members are transcriptional regulators involved in tissue specific differentiation. PRDM5 has been reported to predominantly repress transcription, but a characterization of its molecular functions in a relevant biological context is lacking. We demonstrate here that Prdm5 is highly expressed in developing bones; and, by genome-wide mapping of Prdm5 occupancy in pre-osteoblastic cells, we uncover a novel and unique role for Prdm5 in targeting all mouse collagen genes as well as several SLRP proteoglycan genes. In particular, we show that Prdm5 controls both Collagen I transcription and fibrillogenesis by binding inside the Col1a1 gene body and maintaining RNA polymerase II occupancy. In vivo, Prdm5 loss results in delayed ossification involving a pronounced impairment in the assembly of fibrillar collagens. Collectively, our results define a novel role for Prdm5 in sustaining the transcriptional program necessary to the proper assembly of osteoblastic extracellular matrix.</description><subject>3T3 Cells</subject><subject>Animals</subject><subject>Bars</subject><subject>Biology</subject><subject>Bone density</subject><subject>Bone Development - genetics</subject><subject>Bones</subject><subject>Cell Differentiation - genetics</subject><subject>Collagen</subject><subject>Collagen Type I - genetics</subject><subject>Collagen Type I - metabolism</subject><subject>Collagen Type I, alpha 1 Chain</subject><subject>Decorin - genetics</subject><subject>Decorin - metabolism</subject><subject>Defects</subject><subject>DNA-Binding Proteins - genetics</subject><subject>DNA-Binding Proteins - metabolism</subject><subject>Embryonic Development - genetics</subject><subject>Embryos</subject><subject>Enhancer Elements, Genetic</subject><subject>Extracellular Matrix - genetics</subject><subject>Extracellular Matrix - metabolism</subject><subject>Fibrillar Collagens</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genetic regulation</subject><subject>Genome</subject><subject>Genomes</subject><subject>Grants</subject><subject>Growth</subject><subject>Mice</subject><subject>Organ Specificity</subject><subject>Osteoblasts - cytology</subject><subject>Osteoblasts - metabolism</subject><subject>Physiological aspects</subject><subject>Promoter Regions, Genetic</subject><subject>Proteins</subject><subject>Proteoglycans - genetics</subject><subject>Proteoglycans - metabolism</subject><subject>RNA Polymerase II - genetics</subject><subject>RNA polymerases</subject><subject>Scholarships & fellowships</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><subject>Transcription, Genetic</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqVk12L1DAUhoso7jr6D0QDgujFjEmTft0Iw-LHwLIr68dtSNLTToa0qUm7Ov_edKe7TGUvlJI2TZ_z5uQ9PVH0nOAVoRl5t7ODa4VZdTW0K4JxnBHyIDolSUKXGcPs4dH8JHri_Q5jmuRF9jg6ieNxwtLTqPziyiZBDurBiB48UtYYESRRGIB6J1qvnO56bVsk90h4b5UWN6-_dL9FVxdr1Fmzb8AJD2izQbpFJVyDsZ1uayRtC0-jR5UwHp5Nz0X0_eOHb2efl-eXnzZn6_OlyuK0X8o4lQWLsywhjMRlXCqcKJAVq1KWp7KqmGSKYRpjDJRSFudplTGZyLQkKoeKLqKXB93OWM8ngzwnlNA0jHBbRJsDUVqx453TjXB7boXmNwvW1Vy4XisDPMepUmkmCkErlgtZUCIkZkQSBqxIyqD1ftptkA2UCtrglpmJzr-0estre81D6sH8LAi8mQSc_TmA73mjvYLgfwt2CHnj4APBRch8Eb36C73_dBNVi3AA3VY27KtGUb6OC0YzTPBIre6hwlVCo1UoV6XD-izg7SwgMD387msxeM83X6_-g734d_byx5x9fcRuQZh-660Zxh_Rz0F2AJWz3juo7gpCMB8b59Y5PjYOnxonhL04LuZd0G2n0D8cPhFf</recordid><startdate>20120501</startdate><enddate>20120501</enddate><creator>Galli, Giorgio Giacomo</creator><creator>Honnens de Lichtenberg, Kristian</creator><creator>Carrara, Matteo</creator><creator>Hans, Wolfgang</creator><creator>Wuelling, Manuela</creator><creator>Mentz, Bettina</creator><creator>Multhaupt, Hinke Arnolda</creator><creator>Fog, Cathrine Kolster</creator><creator>Jensen, Klaus Thorleif</creator><creator>Rappsilber, Juri</creator><creator>Vortkamp, Andrea</creator><creator>Coulton, Les</creator><creator>Fuchs, Helmut</creator><creator>Gailus-Durner, Valérie</creator><creator>Hrabě de Angelis, Martin</creator><creator>Calogero, Raffaele Adolfo</creator><creator>Couchman, John Robert</creator><creator>Lund, Anders Henrik</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>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</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>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20120501</creationdate><title>Prdm5 regulates collagen gene transcription by association with RNA polymerase II in developing bone</title><author>Galli, Giorgio Giacomo ; Honnens de Lichtenberg, Kristian ; Carrara, Matteo ; Hans, Wolfgang ; Wuelling, Manuela ; Mentz, Bettina ; Multhaupt, Hinke Arnolda ; Fog, Cathrine Kolster ; Jensen, Klaus Thorleif ; Rappsilber, Juri ; Vortkamp, Andrea ; Coulton, Les ; Fuchs, Helmut ; Gailus-Durner, Valérie ; Hrabě de Angelis, Martin ; Calogero, Raffaele Adolfo ; Couchman, John Robert ; Lund, Anders Henrik</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c726t-b26b9427751412d2dc05cebf4f6486bff4b4c403200e3334286f74b5b6d1c8ef3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>3T3 Cells</topic><topic>Animals</topic><topic>Bars</topic><topic>Biology</topic><topic>Bone density</topic><topic>Bone Development - genetics</topic><topic>Bones</topic><topic>Cell Differentiation - genetics</topic><topic>Collagen</topic><topic>Collagen Type I - genetics</topic><topic>Collagen Type I - metabolism</topic><topic>Collagen Type I, alpha 1 Chain</topic><topic>Decorin - genetics</topic><topic>Decorin - metabolism</topic><topic>Defects</topic><topic>DNA-Binding Proteins - genetics</topic><topic>DNA-Binding Proteins - metabolism</topic><topic>Embryonic Development - genetics</topic><topic>Embryos</topic><topic>Enhancer Elements, Genetic</topic><topic>Extracellular Matrix - genetics</topic><topic>Extracellular Matrix - metabolism</topic><topic>Fibrillar Collagens</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Genes</topic><topic>Genetic aspects</topic><topic>Genetic regulation</topic><topic>Genome</topic><topic>Genomes</topic><topic>Grants</topic><topic>Growth</topic><topic>Mice</topic><topic>Organ Specificity</topic><topic>Osteoblasts - cytology</topic><topic>Osteoblasts - metabolism</topic><topic>Physiological aspects</topic><topic>Promoter Regions, Genetic</topic><topic>Proteins</topic><topic>Proteoglycans - 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PRDM5 has been reported to predominantly repress transcription, but a characterization of its molecular functions in a relevant biological context is lacking. We demonstrate here that Prdm5 is highly expressed in developing bones; and, by genome-wide mapping of Prdm5 occupancy in pre-osteoblastic cells, we uncover a novel and unique role for Prdm5 in targeting all mouse collagen genes as well as several SLRP proteoglycan genes. In particular, we show that Prdm5 controls both Collagen I transcription and fibrillogenesis by binding inside the Col1a1 gene body and maintaining RNA polymerase II occupancy. In vivo, Prdm5 loss results in delayed ossification involving a pronounced impairment in the assembly of fibrillar collagens. Collectively, our results define a novel role for Prdm5 in sustaining the transcriptional program necessary to the proper assembly of osteoblastic extracellular matrix.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>22589746</pmid><doi>10.1371/journal.pgen.1002711</doi><oa>free_for_read</oa></addata></record> |
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| ispartof | PLoS genetics, 2012-05, Vol.8 (5), p.e1002711 |
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| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Public Library of Science (PLoS) |
| subjects | 3T3 Cells Animals Bars Biology Bone density Bone Development - genetics Bones Cell Differentiation - genetics Collagen Collagen Type I - genetics Collagen Type I - metabolism Collagen Type I, alpha 1 Chain Decorin - genetics Decorin - metabolism Defects DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism Embryonic Development - genetics Embryos Enhancer Elements, Genetic Extracellular Matrix - genetics Extracellular Matrix - metabolism Fibrillar Collagens Gene Expression Regulation, Developmental Genes Genetic aspects Genetic regulation Genome Genomes Grants Growth Mice Organ Specificity Osteoblasts - cytology Osteoblasts - metabolism Physiological aspects Promoter Regions, Genetic Proteins Proteoglycans - genetics Proteoglycans - metabolism RNA Polymerase II - genetics RNA polymerases Scholarships & fellowships Transcription Factors - genetics Transcription Factors - metabolism Transcription, Genetic |
| title | Prdm5 regulates collagen gene transcription by association with RNA polymerase II in developing bone |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-09T22%3A13%3A16IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Prdm5%20regulates%20collagen%20gene%20transcription%20by%20association%20with%20RNA%20polymerase%20II%20in%20developing%20bone&rft.jtitle=PLoS%20genetics&rft.au=Galli,%20Giorgio%20Giacomo&rft.date=2012-05-01&rft.volume=8&rft.issue=5&rft.spage=e1002711&rft.pages=e1002711-&rft.issn=1553-7404&rft.eissn=1553-7404&rft_id=info:doi/10.1371/journal.pgen.1002711&rft_dat=%3Cgale_plos_%3EA294370106%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1313631336&rft_id=info:pmid/22589746&rft_galeid=A294370106&rft_doaj_id=oai_doaj_org_article_806cc67a9a3f48ab931ab041b14e495d&rfr_iscdi=true |