Identification and transcriptome analysis of erythroblastic island macrophages

The erythroblastic island (EBI), composed of a central macrophage and surrounding erythroid cells, was the first hematopoietic niche discovered. The identity of EBI macrophages has thus far remained elusive. Given that Epo is essential for erythropoiesis and that Epor is expressed in numerous nonery...

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Published inBlood Vol. 134; no. 5; pp. 480 - 491
Main Authors Li, Wei, Wang, Yaomei, Zhao, Huizhi, Zhang, Huan, Xu, Yuanlin, Wang, Shihui, Guo, Xinhua, Huang, Yumin, Zhang, Shijie, Han, Yongshuai, Wu, Xianfang, Rice, Charles M., Huang, Gang, Gallagher, Patrick G., Mendelson, Avital, Yazdanbakhsh, Karina, Liu, Jing, Chen, Lixiang, An, Xiuli
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 01.08.2019
American Society of Hematology
Subjects
Animals
Biomarkers
Computational Biology - methods
Erythroblasts - metabolism
Erythropoiesis - genetics
Gene Expression
Gene Expression Profiling
Humans
Immunophenotyping
Macrophages - metabolism
Mice
Monocytes - metabolism
Receptors, Erythropoietin - genetics
Receptors, Erythropoietin - metabolism
Red Cells, Iron, and Erythropoiesis
Stem Cell Niche - genetics
Stress, Physiological
Transcriptome
Online AccessGet full text

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Abstract The erythroblastic island (EBI), composed of a central macrophage and surrounding erythroid cells, was the first hematopoietic niche discovered. The identity of EBI macrophages has thus far remained elusive. Given that Epo is essential for erythropoiesis and that Epor is expressed in numerous nonerythroid cells, we hypothesized that EBI macrophages express Epor so that Epo can act on both erythroid cells and EBI macrophages simultaneously to ensure efficient erythropoiesis. To test this notion, we used Epor-eGFPcre knockin mouse model. We show that in bone marrow (BM) and fetal liver, a subset of macrophages express Epor-eGFP. Imaging flow cytometry analyses revealed that >90% of native EBIs comprised F4/80+Epor-eGFP+ macrophages. Human fetal liver EBIs also comprised EPOR+ macrophages. Gene expression profiles of BM F4/80+Epor-eGFP+ macrophages suggest a specialized function in supporting erythropoiesis. Molecules known to be important for EBI macrophage function such as Vcam1, CD169, Mertk, and Dnase2α were highly expressed in F4/80+Epor-eGFP+ macrophages compared with F4/80+Epor-eGFP− macrophages. Key molecules involved in iron recycling were also highly expressed in BM F4/80+Epor-eGFP+ macrophages, suggesting that EBI macrophages may provide an iron source for erythropoiesis within this niche. Thus, we have characterized EBI macrophages in mouse and man. Our findings provide important resources for future studies of EBI macrophage function during normal as well as disordered erythropoiesis in hematologic diseases such as thalassemia, polycythemia vera, and myelodysplastic syndromes. •EBI macrophages are characterized by the expression of Epor in mouse and man.•Transcriptomes data provide resource for future studies of EBI macrophage function in normal and disordered erythropoiesis. [Display omitted]
AbstractList The erythroblastic island (EBI), composed of a central macrophage and surrounding erythroid cells, was the first hematopoietic niche discovered. The identity of EBI macrophages has thus far remained elusive. Given that Epo is essential for erythropoiesis and that Epor is expressed in numerous nonerythroid cells, we hypothesized that EBI macrophages express Epor so that Epo can act on both erythroid cells and EBI macrophages simultaneously to ensure efficient erythropoiesis. To test this notion, we used Epor-eGFPcre knockin mouse model. We show that in bone marrow (BM) and fetal liver, a subset of macrophages express Epor-eGFP. Imaging flow cytometry analyses revealed that >90% of native EBIs comprised F4/80+Epor-eGFP+ macrophages. Human fetal liver EBIs also comprised EPOR+ macrophages. Gene expression profiles of BM F4/80+Epor-eGFP+ macrophages suggest a specialized function in supporting erythropoiesis. Molecules known to be important for EBI macrophage function such as Vcam1, CD169, Mertk, and Dnase2α were highly expressed in F4/80+Epor-eGFP+ macrophages compared with F4/80+Epor-eGFP− macrophages. Key molecules involved in iron recycling were also highly expressed in BM F4/80+Epor-eGFP+ macrophages, suggesting that EBI macrophages may provide an iron source for erythropoiesis within this niche. Thus, we have characterized EBI macrophages in mouse and man. Our findings provide important resources for future studies of EBI macrophage function during normal as well as disordered erythropoiesis in hematologic diseases such as thalassemia, polycythemia vera, and myelodysplastic syndromes.
The erythroblastic island (EBI), composed of a central macrophage and surrounding erythroid cells, was the first hematopoietic niche discovered. The identity of EBI macrophages has thus far remained elusive. Given that Epo is essential for erythropoiesis and that Epor is expressed in numerous nonerythroid cells, we hypothesized that EBI macrophages express Epor so that Epo can act on both erythroid cells and EBI macrophages simultaneously to ensure efficient erythropoiesis. To test this notion, we used Epor-eGFPcre knockin mouse model. We show that in bone marrow (BM) and fetal liver, a subset of macrophages express Epor-eGFP. Imaging flow cytometry analyses revealed that >90% of native EBIs comprised F4/80+Epor-eGFP+ macrophages. Human fetal liver EBIs also comprised EPOR+ macrophages. Gene expression profiles of BM F4/80+Epor-eGFP+ macrophages suggest a specialized function in supporting erythropoiesis. Molecules known to be important for EBI macrophage function such as Vcam1, CD169, Mertk, and Dnase2α were highly expressed in F4/80+Epor-eGFP+ macrophages compared with F4/80+Epor-eGFP- macrophages. Key molecules involved in iron recycling were also highly expressed in BM F4/80+Epor-eGFP+ macrophages, suggesting that EBI macrophages may provide an iron source for erythropoiesis within this niche. Thus, we have characterized EBI macrophages in mouse and man. Our findings provide important resources for future studies of EBI macrophage function during normal as well as disordered erythropoiesis in hematologic diseases such as thalassemia, polycythemia vera, and myelodysplastic syndromes.The erythroblastic island (EBI), composed of a central macrophage and surrounding erythroid cells, was the first hematopoietic niche discovered. The identity of EBI macrophages has thus far remained elusive. Given that Epo is essential for erythropoiesis and that Epor is expressed in numerous nonerythroid cells, we hypothesized that EBI macrophages express Epor so that Epo can act on both erythroid cells and EBI macrophages simultaneously to ensure efficient erythropoiesis. To test this notion, we used Epor-eGFPcre knockin mouse model. We show that in bone marrow (BM) and fetal liver, a subset of macrophages express Epor-eGFP. Imaging flow cytometry analyses revealed that >90% of native EBIs comprised F4/80+Epor-eGFP+ macrophages. Human fetal liver EBIs also comprised EPOR+ macrophages. Gene expression profiles of BM F4/80+Epor-eGFP+ macrophages suggest a specialized function in supporting erythropoiesis. Molecules known to be important for EBI macrophage function such as Vcam1, CD169, Mertk, and Dnase2α were highly expressed in F4/80+Epor-eGFP+ macrophages compared with F4/80+Epor-eGFP- macrophages. Key molecules involved in iron recycling were also highly expressed in BM F4/80+Epor-eGFP+ macrophages, suggesting that EBI macrophages may provide an iron source for erythropoiesis within this niche. Thus, we have characterized EBI macrophages in mouse and man. Our findings provide important resources for future studies of EBI macrophage function during normal as well as disordered erythropoiesis in hematologic diseases such as thalassemia, polycythemia vera, and myelodysplastic syndromes.
The erythroblastic island (EBI), composed of a central macrophage and surrounding erythroid cells, was the first hematopoietic niche discovered. The identity of EBI macrophages has thus far remained elusive. Given that Epo is essential for erythropoiesis and that Epor is expressed in numerous nonerythroid cells, we hypothesized that EBI macrophages express Epor so that Epo can act on both erythroid cells and EBI macrophages simultaneously to ensure efficient erythropoiesis. To test this notion, we used Epor-eGFPcre knockin mouse model. We show that in bone marrow (BM) and fetal liver, a subset of macrophages express Epor-eGFP. Imaging flow cytometry analyses revealed that >90% of native EBIs comprised F4/80 Epor-eGFP macrophages. Human fetal liver EBIs also comprised EPOR macrophages. Gene expression profiles of BM F4/80 Epor-eGFP macrophages suggest a specialized function in supporting erythropoiesis. Molecules known to be important for EBI macrophage function such as , , , and were highly expressed in F4/80 Epor-eGFP macrophages compared with F4/80 Epor-eGFP macrophages. Key molecules involved in iron recycling were also highly expressed in BM F4/80 Epor-eGFP macrophages, suggesting that EBI macrophages may provide an iron source for erythropoiesis within this niche. Thus, we have characterized EBI macrophages in mouse and man. Our findings provide important resources for future studies of EBI macrophage function during normal as well as disordered erythropoiesis in hematologic diseases such as thalassemia, polycythemia vera, and myelodysplastic syndromes.
The erythroblastic island (EBI), composed of a central macrophage and surrounding erythroid cells, was the first hematopoietic niche discovered. The identity of EBI macrophages has thus far remained elusive. Given that Epo is essential for erythropoiesis and that Epor is expressed in numerous nonerythroid cells, we hypothesized that EBI macrophages express Epor so that Epo can act on both erythroid cells and EBI macrophages simultaneously to ensure efficient erythropoiesis. To test this notion, we used Epor-eGFPcre knockin mouse model. We show that in bone marrow (BM) and fetal liver, a subset of macrophages express Epor-eGFP. Imaging flow cytometry analyses revealed that >90% of native EBIs comprised F4/80+Epor-eGFP+ macrophages. Human fetal liver EBIs also comprised EPOR+ macrophages. Gene expression profiles of BM F4/80+Epor-eGFP+ macrophages suggest a specialized function in supporting erythropoiesis. Molecules known to be important for EBI macrophage function such as Vcam1, CD169, Mertk, and Dnase2α were highly expressed in F4/80+Epor-eGFP+ macrophages compared with F4/80+Epor-eGFP− macrophages. Key molecules involved in iron recycling were also highly expressed in BM F4/80+Epor-eGFP+ macrophages, suggesting that EBI macrophages may provide an iron source for erythropoiesis within this niche. Thus, we have characterized EBI macrophages in mouse and man. Our findings provide important resources for future studies of EBI macrophage function during normal as well as disordered erythropoiesis in hematologic diseases such as thalassemia, polycythemia vera, and myelodysplastic syndromes. •EBI macrophages are characterized by the expression of Epor in mouse and man.•Transcriptomes data provide resource for future studies of EBI macrophage function in normal and disordered erythropoiesis. [Display omitted]
Publisher's Note: There is a Blood Commentary on this article in this issue. EBI macrophages are characterized by the expression of Epor in mouse and man. Transcriptomes data provide resource for future studies of EBI macrophage function in normal and disordered erythropoiesis. The erythroblastic island (EBI), composed of a central macrophage and surrounding erythroid cells, was the first hematopoietic niche discovered. The identity of EBI macrophages has thus far remained elusive. Given that Epo is essential for erythropoiesis and that Epor is expressed in numerous nonerythroid cells, we hypothesized that EBI macrophages express Epor so that Epo can act on both erythroid cells and EBI macrophages simultaneously to ensure efficient erythropoiesis. To test this notion, we used Epor-eGFPcre knockin mouse model. We show that in bone marrow (BM) and fetal liver, a subset of macrophages express Epor-eGFP. Imaging flow cytometry analyses revealed that >90% of native EBIs comprised F4/80 + Epor-eGFP + macrophages. Human fetal liver EBIs also comprised EPOR + macrophages. Gene expression profiles of BM F4/80 + Epor-eGFP + macrophages suggest a specialized function in supporting erythropoiesis. Molecules known to be important for EBI macrophage function such as Vcam1 , CD169 , Mertk , and Dnase2α were highly expressed in F4/80 + Epor-eGFP + macrophages compared with F4/80 + Epor-eGFP − macrophages. Key molecules involved in iron recycling were also highly expressed in BM F4/80 + Epor-eGFP + macrophages, suggesting that EBI macrophages may provide an iron source for erythropoiesis within this niche. Thus, we have characterized EBI macrophages in mouse and man. Our findings provide important resources for future studies of EBI macrophage function during normal as well as disordered erythropoiesis in hematologic diseases such as thalassemia, polycythemia vera, and myelodysplastic syndromes.
Author Wang, Yaomei
Liu, Jing
Xu, Yuanlin
Yazdanbakhsh, Karina
Guo, Xinhua
Li, Wei
Han, Yongshuai
Huang, Yumin
Wu, Xianfang
Zhang, Shijie
Rice, Charles M.
Chen, Lixiang
Zhang, Huan
Zhao, Huizhi
Mendelson, Avital
An, Xiuli
Wang, Shihui
Huang, Gang
Gallagher, Patrick G.
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  surname: Li
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  organization: School of Life Sciences, Zhengzhou University, Zhengzhou, China
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  surname: Wang
  fullname: Wang, Yaomei
  organization: School of Life Sciences, Zhengzhou University, Zhengzhou, China
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  surname: Zhao
  fullname: Zhao, Huizhi
  organization: School of Life Sciences, Zhengzhou University, Zhengzhou, China
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  surname: Zhang
  fullname: Zhang, Huan
  organization: School of Life Sciences, Zhengzhou University, Zhengzhou, China
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  surname: Xu
  fullname: Xu, Yuanlin
  organization: School of Life Sciences, Zhengzhou University, Zhengzhou, China
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  organization: School of Life Sciences, Zhengzhou University, Zhengzhou, China
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  surname: Guo
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  organization: Laboratory of Membrane Biology, New York Blood Center, New York, NY
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  organization: Laboratory of Membrane Biology, New York Blood Center, New York, NY
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  fullname: Zhang, Shijie
  organization: School of Life Sciences, Zhengzhou University, Zhengzhou, China
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  surname: Han
  fullname: Han, Yongshuai
  organization: School of Life Sciences, Zhengzhou University, Zhengzhou, China
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  givenname: Xianfang
  surname: Wu
  fullname: Wu, Xianfang
  organization: Laboratory of Virology and Infectious Disease, The Rockefeller University, New York, NY
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  surname: Rice
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  organization: Laboratory of Virology and Infectious Disease, The Rockefeller University, New York, NY
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  givenname: Gang
  surname: Huang
  fullname: Huang, Gang
  organization: Division of Experimental Hematology and Cancer Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH
– sequence: 14
  givenname: Patrick G.
  surname: Gallagher
  fullname: Gallagher, Patrick G.
  organization: Department of Pediatrics, Pathology and Genetics, Yale University School of Medicine, New Haven, CT
– sequence: 15
  givenname: Avital
  surname: Mendelson
  fullname: Mendelson, Avital
  organization: Laboratory of Complement Biology, New York Blood Center, New York, NY
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  surname: Yazdanbakhsh
  fullname: Yazdanbakhsh, Karina
  organization: Laboratory of Complement Biology, New York Blood Center, New York, NY
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  givenname: Jing
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  organization: Molecular Biology Research Center & Center for Medical Genetics, School of Life Sciences, Central South University, Changsha, China
– sequence: 18
  givenname: Lixiang
  orcidid: 0000-0001-7785-2496
  surname: Chen
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  organization: School of Life Sciences, Zhengzhou University, Zhengzhou, China
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  surname: An
  fullname: An, Xiuli
  email: xan@nybc.org
  organization: School of Life Sciences, Zhengzhou University, Zhengzhou, China
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31101625$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright 2019 American Society of Hematology
2019 by The American Society of Hematology.
2019 by The American Society of Hematology 2019
Copyright_xml – notice: 2019 American Society of Hematology
– notice: 2019 by The American Society of Hematology.
– notice: 2019 by The American Society of Hematology 2019
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W.L., Y.W., H. Zhao, and H. Zhang contributed equally to this work.
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Snippet The erythroblastic island (EBI), composed of a central macrophage and surrounding erythroid cells, was the first hematopoietic niche discovered. The identity...
Publisher's Note: There is a Blood Commentary on this article in this issue. EBI macrophages are characterized by the expression of Epor in mouse and man....
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SubjectTerms Animals
Biomarkers
Computational Biology - methods
Erythroblasts - metabolism
Erythropoiesis - genetics
Gene Expression
Gene Expression Profiling
Humans
Immunophenotyping
Macrophages - metabolism
Mice
Monocytes - metabolism
Receptors, Erythropoietin - genetics
Receptors, Erythropoietin - metabolism
Red Cells, Iron, and Erythropoiesis
Stem Cell Niche - genetics
Stress, Physiological
Transcriptome
Title Identification and transcriptome analysis of erythroblastic island macrophages
URI https://dx.doi.org/10.1182/blood.2019000430
https://www.ncbi.nlm.nih.gov/pubmed/31101625
https://www.proquest.com/docview/2232043070
https://pubmed.ncbi.nlm.nih.gov/PMC6676133
Volume 134
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