Direct binding of pRb/E2F-2 to GATA-1 regulates maturation and terminal cell division during erythropoiesis
How cell proliferation subsides as cells terminally differentiate remains largely enigmatic, although this phenomenon is central to the existence of multicellular organisms. Here, we show that GATA-1, the master transcription factor of erythropoiesis, forms a tricomplex with the retinoblastoma prote...
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| Veröffentlicht in: | PLoS biology 2009-06, Vol.7 (6), p.e1000123-e1000123 |
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| creator | Kadri, Zahra Shimizu, Ritsuko Ohneda, Osamu Maouche-Chretien, Leila Gisselbrecht, Sylvie Yamamoto, Masayuki Romeo, Paul-Henri Leboulch, Philippe Chretien, Stany |
| description | How cell proliferation subsides as cells terminally differentiate remains largely enigmatic, although this phenomenon is central to the existence of multicellular organisms. Here, we show that GATA-1, the master transcription factor of erythropoiesis, forms a tricomplex with the retinoblastoma protein (pRb) and E2F-2. This interaction requires a LXCXE motif that is evolutionary conserved among GATA-1 orthologs yet absent from the other GATA family members. GATA-1/pRb/E2F-2 complex formation stalls cell proliferation and steers erythroid precursors towards terminal differentiation. This process can be disrupted in vitro by FOG-1, which displaces pRb/E2F-2 from GATA-1. A GATA-1 mutant unable to bind pRb fails to inhibit cell proliferation and results in mouse embryonic lethality by anemia. These findings clarify the previously suspected cell-autonomous role of pRb during erythropoiesis and may provide a unifying molecular mechanism for several mouse phenotypes and human diseases associated with GATA-1 mutations. |
| doi_str_mv | 10.1371/journal.pbio.1000123 |
| format | Article |
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Here, we show that GATA-1, the master transcription factor of erythropoiesis, forms a tricomplex with the retinoblastoma protein (pRb) and E2F-2. This interaction requires a LXCXE motif that is evolutionary conserved among GATA-1 orthologs yet absent from the other GATA family members. GATA-1/pRb/E2F-2 complex formation stalls cell proliferation and steers erythroid precursors towards terminal differentiation. This process can be disrupted in vitro by FOG-1, which displaces pRb/E2F-2 from GATA-1. A GATA-1 mutant unable to bind pRb fails to inhibit cell proliferation and results in mouse embryonic lethality by anemia. These findings clarify the previously suspected cell-autonomous role of pRb during erythropoiesis and may provide a unifying molecular mechanism for several mouse phenotypes and human diseases associated with GATA-1 mutations.</description><identifier>ISSN: 1545-7885</identifier><identifier>ISSN: 1544-9173</identifier><identifier>EISSN: 1545-7885</identifier><identifier>DOI: 10.1371/journal.pbio.1000123</identifier><identifier>PMID: 19513100</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amino Acid Motifs ; Amino Acid Sequence ; Animals ; Biochemistry ; Biochemistry, Molecular Biology ; Cell Biology/Cell Growth and Division ; Cell Biology/Developmental Molecular Mechanisms ; Cell Biology/Nuclear Structure and Function ; Cell Division ; Cell Proliferation ; Cellular control mechanisms ; E2F2 Transcription Factor ; E2F2 Transcription Factor - metabolism ; Erythroid Cells ; Erythroid Cells - cytology ; Erythroid Cells - metabolism ; Erythropoiesis ; Experiments ; GATA1 Transcription Factor ; GATA1 Transcription Factor - chemistry ; GATA1 Transcription Factor - deficiency ; GATA1 Transcription Factor - metabolism ; Humans ; Life Sciences ; Mice ; Molecular Biology ; Molecular Sequence Data ; Mutation ; NIH 3T3 Cells ; Nuclear Proteins ; Nuclear Proteins - metabolism ; Observations ; Protein Binding ; Proteins ; Retinoblastoma Protein ; Retinoblastoma Protein - deficiency ; Retinoblastoma Protein - metabolism ; Rodents ; Transcription Factors ; Transcription Factors - metabolism</subject><ispartof>PLoS biology, 2009-06, Vol.7 (6), p.e1000123-e1000123</ispartof><rights>COPYRIGHT 2009 Public Library of Science</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>Kadri et al. 2009</rights><rights>2009 Kadri et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Kadri Z, Shimizu R, Ohneda O, Maouche-Chretien L, Gisselbrecht S, et al. (2009) Direct Binding of pRb/E2F-2 to GATA-1 Regulates Maturation and Terminal Cell Division during Erythropoiesis. 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Shimizu, Ritsuko ; Ohneda, Osamu ; Maouche-Chretien, Leila ; Gisselbrecht, Sylvie ; Yamamoto, Masayuki ; Romeo, Paul-Henri ; Leboulch, Philippe ; Chretien, Stany</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c768t-c5702a92fd98ee488cae98b4f27ac2467a1a852390b253c8ec445aaab11d8aeb3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2009</creationdate><topic>Amino Acid Motifs</topic><topic>Amino Acid Sequence</topic><topic>Animals</topic><topic>Biochemistry</topic><topic>Biochemistry, Molecular Biology</topic><topic>Cell Biology/Cell Growth and Division</topic><topic>Cell Biology/Developmental Molecular Mechanisms</topic><topic>Cell Biology/Nuclear Structure and Function</topic><topic>Cell Division</topic><topic>Cell Proliferation</topic><topic>Cellular control mechanisms</topic><topic>E2F2 Transcription Factor</topic><topic>E2F2 Transcription Factor - metabolism</topic><topic>Erythroid Cells</topic><topic>Erythroid Cells - cytology</topic><topic>Erythroid Cells - metabolism</topic><topic>Erythropoiesis</topic><topic>Experiments</topic><topic>GATA1 Transcription Factor</topic><topic>GATA1 Transcription Factor - chemistry</topic><topic>GATA1 Transcription Factor - deficiency</topic><topic>GATA1 Transcription Factor - metabolism</topic><topic>Humans</topic><topic>Life Sciences</topic><topic>Mice</topic><topic>Molecular Biology</topic><topic>Molecular Sequence Data</topic><topic>Mutation</topic><topic>NIH 3T3 Cells</topic><topic>Nuclear Proteins</topic><topic>Nuclear Proteins - metabolism</topic><topic>Observations</topic><topic>Protein Binding</topic><topic>Proteins</topic><topic>Retinoblastoma Protein</topic><topic>Retinoblastoma Protein - deficiency</topic><topic>Retinoblastoma Protein - metabolism</topic><topic>Rodents</topic><topic>Transcription Factors</topic><topic>Transcription Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kadri, Zahra</creatorcontrib><creatorcontrib>Shimizu, Ritsuko</creatorcontrib><creatorcontrib>Ohneda, Osamu</creatorcontrib><creatorcontrib>Maouche-Chretien, Leila</creatorcontrib><creatorcontrib>Gisselbrecht, Sylvie</creatorcontrib><creatorcontrib>Yamamoto, Masayuki</creatorcontrib><creatorcontrib>Romeo, Paul-Henri</creatorcontrib><creatorcontrib>Leboulch, Philippe</creatorcontrib><creatorcontrib>Chretien, Stany</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Opposing Viewpoints in Context (Gale)</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><collection>PLoS Biology</collection><jtitle>PLoS biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kadri, Zahra</au><au>Shimizu, Ritsuko</au><au>Ohneda, Osamu</au><au>Maouche-Chretien, Leila</au><au>Gisselbrecht, Sylvie</au><au>Yamamoto, Masayuki</au><au>Romeo, Paul-Henri</au><au>Leboulch, Philippe</au><au>Chretien, Stany</au><au>Goodell, Margaret A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Direct binding of pRb/E2F-2 to GATA-1 regulates maturation and terminal cell division during erythropoiesis</atitle><jtitle>PLoS biology</jtitle><addtitle>PLoS Biol</addtitle><date>2009-06-09</date><risdate>2009</risdate><volume>7</volume><issue>6</issue><spage>e1000123</spage><epage>e1000123</epage><pages>e1000123-e1000123</pages><issn>1545-7885</issn><issn>1544-9173</issn><eissn>1545-7885</eissn><abstract>How cell proliferation subsides as cells terminally differentiate remains largely enigmatic, although this phenomenon is central to the existence of multicellular organisms. Here, we show that GATA-1, the master transcription factor of erythropoiesis, forms a tricomplex with the retinoblastoma protein (pRb) and E2F-2. This interaction requires a LXCXE motif that is evolutionary conserved among GATA-1 orthologs yet absent from the other GATA family members. GATA-1/pRb/E2F-2 complex formation stalls cell proliferation and steers erythroid precursors towards terminal differentiation. This process can be disrupted in vitro by FOG-1, which displaces pRb/E2F-2 from GATA-1. A GATA-1 mutant unable to bind pRb fails to inhibit cell proliferation and results in mouse embryonic lethality by anemia. These findings clarify the previously suspected cell-autonomous role of pRb during erythropoiesis and may provide a unifying molecular mechanism for several mouse phenotypes and human diseases associated with GATA-1 mutations.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>19513100</pmid><doi>10.1371/journal.pbio.1000123</doi><orcidid>https://orcid.org/0009-0008-2980-034X</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Amino Acid Motifs Amino Acid Sequence Animals Biochemistry Biochemistry, Molecular Biology Cell Biology/Cell Growth and Division Cell Biology/Developmental Molecular Mechanisms Cell Biology/Nuclear Structure and Function Cell Division Cell Proliferation Cellular control mechanisms E2F2 Transcription Factor E2F2 Transcription Factor - metabolism Erythroid Cells Erythroid Cells - cytology Erythroid Cells - metabolism Erythropoiesis Experiments GATA1 Transcription Factor GATA1 Transcription Factor - chemistry GATA1 Transcription Factor - deficiency GATA1 Transcription Factor - metabolism Humans Life Sciences Mice Molecular Biology Molecular Sequence Data Mutation NIH 3T3 Cells Nuclear Proteins Nuclear Proteins - metabolism Observations Protein Binding Proteins Retinoblastoma Protein Retinoblastoma Protein - deficiency Retinoblastoma Protein - metabolism Rodents Transcription Factors Transcription Factors - metabolism |
| title | Direct binding of pRb/E2F-2 to GATA-1 regulates maturation and terminal cell division during erythropoiesis |
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