Ubiquitin fold modifier 1 (UFM1) and its target UFBP1 protect pancreatic beta cells from ER stress-induced apoptosis
UFM1 is a member of the ubiquitin like protein family. While the enzymatic cascade of UFM1 conjugation has been elucidated in recent years, the biological function remains largely unknown. In this report we demonstrate that the recently identified C20orf116, which we name UFM1-binding protein 1 cont...
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| Veröffentlicht in: | PloS one 2011-04, Vol.6 (4), p.e18517 |
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| creator | Lemaire, Katleen Moura, Rodrigo F Granvik, Mikaela Igoillo-Esteve, Mariana Hohmeier, Hans E Hendrickx, Nico Newgard, Christopher B Waelkens, Etienne Cnop, Miriam Schuit, Frans |
| description | UFM1 is a member of the ubiquitin like protein family. While the enzymatic cascade of UFM1 conjugation has been elucidated in recent years, the biological function remains largely unknown. In this report we demonstrate that the recently identified C20orf116, which we name UFM1-binding protein 1 containing a PCI domain (UFBP1), and CDK5RAP3 interact with UFM1. Components of the UFM1 conjugation pathway (UFM1, UFBP1, UFL1 and CDK5RAP3) are highly expressed in pancreatic islets of Langerhans and some other secretory tissues. Co-localization of UFM1 with UFBP1 in the endoplasmic reticulum (ER) depends on UFBP1. We demonstrate that ER stress, which is common in secretory cells, induces expression of Ufm1, Ufbp1 and Ufl1 in the beta-cell line INS-1E. siRNA-mediated Ufm1 or Ufbp1 knockdown enhances apoptosis upon ER stress. Silencing the E3 enzyme UFL1, results in similar outcomes, suggesting that UFM1-UFBP1 conjugation is required to prevent ER stress-induced apoptosis. Together, our data suggest that UFM1-UFBP1 participate in preventing ER stress-induced apoptosis in protein secretory cells. |
| doi_str_mv | 10.1371/journal.pone.0018517 |
| format | Article |
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While the enzymatic cascade of UFM1 conjugation has been elucidated in recent years, the biological function remains largely unknown. In this report we demonstrate that the recently identified C20orf116, which we name UFM1-binding protein 1 containing a PCI domain (UFBP1), and CDK5RAP3 interact with UFM1. Components of the UFM1 conjugation pathway (UFM1, UFBP1, UFL1 and CDK5RAP3) are highly expressed in pancreatic islets of Langerhans and some other secretory tissues. Co-localization of UFM1 with UFBP1 in the endoplasmic reticulum (ER) depends on UFBP1. We demonstrate that ER stress, which is common in secretory cells, induces expression of Ufm1, Ufbp1 and Ufl1 in the beta-cell line INS-1E. siRNA-mediated Ufm1 or Ufbp1 knockdown enhances apoptosis upon ER stress. Silencing the E3 enzyme UFL1, results in similar outcomes, suggesting that UFM1-UFBP1 conjugation is required to prevent ER stress-induced apoptosis. Together, our data suggest that UFM1-UFBP1 participate in preventing ER stress-induced apoptosis in protein secretory cells.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0018517</identifier><identifier>PMID: 21494687</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amino Acid Sequence ; Animals ; Apoptosis ; Apoptosis - drug effects ; Apoptosis - genetics ; Beta cells ; Biology ; Cancer ; Carrier Proteins - metabolism ; Conjugation ; Cytoprotection - drug effects ; Cytotoxicity ; Dehydrogenases ; Diabetes ; Endocrinology ; Endoplasmic reticulum ; Endoplasmic Reticulum - drug effects ; Endoplasmic Reticulum - metabolism ; Endoplasmic Reticulum - pathology ; Enzymes ; Fatty acids ; Gene expression ; Gene Expression Profiling ; Gene Expression Regulation - drug effects ; Gene Knockdown Techniques ; Glucose ; Glucose - pharmacology ; Homeostasis ; Insulin ; Insulin - metabolism ; Insulin Secretion ; Insulin-Secreting Cells - cytology ; Insulin-Secreting Cells - drug effects ; Insulin-Secreting Cells - metabolism ; Islets of Langerhans ; Laboratories ; Localization ; Male ; Mass Spectrometry ; Medicine ; Metabolism ; Mice ; Mice, Inbred C57BL ; Molecular Sequence Data ; Motility ; Nerve Tissue Proteins - metabolism ; Pancreas ; Pancreatic beta cells ; Protein binding ; Protein Binding - drug effects ; Protein folding ; Protein Transport - drug effects ; Proteins - genetics ; Proteins - metabolism ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Rodents ; siRNA ; Stress ; Stress response ; Stress, Physiological - drug effects ; Stress, Physiological - genetics ; Stresses ; Tissues ; Ubiquitin ; Ubiquitin-protein ligase</subject><ispartof>PloS one, 2011-04, Vol.6 (4), p.e18517</ispartof><rights>COPYRIGHT 2011 Public Library of Science</rights><rights>2011 Lemaire 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>Lemaire et al. 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c658t-eae274d946968b4e0feed7ed9b5b20159e033980ce0d3db35aae2add2c106f103</citedby><cites>FETCH-LOGICAL-c658t-eae274d946968b4e0feed7ed9b5b20159e033980ce0d3db35aae2add2c106f103</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/PMC3071830/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3071830/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21494687$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Meurs, Eliane F.</contributor><creatorcontrib>Lemaire, Katleen</creatorcontrib><creatorcontrib>Moura, Rodrigo F</creatorcontrib><creatorcontrib>Granvik, Mikaela</creatorcontrib><creatorcontrib>Igoillo-Esteve, Mariana</creatorcontrib><creatorcontrib>Hohmeier, Hans E</creatorcontrib><creatorcontrib>Hendrickx, Nico</creatorcontrib><creatorcontrib>Newgard, Christopher B</creatorcontrib><creatorcontrib>Waelkens, Etienne</creatorcontrib><creatorcontrib>Cnop, Miriam</creatorcontrib><creatorcontrib>Schuit, Frans</creatorcontrib><title>Ubiquitin fold modifier 1 (UFM1) and its target UFBP1 protect pancreatic beta cells from ER stress-induced apoptosis</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>UFM1 is a member of the ubiquitin like protein family. While the enzymatic cascade of UFM1 conjugation has been elucidated in recent years, the biological function remains largely unknown. In this report we demonstrate that the recently identified C20orf116, which we name UFM1-binding protein 1 containing a PCI domain (UFBP1), and CDK5RAP3 interact with UFM1. Components of the UFM1 conjugation pathway (UFM1, UFBP1, UFL1 and CDK5RAP3) are highly expressed in pancreatic islets of Langerhans and some other secretory tissues. Co-localization of UFM1 with UFBP1 in the endoplasmic reticulum (ER) depends on UFBP1. We demonstrate that ER stress, which is common in secretory cells, induces expression of Ufm1, Ufbp1 and Ufl1 in the beta-cell line INS-1E. siRNA-mediated Ufm1 or Ufbp1 knockdown enhances apoptosis upon ER stress. Silencing the E3 enzyme UFL1, results in similar outcomes, suggesting that UFM1-UFBP1 conjugation is required to prevent ER stress-induced apoptosis. Together, our data suggest that UFM1-UFBP1 participate in preventing ER stress-induced apoptosis in protein secretory cells.</description><subject>Amino Acid Sequence</subject><subject>Animals</subject><subject>Apoptosis</subject><subject>Apoptosis - drug effects</subject><subject>Apoptosis - genetics</subject><subject>Beta cells</subject><subject>Biology</subject><subject>Cancer</subject><subject>Carrier Proteins - metabolism</subject><subject>Conjugation</subject><subject>Cytoprotection - drug effects</subject><subject>Cytotoxicity</subject><subject>Dehydrogenases</subject><subject>Diabetes</subject><subject>Endocrinology</subject><subject>Endoplasmic reticulum</subject><subject>Endoplasmic Reticulum - drug effects</subject><subject>Endoplasmic Reticulum - metabolism</subject><subject>Endoplasmic Reticulum - pathology</subject><subject>Enzymes</subject><subject>Fatty acids</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation - drug effects</subject><subject>Gene Knockdown Techniques</subject><subject>Glucose</subject><subject>Glucose - pharmacology</subject><subject>Homeostasis</subject><subject>Insulin</subject><subject>Insulin - metabolism</subject><subject>Insulin Secretion</subject><subject>Insulin-Secreting Cells - cytology</subject><subject>Insulin-Secreting Cells - drug effects</subject><subject>Insulin-Secreting Cells - metabolism</subject><subject>Islets of Langerhans</subject><subject>Laboratories</subject><subject>Localization</subject><subject>Male</subject><subject>Mass Spectrometry</subject><subject>Medicine</subject><subject>Metabolism</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Molecular Sequence Data</subject><subject>Motility</subject><subject>Nerve Tissue Proteins - metabolism</subject><subject>Pancreas</subject><subject>Pancreatic beta cells</subject><subject>Protein binding</subject><subject>Protein Binding - drug effects</subject><subject>Protein folding</subject><subject>Protein Transport - drug effects</subject><subject>Proteins - genetics</subject><subject>Proteins - metabolism</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>Rodents</subject><subject>siRNA</subject><subject>Stress</subject><subject>Stress response</subject><subject>Stress, Physiological - drug effects</subject><subject>Stress, Physiological - genetics</subject><subject>Stresses</subject><subject>Tissues</subject><subject>Ubiquitin</subject><subject>Ubiquitin-protein ligase</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</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>eNp1Ul1rFDEUHUSxtfoPRAO-6MOs-ZiZZF6EWrptoaKI-xwyyc2aZWYyTTKC_96sOy1dUPJww805J-deTlG8JnhFGCcfd34Oo-pXkx9hhTERNeFPilPSMlo2FLOnj-4nxYsYdxjXTDTN8-KEkqqtGsFPi7Tp3N3skhuR9b1BgzfOOgiIoPeb9RfyAanRIJciSipsIaHN-vM3gqbgE-iEJjXqACo5jTpICmno-4hs8AO6_I5iChBj6UYzazBITX5KPrr4snhmVR_h1VLPis368sfFdXn79erm4vy21E0tUgkKKK9Mdto2oqsAWwDDwbRd3VFM6hYwY63AGrBhpmO1ygRlDNUEN5Zgdla8PehOvY9yWViUhBFKBK1blhE3B4Txaien4AYVfkuvnPzb8GErVcjT9SBxTVhNLRWMd5UAIzhgbAXubKcqzlXW-rT8NncDGA1jCqo_Ej1-Gd1PufW_JMOcCLa3-24RCP5uhpj-Y3lBbVV25Ubrs5geXNTyvOKNaEWF91qrf6DyMTA4nSNjXe4fEaoDQQcfYwD7YJxguQ_cvRm5D5xcApdpbx4P_UC6Txj7Axkd0u0</recordid><startdate>20110406</startdate><enddate>20110406</enddate><creator>Lemaire, Katleen</creator><creator>Moura, Rodrigo F</creator><creator>Granvik, Mikaela</creator><creator>Igoillo-Esteve, Mariana</creator><creator>Hohmeier, Hans E</creator><creator>Hendrickx, Nico</creator><creator>Newgard, Christopher B</creator><creator>Waelkens, Etienne</creator><creator>Cnop, Miriam</creator><creator>Schuit, Frans</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>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>20110406</creationdate><title>Ubiquitin fold modifier 1 (UFM1) and its target UFBP1 protect pancreatic beta cells from ER stress-induced apoptosis</title><author>Lemaire, Katleen ; Moura, Rodrigo F ; Granvik, Mikaela ; Igoillo-Esteve, Mariana ; Hohmeier, Hans E ; Hendrickx, Nico ; Newgard, Christopher B ; Waelkens, Etienne ; Cnop, Miriam ; Schuit, Frans</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c658t-eae274d946968b4e0feed7ed9b5b20159e033980ce0d3db35aae2add2c106f103</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Amino Acid Sequence</topic><topic>Animals</topic><topic>Apoptosis</topic><topic>Apoptosis - drug effects</topic><topic>Apoptosis - genetics</topic><topic>Beta cells</topic><topic>Biology</topic><topic>Cancer</topic><topic>Carrier Proteins - metabolism</topic><topic>Conjugation</topic><topic>Cytoprotection - drug effects</topic><topic>Cytotoxicity</topic><topic>Dehydrogenases</topic><topic>Diabetes</topic><topic>Endocrinology</topic><topic>Endoplasmic reticulum</topic><topic>Endoplasmic Reticulum - drug effects</topic><topic>Endoplasmic Reticulum - metabolism</topic><topic>Endoplasmic Reticulum - pathology</topic><topic>Enzymes</topic><topic>Fatty acids</topic><topic>Gene expression</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation - drug effects</topic><topic>Gene Knockdown Techniques</topic><topic>Glucose</topic><topic>Glucose - pharmacology</topic><topic>Homeostasis</topic><topic>Insulin</topic><topic>Insulin - metabolism</topic><topic>Insulin Secretion</topic><topic>Insulin-Secreting Cells - cytology</topic><topic>Insulin-Secreting Cells - drug effects</topic><topic>Insulin-Secreting Cells - 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While the enzymatic cascade of UFM1 conjugation has been elucidated in recent years, the biological function remains largely unknown. In this report we demonstrate that the recently identified C20orf116, which we name UFM1-binding protein 1 containing a PCI domain (UFBP1), and CDK5RAP3 interact with UFM1. Components of the UFM1 conjugation pathway (UFM1, UFBP1, UFL1 and CDK5RAP3) are highly expressed in pancreatic islets of Langerhans and some other secretory tissues. Co-localization of UFM1 with UFBP1 in the endoplasmic reticulum (ER) depends on UFBP1. We demonstrate that ER stress, which is common in secretory cells, induces expression of Ufm1, Ufbp1 and Ufl1 in the beta-cell line INS-1E. siRNA-mediated Ufm1 or Ufbp1 knockdown enhances apoptosis upon ER stress. Silencing the E3 enzyme UFL1, results in similar outcomes, suggesting that UFM1-UFBP1 conjugation is required to prevent ER stress-induced apoptosis. Together, our data suggest that UFM1-UFBP1 participate in preventing ER stress-induced apoptosis in protein secretory cells.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>21494687</pmid><doi>10.1371/journal.pone.0018517</doi><oa>free_for_read</oa></addata></record> |
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| recordid | cdi_plos_journals_1312182593 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Amino Acid Sequence Animals Apoptosis Apoptosis - drug effects Apoptosis - genetics Beta cells Biology Cancer Carrier Proteins - metabolism Conjugation Cytoprotection - drug effects Cytotoxicity Dehydrogenases Diabetes Endocrinology Endoplasmic reticulum Endoplasmic Reticulum - drug effects Endoplasmic Reticulum - metabolism Endoplasmic Reticulum - pathology Enzymes Fatty acids Gene expression Gene Expression Profiling Gene Expression Regulation - drug effects Gene Knockdown Techniques Glucose Glucose - pharmacology Homeostasis Insulin Insulin - metabolism Insulin Secretion Insulin-Secreting Cells - cytology Insulin-Secreting Cells - drug effects Insulin-Secreting Cells - metabolism Islets of Langerhans Laboratories Localization Male Mass Spectrometry Medicine Metabolism Mice Mice, Inbred C57BL Molecular Sequence Data Motility Nerve Tissue Proteins - metabolism Pancreas Pancreatic beta cells Protein binding Protein Binding - drug effects Protein folding Protein Transport - drug effects Proteins - genetics Proteins - metabolism RNA, Messenger - genetics RNA, Messenger - metabolism Rodents siRNA Stress Stress response Stress, Physiological - drug effects Stress, Physiological - genetics Stresses Tissues Ubiquitin Ubiquitin-protein ligase |
| title | Ubiquitin fold modifier 1 (UFM1) and its target UFBP1 protect pancreatic beta cells from ER stress-induced apoptosis |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-25T20%3A32%3A31IST&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=Ubiquitin%20fold%20modifier%201%20(UFM1)%20and%20its%20target%20UFBP1%20protect%20pancreatic%20beta%20cells%20from%20ER%20stress-induced%20apoptosis&rft.jtitle=PloS%20one&rft.au=Lemaire,%20Katleen&rft.date=2011-04-06&rft.volume=6&rft.issue=4&rft.spage=e18517&rft.pages=e18517-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0018517&rft_dat=%3Cgale_plos_%3EA476898400%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=1312182593&rft_id=info:pmid/21494687&rft_galeid=A476898400&rft_doaj_id=oai_doaj_org_article_051352f2837b48ed87e00f80bfba477a&rfr_iscdi=true |