Endothelium-derived stromal cells contribute to hematopoietic bone marrow niche formation

Keane Jared Guillaume Kenswil; Paola Pisterzi; Gonzalo Sanchez-Duffhues; Claire van Dijk; Andrea Lolli; Callie Knuth; Byambasuren Vanchin; Adrian Christopher Jaramillo; Remco Michiel Hoogenboezem; Mathijs Arnoud Sanders; Jacqueline Feyen; Tom Cupedo; Ivan G. Costa; Ronghui Li; Eric Monique Johannes Bindels; Kirsten Lodder; Bianca Blom; Pieter Koen Bos; Marie-Jose Goumans; Peter ten Dijke; Eric Farrell; Guido Krenning; Marc Hermanus Gerardus Petrus Raaijmakers

doi:10.1016/j.stem.2021.01.006

Endothelium-derived stromal cells contribute to hematopoietic bone marrow niche formation

Keane Jared Guillaume Kenswil, Paola Pisterzi, Gonzalo Sanchez-Duffhues, Claire van Dijk, Andrea Lolli, Callie Knuth, Byambasuren Vanchin, Adrian Christopher Jaramillo, Remco Michiel Hoogenboezem, Mathijs Arnoud Sanders, Jacqueline Feyen, Tom Cupedo, Ivan G. Costa, Ronghui Li, Eric Monique Johannes Bindels, Kirsten Lodder, Bianca Blom, Pieter Koen Bos, Marie-Jose Goumans, Peter ten DijkeEric Farrell, Guido Krenning, Marc Hermanus Gerardus Petrus Raaijmakers^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

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Abstract

Bone marrow stromal cells (BMSCs) play pivotal roles in tissue maintenance and regeneration. Their origins, however, remain incompletely understood. Here we identify rare LNGFR(+) cells in human fetal and regenerative bone marrow that co-express endothelial and stromal markers. This endothelial subpopulation displays transcriptional reprogramming consistent with endothelial-to-mesenchymal transition (EndoMT) and can generate multipotent stromal cells that reconstitute the bone marrow (BM) niche upon transplantation. Single-cell transcriptomics and lineage tracing in mice confirm robust and sustained contributions of EndoMT to bone precursor and hematopoietic niche pools. Interleukin-33 (IL-33) is overexpressed in subsets of EndoMT cells and drives this conversion process through ST2 receptor signaling. These data reveal generation of tissue-forming BMSCs from mouse and human endothelial cells and may be instructive for approaches to human tissue regeneration.

Original language	English
Pages (from-to)	653-670.e11
Number of pages	29
Journal	Cell stem cell
Volume	28
Issue number	4
Early online date	1-Feb-2021
DOIs	https://doi.org/10.1016/j.stem.2021.01.006
Publication status	Published - 1-Apr-2021

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10.1016/j.stem.2021.01.006

Endothelium-derived stromal cells contribute to hematopoietic bone marrow niche formationFinal publisher's version, 8.08 MBLicence: Taverne

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Kenswil, K. J. G., Pisterzi, P., Sanchez-Duffhues, G., van Dijk, C., Lolli, A., Knuth, C., Vanchin, B., Jaramillo, A. C., Hoogenboezem, R. M., Sanders, M. A., Feyen, J., Cupedo, T., Costa, I. G., Li, R., Bindels, E. M. J., Lodder, K., Blom, B., Bos, P. K., Goumans, M-J., ... Raaijmakers, M. H. G. P. (2021). Endothelium-derived stromal cells contribute to hematopoietic bone marrow niche formation. Cell stem cell, 28(4), 653-670.e11. https://doi.org/10.1016/j.stem.2021.01.006

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title = "Endothelium-derived stromal cells contribute to hematopoietic bone marrow niche formation",

abstract = "Bone marrow stromal cells (BMSCs) play pivotal roles in tissue maintenance and regeneration. Their origins, however, remain incompletely understood. Here we identify rare LNGFR(+) cells in human fetal and regenerative bone marrow that co-express endothelial and stromal markers. This endothelial subpopulation displays transcriptional reprogramming consistent with endothelial-to-mesenchymal transition (EndoMT) and can generate multipotent stromal cells that reconstitute the bone marrow (BM) niche upon transplantation. Single-cell transcriptomics and lineage tracing in mice confirm robust and sustained contributions of EndoMT to bone precursor and hematopoietic niche pools. Interleukin-33 (IL-33) is overexpressed in subsets of EndoMT cells and drives this conversion process through ST2 receptor signaling. These data reveal generation of tissue-forming BMSCs from mouse and human endothelial cells and may be instructive for approaches to human tissue regeneration.",

author = "Kenswil, {Keane Jared Guillaume} and Paola Pisterzi and Gonzalo Sanchez-Duffhues and {van Dijk}, Claire and Andrea Lolli and Callie Knuth and Byambasuren Vanchin and Jaramillo, {Adrian Christopher} and Hoogenboezem, {Remco Michiel} and Sanders, {Mathijs Arnoud} and Jacqueline Feyen and Tom Cupedo and Costa, {Ivan G.} and Ronghui Li and Bindels, {Eric Monique Johannes} and Kirsten Lodder and Bianca Blom and Bos, {Pieter Koen} and Marie-Jose Goumans and {ten Dijke}, Peter and Eric Farrell and Guido Krenning and Raaijmakers, {Marc Hermanus Gerardus Petrus}",

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Kenswil, KJG, Pisterzi, P, Sanchez-Duffhues, G, van Dijk, C, Lolli, A, Knuth, C, Vanchin, B, Jaramillo, AC, Hoogenboezem, RM, Sanders, MA, Feyen, J, Cupedo, T, Costa, IG, Li, R, Bindels, EMJ, Lodder, K, Blom, B, Bos, PK, Goumans, M-J, ten Dijke, P, Farrell, E, Krenning, G & Raaijmakers, MHGP 2021, 'Endothelium-derived stromal cells contribute to hematopoietic bone marrow niche formation', Cell stem cell, vol. 28, no. 4, pp. 653-670.e11. https://doi.org/10.1016/j.stem.2021.01.006

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T1 - Endothelium-derived stromal cells contribute to hematopoietic bone marrow niche formation

AU - Kenswil, Keane Jared Guillaume

AU - Pisterzi, Paola

AU - Sanchez-Duffhues, Gonzalo

AU - van Dijk, Claire

AU - Lolli, Andrea

AU - Knuth, Callie

AU - Vanchin, Byambasuren

AU - Jaramillo, Adrian Christopher

AU - Hoogenboezem, Remco Michiel

AU - Sanders, Mathijs Arnoud

AU - Feyen, Jacqueline

AU - Cupedo, Tom

AU - Costa, Ivan G.

AU - Li, Ronghui

AU - Bindels, Eric Monique Johannes

AU - Lodder, Kirsten

AU - Blom, Bianca

AU - Bos, Pieter Koen

AU - Goumans, Marie-Jose

AU - ten Dijke, Peter

AU - Farrell, Eric

AU - Krenning, Guido

AU - Raaijmakers, Marc Hermanus Gerardus Petrus

PY - 2021/4/1

Y1 - 2021/4/1

N2 - Bone marrow stromal cells (BMSCs) play pivotal roles in tissue maintenance and regeneration. Their origins, however, remain incompletely understood. Here we identify rare LNGFR(+) cells in human fetal and regenerative bone marrow that co-express endothelial and stromal markers. This endothelial subpopulation displays transcriptional reprogramming consistent with endothelial-to-mesenchymal transition (EndoMT) and can generate multipotent stromal cells that reconstitute the bone marrow (BM) niche upon transplantation. Single-cell transcriptomics and lineage tracing in mice confirm robust and sustained contributions of EndoMT to bone precursor and hematopoietic niche pools. Interleukin-33 (IL-33) is overexpressed in subsets of EndoMT cells and drives this conversion process through ST2 receptor signaling. These data reveal generation of tissue-forming BMSCs from mouse and human endothelial cells and may be instructive for approaches to human tissue regeneration.

AB - Bone marrow stromal cells (BMSCs) play pivotal roles in tissue maintenance and regeneration. Their origins, however, remain incompletely understood. Here we identify rare LNGFR(+) cells in human fetal and regenerative bone marrow that co-express endothelial and stromal markers. This endothelial subpopulation displays transcriptional reprogramming consistent with endothelial-to-mesenchymal transition (EndoMT) and can generate multipotent stromal cells that reconstitute the bone marrow (BM) niche upon transplantation. Single-cell transcriptomics and lineage tracing in mice confirm robust and sustained contributions of EndoMT to bone precursor and hematopoietic niche pools. Interleukin-33 (IL-33) is overexpressed in subsets of EndoMT cells and drives this conversion process through ST2 receptor signaling. These data reveal generation of tissue-forming BMSCs from mouse and human endothelial cells and may be instructive for approaches to human tissue regeneration.

U2 - 10.1016/j.stem.2021.01.006

DO - 10.1016/j.stem.2021.01.006

M3 - Article

C2 - 33561425

SN - 1934-5909

VL - 28

SP - 653-670.e11

JO - Cell stem cell

JF - Cell stem cell

IS - 4

ER -