Coactivator-Associated Arginine Methyltransferase 1 (CARM1) Is a Positive Regulator of the Cyclin E1 Gene
The Cyclin El gene (CCNE1) is an ideal model to explore the mechanisms that control the transcription of cell cycle-regulated genes whose expression rises transiently before entry into S phase. E2F-dependent regulation of the CCNE1 promoter was shown to correlate with changes in the level of H3-K9 a...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 103; no. 36; pp. 13351 - 13356 |
|---|---|
| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
05.09.2006
National Acad Sciences |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0027-8424 1091-6490 |
| DOI | 10.1073/pnas.0605692103 |
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| Abstract | The Cyclin El gene (CCNE1) is an ideal model to explore the mechanisms that control the transcription of cell cycle-regulated genes whose expression rises transiently before entry into S phase. E2F-dependent regulation of the CCNE1 promoter was shown to correlate with changes in the level of H3-K9 acetylation/methylation of nucleosomal histones positioned at the transcriptional start site region. Here we show that, upon growth stimulation, the same region is subject to variations of H3-R17 and H3-R26 methylation that correlate with the recruitment of coactivator-associated arginine methyltransferase 1 (CARM1) onto the CCNE1 and DHFR promoters. Accordingly, CARM1-deficient cells lack these modifications and present lowered levels and altered kinetics of CCNE1 and DHFR mRNA expression. Consistently, reporter gene assays demonstrate that CARM1 functions as a transcriptional coactivator for their E2F1/DP1-stimulated expression. CARM1 recruitment at the CCNE1 gene requires activator E2Fs and ACTR, a member of the p160 coactivator family that is frequently overexpressed in human breast cancer. Finally, we show that grade-3 breast tumors present coelevated mRNA levels of ACTR and CARM1, along with their transcriptional target CCNE1. All together, our results indicate that CARM1 is an important regulator of the CCNE1 gene. |
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| AbstractList | The Cyclin El gene (CCNE1) is an ideal model to explore the mechanisms that control the transcription of cell cycle-regulated genes whose expression rises transiently before entry into S phase. E2F-dependent regulation of the CCNE1 promoter was shown to correlate with changes in the level of H3-K9 acetylation/methylation of nucleosomal histones positioned at the transcriptional start site region. Here we show that, upon growth stimulation, the same region is subject to variations of H3-R17 and H3-R26 methylation that correlate with the recruitment of coactivator-associated arginine methyltransferase 1 (CARM1) onto the CCNE1 and DHFR promoters. Accordingly, CARM1-deficient cells lack these modifications and present lowered levels and altered kinetics of CCNE1 and DHFR mRNA expression. Consistently, reporter gene assays demonstrate that CARM1 functions as a transcriptional coactivator for their E2F1/DP1-stimulated expression. CARM1 recruitment at the CCNE1 gene requires activator E2Fs and ACTR, a member of the p160 coactivator family that is frequently overexpressed in human breast cancer. Finally, we show that grade-3 breast tumors present coelevated mRNA levels of ACTR and CARM1, along with their transcriptional target CCNE1. All together, our results indicate that CARM1 is an important regulator of the CCNE1 gene. The Cyclin E1 gene ( CCNE1 ) is an ideal model to explore the mechanisms that control the transcription of cell cycle-regulated genes whose expression rises transiently before entry into S phase. E2F-dependent regulation of the CCNE1 promoter was shown to correlate with changes in the level of H3-K9 acetylation/methylation of nucleosomal histones positioned at the transcriptional start site region. Here we show that, upon growth stimulation, the same region is subject to variations of H3-R17 and H3-R26 methylation that correlate with the recruitment of coactivator-associated arginine methyltransferase 1 (CARM1) onto the CCNE1 and DHFR promoters. Accordingly, CARM1-deficient cells lack these modifications and present lowered levels and altered kinetics of CCNE1 and DHFR mRNA expression. Consistently, reporter gene assays demonstrate that CARM1 functions as a transcriptional coactivator for their E2F1/DP1-stimulated expression. CARM1 recruitment at the CCNE1 gene requires activator E2Fs and ACTR, a member of the p160 coactivator family that is frequently overexpressed in human breast cancer. Finally, we show that grade-3 breast tumors present coelevated mRNA levels of ACTR and CARM1 , along with their transcriptional target CCNE1 . All together, our results indicate that CARM1 is an important regulator of the CCNE1 gene. ACTR CCNE1 histone arginine methylation breast tumor The Cyclin E1 gene (CCNE1) is an ideal model to explore the mechanisms that control the transcription of cell cycle-regulated genes whose expression rises transiently before entry into S phase. E2F-dependent regulation of the CCNE1 promoter was shown to correlate with changes in the level of H3-K9 acetylation/methylation of nucleosomal histones positioned at the transcriptional start site region. Here we show that, upon growth stimulation, the same region is subject to variations of H3-R17 and H3-R26 methylation that correlate with the recruitment of coactivator-associated arginine methyltransferase 1 (CARM1) onto the CCNE1 and DHFR promoters. Accordingly, CARM1-deficient cells lack these modifications and present lowered levels and altered kinetics of CCNE1 and DHFR mRNA expression. Consistently, reporter gene assays demonstrate that CARM1 functions as a transcriptional coactivator for their E2F1/DP1-stimulated expression. CARM1 recruitment at the CCNE1 gene requires activator E2Fs and ACTR, a member of the p160 coactivator family that is frequently overexpressed in human breast cancer. Finally, we show that grade-3 breast tumors present coelevated mRNA levels of ACTR and CARM1, along with their transcriptional target CCNE1. All together, our results indicate that CARM1 is an important regulator of the CCNE1 gene.The Cyclin E1 gene (CCNE1) is an ideal model to explore the mechanisms that control the transcription of cell cycle-regulated genes whose expression rises transiently before entry into S phase. E2F-dependent regulation of the CCNE1 promoter was shown to correlate with changes in the level of H3-K9 acetylation/methylation of nucleosomal histones positioned at the transcriptional start site region. Here we show that, upon growth stimulation, the same region is subject to variations of H3-R17 and H3-R26 methylation that correlate with the recruitment of coactivator-associated arginine methyltransferase 1 (CARM1) onto the CCNE1 and DHFR promoters. Accordingly, CARM1-deficient cells lack these modifications and present lowered levels and altered kinetics of CCNE1 and DHFR mRNA expression. Consistently, reporter gene assays demonstrate that CARM1 functions as a transcriptional coactivator for their E2F1/DP1-stimulated expression. CARM1 recruitment at the CCNE1 gene requires activator E2Fs and ACTR, a member of the p160 coactivator family that is frequently overexpressed in human breast cancer. Finally, we show that grade-3 breast tumors present coelevated mRNA levels of ACTR and CARM1, along with their transcriptional target CCNE1. All together, our results indicate that CARM1 is an important regulator of the CCNE1 gene. The Cyclin E1 gene (CCNE1) is an ideal model to explore the mechanisms that control the transcription of cell cycle-regulated genes whose expression rises transiently before entry into S phase. E2F-dependent regulation of the CCNE1 promoter was shown to correlate with changes in the level of H3-K9 acetylation/methylation of nucleosomal histones positioned at the transcriptional start site region. Here we show that, upon growth stimulation, the same region is subject to variations of H3-R17 and H3-R26 methylation that correlate with the recruitment of coactivator-associated arginine methyltransferase 1 (CARM1) onto the CCNE1 and DHFR promoters. Accordingly, CARM1-deficient cells lack these modifications and present lowered levels and altered kinetics of CCNE1 and DHFR mRNA expression. Consistently, reporter gene assays demonstrate that CARM1 functions as a transcriptional coactivator for their E2F1/DP1-stimulated expression. CARM1 recruitment at the CCNE1 gene requires activator E2Fs and ACTR, a member of the p160 coactivator family that is frequently overexpressed in human breast cancer. Finally, we show that grade-3 breast tumors present coelevated mRNA levels of ACTR and CARM1, along with their transcriptional target CCNE1. All together, our results indicate that CARM1 is an important regulator of the CCNE1 gene. The Cyclin E1 gene ( CCNE1 ) is an ideal model to explore the mechanisms that control the transcription of cell cycle-regulated genes whose expression rises transiently before entry into S phase. E2F-dependent regulation of the CCNE1 promoter was shown to correlate with changes in the level of H3-K9 acetylation/methylation of nucleosomal histones positioned at the transcriptional start site region. Here we show that, upon growth stimulation, the same region is subject to variations of H3-R17 and H3-R26 methylation that correlate with the recruitment of coactivator-associated arginine methyltransferase 1 (CARM1) onto the CCNE1 and DHFR promoters. Accordingly, CARM1-deficient cells lack these modifications and present lowered levels and altered kinetics of CCNE1 and DHFR mRNA expression. Consistently, reporter gene assays demonstrate that CARM1 functions as a transcriptional coactivator for their E2F1/DP1-stimulated expression. CARM1 recruitment at the CCNE1 gene requires activator E2Fs and ACTR, a member of the p160 coactivator family that is frequently overexpressed in human breast cancer. Finally, we show that grade-3 breast tumors present coelevated mRNA levels of ACTR and CARM1 , along with their transcriptional target CCNE1 . All together, our results indicate that CARM1 is an important regulator of the CCNE1 gene. The Cyclin E1 gene (CCNE1) is an ideal model to explore the mechanisms that control the transcription of cell cycle-regulated genes whose expression rises transiently before entry into S phase. E2F-dependent regulation of the CCNE1 promoter was shown to correlate with changes in the level of H3-K9 acetylation/methylation of nucleosomal histones positioned at the transcriptional start site region. Here we show that, upon growth stimulation, the same region is subject to variations of H3-R17 and H3-R26 methylation that correlate with the recruitment of coactivator-associated arginine methyltransferase 1 (CARM1) onto the CCNE1 and DHFR promoters. Accordingly, CARM1-deficient cells lack these modifications and present lowered levels and altered kinetics of CCNE1 and DHFR mRNA expression. Consistently, reporter gene assays demonstrate that CARM1 functions as a transcriptional coactivator for their [ZF1/DP1-stimulated expression. CARM1 recruitment at the CCNE1 gene requires activator [ZEs and ACIR, a member of the p160 coactivator family that is frequently overexpressed in human breast cancer. Finally, we show that grade-3 breast tumors present coelevated mRNA levels of ACTR and CARM1, along with their transcriptional target CCNE1. All together, our results indicate that CARM1 is an important regulator of the CCNE1 gene. [PUBLICATION ABSTRACT] |
| Author | Cheng, Donghang Messaoudi, Selma El Fauquier, Lucas Bedford, Mark T. Rodriguez, Carmen Fabbrizio, Eric Theillet, Charles Vandel, Laurence Sardet, Claude Chuchana, Paul |
| Author_xml | – sequence: 1 givenname: Selma El surname: Messaoudi fullname: Messaoudi, Selma El – sequence: 2 givenname: Eric surname: Fabbrizio fullname: Fabbrizio, Eric – sequence: 3 givenname: Carmen surname: Rodriguez fullname: Rodriguez, Carmen – sequence: 4 givenname: Paul surname: Chuchana fullname: Chuchana, Paul – sequence: 5 givenname: Lucas surname: Fauquier fullname: Fauquier, Lucas – sequence: 6 givenname: Donghang surname: Cheng fullname: Cheng, Donghang – sequence: 7 givenname: Charles surname: Theillet fullname: Theillet, Charles – sequence: 8 givenname: Laurence surname: Vandel fullname: Vandel, Laurence – sequence: 9 givenname: Mark T. surname: Bedford fullname: Bedford, Mark T. – sequence: 10 givenname: Claude surname: Sardet fullname: Sardet, Claude |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/16938873$$D View this record in MEDLINE/PubMed https://hal.science/hal-00169734$$DView record in HAL |
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| Copyright | Copyright 2006 National Academy of Sciences of the United States of America Copyright National Academy of Sciences Sep 5, 2006 Distributed under a Creative Commons Attribution 4.0 International License 2006 by The National Academy of Sciences of the USA 2006 |
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| Notes | SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 14 ObjectType-Article-1 ObjectType-Feature-2 content type line 23 ObjectType-Article-2 PMCID: PMC1569167 Author contributions: C.T., M.T.B., and C.S. designed research; S.E.M., E.F., C.R., and D.C. performed research; L.F., C.T., L.V., and M.T.B. contributed new reagents/analytic tools; P.C. analyzed data; and C.S. wrote the paper. Communicated by Robert A. Weinberg, Whitehead Institute for Biomedical Research, Cambridge, MA, July 18, 2006 S.E.M. and E.F. contributed equally to this work. |
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| Snippet | The Cyclin El gene (CCNE1) is an ideal model to explore the mechanisms that control the transcription of cell cycle-regulated genes whose expression rises... The Cyclin E1 gene ( CCNE1 ) is an ideal model to explore the mechanisms that control the transcription of cell cycle-regulated genes whose expression rises... The Cyclin E1 gene ( CCNE1 ) is an ideal model to explore the mechanisms that control the transcription of cell cycle-regulated genes whose expression rises... The Cyclin E1 gene (CCNE1) is an ideal model to explore the mechanisms that control the transcription of cell cycle-regulated genes whose expression rises... |
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| SubjectTerms | 3T3 cells Activin Receptors, Type I Activin Receptors, Type I - metabolism Animals Biochemistry, Molecular Biology Biological Sciences Cell Culture Techniques Cell cycle Cell lines Cell Proliferation Cells, Cultured Chromatin E2F Transcription Factors E2F Transcription Factors - genetics E2F Transcription Factors - metabolism Enzymes Fibroblasts Fibroblasts - metabolism Gene Expression Regulation Genes Genes, cdc Genes, Reporter Histones Histones - metabolism Kinetics Life Sciences Luciferases Luciferases - analysis Luciferases - metabolism Messenger RNA Methylation Mice MicroRNAs MicroRNAs - metabolism NIH 3T3 Cells Nucleosomes Nucleosomes - chemistry Nucleosomes - metabolism Promoter regions Promoter Regions (Genetics) Promoter Regions, Genetic Protein-Arginine N-Methyltransferase Protein-Arginine N-Methyltransferases - deficiency Protein-Arginine N-Methyltransferases - genetics Protein-Arginine N-Methyltransferases - metabolism Ribonucleic acid RNA RNA, Messenger RNA, Messenger - metabolism RNA, Small Interfering RNA, Small Interfering - metabolism Swiss 3T3 Cells Trans-Activators Trans-Activators - metabolism Transcription Factor DP1 Transcription Factor DP1 - genetics Transcription Factor DP1 - metabolism Tumors |
| Title | Coactivator-Associated Arginine Methyltransferase 1 (CARM1) Is a Positive Regulator of the Cyclin E1 Gene |
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