Transcriptional Heterogeneity and Lineage Commitment in Myeloid Progenitors
Within the bone marrow, stem cells differentiate and give rise to diverse blood cell types and functions. Currently, hematopoietic progenitors are defined using surface markers combined with functional assays that are not directly linked with in vivo differentiation potential or gene regulatory mech...
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Published in | Cell Vol. 163; no. 7; pp. 1663 - 1677 |
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Main Authors | , , , , , , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Elsevier Inc
17.12.2015
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Subjects | |
Online Access | Get full text |
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Abstract | Within the bone marrow, stem cells differentiate and give rise to diverse blood cell types and functions. Currently, hematopoietic progenitors are defined using surface markers combined with functional assays that are not directly linked with in vivo differentiation potential or gene regulatory mechanisms. Here, we comprehensively map myeloid progenitor subpopulations by transcriptional sorting of single cells from the bone marrow. We describe multiple progenitor subgroups, showing unexpected transcriptional priming toward seven differentiation fates but no progenitors with a mixed state. Transcriptional differentiation is correlated with combinations of known and previously undefined transcription factors, suggesting that the process is tightly regulated. Histone maps and knockout assays are consistent with early transcriptional priming, while traditional transplantation experiments suggest that in vivo priming may still allow for plasticity given strong perturbations. These data establish a reference model and general framework for studying hematopoiesis at single-cell resolution.
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•Transcriptionally primed single-cell subpopulations in early myeloid progenitors•Transcription factors and epigenetic landscapes that regulate myeloid priming•Mixed lineage states are not observed but appear when regulation is perturbed•New reference model for studying hematopoiesis at single-cell resolution
Single-cell transcriptomic analysis of bone marrow myeloid progenitor populations reveals early transcriptional priming toward seven different fates and absence of progenitors of mixed lineages, challenging the current models of hematopoiesis based on progressive loss of differentiation potential. |
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AbstractList | Within the bone marrow, stem cells differentiate and give rise to diverse blood cell types and functions. Currently, hematopoietic progenitors are defined using surface markers combined with functional assays that are not directly linked with in vivo differentiation potential or gene regulatory mechanisms. Here, we comprehensively map myeloid progenitor subpopulations by transcriptional sorting of single cells from the bone marrow. We describe multiple progenitor subgroups, showing unexpected transcriptional priming toward seven differentiation fates but no progenitors with a mixed state. Transcriptional differentiation is correlated with combinations of known and previously undefined transcription factors, suggesting that the process is tightly regulated. Histone maps and knockout assays are consistent with early transcriptional priming, while traditional transplantation experiments suggest that in vivo priming may still allow for plasticity given strong perturbations. These data establish a reference model and general framework for studying hematopoiesis at single-cell resolution. Within the bone marrow, stem cells differentiate and give rise to diverse blood cell types and functions. Currently, hematopoietic progenitors are defined using surface markers combined with functional assays that are not directly linked with in vivo differentiation potential or gene regulatory mechanisms. Here, we comprehensively map myeloid progenitor subpopulations by transcriptional sorting of single cells from the bone marrow. We describe multiple progenitor subgroups, showing unexpected transcriptional priming toward seven differentiation fates but no progenitors with a mixed state. Transcriptional differentiation is correlated with combinations of known and previously undefined transcription factors, suggesting that the process is tightly regulated. Histone maps and knockout assays are consistent with early transcriptional priming, while traditional transplantation experiments suggest that in vivo priming may still allow for plasticity given strong perturbations. These data establish a reference model and general framework for studying hematopoiesis at single-cell resolution. [Display omitted] •Transcriptionally primed single-cell subpopulations in early myeloid progenitors•Transcription factors and epigenetic landscapes that regulate myeloid priming•Mixed lineage states are not observed but appear when regulation is perturbed•New reference model for studying hematopoiesis at single-cell resolution Single-cell transcriptomic analysis of bone marrow myeloid progenitor populations reveals early transcriptional priming toward seven different fates and absence of progenitors of mixed lineages, challenging the current models of hematopoiesis based on progressive loss of differentiation potential. |
Author | Jaitin, Diego Adhemar Paul, Franziska Weiner, Assaf David, Eyal Schlitzer, Andreas Cohen, Nadav Mildner, Alexander Lara-Astiaso, David Gury, Meital Porse, Bo Torben Giladi, Amir Trumpp, Andreas Winter, Deborah Jung, Steffen Ginhoux, Florent Amit, Ido Lauridsen, Felicia Kathrine Bratt Kenigsberg, Ephraim Arkin, Ya’ara Keren-Shaul, Hadas Haas, Simon Tanay, Amos |
Author_xml | – sequence: 1 givenname: Franziska surname: Paul fullname: Paul, Franziska organization: Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 2 givenname: Ya’ara surname: Arkin fullname: Arkin, Ya’ara organization: Department of Computer Science and Applied Mathematics and Department of Biological Regulation, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 3 givenname: Amir surname: Giladi fullname: Giladi, Amir organization: Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 4 givenname: Diego Adhemar surname: Jaitin fullname: Jaitin, Diego Adhemar organization: Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 5 givenname: Ephraim surname: Kenigsberg fullname: Kenigsberg, Ephraim organization: Department of Computer Science and Applied Mathematics and Department of Biological Regulation, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 6 givenname: Hadas surname: Keren-Shaul fullname: Keren-Shaul, Hadas organization: Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 7 givenname: Deborah surname: Winter fullname: Winter, Deborah organization: Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 8 givenname: David surname: Lara-Astiaso fullname: Lara-Astiaso, David organization: Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 9 givenname: Meital surname: Gury fullname: Gury, Meital organization: Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 10 givenname: Assaf surname: Weiner fullname: Weiner, Assaf organization: Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 11 givenname: Eyal surname: David fullname: David, Eyal organization: Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 12 givenname: Nadav surname: Cohen fullname: Cohen, Nadav organization: Department of Computer Science and Applied Mathematics and Department of Biological Regulation, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 13 givenname: Felicia Kathrine Bratt surname: Lauridsen fullname: Lauridsen, Felicia Kathrine Bratt organization: The Finsen Laboratory, Rigshospitalet, University of Copenhagen, Copenhagen 2200, Denmark – sequence: 14 givenname: Simon surname: Haas fullname: Haas, Simon organization: Division of Stem Cells and Cancer, Deutsches Krebsforschungszentrum (DKFZ), 69120 Heidelberg, Germany – sequence: 15 givenname: Andreas surname: Schlitzer fullname: Schlitzer, Andreas organization: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (A∗STAR), BIOPOLIS 138648, Singapore – sequence: 16 givenname: Alexander surname: Mildner fullname: Mildner, Alexander organization: Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 17 givenname: Florent surname: Ginhoux fullname: Ginhoux, Florent organization: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (A∗STAR), BIOPOLIS 138648, Singapore – sequence: 18 givenname: Steffen surname: Jung fullname: Jung, Steffen organization: Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 19 givenname: Andreas surname: Trumpp fullname: Trumpp, Andreas organization: Division of Stem Cells and Cancer, Deutsches Krebsforschungszentrum (DKFZ), 69120 Heidelberg, Germany – sequence: 20 givenname: Bo Torben surname: Porse fullname: Porse, Bo Torben organization: The Finsen Laboratory, Rigshospitalet, University of Copenhagen, Copenhagen 2200, Denmark – sequence: 21 givenname: Amos surname: Tanay fullname: Tanay, Amos email: amos.tanay@weizmann.ac.il organization: Department of Computer Science and Applied Mathematics and Department of Biological Regulation, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 22 givenname: Ido surname: Amit fullname: Amit, Ido email: ido.amit@weizmann.ac.il organization: Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26627738$$D View this record in MEDLINE/PubMed |
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SubjectTerms | Animals Bone Marrow Transplantation CCAAT-Enhancer-Binding Proteins - genetics Gene Knockout Techniques Hematopoiesis High-Throughput Nucleotide Sequencing Mice Mice, Inbred C57BL Myeloid Progenitor Cells - cytology Myeloid Progenitor Cells - metabolism Sequence Analysis, RNA Single-Cell Analysis Transcription Factors - metabolism Transcriptome |
Title | Transcriptional Heterogeneity and Lineage Commitment in Myeloid Progenitors |
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