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
Hauptverfasser: 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
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container_title Biochemical and biophysical research communications
container_volume 478
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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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. 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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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identifier ISSN: 0006-291X
ispartof Biochemical and biophysical research communications, 2016-09, Vol.478 (2), p.873-880
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source MEDLINE; Elsevier ScienceDirect Journals
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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