RINT-1 interacts with MSP58 within nucleoli and plays a role in ribosomal gene transcription
The nucleolus is the cellular site of ribosomal (r)DNA transcription and ribosome biogenesis. The 58-kDa microspherule protein (MSP58) is a nucleolar protein involved in rDNA transcription and cell proliferation. However, regulation of MSP58-mediated rDNA transcription remains unknown. Using a yeast...
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Veröffentlicht in: | Biochemical and biophysical research communications 2016-09, Vol.478 (2), p.873-880 |
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creator | Yang, Chuan-Pin Kuo, Yu-Liang Lee, Yi-Chao Lee, Kuen-Haur Chiang, Chi-Wu Wang, Ju-Ming Hsu, Che-Chia Chang, Wen-Chang Lin, Ding-Yen |
description | The nucleolus is the cellular site of ribosomal (r)DNA transcription and ribosome biogenesis. The 58-kDa microspherule protein (MSP58) is a nucleolar protein involved in rDNA transcription and cell proliferation. However, regulation of MSP58-mediated rDNA transcription remains unknown. Using a yeast two-hybrid system with MSP58 as bait, we isolated complementary (c)DNA encoding Rad50-interacting protein 1 (RINT-1), as a MSP58-binding protein. RINT-1 was implicated in the cell cycle checkpoint, membrane trafficking, Golgi apparatus and centrosome dynamic integrity, and telomere length control. Both in vitro and in vivo interaction assays showed that MSP58 directly interacts with RINT-1. Interestingly, microscopic studies revealed the co-localization of MSP58, RINT-1, and the upstream binding factor (UBF), a rRNA transcription factor, in the nucleolus. We showed that ectopic expression of MSP58 or RINT-1 resulted in decreased rRNA expression and rDNA promoter activity, whereas knockdown of MSP58 or RINT-1 by siRNA exerted the opposite effect. Coexpression of MSP58 and RINT-1 robustly decreased rRNA synthesis compared to overexpression of either protein alone, whereas depletion of RINT-1 from MSP58-transfected cells enhanced rRNA synthesis. We also found that MSP58, RINT-1, and the UBF were associated with the rDNA promoter using a chromatin immunoprecipitation assay. Because aberrant ribosome biogenesis contributes to neoplastic transformation, our results revealed a novel protein complex involved in the regulation of rRNA gene expression, suggesting a role for MSP58 and RINT-1 in cancer development.
•RINT-1 is a novel MSP58-interacting protein.•RINT-1 is a nucleolar protein that suppresses ribosomal RNA gene transcription.•RINT-1 and MSP58 cooperate to suppress ribosomal RNA gene transcription.•RINT-1, MSP58, and UBF form a complex on the rDNA promoter. |
doi_str_mv | 10.1016/j.bbrc.2016.08.044 |
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•RINT-1 is a novel MSP58-interacting protein.•RINT-1 is a nucleolar protein that suppresses ribosomal RNA gene transcription.•RINT-1 and MSP58 cooperate to suppress ribosomal RNA gene transcription.•RINT-1, MSP58, and UBF form a complex on the rDNA promoter.</description><identifier>ISSN: 0006-291X</identifier><identifier>EISSN: 1090-2104</identifier><identifier>DOI: 10.1016/j.bbrc.2016.08.044</identifier><identifier>PMID: 27530925</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>60 APPLIED LIFE SCIENCES ; CELL CYCLE ; Cell Cycle Proteins - genetics ; Cell Cycle Proteins - metabolism ; Cell Fractionation ; Cell Line, Tumor ; Cell Nucleolus - metabolism ; CELL PROLIFERATION ; Cytosol - metabolism ; DNA, Ribosomal - genetics ; DNA, Ribosomal - metabolism ; Fibroblasts - cytology ; Fibroblasts - metabolism ; Gene Expression Regulation ; GENES ; GOLGI COMPLEXES ; Humans ; IN VIVO ; INTERACTIONS ; MSP58 ; Nuclear Proteins - genetics ; Nuclear Proteins - metabolism ; NUCLEOLI ; Nucleolus ; Organelle Biogenesis ; Pol1 Transcription Initiation Complex Proteins - genetics ; Pol1 Transcription Initiation Complex Proteins - metabolism ; Promoter Regions, Genetic ; PROMOTERS ; Protein Binding ; Ribosomal genes ; RIBOSOMAL RNA ; RIBOSOMES ; Ribosomes - genetics ; Ribosomes - metabolism ; RINT-1 ; RNA, Ribosomal - biosynthesis ; RNA, Ribosomal - genetics ; RNA, Small Interfering - genetics ; RNA, Small Interfering - metabolism ; RNA-Binding Proteins - genetics ; RNA-Binding Proteins - metabolism ; TRANSCRIPTION FACTORS ; Transcription, Genetic ; Two-Hybrid System Techniques</subject><ispartof>Biochemical and biophysical research communications, 2016-09, Vol.478 (2), p.873-880</ispartof><rights>2016 Elsevier Inc.</rights><rights>Copyright © 2016 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c417t-4cdd6e43055f98e2ff60f57843da4ff28b430d71bdf260d9d0795b1a388fd8fe3</citedby><cites>FETCH-LOGICAL-c417t-4cdd6e43055f98e2ff60f57843da4ff28b430d71bdf260d9d0795b1a388fd8fe3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.bbrc.2016.08.044$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,314,777,781,882,3537,27905,27906,45976</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27530925$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/biblio/22696591$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Yang, Chuan-Pin</creatorcontrib><creatorcontrib>Kuo, Yu-Liang</creatorcontrib><creatorcontrib>Lee, Yi-Chao</creatorcontrib><creatorcontrib>Lee, Kuen-Haur</creatorcontrib><creatorcontrib>Chiang, Chi-Wu</creatorcontrib><creatorcontrib>Wang, Ju-Ming</creatorcontrib><creatorcontrib>Hsu, Che-Chia</creatorcontrib><creatorcontrib>Chang, Wen-Chang</creatorcontrib><creatorcontrib>Lin, Ding-Yen</creatorcontrib><title>RINT-1 interacts with MSP58 within nucleoli and plays a role in ribosomal gene transcription</title><title>Biochemical and biophysical research communications</title><addtitle>Biochem Biophys Res Commun</addtitle><description>The nucleolus is the cellular site of ribosomal (r)DNA transcription and ribosome biogenesis. The 58-kDa microspherule protein (MSP58) is a nucleolar protein involved in rDNA transcription and cell proliferation. However, regulation of MSP58-mediated rDNA transcription remains unknown. Using a yeast two-hybrid system with MSP58 as bait, we isolated complementary (c)DNA encoding Rad50-interacting protein 1 (RINT-1), as a MSP58-binding protein. RINT-1 was implicated in the cell cycle checkpoint, membrane trafficking, Golgi apparatus and centrosome dynamic integrity, and telomere length control. Both in vitro and in vivo interaction assays showed that MSP58 directly interacts with RINT-1. Interestingly, microscopic studies revealed the co-localization of MSP58, RINT-1, and the upstream binding factor (UBF), a rRNA transcription factor, in the nucleolus. We showed that ectopic expression of MSP58 or RINT-1 resulted in decreased rRNA expression and rDNA promoter activity, whereas knockdown of MSP58 or RINT-1 by siRNA exerted the opposite effect. Coexpression of MSP58 and RINT-1 robustly decreased rRNA synthesis compared to overexpression of either protein alone, whereas depletion of RINT-1 from MSP58-transfected cells enhanced rRNA synthesis. We also found that MSP58, RINT-1, and the UBF were associated with the rDNA promoter using a chromatin immunoprecipitation assay. Because aberrant ribosome biogenesis contributes to neoplastic transformation, our results revealed a novel protein complex involved in the regulation of rRNA gene expression, suggesting a role for MSP58 and RINT-1 in cancer development.
•RINT-1 is a novel MSP58-interacting protein.•RINT-1 is a nucleolar protein that suppresses ribosomal RNA gene transcription.•RINT-1 and MSP58 cooperate to suppress ribosomal RNA gene transcription.•RINT-1, MSP58, and UBF form a complex on the rDNA promoter.</description><subject>60 APPLIED LIFE SCIENCES</subject><subject>CELL CYCLE</subject><subject>Cell Cycle Proteins - genetics</subject><subject>Cell Cycle Proteins - metabolism</subject><subject>Cell Fractionation</subject><subject>Cell Line, Tumor</subject><subject>Cell Nucleolus - metabolism</subject><subject>CELL PROLIFERATION</subject><subject>Cytosol - metabolism</subject><subject>DNA, Ribosomal - genetics</subject><subject>DNA, Ribosomal - metabolism</subject><subject>Fibroblasts - cytology</subject><subject>Fibroblasts - metabolism</subject><subject>Gene Expression Regulation</subject><subject>GENES</subject><subject>GOLGI COMPLEXES</subject><subject>Humans</subject><subject>IN VIVO</subject><subject>INTERACTIONS</subject><subject>MSP58</subject><subject>Nuclear Proteins - genetics</subject><subject>Nuclear Proteins - metabolism</subject><subject>NUCLEOLI</subject><subject>Nucleolus</subject><subject>Organelle Biogenesis</subject><subject>Pol1 Transcription Initiation Complex Proteins - genetics</subject><subject>Pol1 Transcription Initiation Complex Proteins - metabolism</subject><subject>Promoter Regions, Genetic</subject><subject>PROMOTERS</subject><subject>Protein Binding</subject><subject>Ribosomal genes</subject><subject>RIBOSOMAL RNA</subject><subject>RIBOSOMES</subject><subject>Ribosomes - genetics</subject><subject>Ribosomes - metabolism</subject><subject>RINT-1</subject><subject>RNA, Ribosomal - biosynthesis</subject><subject>RNA, Ribosomal - genetics</subject><subject>RNA, Small Interfering - genetics</subject><subject>RNA, Small Interfering - metabolism</subject><subject>RNA-Binding Proteins - genetics</subject><subject>RNA-Binding Proteins - metabolism</subject><subject>TRANSCRIPTION FACTORS</subject><subject>Transcription, Genetic</subject><subject>Two-Hybrid System Techniques</subject><issn>0006-291X</issn><issn>1090-2104</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkU2LFDEQhoMo7rj6BzxIwIuXbivp7nQCXmTxY2H9QFfwIIR0UnEz9CSzSY-y_960s3oUTynI875Q9RDymEHLgInn23aasm15nVuQLfT9HbJhoKDhDPq7ZAMAouGKfT0hD0rZAjDWC3WfnPBx6EDxYUO-fTp_f9kwGuKC2dil0J9huaLvPn8c5O8xRBoPdsY0B2qio_vZ3BRqaE4z1hTNYUol7cxMv2NEumQTi81hv4QUH5J73swFH92-p-TL61eXZ2-biw9vzs9eXjS2Z-PS9NY5gX0Hw-CVRO69AD-Msu-c6b3ncqp_bmST81yAUw5GNUzMdFJ6Jz12p-TpsTeVJehiw4L2yqYY0S6ac6HEoFilnh2pfU7XByyL3oVicZ5NxHQomkk-SqVGAf-B1kMKDoOoKD-iNqdSMnq9z2Fn8o1moFdNeqtXTXrVpEHqqqmGntz2H6Ydur-RP14q8OIIYD3bj4B53QqjRRfyupRL4V_9vwATKqIg</recordid><startdate>20160916</startdate><enddate>20160916</enddate><creator>Yang, Chuan-Pin</creator><creator>Kuo, Yu-Liang</creator><creator>Lee, Yi-Chao</creator><creator>Lee, Kuen-Haur</creator><creator>Chiang, Chi-Wu</creator><creator>Wang, Ju-Ming</creator><creator>Hsu, Che-Chia</creator><creator>Chang, Wen-Chang</creator><creator>Lin, Ding-Yen</creator><general>Elsevier Inc</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>7X8</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>OTOTI</scope></search><sort><creationdate>20160916</creationdate><title>RINT-1 interacts with MSP58 within nucleoli and plays a role in ribosomal gene transcription</title><author>Yang, Chuan-Pin ; Kuo, Yu-Liang ; Lee, Yi-Chao ; Lee, Kuen-Haur ; Chiang, Chi-Wu ; Wang, Ju-Ming ; Hsu, Che-Chia ; Chang, Wen-Chang ; Lin, Ding-Yen</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c417t-4cdd6e43055f98e2ff60f57843da4ff28b430d71bdf260d9d0795b1a388fd8fe3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>60 APPLIED LIFE SCIENCES</topic><topic>CELL CYCLE</topic><topic>Cell Cycle Proteins - genetics</topic><topic>Cell Cycle Proteins - metabolism</topic><topic>Cell Fractionation</topic><topic>Cell Line, Tumor</topic><topic>Cell Nucleolus - metabolism</topic><topic>CELL PROLIFERATION</topic><topic>Cytosol - metabolism</topic><topic>DNA, Ribosomal - genetics</topic><topic>DNA, Ribosomal - metabolism</topic><topic>Fibroblasts - cytology</topic><topic>Fibroblasts - metabolism</topic><topic>Gene Expression Regulation</topic><topic>GENES</topic><topic>GOLGI COMPLEXES</topic><topic>Humans</topic><topic>IN VIVO</topic><topic>INTERACTIONS</topic><topic>MSP58</topic><topic>Nuclear Proteins - genetics</topic><topic>Nuclear Proteins - metabolism</topic><topic>NUCLEOLI</topic><topic>Nucleolus</topic><topic>Organelle Biogenesis</topic><topic>Pol1 Transcription Initiation Complex Proteins - genetics</topic><topic>Pol1 Transcription Initiation Complex Proteins - metabolism</topic><topic>Promoter Regions, Genetic</topic><topic>PROMOTERS</topic><topic>Protein Binding</topic><topic>Ribosomal genes</topic><topic>RIBOSOMAL RNA</topic><topic>RIBOSOMES</topic><topic>Ribosomes - genetics</topic><topic>Ribosomes - metabolism</topic><topic>RINT-1</topic><topic>RNA, Ribosomal - biosynthesis</topic><topic>RNA, Ribosomal - genetics</topic><topic>RNA, Small Interfering - genetics</topic><topic>RNA, Small Interfering - metabolism</topic><topic>RNA-Binding Proteins - genetics</topic><topic>RNA-Binding Proteins - metabolism</topic><topic>TRANSCRIPTION FACTORS</topic><topic>Transcription, Genetic</topic><topic>Two-Hybrid System Techniques</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yang, Chuan-Pin</creatorcontrib><creatorcontrib>Kuo, Yu-Liang</creatorcontrib><creatorcontrib>Lee, Yi-Chao</creatorcontrib><creatorcontrib>Lee, Kuen-Haur</creatorcontrib><creatorcontrib>Chiang, Chi-Wu</creatorcontrib><creatorcontrib>Wang, Ju-Ming</creatorcontrib><creatorcontrib>Hsu, Che-Chia</creatorcontrib><creatorcontrib>Chang, Wen-Chang</creatorcontrib><creatorcontrib>Lin, Ding-Yen</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>OSTI.GOV</collection><jtitle>Biochemical and biophysical research communications</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yang, Chuan-Pin</au><au>Kuo, Yu-Liang</au><au>Lee, Yi-Chao</au><au>Lee, Kuen-Haur</au><au>Chiang, Chi-Wu</au><au>Wang, Ju-Ming</au><au>Hsu, Che-Chia</au><au>Chang, Wen-Chang</au><au>Lin, Ding-Yen</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>RINT-1 interacts with MSP58 within nucleoli and plays a role in ribosomal gene transcription</atitle><jtitle>Biochemical and biophysical research communications</jtitle><addtitle>Biochem Biophys Res Commun</addtitle><date>2016-09-16</date><risdate>2016</risdate><volume>478</volume><issue>2</issue><spage>873</spage><epage>880</epage><pages>873-880</pages><issn>0006-291X</issn><eissn>1090-2104</eissn><abstract>The nucleolus is the cellular site of ribosomal (r)DNA transcription and ribosome biogenesis. The 58-kDa microspherule protein (MSP58) is a nucleolar protein involved in rDNA transcription and cell proliferation. However, regulation of MSP58-mediated rDNA transcription remains unknown. Using a yeast two-hybrid system with MSP58 as bait, we isolated complementary (c)DNA encoding Rad50-interacting protein 1 (RINT-1), as a MSP58-binding protein. RINT-1 was implicated in the cell cycle checkpoint, membrane trafficking, Golgi apparatus and centrosome dynamic integrity, and telomere length control. Both in vitro and in vivo interaction assays showed that MSP58 directly interacts with RINT-1. Interestingly, microscopic studies revealed the co-localization of MSP58, RINT-1, and the upstream binding factor (UBF), a rRNA transcription factor, in the nucleolus. We showed that ectopic expression of MSP58 or RINT-1 resulted in decreased rRNA expression and rDNA promoter activity, whereas knockdown of MSP58 or RINT-1 by siRNA exerted the opposite effect. Coexpression of MSP58 and RINT-1 robustly decreased rRNA synthesis compared to overexpression of either protein alone, whereas depletion of RINT-1 from MSP58-transfected cells enhanced rRNA synthesis. We also found that MSP58, RINT-1, and the UBF were associated with the rDNA promoter using a chromatin immunoprecipitation assay. Because aberrant ribosome biogenesis contributes to neoplastic transformation, our results revealed a novel protein complex involved in the regulation of rRNA gene expression, suggesting a role for MSP58 and RINT-1 in cancer development.
•RINT-1 is a novel MSP58-interacting protein.•RINT-1 is a nucleolar protein that suppresses ribosomal RNA gene transcription.•RINT-1 and MSP58 cooperate to suppress ribosomal RNA gene transcription.•RINT-1, MSP58, and UBF form a complex on the rDNA promoter.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>27530925</pmid><doi>10.1016/j.bbrc.2016.08.044</doi><tpages>8</tpages></addata></record> |
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subjects | 60 APPLIED LIFE SCIENCES CELL CYCLE Cell Cycle Proteins - genetics Cell Cycle Proteins - metabolism Cell Fractionation Cell Line, Tumor Cell Nucleolus - metabolism CELL PROLIFERATION Cytosol - metabolism DNA, Ribosomal - genetics DNA, Ribosomal - metabolism Fibroblasts - cytology Fibroblasts - metabolism Gene Expression Regulation GENES GOLGI COMPLEXES Humans IN VIVO INTERACTIONS MSP58 Nuclear Proteins - genetics Nuclear Proteins - metabolism NUCLEOLI Nucleolus Organelle Biogenesis Pol1 Transcription Initiation Complex Proteins - genetics Pol1 Transcription Initiation Complex Proteins - metabolism Promoter Regions, Genetic PROMOTERS Protein Binding Ribosomal genes RIBOSOMAL RNA RIBOSOMES Ribosomes - genetics Ribosomes - metabolism RINT-1 RNA, Ribosomal - biosynthesis RNA, Ribosomal - genetics RNA, Small Interfering - genetics RNA, Small Interfering - metabolism RNA-Binding Proteins - genetics RNA-Binding Proteins - metabolism TRANSCRIPTION FACTORS Transcription, Genetic Two-Hybrid System Techniques |
title | RINT-1 interacts with MSP58 within nucleoli and plays a role in ribosomal gene transcription |
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