N-Cadherin-Expressing Bone and Marrow Stromal Progenitor Cells Maintain Reserve Hematopoietic Stem Cells

Regulation of hematopoietic stem cells (HSCs) by bone marrow (BM) niches has been extensively studied; however, whether and how HSC subpopulations are distinctively regulated by BM niches remain unclear. Here, we functionally distinguished reserve HSCs (rHSCs) from primed HSCs (pHSCs) based on their...

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Published inCell reports (Cambridge) Vol. 26; no. 3; pp. 652 - 669.e6
Main Authors Zhao, Meng, Tao, Fang, Venkatraman, Aparna, Li, Zhenrui, Smith, Sarah E., Unruh, Jay, Chen, Shiyuan, Ward, Christina, Qian, Pengxu, Perry, John M., Marshall, Heather, Wang, Jinxi, He, Xi C., Li, Linheng
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 15.01.2019
Subjects
Cadherins - metabolism
endosteum
Hematopoietic Stem Cells - physiology
Humans
MSC
N-cadherin
niche
reserve stem cell
Stem Cells - metabolism
stress response
Stromal Cells - metabolism
niche
stress response
MSC
endosteum
N-cadherin
reserve stem cell
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Abstract Regulation of hematopoietic stem cells (HSCs) by bone marrow (BM) niches has been extensively studied; however, whether and how HSC subpopulations are distinctively regulated by BM niches remain unclear. Here, we functionally distinguished reserve HSCs (rHSCs) from primed HSCs (pHSCs) based on their response to chemotherapy and examined how they are dichotomously regulated by BM niches. Both pHSCs and rHSCs supported long-term hematopoiesis in homeostasis; however, pHSCs were sensitive but rHSCs were resistant to chemotherapy. Surviving rHSCs restored the HSC pool and supported hematopoietic regeneration after chemotherapy. The rHSCs were preferentially maintained in the endosteal region that enriches N-cadherin+ (N-cad+) bone-lining cells in homeostasis and post-chemotherapy. N-cad+ cells were functional bone and marrow stromal progenitor cells (BMSPCs), giving rise to osteoblasts, adipocytes, and chondrocytes in vitro and in vivo. Finally, ablation of N-cad+ niche cells or deletion of SCF from N-cad+ niche cells impaired rHSC maintenance during homeostasis and regeneration. [Display omitted] •rHSC and pHSCs are distinguished by their resistance or sensitivity to chemotherapy•pHSCs in the perivascular niche are largely eliminated by chemotherapy•rHSCs are maintained by N-cad+ cells and restore the HSC pool after chemotherapy•N-cad+ BMSPCs expand and produce SCF and other cytokines for rHSCs upon stress Zhao et al. demonstrate that blood-forming stem cells have a back-up system in stressed condition. Both reserve and active stem cells are maintained in the bone marrow by specific niches. While the latter are chemo-sensitive, the former survive and restore stem cells, and thereby generate the blood system.
AbstractList Regulation of hematopoietic stem cells (HSCs) by bone marrow (BM) niches has been extensively studied; however, whether and how HSC subpopulations are distinctively regulated by BM niches remain unclear. Here, we functionally distinguished reserve HSCs (rHSCs) from primed HSCs (pHSCs) based on their response to chemotherapy and examined how they are dichotomously regulated by BM niches. Both pHSCs and rHSCs supported long-term hematopoiesis in homeostasis; however, pHSCs were sensitive but rHSCs were resistant to chemotherapy. Surviving rHSCs restored the HSC pool and supported hematopoietic regeneration after chemotherapy. The rHSCs were preferentially maintained in the endosteal region that enriches N-cadherin + (N-cad + ) bone-lining cells in homeostasis and post-chemotherapy. N-cad + cells were functional bone and marrow stromal progenitor cells (BMSPCs), giving rise to osteoblasts, adipocytes, and chondrocytes in vitro and in vivo . Finally, ablation of N-cad + niche cells or deletion of SCF from N-cad + niche cells impaired rHSC maintenance during homeostasis and regeneration. Zhao et al. demonstrate that blood-forming stem cells have a back-up system in stressed condition. Both reserve and active stem cells are maintained in the bone marrow by specific niches. While the latter are chemo-sensitive, the former survive and restore stem cells, and thereby generate the blood system.
Regulation of hematopoietic stem cells (HSCs) by bone marrow (BM) niches has been extensively studied; however, whether and how HSC subpopulations are distinctively regulated by BM niches remain unclear. Here, we functionally distinguished reserve HSCs (rHSCs) from primed HSCs (pHSCs) based on their response to chemotherapy and examined how they are dichotomously regulated by BM niches. Both pHSCs and rHSCs supported long-term hematopoiesis in homeostasis; however, pHSCs were sensitive but rHSCs were resistant to chemotherapy. Surviving rHSCs restored the HSC pool and supported hematopoietic regeneration after chemotherapy. The rHSCs were preferentially maintained in the endosteal region that enriches N-cadherin+ (N-cad+) bone-lining cells in homeostasis and post-chemotherapy. N-cad+ cells were functional bone and marrow stromal progenitor cells (BMSPCs), giving rise to osteoblasts, adipocytes, and chondrocytes in vitro and in vivo. Finally, ablation of N-cad+ niche cells or deletion of SCF from N-cad+ niche cells impaired rHSC maintenance during homeostasis and regeneration.Regulation of hematopoietic stem cells (HSCs) by bone marrow (BM) niches has been extensively studied; however, whether and how HSC subpopulations are distinctively regulated by BM niches remain unclear. Here, we functionally distinguished reserve HSCs (rHSCs) from primed HSCs (pHSCs) based on their response to chemotherapy and examined how they are dichotomously regulated by BM niches. Both pHSCs and rHSCs supported long-term hematopoiesis in homeostasis; however, pHSCs were sensitive but rHSCs were resistant to chemotherapy. Surviving rHSCs restored the HSC pool and supported hematopoietic regeneration after chemotherapy. The rHSCs were preferentially maintained in the endosteal region that enriches N-cadherin+ (N-cad+) bone-lining cells in homeostasis and post-chemotherapy. N-cad+ cells were functional bone and marrow stromal progenitor cells (BMSPCs), giving rise to osteoblasts, adipocytes, and chondrocytes in vitro and in vivo. Finally, ablation of N-cad+ niche cells or deletion of SCF from N-cad+ niche cells impaired rHSC maintenance during homeostasis and regeneration.
Regulation of hematopoietic stem cells (HSCs) by bone marrow (BM) niches has been extensively studied; however, whether and how HSC subpopulations are distinctively regulated by BM niches remain unclear. Here, we functionally distinguished reserve HSCs (rHSCs) from primed HSCs (pHSCs) based on their response to chemotherapy and examined how they are dichotomously regulated by BM niches. Both pHSCs and rHSCs supported long-term hematopoiesis in homeostasis; however, pHSCs were sensitive but rHSCs were resistant to chemotherapy. Surviving rHSCs restored the HSC pool and supported hematopoietic regeneration after chemotherapy. The rHSCs were preferentially maintained in the endosteal region that enriches N-cadherin (N-cad ) bone-lining cells in homeostasis and post-chemotherapy. N-cad cells were functional bone and marrow stromal progenitor cells (BMSPCs), giving rise to osteoblasts, adipocytes, and chondrocytes in vitro and in vivo. Finally, ablation of N-cad niche cells or deletion of SCF from N-cad niche cells impaired rHSC maintenance during homeostasis and regeneration.
Regulation of hematopoietic stem cells (HSCs) by bone marrow (BM) niches has been extensively studied; however, whether and how HSC subpopulations are distinctively regulated by BM niches remain unclear. Here, we functionally distinguished reserve HSCs (rHSCs) from primed HSCs (pHSCs) based on their response to chemotherapy and examined how they are dichotomously regulated by BM niches. Both pHSCs and rHSCs supported long-term hematopoiesis in homeostasis; however, pHSCs were sensitive but rHSCs were resistant to chemotherapy. Surviving rHSCs restored the HSC pool and supported hematopoietic regeneration after chemotherapy. The rHSCs were preferentially maintained in the endosteal region that enriches N-cadherin+ (N-cad+) bone-lining cells in homeostasis and post-chemotherapy. N-cad+ cells were functional bone and marrow stromal progenitor cells (BMSPCs), giving rise to osteoblasts, adipocytes, and chondrocytes in vitro and in vivo. Finally, ablation of N-cad+ niche cells or deletion of SCF from N-cad+ niche cells impaired rHSC maintenance during homeostasis and regeneration. [Display omitted] •rHSC and pHSCs are distinguished by their resistance or sensitivity to chemotherapy•pHSCs in the perivascular niche are largely eliminated by chemotherapy•rHSCs are maintained by N-cad+ cells and restore the HSC pool after chemotherapy•N-cad+ BMSPCs expand and produce SCF and other cytokines for rHSCs upon stress Zhao et al. demonstrate that blood-forming stem cells have a back-up system in stressed condition. Both reserve and active stem cells are maintained in the bone marrow by specific niches. While the latter are chemo-sensitive, the former survive and restore stem cells, and thereby generate the blood system.
Author Zhao, Meng
He, Xi C.
Smith, Sarah E.
Li, Linheng
Li, Zhenrui
Marshall, Heather
Perry, John M.
Venkatraman, Aparna
Wang, Jinxi
Tao, Fang
Ward, Christina
Qian, Pengxu
Chen, Shiyuan
Unruh, Jay
AuthorAffiliation 1 Institute of Hematology, the Third Affiliated Hospital of Sun Yat-Sen University; Key Laboratory of Stem Cells and Tissue Engineering Sun Yat-Sen University, Guangzhou 510000, China
6 Children’s Research Institute, Children’s Mercy, Kansas City, MO 64108, USA
7 These authors contributed equally
4 Department of Orthopedic Surgery, University of Kansas Medical Center, Kansas City, KS 66160, USA
5 Center of Stem Cell and Regenerative Medicine, Institute of Hematology, and Bone Marrow Transplantation Center of the First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China 310058
8 Lead Contact
2 Stowers Institute for Medical Research, Kansas City, MO 66110, USA
3 Department of Pathology and Laboratory Medicine, University of Kansas Medical Center, Kansas City, KS 66160, USA
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/30650358$$D View this record in MEDLINE/PubMed
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Copyright 2018 Stowers Institute for Medical Research
Copyright © 2018 Stowers Institute for Medical Research. Published by Elsevier Inc. All rights reserved.
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ISSN 2211-1247
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Fri Jul 11 01:39:32 EDT 2025
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Wed May 17 00:03:08 EDT 2023
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 3
Keywords niche
stress response
MSC
endosteum
N-cadherin
reserve stem cell
Language English
License This is an open access article under the CC BY-NC-ND license.
Copyright © 2018 Stowers Institute for Medical Research. Published by Elsevier Inc. All rights reserved.
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Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
AUTHOR CONTRIBUTIONS
Conceptualization, L.L.; Investigation, M.Z., F.T., A.V., Z.L., P.Q., and H.M.; Methodology, S.E.S.; Software, J.U.; Formal Analysis, S.C. and C.W.; Resources, J.W. and X.C.H.; Writing – Original Draft, M.Z., F.T., and A.V.; Writing – Review & Editing, M.Z., F.T., A.V., J.M.P., and L.L.; Supervision, L.L.
OpenAccessLink https://www.sciencedirect.com/science/article/pii/S2211124718320539
PMID 30650358
PQID 2179417228
PQPubID 23479
ParticipantIDs pubmedcentral_primary_oai_pubmedcentral_nih_gov_6890378
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30849365 - Cell Stem Cell. 2019 Mar 7;24(3):355-356
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Snippet Regulation of hematopoietic stem cells (HSCs) by bone marrow (BM) niches has been extensively studied; however, whether and how HSC subpopulations are...
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SubjectTerms Cadherins - metabolism
endosteum
Hematopoietic Stem Cells - physiology
Humans
MSC
N-cadherin
niche
reserve stem cell
Stem Cells - metabolism
stress response
Stromal Cells - metabolism
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Title N-Cadherin-Expressing Bone and Marrow Stromal Progenitor Cells Maintain Reserve Hematopoietic Stem Cells
URI https://dx.doi.org/10.1016/j.celrep.2018.12.093
https://www.ncbi.nlm.nih.gov/pubmed/30650358
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https://pubmed.ncbi.nlm.nih.gov/PMC6890378
Volume 26
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