Characterization of Endothelial Cells Associated with Hematopoietic Niche Formation in Humans Identifies IL-33 As an Anabolic Factor

Bone marrow formation requires an orchestrated interplay between osteogenesis, angiogenesis, and hematopoiesis that is thought to be mediated by endothelial cells. The nature of the endothelial cells and the molecular mechanisms underlying these events remain unclear in humans. Here, we identify a s...

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Main Authors: Keane Jared Guillaume Kenswil, Adrian Christopher Jaramillo, Zhen Ping, Si Chen, Remco Michiel Hoogenboezem, Maria Athina Mylona, Maria Niken Adisty, Eric Moniqué Johannes Bindels, Pieter Koen Bos, Hans Stoop, King Hong Lam, Bram van Eerden, Tom Cupedo, Marc Hermanus Gerardus Petrus Raaijmakers
Format: Article
Language:English
Published: Elsevier 2018-01-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124717319071
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author Keane Jared Guillaume Kenswil
Adrian Christopher Jaramillo
Zhen Ping
Si Chen
Remco Michiel Hoogenboezem
Maria Athina Mylona
Maria Niken Adisty
Eric Moniqué Johannes Bindels
Pieter Koen Bos
Hans Stoop
King Hong Lam
Bram van Eerden
Tom Cupedo
Marc Hermanus Gerardus Petrus Raaijmakers
author_facet Keane Jared Guillaume Kenswil
Adrian Christopher Jaramillo
Zhen Ping
Si Chen
Remco Michiel Hoogenboezem
Maria Athina Mylona
Maria Niken Adisty
Eric Moniqué Johannes Bindels
Pieter Koen Bos
Hans Stoop
King Hong Lam
Bram van Eerden
Tom Cupedo
Marc Hermanus Gerardus Petrus Raaijmakers
author_sort Keane Jared Guillaume Kenswil
collection DOAJ
description Bone marrow formation requires an orchestrated interplay between osteogenesis, angiogenesis, and hematopoiesis that is thought to be mediated by endothelial cells. The nature of the endothelial cells and the molecular mechanisms underlying these events remain unclear in humans. Here, we identify a subset of endoglin-expressing endothelial cells enriched in human bone marrow during fetal ontogeny and upon regeneration after chemotherapeutic injury. Comprehensive transcriptional characterization by massive parallel RNA sequencing of these cells reveals a phenotypic and molecular similarity to murine type H endothelium and activation of angiocrine factors implicated in hematopoiesis, osteogenesis, and angiogenesis. Interleukin-33 (IL-33) was significantly overexpressed in these endothelial cells and promoted the expansion of distinct subsets of hematopoietic precursor cells, endothelial cells, as well as osteogenic differentiation. The identification and molecular characterization of these human regeneration-associated endothelial cells is thus anticipated to instruct the discovery of angiocrine factors driving bone marrow formation and recovery after injury.
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spelling doaj.art-a5063066a1904e7097ddea94317be7382022-12-21T21:47:26ZengElsevierCell Reports2211-12472018-01-0122366667810.1016/j.celrep.2017.12.070Characterization of Endothelial Cells Associated with Hematopoietic Niche Formation in Humans Identifies IL-33 As an Anabolic FactorKeane Jared Guillaume Kenswil0Adrian Christopher Jaramillo1Zhen Ping2Si Chen3Remco Michiel Hoogenboezem4Maria Athina Mylona5Maria Niken Adisty6Eric Moniqué Johannes Bindels7Pieter Koen Bos8Hans Stoop9King Hong Lam10Bram van Eerden11Tom Cupedo12Marc Hermanus Gerardus Petrus Raaijmakers13Department of Hematology, Erasmus MC Cancer Institute, Rotterdam 3015CN, the NetherlandsDepartment of Hematology, Erasmus MC Cancer Institute, Rotterdam 3015CN, the NetherlandsDepartment of Hematology, Erasmus MC Cancer Institute, Rotterdam 3015CN, the NetherlandsDepartment of Hematology, Erasmus MC Cancer Institute, Rotterdam 3015CN, the NetherlandsDepartment of Hematology, Erasmus MC Cancer Institute, Rotterdam 3015CN, the NetherlandsDepartment of Hematology, Erasmus MC Cancer Institute, Rotterdam 3015CN, the NetherlandsDepartment of Hematology, Erasmus MC Cancer Institute, Rotterdam 3015CN, the NetherlandsDepartment of Hematology, Erasmus MC Cancer Institute, Rotterdam 3015CN, the NetherlandsDepartment of Orthopaedics, Erasmus MC, 3015 CE Rotterdam, the NetherlandsDepartment of Pathology, Erasmus MC Cancer Institute, Rotterdam 3015CN, the NetherlandsDepartment of Pathology, Erasmus MC Cancer Institute, Rotterdam 3015CN, the NetherlandsDepartment of Internal Medicine, Erasmus MC Cancer Institute, Rotterdam 3015CN, the NetherlandsDepartment of Hematology, Erasmus MC Cancer Institute, Rotterdam 3015CN, the NetherlandsDepartment of Hematology, Erasmus MC Cancer Institute, Rotterdam 3015CN, the NetherlandsBone marrow formation requires an orchestrated interplay between osteogenesis, angiogenesis, and hematopoiesis that is thought to be mediated by endothelial cells. The nature of the endothelial cells and the molecular mechanisms underlying these events remain unclear in humans. Here, we identify a subset of endoglin-expressing endothelial cells enriched in human bone marrow during fetal ontogeny and upon regeneration after chemotherapeutic injury. Comprehensive transcriptional characterization by massive parallel RNA sequencing of these cells reveals a phenotypic and molecular similarity to murine type H endothelium and activation of angiocrine factors implicated in hematopoiesis, osteogenesis, and angiogenesis. Interleukin-33 (IL-33) was significantly overexpressed in these endothelial cells and promoted the expansion of distinct subsets of hematopoietic precursor cells, endothelial cells, as well as osteogenic differentiation. The identification and molecular characterization of these human regeneration-associated endothelial cells is thus anticipated to instruct the discovery of angiocrine factors driving bone marrow formation and recovery after injury.http://www.sciencedirect.com/science/article/pii/S2211124717319071endothelialbone marrownicheregenerationdevelopmenthematopoietic stem/progenitor cellbone formationinterleukin-33
spellingShingle Keane Jared Guillaume Kenswil
Adrian Christopher Jaramillo
Zhen Ping
Si Chen
Remco Michiel Hoogenboezem
Maria Athina Mylona
Maria Niken Adisty
Eric Moniqué Johannes Bindels
Pieter Koen Bos
Hans Stoop
King Hong Lam
Bram van Eerden
Tom Cupedo
Marc Hermanus Gerardus Petrus Raaijmakers
Characterization of Endothelial Cells Associated with Hematopoietic Niche Formation in Humans Identifies IL-33 As an Anabolic Factor
Cell Reports
endothelial
bone marrow
niche
regeneration
development
hematopoietic stem/progenitor cell
bone formation
interleukin-33
title Characterization of Endothelial Cells Associated with Hematopoietic Niche Formation in Humans Identifies IL-33 As an Anabolic Factor
title_full Characterization of Endothelial Cells Associated with Hematopoietic Niche Formation in Humans Identifies IL-33 As an Anabolic Factor
title_fullStr Characterization of Endothelial Cells Associated with Hematopoietic Niche Formation in Humans Identifies IL-33 As an Anabolic Factor
title_full_unstemmed Characterization of Endothelial Cells Associated with Hematopoietic Niche Formation in Humans Identifies IL-33 As an Anabolic Factor
title_short Characterization of Endothelial Cells Associated with Hematopoietic Niche Formation in Humans Identifies IL-33 As an Anabolic Factor
title_sort characterization of endothelial cells associated with hematopoietic niche formation in humans identifies il 33 as an anabolic factor
topic endothelial
bone marrow
niche
regeneration
development
hematopoietic stem/progenitor cell
bone formation
interleukin-33
url http://www.sciencedirect.com/science/article/pii/S2211124717319071
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