ArticleNature communications2021
Niche derived netrin-1 regulates hematopoietic stem cell dormancy via its receptor neogenin-1.
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Article in Nature communications, 2021. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 56 papers.
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56 citing papers in PubMed, 84 citations in OpenAlex.
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- Lack of MDA5 delays hematopoietic aging by modulating inflammaging and proteostasis in mice.Nature communications · 2026Article
- Aging-declined RNA exportation impairs hematopoietic stem cells by inducing R-loop.Haematologica · 2026Article
- MAFB regulates hematopoietic stem cell proliferation and maintenance.Scientific reports · 2025Article
- Interactions of Hematopoietic and Associated Mesenchymal Stem Cell Populations in the Bone Marrow Microenvironment, In Vivo and In Vitro Model.International journal of molecular sciences · 2025Review
- Ischemic Injury Drives Nascent Tumor Growth Via Accelerated Hematopoietic Aging.JACC. CardioOncology · 2025Article
- The Function and Regulation of celsr1a in Skeletal Age-associated Homeostasis and Repair in Zebrafish.The journals of gerontology. Series A, Biological sciences and medical sciences · 2025Article
- Function of hematopoiesis and bone marrow niche in inflammation and non-hematopoietic diseases.Life medicine · 2025Review
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- Modulation of bone marrow haematopoietic stem cell activity as a therapeutic strategy after myocardial infarction: a preclinical study.Nature cell biology · 2025Article
- Cannabidiol restores hematopoietic stem cell stemness in mouse through Atf2-Lrp6 axis after acute irradiation.MedComm · 2025Article
- GATA2 mutated allele specific expression is associated with a hyporesponsive state of HSC in GATA2 deficiency syndrome.Blood cancer journal · 2025Article
- Maintenance of hematopoietic stem cells by tyrosine-unphosphorylated STAT5 and JAK inhibition.Blood advances · 2025Article
- Insights from the single-cell level: lineage trajectory and somatic-germline interactions during spermatogenesis in dwarf surfclam Mulinia lateralis.BMC genomics · 2025Article
- "Netrin-slaying nanoparticles: A new frontier in cancer therapy".BBA advances · 2025Review
- The role of the haematopoietic stem cell niche in development and ageing.Nature reviews. Molecular cell biology · 2025Review
- Endothelial heterogeneity in bone marrow: insights across development, adult life and leukemia.Leukemia · 2025Review
- Why an integrated view of gene expression studies on hematopoiesis in mouse aging is better than the sum of their parts.FEBS letters · 2024Review
- YTHDC1-mediated microRNA maturation is essential for hematopoietic stem cells maintenance.Cell death discovery · 2024Article
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Authors and funding
32 authors at 7 institutions in 5 countries.
Simon RendersDivision of Stem Cells and Cancer, German Cancer Research Center (DKFZ) and DKFZ-ZMBH Alliance, 69120, Heidelberg, Germany.
Arthur Flohr Svendsen *Laboratory of Ageing Biology and Stem Cells, European Research Institute for the Biology of Ageing, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands.
Jasper Panten *Division of Stem Cells and Cancer, German Cancer Research Center (DKFZ) and DKFZ-ZMBH Alliance, 69120, Heidelberg, Germany.
Nicolas Rama *Apoptosis, Cancer and Development Laboratory, Equipe labellisée "La Ligue," LabEx DEVweCAN, Institut Convergence Rabelais, Centre de Recherche en Cancérologie de Lyon, INSERM U1052-CNRS UMR5286, Université de Lyon1, Centre Léon Bérard, 69008, Lyon, France.ORCID http://orcid.org/0000-0003-1614-7755
Maria MaryanovichRuth L. and David S. Gottesman Institute for Stem Cell and Regenerative Medicine Research, Albert Einstein College of Medicine, Bronx, NY, USA.ORCID http://orcid.org/0000-0002-2015-0538
Pia SommerkampDivision of Stem Cells and Cancer, German Cancer Research Center (DKFZ) and DKFZ-ZMBH Alliance, 69120, Heidelberg, Germany.
Luisa LadelDivision of Stem Cells and Cancer, German Cancer Research Center (DKFZ) and DKFZ-ZMBH Alliance, 69120, Heidelberg, Germany.
Anna Rita RedavidApoptosis, Cancer and Development Laboratory, Equipe labellisée "La Ligue," LabEx DEVweCAN, Institut Convergence Rabelais, Centre de Recherche en Cancérologie de Lyon, INSERM U1052-CNRS UMR5286, Université de Lyon1, Centre Léon Bérard, 69008, Lyon, France.
Benjamin GibertApoptosis, Cancer and Development Laboratory, Equipe labellisée "La Ligue," LabEx DEVweCAN, Institut Convergence Rabelais, Centre de Recherche en Cancérologie de Lyon, INSERM U1052-CNRS UMR5286, Université de Lyon1, Centre Léon Bérard, 69008, Lyon, France.ORCID http://orcid.org/0000-0002-5295-3124
Seka LazareLaboratory of Ageing Biology and Stem Cells, European Research Institute for the Biology of Ageing, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands.
Benjamin DucarougeApoptosis, Cancer and Development Laboratory, Equipe labellisée "La Ligue," LabEx DEVweCAN, Institut Convergence Rabelais, Centre de Recherche en Cancérologie de Lyon, INSERM U1052-CNRS UMR5286, Université de Lyon1, Centre Léon Bérard, 69008, Lyon, France.
Katharina SchönbergerMax Planck Institute of Immunobiology and Epigenetics, 79108, Freiburg, Germany.
Andreas NarrDivision of Stem Cells and Cancer, German Cancer Research Center (DKFZ) and DKFZ-ZMBH Alliance, 69120, Heidelberg, Germany.
Manon TourbezLaboratory of Ageing Biology and Stem Cells, European Research Institute for the Biology of Ageing, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands.
Bertien Dethmers-AusemaLaboratory of Ageing Biology and Stem Cells, European Research Institute for the Biology of Ageing, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands.
Erik ZwartLaboratory of Ageing Biology and Stem Cells, European Research Institute for the Biology of Ageing, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands.ORCID http://orcid.org/0000-0002-4552-003X
Agnes Hotz-WagenblattCore Facility Omics IT and Data Management, German Cancer Research Center (DKFZ), Heidelberg, Germany.
Dachuan ZhangRuth L. and David S. Gottesman Institute for Stem Cell and Regenerative Medicine Research, Albert Einstein College of Medicine, Bronx, NY, USA.ORCID http://orcid.org/0000-0002-1746-275X
Claudia KornWellcome Trust/MRC Cambridge Stem Cell Institute, University of Cambridge, Cambridge, CB2 0AH, UK.
Petra ZeisbergerDivision of Stem Cells and Cancer, German Cancer Research Center (DKFZ) and DKFZ-ZMBH Alliance, 69120, Heidelberg, Germany.
Adriana PrzybyllaDivision of Stem Cells and Cancer, German Cancer Research Center (DKFZ) and DKFZ-ZMBH Alliance, 69120, Heidelberg, Germany.
Markus SohnDivision of Stem Cells and Cancer, German Cancer Research Center (DKFZ) and DKFZ-ZMBH Alliance, 69120, Heidelberg, Germany.
Simon Mendez-FerrerWellcome Trust/MRC Cambridge Stem Cell Institute, University of Cambridge, Cambridge, CB2 0AH, UK.ORCID http://orcid.org/0000-0002-9805-9988
Mathias HeikenwälderDivision of Chronic Inflammation and Cancer, German Cancer Research Center Heidelberg (DKFZ), Heidelberg, Germany.ORCID http://orcid.org/0000-0002-3135-2274
Maik BruneDepartment of Internal Medicine I and Clinical Chemistry, Heidelberg University Hospital, Heidelberg, Germany.
Daniel KlimmeckDivision of Stem Cells and Cancer, German Cancer Research Center (DKFZ) and DKFZ-ZMBH Alliance, 69120, Heidelberg, Germany.
Leonid BystrykhLaboratory of Ageing Biology and Stem Cells, European Research Institute for the Biology of Ageing, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands.ORCID http://orcid.org/0000-0001-6924-5602
Paul S FrenetteRuth L. and David S. Gottesman Institute for Stem Cell and Regenerative Medicine Research, Albert Einstein College of Medicine, Bronx, NY, USA.ORCID http://orcid.org/0000-0003-0862-9922
Patrick MehlenApoptosis, Cancer and Development Laboratory, Equipe labellisée "La Ligue," LabEx DEVweCAN, Institut Convergence Rabelais, Centre de Recherche en Cancérologie de Lyon, INSERM U1052-CNRS UMR5286, Université de Lyon1, Centre Léon Bérard, 69008, Lyon, France.
Gerald de HaanLaboratory of Ageing Biology and Stem Cells, European Research Institute for the Biology of Ageing, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands.ORCID http://orcid.org/0000-0001-9706-0138
Nina Cabezas-WallscheidMax Planck Institute of Immunobiology and Epigenetics, 79108, Freiburg, Germany. cabezas@ie-freiburg.mpg.de.ORCID http://orcid.org/0000-0003-0870-0530
Andreas TrumppDivision of Stem Cells and Cancer, German Cancer Research Center (DKFZ) and DKFZ-ZMBH Alliance, 69120, Heidelberg, Germany. a.trumpp@dkfz.de.ORCID http://orcid.org/0000-0002-6212-3466
German Cancer Research Center · DEUniversity Medical Center Groningen · NLUniversité Claude Bernard Lyon 1 · FRAlbert Einstein College of Medicine · USMax Planck Institute of Immunobiology and Epigenetics · DENHS Blood and Transplant · GBHeidelberg University · DE
Funding
In Vivo Sickle Cell Vasoocclusion: Adhesion MechanismsR01HL069438 · NHLBI · MOUNT SINAI SCHOOL OF MEDICINE OF NYU · PI KELLY, LIBUSHA · 2001 to 2024
$9.5MRegulation and function of hematopoietic stem cell nichesR01DK056638 · NIDDK · MOUNT SINAI SCHOOL OF MEDICINE OF NYU · PI GRITSMAN, KIRA · 2000 to 2023
$8.7MIn vivo function of macrophage in healthy and diseased erythropoiesisR01HL116340 · NHLBI · ALBERT EINSTEIN COLLEGE OF MEDICINE, INC · PI FRENETTE, PAUL S · 2012 to 2015
$1.7MCancer Research UK 26670Medical Research Council MC_PC_17230Medical Research Council MR/V005421/1NHLBI NIH HHS R01 HL069438NHLBI NIH HHS R01 HL116340NIDDK NIH HHS R01 DK056638
Abstract
Haematopoietic stem cells (HSCs) are characterized by their self-renewal potential associated to dormancy. Here we identify the cell surface receptor neogenin-1 as specifically expressed in dormant HSCs. Loss of neogenin-1 initially leads to increased HSC expansion but subsequently to loss of self-renewal and premature exhaustion in vivo. Its ligand netrin-1 induces Egr1 expression and maintains quiescence and function of cultured HSCs in a Neo1 dependent manner. Produced by arteriolar endothelial and periarteriolar stromal cells, conditional netrin-1 deletion in the bone marrow niche reduces HSC numbers, quiescence and self-renewal, while overexpression increases quiescence in vivo. Ageing associated bone marrow remodelling leads to the decline of netrin-1 expression in niches and a compensatory but reversible upregulation of neogenin-1 on HSCs. Our study suggests that niche produced netrin-1 preserves HSC quiescence and self-renewal via neogenin-1 function. Decline of netrin-1 production during ageing leads to the gradual decrease of Neo1 mediated HSC self-renewal.
Indexed as
Stem Cell NicheAnimalsArteriolesCell DifferentiationCell ProliferationCellular SenescenceGene DeletionHematopoietic Stem CellsHematopoietic Stem Cell TransplantationMembrane ProteinsMiceMice, Mutant StrainsMice, TransgenicNetrin-1Signal TransductionMembrane ProteinsneogeninNetrin-1
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