RUNX1B Expression Is Highly Heterogeneous and Distinguishes Megakaryocytic and Erythroid Lineage Fate in Adult Mouse Hematopoiesis
The Core Binding Factor (CBF) protein RUNX1 is a master regulator of definitive hematopoiesis, crucial for hematopoietic stem cell (HSC) emergence during ontogeny. RUNX1 also plays vital roles in adult mice, in regulating the correct specification of numerous blood lineages. Akin to the other mammal...
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| description | The Core Binding Factor (CBF) protein RUNX1 is a master regulator of definitive hematopoiesis, crucial for hematopoietic stem cell (HSC) emergence during ontogeny. RUNX1 also plays vital roles in adult mice, in regulating the correct specification of numerous blood lineages. Akin to the other mammalian Runx genes, Runx1 has two promoters P1 (distal) and P2 (proximal) which generate distinct protein isoforms. The activities and specific relevance of these two promoters in adult hematopoiesis remain to be fully elucidated. Utilizing a dual reporter mouse model we demonstrate that the distal P1 promoter is broadly active in adult hematopoietic stem and progenitor cell (HSPC) populations. By contrast the activity of the proximal P2 promoter is more restricted and its upregulation, in both the immature Lineage- Sca1high cKithigh (LSK) and bipotential Pre-Megakaryocytic/Erythroid Progenitor (PreMegE) populations, coincides with a loss of erythroid (Ery) specification. Accordingly the PreMegE population can be prospectively separated into "pro-erythroid" and "pro-megakaryocyte" populations based on Runx1 P2 activity. Comparative gene expression analyses between Runx1 P2+ and P2- populations indicated that levels of CD34 expression could substitute for P2 activity to distinguish these two cell populations in wild type (WT) bone marrow (BM). Prospective isolation of these two populations will enable the further investigation of molecular mechanisms involved in megakaryocytic/erythroid (Mk/Ery) cell fate decisions. Having characterized the extensive activity of P1, we utilized a P1-GFP homozygous mouse model to analyze the impact of the complete absence of Runx1 P1 expression in adult mice and observed strong defects in the T cell lineage. Finally, we investigated how the leukemic fusion protein AML1-ETO9a might influence Runx1 promoter usage. Short-term AML1-ETO9a induction in BM resulted in preferential P2 upregulation, suggesting its expression may be important to establish a pre-leukemic environment. |
| doi_str_mv | 10.1371/journal.pgen.1005814 |
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Leighton</contributor><creatorcontrib>Draper, Julia E ; Sroczynska, Patrycja ; Tsoulaki, Olga ; Leong, Hui Sun ; Fadlullah, Muhammad Z H ; Miller, Crispin ; Kouskoff, Valerie ; Lacaud, Georges ; Grimes, H. Leighton</creatorcontrib><description>The Core Binding Factor (CBF) protein RUNX1 is a master regulator of definitive hematopoiesis, crucial for hematopoietic stem cell (HSC) emergence during ontogeny. RUNX1 also plays vital roles in adult mice, in regulating the correct specification of numerous blood lineages. Akin to the other mammalian Runx genes, Runx1 has two promoters P1 (distal) and P2 (proximal) which generate distinct protein isoforms. The activities and specific relevance of these two promoters in adult hematopoiesis remain to be fully elucidated. Utilizing a dual reporter mouse model we demonstrate that the distal P1 promoter is broadly active in adult hematopoietic stem and progenitor cell (HSPC) populations. By contrast the activity of the proximal P2 promoter is more restricted and its upregulation, in both the immature Lineage- Sca1high cKithigh (LSK) and bipotential Pre-Megakaryocytic/Erythroid Progenitor (PreMegE) populations, coincides with a loss of erythroid (Ery) specification. Accordingly the PreMegE population can be prospectively separated into "pro-erythroid" and "pro-megakaryocyte" populations based on Runx1 P2 activity. Comparative gene expression analyses between Runx1 P2+ and P2- populations indicated that levels of CD34 expression could substitute for P2 activity to distinguish these two cell populations in wild type (WT) bone marrow (BM). Prospective isolation of these two populations will enable the further investigation of molecular mechanisms involved in megakaryocytic/erythroid (Mk/Ery) cell fate decisions. Having characterized the extensive activity of P1, we utilized a P1-GFP homozygous mouse model to analyze the impact of the complete absence of Runx1 P1 expression in adult mice and observed strong defects in the T cell lineage. Finally, we investigated how the leukemic fusion protein AML1-ETO9a might influence Runx1 promoter usage. Short-term AML1-ETO9a induction in BM resulted in preferential P2 upregulation, suggesting its expression may be important to establish a pre-leukemic environment.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1005814</identifier><identifier>PMID: 26808730</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Biology and Life Sciences ; Blood ; Blood platelets ; Bone marrow ; Cell Differentiation - genetics ; Cell Lineage - genetics ; Core Binding Factor Alpha 2 Subunit - biosynthesis ; Core Binding Factor Alpha 2 Subunit - genetics ; Defects ; Embryo, Mammalian ; Experiments ; Flow cytometry ; Gene expression ; Gene Expression Regulation, Developmental ; Genetic aspects ; Health aspects ; Hematopoiesis - genetics ; Hematopoietic Stem Cells ; Leukemia ; Mammals ; Medical research ; Medicine and Health Sciences ; Megakaryocytes - cytology ; Mice ; Observations ; Ontogeny ; People and Places ; Promoter Regions, Genetic ; Proteins ; Research and Analysis Methods ; Rodents ; Stem cells ; Studies ; T-Lymphocytes - metabolism ; Transcription factors</subject><ispartof>PLoS genetics, 2016-01, Vol.12 (1), p.e1005814</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Draper et al 2016 Draper et al</rights><rights>2016 Public Library of Science. 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: Draper JE, Sroczynska P, Tsoulaki O, Leong HS, Fadlullah MZH, Miller C, et al. (2016) RUNX1B Expression Is Highly Heterogeneous and Distinguishes Megakaryocytic and Erythroid Lineage Fate in Adult Mouse Hematopoiesis. 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Leighton</contributor><creatorcontrib>Draper, Julia E</creatorcontrib><creatorcontrib>Sroczynska, Patrycja</creatorcontrib><creatorcontrib>Tsoulaki, Olga</creatorcontrib><creatorcontrib>Leong, Hui Sun</creatorcontrib><creatorcontrib>Fadlullah, Muhammad Z H</creatorcontrib><creatorcontrib>Miller, Crispin</creatorcontrib><creatorcontrib>Kouskoff, Valerie</creatorcontrib><creatorcontrib>Lacaud, Georges</creatorcontrib><title>RUNX1B Expression Is Highly Heterogeneous and Distinguishes Megakaryocytic and Erythroid Lineage Fate in Adult Mouse Hematopoiesis</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>The Core Binding Factor (CBF) protein RUNX1 is a master regulator of definitive hematopoiesis, crucial for hematopoietic stem cell (HSC) emergence during ontogeny. RUNX1 also plays vital roles in adult mice, in regulating the correct specification of numerous blood lineages. Akin to the other mammalian Runx genes, Runx1 has two promoters P1 (distal) and P2 (proximal) which generate distinct protein isoforms. The activities and specific relevance of these two promoters in adult hematopoiesis remain to be fully elucidated. Utilizing a dual reporter mouse model we demonstrate that the distal P1 promoter is broadly active in adult hematopoietic stem and progenitor cell (HSPC) populations. By contrast the activity of the proximal P2 promoter is more restricted and its upregulation, in both the immature Lineage- Sca1high cKithigh (LSK) and bipotential Pre-Megakaryocytic/Erythroid Progenitor (PreMegE) populations, coincides with a loss of erythroid (Ery) specification. Accordingly the PreMegE population can be prospectively separated into "pro-erythroid" and "pro-megakaryocyte" populations based on Runx1 P2 activity. Comparative gene expression analyses between Runx1 P2+ and P2- populations indicated that levels of CD34 expression could substitute for P2 activity to distinguish these two cell populations in wild type (WT) bone marrow (BM). Prospective isolation of these two populations will enable the further investigation of molecular mechanisms involved in megakaryocytic/erythroid (Mk/Ery) cell fate decisions. Having characterized the extensive activity of P1, we utilized a P1-GFP homozygous mouse model to analyze the impact of the complete absence of Runx1 P1 expression in adult mice and observed strong defects in the T cell lineage. Finally, we investigated how the leukemic fusion protein AML1-ETO9a might influence Runx1 promoter usage. Short-term AML1-ETO9a induction in BM resulted in preferential P2 upregulation, suggesting its expression may be important to establish a pre-leukemic environment.</description><subject>Animals</subject><subject>Biology and Life Sciences</subject><subject>Blood</subject><subject>Blood platelets</subject><subject>Bone marrow</subject><subject>Cell Differentiation - genetics</subject><subject>Cell Lineage - genetics</subject><subject>Core Binding Factor Alpha 2 Subunit - biosynthesis</subject><subject>Core Binding Factor Alpha 2 Subunit - genetics</subject><subject>Defects</subject><subject>Embryo, Mammalian</subject><subject>Experiments</subject><subject>Flow cytometry</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Genetic aspects</subject><subject>Health aspects</subject><subject>Hematopoiesis - genetics</subject><subject>Hematopoietic Stem Cells</subject><subject>Leukemia</subject><subject>Mammals</subject><subject>Medical research</subject><subject>Medicine and Health Sciences</subject><subject>Megakaryocytes - cytology</subject><subject>Mice</subject><subject>Observations</subject><subject>Ontogeny</subject><subject>People and Places</subject><subject>Promoter Regions, Genetic</subject><subject>Proteins</subject><subject>Research and Analysis Methods</subject><subject>Rodents</subject><subject>Stem cells</subject><subject>Studies</subject><subject>T-Lymphocytes - metabolism</subject><subject>Transcription factors</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNqVk1Fv0zAQxyMEYmPwDRBEQkLiocWO7dh5mVRGRyt1mzQY4s1ynEvikcaV7aD1lU-Ou3ZTK_EAsiVb59_9z3f2JclrjMaYcPzx1g6uV9141UA_xggxgemT5BgzRkacIvp0b3-UvPD-FiHCRMGfJ0dZLpDgBB0nv69vLn_gT-n0buXAe2P7dO7TmWnabp3OIICzUR_s4FPVV-ln44Ppm8H4Fnx6AY36qdza6nUw-h6YunVonTVVujA9qAbScxUgNX06qYYupBdRCaLwUgW7sga88S-TZ7XqPLzarSfJzfn029lstLj6Mj-bLEY6z1kYMZqTMhOclliAKBjnkOFaM065ViLLqozWGgiiCueMEK54STWIkhaKVTRD5CR5u9VdddbLXfm8xDynhFHBWSTmW6Ky6launFnG5KRVRt4brGukcjHTDmSJMlaRqlCCVrTmqqgrjPK8BpyJmhcQtU530YZyCZWGPjjVHYgenvSmlY39JSnP8hxtLvNuK9CoGM_0tY2YXhqv5YQyEV8wzkiN_0LFUcHSaNtDbaL9wOHDgUNkAtyFRg3ey_nX6_9gL_-dvfp-yL7fY1tQXWi97YYQv58_BOkW1M5676B-rB9GctMFD88oN10gd10Q3d7s1_7R6eHbkz-aHAMO</recordid><startdate>20160101</startdate><enddate>20160101</enddate><creator>Draper, Julia E</creator><creator>Sroczynska, Patrycja</creator><creator>Tsoulaki, Olga</creator><creator>Leong, Hui Sun</creator><creator>Fadlullah, Muhammad Z H</creator><creator>Miller, Crispin</creator><creator>Kouskoff, Valerie</creator><creator>Lacaud, Georges</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20160101</creationdate><title>RUNX1B Expression Is Highly Heterogeneous and Distinguishes Megakaryocytic and Erythroid Lineage Fate in Adult Mouse Hematopoiesis</title><author>Draper, Julia E ; Sroczynska, Patrycja ; Tsoulaki, Olga ; Leong, Hui Sun ; Fadlullah, Muhammad Z H ; Miller, Crispin ; Kouskoff, Valerie ; Lacaud, Georges</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c665t-5463b2874b18e89577e21fc5747ca822d24fce304a165337a7b4ce8b49a5d4203</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Animals</topic><topic>Biology and Life Sciences</topic><topic>Blood</topic><topic>Blood platelets</topic><topic>Bone marrow</topic><topic>Cell Differentiation - genetics</topic><topic>Cell Lineage - genetics</topic><topic>Core Binding Factor Alpha 2 Subunit - biosynthesis</topic><topic>Core Binding Factor Alpha 2 Subunit - genetics</topic><topic>Defects</topic><topic>Embryo, Mammalian</topic><topic>Experiments</topic><topic>Flow cytometry</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Genetic aspects</topic><topic>Health aspects</topic><topic>Hematopoiesis - genetics</topic><topic>Hematopoietic Stem Cells</topic><topic>Leukemia</topic><topic>Mammals</topic><topic>Medical research</topic><topic>Medicine and Health Sciences</topic><topic>Megakaryocytes - cytology</topic><topic>Mice</topic><topic>Observations</topic><topic>Ontogeny</topic><topic>People and Places</topic><topic>Promoter Regions, Genetic</topic><topic>Proteins</topic><topic>Research and Analysis Methods</topic><topic>Rodents</topic><topic>Stem cells</topic><topic>Studies</topic><topic>T-Lymphocytes - metabolism</topic><topic>Transcription factors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Draper, Julia E</creatorcontrib><creatorcontrib>Sroczynska, Patrycja</creatorcontrib><creatorcontrib>Tsoulaki, Olga</creatorcontrib><creatorcontrib>Leong, Hui Sun</creatorcontrib><creatorcontrib>Fadlullah, Muhammad Z H</creatorcontrib><creatorcontrib>Miller, Crispin</creatorcontrib><creatorcontrib>Kouskoff, Valerie</creatorcontrib><creatorcontrib>Lacaud, Georges</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Draper, Julia E</au><au>Sroczynska, Patrycja</au><au>Tsoulaki, Olga</au><au>Leong, Hui Sun</au><au>Fadlullah, Muhammad Z H</au><au>Miller, Crispin</au><au>Kouskoff, Valerie</au><au>Lacaud, Georges</au><au>Grimes, H. Leighton</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>RUNX1B Expression Is Highly Heterogeneous and Distinguishes Megakaryocytic and Erythroid Lineage Fate in Adult Mouse Hematopoiesis</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2016-01-01</date><risdate>2016</risdate><volume>12</volume><issue>1</issue><spage>e1005814</spage><pages>e1005814-</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>The Core Binding Factor (CBF) protein RUNX1 is a master regulator of definitive hematopoiesis, crucial for hematopoietic stem cell (HSC) emergence during ontogeny. RUNX1 also plays vital roles in adult mice, in regulating the correct specification of numerous blood lineages. Akin to the other mammalian Runx genes, Runx1 has two promoters P1 (distal) and P2 (proximal) which generate distinct protein isoforms. The activities and specific relevance of these two promoters in adult hematopoiesis remain to be fully elucidated. Utilizing a dual reporter mouse model we demonstrate that the distal P1 promoter is broadly active in adult hematopoietic stem and progenitor cell (HSPC) populations. By contrast the activity of the proximal P2 promoter is more restricted and its upregulation, in both the immature Lineage- Sca1high cKithigh (LSK) and bipotential Pre-Megakaryocytic/Erythroid Progenitor (PreMegE) populations, coincides with a loss of erythroid (Ery) specification. Accordingly the PreMegE population can be prospectively separated into "pro-erythroid" and "pro-megakaryocyte" populations based on Runx1 P2 activity. Comparative gene expression analyses between Runx1 P2+ and P2- populations indicated that levels of CD34 expression could substitute for P2 activity to distinguish these two cell populations in wild type (WT) bone marrow (BM). Prospective isolation of these two populations will enable the further investigation of molecular mechanisms involved in megakaryocytic/erythroid (Mk/Ery) cell fate decisions. Having characterized the extensive activity of P1, we utilized a P1-GFP homozygous mouse model to analyze the impact of the complete absence of Runx1 P1 expression in adult mice and observed strong defects in the T cell lineage. Finally, we investigated how the leukemic fusion protein AML1-ETO9a might influence Runx1 promoter usage. Short-term AML1-ETO9a induction in BM resulted in preferential P2 upregulation, suggesting its expression may be important to establish a pre-leukemic environment.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26808730</pmid><doi>10.1371/journal.pgen.1005814</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Biology and Life Sciences Blood Blood platelets Bone marrow Cell Differentiation - genetics Cell Lineage - genetics Core Binding Factor Alpha 2 Subunit - biosynthesis Core Binding Factor Alpha 2 Subunit - genetics Defects Embryo, Mammalian Experiments Flow cytometry Gene expression Gene Expression Regulation, Developmental Genetic aspects Health aspects Hematopoiesis - genetics Hematopoietic Stem Cells Leukemia Mammals Medical research Medicine and Health Sciences Megakaryocytes - cytology Mice Observations Ontogeny People and Places Promoter Regions, Genetic Proteins Research and Analysis Methods Rodents Stem cells Studies T-Lymphocytes - metabolism Transcription factors |
| title | RUNX1B Expression Is Highly Heterogeneous and Distinguishes Megakaryocytic and Erythroid Lineage Fate in Adult Mouse Hematopoiesis |
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