V-erbA generates ribosomes devoid of RPL11 and regulates translational activity in avian erythroid progenitors
The v-erbA oncogene transforms chicken erythrocytic progenitors (T2EC) by blocking their differentiation and freezing them in a state of self-renewal. Transcriptomes of T2EC, expressing either v-erbA or a non-transforming form of v-erbA ( S61G ), were compared using serial analysis of gene expressio...
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creator | Nguyen-Lefebvre, A T Leprun, G Morin, V Viñuelas, J Couté, Y Madjar, J-J Gandrillon, O Gonin-Giraud, S |
description | The
v-erbA
oncogene transforms chicken erythrocytic progenitors (T2EC) by blocking their differentiation and freezing them in a state of self-renewal. Transcriptomes of T2EC, expressing either
v-erbA
or a non-transforming form of
v-erbA
(
S61G
), were compared using serial analysis of gene expression and some, but not all, mRNA-encoding ribosomal proteins were seen to be affected by
v-erbA
. These results suggest that this oncogene could modulate the composition of ribosomes. In the present study, we demonstrate, using two-dimensional difference in gel electrophoresis, that
v-erbA-
expressing cells have a lower amount of RPL11 associated with the ribosomes. The presence of ribosomes devoid of RPL11 in
v-erbA-
expressing cells was further confirmed by immunoprecipitation. In order to assess the possible impact of these specialized ribosomes on the translational activity, we analyzed proteomes of either
v-erbA
or
S61G-
expressing cells using 2D/mass spectrometry, and identified nine proteins present in differing amounts within these cells. Among these proteins, we focused on HSP70 because of its involvement in erythroid differentiation. Our results indicate that, in
v-erbA-
expressing cells,
hsp70
is not only transcribed but also translated more efficiently, as shown by polyribosome fractionation experiments. We demonstrate here, for the first time, the existence of ribosomes with different protein components, notably ribosomes devoid of RPL11, and a regulation of mRNA translation depending on
v-erbA
oncogene expression. |
doi_str_mv | 10.1038/onc.2013.93 |
format | Article |
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v-erbA
oncogene transforms chicken erythrocytic progenitors (T2EC) by blocking their differentiation and freezing them in a state of self-renewal. Transcriptomes of T2EC, expressing either
v-erbA
or a non-transforming form of
v-erbA
(
S61G
), were compared using serial analysis of gene expression and some, but not all, mRNA-encoding ribosomal proteins were seen to be affected by
v-erbA
. These results suggest that this oncogene could modulate the composition of ribosomes. In the present study, we demonstrate, using two-dimensional difference in gel electrophoresis, that
v-erbA-
expressing cells have a lower amount of RPL11 associated with the ribosomes. The presence of ribosomes devoid of RPL11 in
v-erbA-
expressing cells was further confirmed by immunoprecipitation. In order to assess the possible impact of these specialized ribosomes on the translational activity, we analyzed proteomes of either
v-erbA
or
S61G-
expressing cells using 2D/mass spectrometry, and identified nine proteins present in differing amounts within these cells. Among these proteins, we focused on HSP70 because of its involvement in erythroid differentiation. Our results indicate that, in
v-erbA-
expressing cells,
hsp70
is not only transcribed but also translated more efficiently, as shown by polyribosome fractionation experiments. We demonstrate here, for the first time, the existence of ribosomes with different protein components, notably ribosomes devoid of RPL11, and a regulation of mRNA translation depending on
v-erbA
oncogene expression.</description><identifier>ISSN: 0950-9232</identifier><identifier>EISSN: 1476-5594</identifier><identifier>DOI: 10.1038/onc.2013.93</identifier><identifier>PMID: 23563180</identifier><identifier>CODEN: ONCNES</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/208/200 ; 631/337/574/1789 ; 631/67/395 ; Animals ; Apoptosis ; Birds ; Cell Biology ; Cell self-renewal ; Cell Transformation, Viral ; Chickens ; Erythrocytes - cytology ; Freezing ; Gel electrophoresis ; Gene expression ; Genetic research ; HSP70 Heat-Shock Proteins - biosynthesis ; HSP70 Heat-Shock Proteins - genetics ; Hsp70 protein ; Human Genetics ; Humans ; Identification and classification ; Immunoprecipitation ; Internal Medicine ; Life Sciences ; Mass spectroscopy ; Medicine ; Medicine & Public Health ; Oncogene Proteins v-erbA - genetics ; Oncogenes ; Oncology ; original-article ; Poultry ; Progenitor cells ; Properties ; Protein Biosynthesis ; Proteins ; Proteomes ; Ribonucleic acid ; Ribosomal proteins ; Ribosomal Proteins - biosynthesis ; Ribosomal Proteins - deficiency ; Ribosomal Proteins - genetics ; Ribosomes ; Ribosomes - genetics ; Ribosomes - metabolism ; RNA ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Serial analysis of gene expression ; Stem Cells - cytology ; Stem Cells - metabolism ; Transcription, Genetic ; Transcriptomes ; Translation</subject><ispartof>Oncogene, 2014-03, Vol.33 (12), p.1581-1589</ispartof><rights>Macmillan Publishers Limited 2014</rights><rights>COPYRIGHT 2014 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Mar 20, 2014</rights><rights>Macmillan Publishers Limited 2014.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c553t-269a3e26e54cab0b3faaf9a3474660e8f5420911eb93743c52632f0f8cfaf3753</citedby><cites>FETCH-LOGICAL-c553t-269a3e26e54cab0b3faaf9a3474660e8f5420911eb93743c52632f0f8cfaf3753</cites><orcidid>0000-0003-3896-6196</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/onc.2013.93$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/onc.2013.93$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,776,780,881,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23563180$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-02135124$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Nguyen-Lefebvre, A T</creatorcontrib><creatorcontrib>Leprun, G</creatorcontrib><creatorcontrib>Morin, V</creatorcontrib><creatorcontrib>Viñuelas, J</creatorcontrib><creatorcontrib>Couté, Y</creatorcontrib><creatorcontrib>Madjar, J-J</creatorcontrib><creatorcontrib>Gandrillon, O</creatorcontrib><creatorcontrib>Gonin-Giraud, S</creatorcontrib><title>V-erbA generates ribosomes devoid of RPL11 and regulates translational activity in avian erythroid progenitors</title><title>Oncogene</title><addtitle>Oncogene</addtitle><addtitle>Oncogene</addtitle><description>The
v-erbA
oncogene transforms chicken erythrocytic progenitors (T2EC) by blocking their differentiation and freezing them in a state of self-renewal. Transcriptomes of T2EC, expressing either
v-erbA
or a non-transforming form of
v-erbA
(
S61G
), were compared using serial analysis of gene expression and some, but not all, mRNA-encoding ribosomal proteins were seen to be affected by
v-erbA
. These results suggest that this oncogene could modulate the composition of ribosomes. In the present study, we demonstrate, using two-dimensional difference in gel electrophoresis, that
v-erbA-
expressing cells have a lower amount of RPL11 associated with the ribosomes. The presence of ribosomes devoid of RPL11 in
v-erbA-
expressing cells was further confirmed by immunoprecipitation. In order to assess the possible impact of these specialized ribosomes on the translational activity, we analyzed proteomes of either
v-erbA
or
S61G-
expressing cells using 2D/mass spectrometry, and identified nine proteins present in differing amounts within these cells. Among these proteins, we focused on HSP70 because of its involvement in erythroid differentiation. Our results indicate that, in
v-erbA-
expressing cells,
hsp70
is not only transcribed but also translated more efficiently, as shown by polyribosome fractionation experiments. We demonstrate here, for the first time, the existence of ribosomes with different protein components, notably ribosomes devoid of RPL11, and a regulation of mRNA translation depending on
v-erbA
oncogene expression.</description><subject>631/208/200</subject><subject>631/337/574/1789</subject><subject>631/67/395</subject><subject>Animals</subject><subject>Apoptosis</subject><subject>Birds</subject><subject>Cell Biology</subject><subject>Cell self-renewal</subject><subject>Cell Transformation, Viral</subject><subject>Chickens</subject><subject>Erythrocytes - cytology</subject><subject>Freezing</subject><subject>Gel electrophoresis</subject><subject>Gene expression</subject><subject>Genetic research</subject><subject>HSP70 Heat-Shock Proteins - biosynthesis</subject><subject>HSP70 Heat-Shock Proteins - genetics</subject><subject>Hsp70 protein</subject><subject>Human Genetics</subject><subject>Humans</subject><subject>Identification and classification</subject><subject>Immunoprecipitation</subject><subject>Internal Medicine</subject><subject>Life Sciences</subject><subject>Mass spectroscopy</subject><subject>Medicine</subject><subject>Medicine & Public Health</subject><subject>Oncogene Proteins v-erbA - genetics</subject><subject>Oncogenes</subject><subject>Oncology</subject><subject>original-article</subject><subject>Poultry</subject><subject>Progenitor cells</subject><subject>Properties</subject><subject>Protein Biosynthesis</subject><subject>Proteins</subject><subject>Proteomes</subject><subject>Ribonucleic acid</subject><subject>Ribosomal proteins</subject><subject>Ribosomal Proteins - biosynthesis</subject><subject>Ribosomal Proteins - deficiency</subject><subject>Ribosomal Proteins - genetics</subject><subject>Ribosomes</subject><subject>Ribosomes - genetics</subject><subject>Ribosomes - metabolism</subject><subject>RNA</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>Serial analysis of gene expression</subject><subject>Stem Cells - cytology</subject><subject>Stem Cells - metabolism</subject><subject>Transcription, Genetic</subject><subject>Transcriptomes</subject><subject>Translation</subject><issn>0950-9232</issn><issn>1476-5594</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>BENPR</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNqNkk2LFDEQhhtR3HH15F0CXhTtMd_dOQ6LusKAIuo1pNOV2SzdyZp0D8y_N72zrh8sIjmkqDz1pqp4q-opwWuCWfsmBrummLC1YveqFeGNrIVQ_H61wkrgWlFGT6pHOV9ijBuF6cPqhDIhGWnxqgrfakjdBu0gQDITZJR8F3McS9TDPvoeRYc-f9oSgkzoUYLdPFxzUzIhl9DHYAZk7OT3fjogH5DZexMQpMN0kRaBqxSLvJ9iyo-rB84MGZ7c3KfV13dvv5yd19uP7z-cbba1FYJNNZXKMKASBLemwx1zxriS4g2XEkPrBKdYEQKdYg1nVlDJqMOutc441gh2Wr086l6YQV8lP5p00NF4fb7Z6iWHKWGCUL4nhX1xZEuf32fIkx59tjAMJkCcsyaCyIYLgpv_QLHihDHFCvr8L_QyzqmsKmsqORGUt1T8iyparVSFkb-onRlA--BiWb5dvtYbJoVsFZXLHOs7qHJ6GL2NAZwv-T8KXh0LbIo5J3C3myJYL9bSxVp6sZa-HujZTatzN0J_y_70UgFeH4FcnsIO0m-z3KH3A_7H1Cc</recordid><startdate>20140320</startdate><enddate>20140320</enddate><creator>Nguyen-Lefebvre, A T</creator><creator>Leprun, G</creator><creator>Morin, V</creator><creator>Viñuelas, J</creator><creator>Couté, Y</creator><creator>Madjar, J-J</creator><creator>Gandrillon, O</creator><creator>Gonin-Giraud, S</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><general>Nature Publishing Group [1987-....]</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>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</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>GUQSH</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0003-3896-6196</orcidid></search><sort><creationdate>20140320</creationdate><title>V-erbA generates ribosomes devoid of RPL11 and regulates translational activity in avian erythroid progenitors</title><author>Nguyen-Lefebvre, A T ; Leprun, G ; Morin, V ; Viñuelas, J ; Couté, Y ; Madjar, J-J ; Gandrillon, O ; Gonin-Giraud, S</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c553t-269a3e26e54cab0b3faaf9a3474660e8f5420911eb93743c52632f0f8cfaf3753</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>631/208/200</topic><topic>631/337/574/1789</topic><topic>631/67/395</topic><topic>Animals</topic><topic>Apoptosis</topic><topic>Birds</topic><topic>Cell Biology</topic><topic>Cell self-renewal</topic><topic>Cell Transformation, Viral</topic><topic>Chickens</topic><topic>Erythrocytes - cytology</topic><topic>Freezing</topic><topic>Gel electrophoresis</topic><topic>Gene expression</topic><topic>Genetic research</topic><topic>HSP70 Heat-Shock Proteins - biosynthesis</topic><topic>HSP70 Heat-Shock Proteins - genetics</topic><topic>Hsp70 protein</topic><topic>Human Genetics</topic><topic>Humans</topic><topic>Identification and classification</topic><topic>Immunoprecipitation</topic><topic>Internal Medicine</topic><topic>Life Sciences</topic><topic>Mass spectroscopy</topic><topic>Medicine</topic><topic>Medicine & Public Health</topic><topic>Oncogene Proteins v-erbA - genetics</topic><topic>Oncogenes</topic><topic>Oncology</topic><topic>original-article</topic><topic>Poultry</topic><topic>Progenitor cells</topic><topic>Properties</topic><topic>Protein Biosynthesis</topic><topic>Proteins</topic><topic>Proteomes</topic><topic>Ribonucleic acid</topic><topic>Ribosomal proteins</topic><topic>Ribosomal Proteins - biosynthesis</topic><topic>Ribosomal Proteins - deficiency</topic><topic>Ribosomal Proteins - genetics</topic><topic>Ribosomes</topic><topic>Ribosomes - genetics</topic><topic>Ribosomes - metabolism</topic><topic>RNA</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><topic>Serial analysis of gene expression</topic><topic>Stem Cells - cytology</topic><topic>Stem Cells - metabolism</topic><topic>Transcription, Genetic</topic><topic>Transcriptomes</topic><topic>Translation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Nguyen-Lefebvre, A T</creatorcontrib><creatorcontrib>Leprun, G</creatorcontrib><creatorcontrib>Morin, V</creatorcontrib><creatorcontrib>Viñuelas, J</creatorcontrib><creatorcontrib>Couté, Y</creatorcontrib><creatorcontrib>Madjar, J-J</creatorcontrib><creatorcontrib>Gandrillon, O</creatorcontrib><creatorcontrib>Gonin-Giraud, S</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Research Library</collection><collection>Biological Science Database</collection><collection>Research Library (Corporate)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Oncogene</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nguyen-Lefebvre, A T</au><au>Leprun, G</au><au>Morin, V</au><au>Viñuelas, J</au><au>Couté, Y</au><au>Madjar, J-J</au><au>Gandrillon, O</au><au>Gonin-Giraud, S</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>V-erbA generates ribosomes devoid of RPL11 and regulates translational activity in avian erythroid progenitors</atitle><jtitle>Oncogene</jtitle><stitle>Oncogene</stitle><addtitle>Oncogene</addtitle><date>2014-03-20</date><risdate>2014</risdate><volume>33</volume><issue>12</issue><spage>1581</spage><epage>1589</epage><pages>1581-1589</pages><issn>0950-9232</issn><eissn>1476-5594</eissn><coden>ONCNES</coden><abstract>The
v-erbA
oncogene transforms chicken erythrocytic progenitors (T2EC) by blocking their differentiation and freezing them in a state of self-renewal. Transcriptomes of T2EC, expressing either
v-erbA
or a non-transforming form of
v-erbA
(
S61G
), were compared using serial analysis of gene expression and some, but not all, mRNA-encoding ribosomal proteins were seen to be affected by
v-erbA
. These results suggest that this oncogene could modulate the composition of ribosomes. In the present study, we demonstrate, using two-dimensional difference in gel electrophoresis, that
v-erbA-
expressing cells have a lower amount of RPL11 associated with the ribosomes. The presence of ribosomes devoid of RPL11 in
v-erbA-
expressing cells was further confirmed by immunoprecipitation. In order to assess the possible impact of these specialized ribosomes on the translational activity, we analyzed proteomes of either
v-erbA
or
S61G-
expressing cells using 2D/mass spectrometry, and identified nine proteins present in differing amounts within these cells. Among these proteins, we focused on HSP70 because of its involvement in erythroid differentiation. Our results indicate that, in
v-erbA-
expressing cells,
hsp70
is not only transcribed but also translated more efficiently, as shown by polyribosome fractionation experiments. We demonstrate here, for the first time, the existence of ribosomes with different protein components, notably ribosomes devoid of RPL11, and a regulation of mRNA translation depending on
v-erbA
oncogene expression.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>23563180</pmid><doi>10.1038/onc.2013.93</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0003-3896-6196</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | 631/208/200 631/337/574/1789 631/67/395 Animals Apoptosis Birds Cell Biology Cell self-renewal Cell Transformation, Viral Chickens Erythrocytes - cytology Freezing Gel electrophoresis Gene expression Genetic research HSP70 Heat-Shock Proteins - biosynthesis HSP70 Heat-Shock Proteins - genetics Hsp70 protein Human Genetics Humans Identification and classification Immunoprecipitation Internal Medicine Life Sciences Mass spectroscopy Medicine Medicine & Public Health Oncogene Proteins v-erbA - genetics Oncogenes Oncology original-article Poultry Progenitor cells Properties Protein Biosynthesis Proteins Proteomes Ribonucleic acid Ribosomal proteins Ribosomal Proteins - biosynthesis Ribosomal Proteins - deficiency Ribosomal Proteins - genetics Ribosomes Ribosomes - genetics Ribosomes - metabolism RNA RNA, Messenger - genetics RNA, Messenger - metabolism Serial analysis of gene expression Stem Cells - cytology Stem Cells - metabolism Transcription, Genetic Transcriptomes Translation |
title | V-erbA generates ribosomes devoid of RPL11 and regulates translational activity in avian erythroid progenitors |
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