Identification of the Common Origins of Osteoclasts, Macrophages, and Dendritic Cells in Human Hematopoiesis

Osteoclasts (OCs) originate from the myeloid cell lineage, but the successive steps in their lineage commitment are ill-defined, especially in humans. To clarify OC origin, we sorted cell populations from pediatric bone marrow (BM) by flow cytometry and assessed their differentiation potential in vi...

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Vydané v:	Stem cell reports Ročník 4; číslo 6; s. 984 - 994
Hlavní autori:	Xiao, Yanling, Zijl, Sebastiaan, Wang, Liqin, de Groot, Daniel C., van Tol, Maarten J., Lankester, Arjan C., Borst, Jannie
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	United States Elsevier Inc 09.06.2015 Elsevier
Predmet:	Antigens, CD34 - metabolism Base Sequence Bone Marrow Cells - cytology Bone Marrow Cells - metabolism CD11b Antigen - metabolism Cell Differentiation Cell Lineage Dendritic Cells - cytology Dendritic Cells - metabolism fms-Like Tyrosine Kinase 3 - metabolism Gene Expression Profiling Hematopoiesis High-Throughput Nucleotide Sequencing Humans Interleukin-3 Receptor alpha Subunit - metabolism Macrophages - cytology Macrophages - metabolism Molecular Sequence Data Osteoclasts - cytology Osteoclasts - metabolism Proto-Oncogene Proteins c-kit - metabolism RNA, Messenger - chemistry RNA, Messenger - metabolism Sequence Analysis, DNA Transcriptome
ISSN:	2213-6711, 2213-6711
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Abstract	Osteoclasts (OCs) originate from the myeloid cell lineage, but the successive steps in their lineage commitment are ill-defined, especially in humans. To clarify OC origin, we sorted cell populations from pediatric bone marrow (BM) by flow cytometry and assessed their differentiation potential in vitro. Within the CD11b−CD34+c-KIT+ BM cell population, OC-differentiation potential was restricted to FLT3+ cells and enriched in an IL3 receptor (R)αhigh subset that constituted less than 0.5% of total BM. These IL3Rαhigh cells also generated macrophages (MΦs) and dendritic cells (DCs) but lacked granulocyte (GR)-differentiation potential, as demonstrated at the clonal level. The IL3Rαlow subset was re-defined as common progenitor of GR, MΦ, OC, and DC (GMODP) and gave rise to the IL3Rαhigh subset that was identified as common progenitor of MΦ, OC, and DC (MODP). Unbiased transcriptome analysis of CD11b−CD34+c-KIT+FLT3+ IL3Rαlow and IL3Rαhigh subsets corroborated our definitions of the GMODP and MODP and their developmental relationship. [Display omitted] •CD34+c-Kit+Flt3+ IL3Rαhigh phenotype identifies human MΦ/OC/DC progenitor (MODP)•CD34+c-Kit+Flt3+ IL3Rαlow phenotype identifies GMODP, oligopotent for GR/MΦ/OC/DC•CD34+c-Kit+Flt3+ IL3Rαlow GMODP is upstream of CD34+c-Kit+Flt3+ IL3Rαhigh MODP•Transcriptome analysis supports definition and relationship of GMODP and MODP In this article, Borst, Xiao, and colleagues identify two hierarchically related hematopoietic progenitors in the human bone marrow that can give rise to osteoclasts, the cells that can resorb bone and are involved in various diseases. They show that osteoclasts share their developmental origin with macrophages and dendritic cells that have important immune regulatory functions.
AbstractList	Osteoclasts (OCs) originate from the myeloid cell lineage, but the successive steps in their lineage commitment are ill-defined, especially in humans. To clarify OC origin, we sorted cell populations from pediatric bone marrow (BM) by flow cytometry and assessed their differentiation potential in vitro. Within the CD11b−CD34+c-KIT+ BM cell population, OC-differentiation potential was restricted to FLT3+ cells and enriched in an IL3 receptor (R)αhigh subset that constituted less than 0.5% of total BM. These IL3Rαhigh cells also generated macrophages (MΦs) and dendritic cells (DCs) but lacked granulocyte (GR)-differentiation potential, as demonstrated at the clonal level. The IL3Rαlow subset was re-defined as common progenitor of GR, MΦ, OC, and DC (GMODP) and gave rise to the IL3Rαhigh subset that was identified as common progenitor of MΦ, OC, and DC (MODP). Unbiased transcriptome analysis of CD11b−CD34+c-KIT+FLT3+ IL3Rαlow and IL3Rαhigh subsets corroborated our definitions of the GMODP and MODP and their developmental relationship. [Display omitted] •CD34+c-Kit+Flt3+ IL3Rαhigh phenotype identifies human MΦ/OC/DC progenitor (MODP)•CD34+c-Kit+Flt3+ IL3Rαlow phenotype identifies GMODP, oligopotent for GR/MΦ/OC/DC•CD34+c-Kit+Flt3+ IL3Rαlow GMODP is upstream of CD34+c-Kit+Flt3+ IL3Rαhigh MODP•Transcriptome analysis supports definition and relationship of GMODP and MODP In this article, Borst, Xiao, and colleagues identify two hierarchically related hematopoietic progenitors in the human bone marrow that can give rise to osteoclasts, the cells that can resorb bone and are involved in various diseases. They show that osteoclasts share their developmental origin with macrophages and dendritic cells that have important immune regulatory functions. Osteoclasts (OCs) originate from the myeloid cell lineage, but the successive steps in their lineage commitment are ill-defined, especially in humans. To clarify OC origin, we sorted cell populations from pediatric bone marrow (BM) by flow cytometry and assessed their differentiation potential in vitro. Within the CD11b(-)CD34(+)c-KIT(+) BM cell population, OC-differentiation potential was restricted to FLT3(+) cells and enriched in an IL3 receptor (R)α(high) subset that constituted less than 0.5% of total BM. These IL3Rα(high) cells also generated macrophages (MΦs) and dendritic cells (DCs) but lacked granulocyte (GR)-differentiation potential, as demonstrated at the clonal level. The IL3Rα(low) subset was re-defined as common progenitor of GR, MΦ, OC, and DC (GMODP) and gave rise to the IL3Rα(high) subset that was identified as common progenitor of MΦ, OC, and DC (MODP). Unbiased transcriptome analysis of CD11b(-)CD34(+)c-KIT(+)FLT3(+) IL3Rα(low) and IL3Rα(high) subsets corroborated our definitions of the GMODP and MODP and their developmental relationship. Osteoclasts (OCs) originate from the myeloid cell lineage, but the successive steps in their lineage commitment are ill-defined, especially in humans. To clarify OC origin, we sorted cell populations from pediatric bone marrow (BM) by flow cytometry and assessed their differentiation potential in vitro. Within the CD11b−CD34+c-KIT+ BM cell population, OC-differentiation potential was restricted to FLT3+ cells and enriched in an IL3 receptor (R)αhigh subset that constituted less than 0.5% of total BM. These IL3Rαhigh cells also generated macrophages (MΦs) and dendritic cells (DCs) but lacked granulocyte (GR)-differentiation potential, as demonstrated at the clonal level. The IL3Rαlow subset was re-defined as common progenitor of GR, MΦ, OC, and DC (GMODP) and gave rise to the IL3Rαhigh subset that was identified as common progenitor of MΦ, OC, and DC (MODP). Unbiased transcriptome analysis of CD11b−CD34+c-KIT+FLT3+ IL3Rαlow and IL3Rαhigh subsets corroborated our definitions of the GMODP and MODP and their developmental relationship. • CD34+c-Kit+Flt3+ IL3Rαhigh phenotype identifies human MΦ/OC/DC progenitor (MODP) • CD34+c-Kit+Flt3+ IL3Rαlow phenotype identifies GMODP, oligopotent for GR/MΦ/OC/DC • CD34+c-Kit+Flt3+ IL3Rαlow GMODP is upstream of CD34+c-Kit+Flt3+ IL3Rαhigh MODP • Transcriptome analysis supports definition and relationship of GMODP and MODP In this article, Borst, Xiao, and colleagues identify two hierarchically related hematopoietic progenitors in the human bone marrow that can give rise to osteoclasts, the cells that can resorb bone and are involved in various diseases. They show that osteoclasts share their developmental origin with macrophages and dendritic cells that have important immune regulatory functions. Osteoclasts (OCs) originate from the myeloid cell lineage, but the successive steps in their lineage commitment are ill-defined, especially in humans. To clarify OC origin, we sorted cell populations from pediatric bone marrow (BM) by flow cytometry and assessed their differentiation potential in vitro. Within the CD11b−CD34+c-KIT+ BM cell population, OC-differentiation potential was restricted to FLT3+ cells and enriched in an IL3 receptor (R)αhigh subset that constituted less than 0.5% of total BM. These IL3Rαhigh cells also generated macrophages (MΦs) and dendritic cells (DCs) but lacked granulocyte (GR)-differentiation potential, as demonstrated at the clonal level. The IL3Rαlow subset was re-defined as common progenitor of GR, MΦ, OC, and DC (GMODP) and gave rise to the IL3Rαhigh subset that was identified as common progenitor of MΦ, OC, and DC (MODP). Unbiased transcriptome analysis of CD11b−CD34+c-KIT+FLT3+ IL3Rαlow and IL3Rαhigh subsets corroborated our definitions of the GMODP and MODP and their developmental relationship. Osteoclasts (OCs) originate from the myeloid cell lineage, but the successive steps in their lineage commitment are ill-defined, especially in humans. To clarify OC origin, we sorted cell populations from pediatric bone marrow (BM) by flow cytometry and assessed their differentiation potential in vitro. Within the CD11b(-)CD34(+)c-KIT(+) BM cell population, OC-differentiation potential was restricted to FLT3(+) cells and enriched in an IL3 receptor (R)α(high) subset that constituted less than 0.5% of total BM. These IL3Rα(high) cells also generated macrophages (MΦs) and dendritic cells (DCs) but lacked granulocyte (GR)-differentiation potential, as demonstrated at the clonal level. The IL3Rα(low) subset was re-defined as common progenitor of GR, MΦ, OC, and DC (GMODP) and gave rise to the IL3Rα(high) subset that was identified as common progenitor of MΦ, OC, and DC (MODP). Unbiased transcriptome analysis of CD11b(-)CD34(+)c-KIT(+)FLT3(+) IL3Rα(low) and IL3Rα(high) subsets corroborated our definitions of the GMODP and MODP and their developmental relationship.Osteoclasts (OCs) originate from the myeloid cell lineage, but the successive steps in their lineage commitment are ill-defined, especially in humans. To clarify OC origin, we sorted cell populations from pediatric bone marrow (BM) by flow cytometry and assessed their differentiation potential in vitro. Within the CD11b(-)CD34(+)c-KIT(+) BM cell population, OC-differentiation potential was restricted to FLT3(+) cells and enriched in an IL3 receptor (R)α(high) subset that constituted less than 0.5% of total BM. These IL3Rα(high) cells also generated macrophages (MΦs) and dendritic cells (DCs) but lacked granulocyte (GR)-differentiation potential, as demonstrated at the clonal level. The IL3Rα(low) subset was re-defined as common progenitor of GR, MΦ, OC, and DC (GMODP) and gave rise to the IL3Rα(high) subset that was identified as common progenitor of MΦ, OC, and DC (MODP). Unbiased transcriptome analysis of CD11b(-)CD34(+)c-KIT(+)FLT3(+) IL3Rα(low) and IL3Rα(high) subsets corroborated our definitions of the GMODP and MODP and their developmental relationship.
Author	Lankester, Arjan C. Xiao, Yanling Wang, Liqin Zijl, Sebastiaan de Groot, Daniel C. van Tol, Maarten J. Borst, Jannie
AuthorAffiliation	1 Division of Immunology, The Netherlands Cancer Institute-Antoni van Leeuwenhoek, Amsterdam 1066 CX, the Netherlands 2 Division of Stem Cell Transplantation, Department of Pediatrics, Leiden University Medical Center, Leiden 2300 RC, the Netherlands
AuthorAffiliation_xml	– name: 2 Division of Stem Cell Transplantation, Department of Pediatrics, Leiden University Medical Center, Leiden 2300 RC, the Netherlands – name: 1 Division of Immunology, The Netherlands Cancer Institute-Antoni van Leeuwenhoek, Amsterdam 1066 CX, the Netherlands
Author_xml	– sequence: 1 givenname: Yanling surname: Xiao fullname: Xiao, Yanling email: y.xiao@nki.nl organization: Division of Immunology, The Netherlands Cancer Institute-Antoni van Leeuwenhoek, Amsterdam 1066 CX, the Netherlands – sequence: 2 givenname: Sebastiaan surname: Zijl fullname: Zijl, Sebastiaan organization: Division of Immunology, The Netherlands Cancer Institute-Antoni van Leeuwenhoek, Amsterdam 1066 CX, the Netherlands – sequence: 3 givenname: Liqin surname: Wang fullname: Wang, Liqin organization: Division of Immunology, The Netherlands Cancer Institute-Antoni van Leeuwenhoek, Amsterdam 1066 CX, the Netherlands – sequence: 4 givenname: Daniel C. surname: de Groot fullname: de Groot, Daniel C. organization: Division of Immunology, The Netherlands Cancer Institute-Antoni van Leeuwenhoek, Amsterdam 1066 CX, the Netherlands – sequence: 5 givenname: Maarten J. surname: van Tol fullname: van Tol, Maarten J. organization: Division of Stem Cell Transplantation, Department of Pediatrics, Leiden University Medical Center, Leiden 2300 RC, the Netherlands – sequence: 6 givenname: Arjan C. surname: Lankester fullname: Lankester, Arjan C. organization: Division of Stem Cell Transplantation, Department of Pediatrics, Leiden University Medical Center, Leiden 2300 RC, the Netherlands – sequence: 7 givenname: Jannie surname: Borst fullname: Borst, Jannie email: j.borst@nki.nl organization: Division of Immunology, The Netherlands Cancer Institute-Antoni van Leeuwenhoek, Amsterdam 1066 CX, the Netherlands
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Snippet	Osteoclasts (OCs) originate from the myeloid cell lineage, but the successive steps in their lineage commitment are ill-defined, especially in humans. To...
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SubjectTerms	Antigens, CD34 - metabolism Base Sequence Bone Marrow Cells - cytology Bone Marrow Cells - metabolism CD11b Antigen - metabolism Cell Differentiation Cell Lineage Dendritic Cells - cytology Dendritic Cells - metabolism fms-Like Tyrosine Kinase 3 - metabolism Gene Expression Profiling Hematopoiesis High-Throughput Nucleotide Sequencing Humans Interleukin-3 Receptor alpha Subunit - metabolism Macrophages - cytology Macrophages - metabolism Molecular Sequence Data Osteoclasts - cytology Osteoclasts - metabolism Proto-Oncogene Proteins c-kit - metabolism RNA, Messenger - chemistry RNA, Messenger - metabolism Sequence Analysis, DNA Transcriptome
Title	Identification of the Common Origins of Osteoclasts, Macrophages, and Dendritic Cells in Human Hematopoiesis
URI	https://dx.doi.org/10.1016/j.stemcr.2015.04.012 https://www.ncbi.nlm.nih.gov/pubmed/26004632 https://www.proquest.com/docview/1687998933 https://pubmed.ncbi.nlm.nih.gov/PMC4471835 https://doaj.org/article/75550d38fe824516a55a24950ce8529f
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