Mapping human haematopoietic stem cells from haemogenic endothelium to birth.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
04 2022
Historique:
received: 31 12 2020
accepted: 22 02 2022
pubmed: 15 4 2022
medline: 23 4 2022
entrez: 14 4 2022
Statut: ppublish

Résumé

The ontogeny of human haematopoietic stem cells (HSCs) is poorly defined owing to the inability to identify HSCs as they emerge and mature at different haematopoietic sites

Identifiants

pubmed: 35418685
doi: 10.1038/s41586-022-04571-x
pii: 10.1038/s41586-022-04571-x
pmc: PMC9645817
mid: NIHMS1808640
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

534-540

Subventions

Organisme : NHLBI NIH HHS
ID : R01 HL148714
Pays : United States
Organisme : NHLBI NIH HHS
ID : R35 HL140014
Pays : United States
Organisme : NHLBI NIH HHS
ID : T32 HL086345
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK100959
Pays : United States
Organisme : NHLBI NIH HHS
ID : T32 HL069766
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK125097
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK121557
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA016042
Pays : United States
Organisme : NIAID NIH HHS
ID : P30 AI028697
Pays : United States

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Tavian, M., Hallais, M. F. & Peault, B. Emergence of intraembryonic hematopoietic precursors in the pre-liver human embryo. Development 126, 793–803 (1999).
doi: 10.1242/dev.126.4.793 pubmed: 9895326
Ivanovs, A. et al. Highly potent human hematopoietic stem cells first emerge in the intraembryonic aorta-gonad-mesonephros region. J. Exp. Med. 208, 2417–2427 (2011).
doi: 10.1084/jem.20111688 pubmed: 22042975 pmcid: 3256972
Boisset, J. C. et al. Progressive maturation toward hematopoietic stem cells in the mouse embryo aorta. Blood 125, 465–469 (2015).
doi: 10.1182/blood-2014-07-588954 pubmed: 25301706 pmcid: 4296008
Ivanovs, A. et al. Human haematopoietic stem cell development: from the embryo to the dish. Development 144, 2323–2337 (2017).
doi: 10.1242/dev.134866 pubmed: 28676567
Hadland, B. K. et al. Endothelium and NOTCH specify and amplify aorta-gonad-mesonephros–derived hematopoietic stem cells. J. Clin. Invest. 125, 2032–2045 (2015).
doi: 10.1172/JCI80137 pubmed: 25866967 pmcid: 4463208
Ivanovs, A., Rybtsov, S., Anderson, R. A. & Medvinsky, A. Vast self-renewal potential of human AGM region HSCs dramatically declines in the umbilical cord blood. Stem Cell Rep. 15, 811–816 (2020).
doi: 10.1016/j.stemcr.2020.08.008
Ghosn, E., Yoshimoto, M., Nakauchi, H., Weissman, I. L. & Herzenberg, L. A. Hematopoietic stem cell-independent hematopoiesis and the origins of innate-like B lymphocytes. Development 146, dev170571 (2019).
doi: 10.1242/dev.170571 pubmed: 31371526 pmcid: 6703711
Palis, J. Hematopoietic stem cell-independent hematopoiesis: emergence of erythroid, megakaryocyte, and myeloid potential in the mammalian embryo. FEBS Lett. 590, 3965–3974 (2016).
doi: 10.1002/1873-3468.12459 pubmed: 27790707
Soares-da-Silva, F. et al. Yolk sac, but not hematopoietic stem cell-derived progenitors, sustain erythropoiesis throughout murine embryonic life. J. Exp. Med. 218, e20201729 (2021).
doi: 10.1084/jem.20201729 pubmed: 33566111 pmcid: 7879581
Bian, Z. et al. Deciphering human macrophage development at single-cell resolution. Nature 582, 571–576 (2020).
doi: 10.1038/s41586-020-2316-7 pubmed: 32499656
Ginhoux, F. et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330, 841–845 (2010).
doi: 10.1126/science.1194637 pubmed: 20966214 pmcid: 3719181
Gomez Perdiguero, E. et al. Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature 518, 547–551 (2015).
pubmed: 25470051
Zeng, Y. et al. Single-cell RNA sequencing resolves spatiotemporal development of pre-thymic lymphoid progenitors and thymus organogenesis in human embryos. Immunity 51, 930–948 (2019).
doi: 10.1016/j.immuni.2019.09.008 pubmed: 31604687
Zhou, F. et al. Tracing haematopoietic stem cell formation at single-cell resolution. Nature 533, 487–492 (2016).
doi: 10.1038/nature17997 pubmed: 27225119
Beaudin, A. E. et al. A transient developmental hematopoietic stem cell gives rise to innate-like B and T cells. Cell Stem Cell 19, 768–783 (2016).
doi: 10.1016/j.stem.2016.08.013 pubmed: 27666010 pmcid: 5524382
Zeng, Y. et al. Tracing the first hematopoietic stem cell generation in human embryo by single-cell RNA sequencing. Cell Res. 29, 881–894 (2019).
doi: 10.1038/s41422-019-0228-6 pubmed: 31501518 pmcid: 6888893
Popescu, D.-M. et al. Decoding human fetal liver haematopoiesis. Nature 574, 365–371 (2019).
doi: 10.1038/s41586-019-1652-y pubmed: 31597962 pmcid: 6861135
de Bruijn, M. F., Speck, N. A., Peeters, M. C. & Dzierzak, E. Definitive hematopoietic stem cells first develop within the major arterial regions of the mouse embryo. EMBO J. 19, 2465–2474 (2000).
doi: 10.1093/emboj/19.11.2465 pubmed: 10835345 pmcid: 212758
Gekas, C., Dieterlen-Lievre, F., Orkin, S. H. & Mikkola, H. K. The placenta is a niche for hematopoietic stem cells. Dev. Cell 8, 365–375 (2005).
doi: 10.1016/j.devcel.2004.12.016 pubmed: 15737932
Ottersbach, K. & Dzierzak, E. The murine placenta contains hematopoietic stem cells within the vascular labyrinth region. Dev. Cell 8, 377–387 (2005).
doi: 10.1016/j.devcel.2005.02.001 pubmed: 15737933
Rhodes, K. E. et al. The emergence of hematopoietic stem cells is initiated in the placental vasculature in the absence of circulation. Cell Stem Cell 2, 252–263 (2008).
doi: 10.1016/j.stem.2008.01.001 pubmed: 18371450 pmcid: 2888040
Li, Z. et al. Mouse embryonic head as a site for hematopoietic stem cell development. Cell Stem Cell 11, 663–675 (2012).
doi: 10.1016/j.stem.2012.07.004 pubmed: 23122290
Nakano, H. et al. Haemogenic endocardium contributes to transient definitive haematopoiesis. Nat. Commun. 4, 1564 (2013).
doi: 10.1038/ncomms2569 pubmed: 23463007
Bárcena, A., Muench, M. O., Kapidzic, M. & Fisher, S. J. A new role for the human placenta as a hematopoietic site throughout gestation. Reprod. Sci. 16, 178–187 (2009).
doi: 10.1177/1933719108327621 pubmed: 19208786
Robin, C. et al. Human placenta is a potent hematopoietic niche containing hematopoietic stem and progenitor cells throughout development. Cell Stem Cell 5, 385–395 (2009).
doi: 10.1016/j.stem.2009.08.020 pubmed: 19796619 pmcid: 2812802
Van Handel, B. et al. The first trimester human placenta is a site for terminal maturation of primitive erythroid cells. Blood 116, 3321–3330 (2010).
doi: 10.1182/blood-2010-04-279489 pubmed: 20628147 pmcid: 2995359
Heck, A. M., Ishida, T. & Hadland, B. Location, location, location: how vascular specialization influences hematopoietic fates during development. Front. Cell Dev. Biol. 8, 602617 (2020).
doi: 10.3389/fcell.2020.602617 pubmed: 33282876 pmcid: 7691428
Zovein, A. C. et al. Fate tracing reveals the endothelial origin of hematopoietic stem cells. Cell Stem Cell 3, 625–636 (2008).
doi: 10.1016/j.stem.2008.09.018 pubmed: 19041779 pmcid: 2631552
Zhu, Q. et al. Developmental trajectory of prehematopoietic stem cell formation from endothelium. Blood 136, 845–856 (2020).
doi: 10.1182/blood.2020004801 pubmed: 32392346 pmcid: 7426642
Crosse, E. I. et al. Multi-layered spatial transcriptomics identify secretory factors promoting human hematopoietic stem cell development. Cell Stem Cell 27, 822–839 (2020).
doi: 10.1016/j.stem.2020.08.004 pubmed: 32946788 pmcid: 7671940
Ditadi, A. et al. Human definitive haemogenic endothelium and arterial vascular endothelium represent distinct lineages. Nat. Cell Biol. 17, 580–591 (2015).
doi: 10.1038/ncb3161 pubmed: 25915127 pmcid: 4551438
Dou, D. R. et al. Medial HOXA genes demarcate haematopoietic stem cell fate during human development. Nat. Cell Biol. 18, 595–606 (2016).
doi: 10.1038/ncb3354 pubmed: 27183470 pmcid: 4981340
Ng, E. S. et al. Differentiation of human embryonic stem cells to HOXA
doi: 10.1038/nbt.3702 pubmed: 27748754
Calvanese, V. et al. MLLT3 governs human haematopoietic stem-cell self-renewal and engraftment. Nature 576, 281–286 (2019).
doi: 10.1038/s41586-019-1790-2 pubmed: 31776511 pmcid: 7278275
Kataoka, K. et al. Evi1 is essential for hematopoietic stem cell self-renewal, and its expression marks hematopoietic cells with long-term multilineage repopulating activity. J. Exp. Med. 208, 2403–2416 (2011).
doi: 10.1084/jem.20110447 pubmed: 22084405 pmcid: 3256960
Komorowska, K. et al. Hepatic leukemia factor maintains quiescence of hematopoietic stem cells and protects the stem cell pool during regeneration. Cell Rep. 21, 3514–3523 (2017).
doi: 10.1016/j.celrep.2017.11.084 pubmed: 29262330
Jokubaitis, V. J. et al. Angiotensin-converting enzyme (CD143) marks hematopoietic stem cells in human embryonic, fetal, and adult hematopoietic tissues. Blood 111, 4055–4063 (2008).
doi: 10.1182/blood-2007-05-091710 pubmed: 17993616
Pellin, D. et al. A comprehensive single cell transcriptional landscape of human hematopoietic progenitors. Nat. Commun. 10, 2395 (2019).
doi: 10.1038/s41467-019-10291-0 pubmed: 31160568 pmcid: 6546699
Lehnertz, B. et al. HLF expression defines the human hematopoietic stem cell state. Blood 138, 2642–2654 (2021).
doi: 10.1182/blood.2021010745 pubmed: 34499717
Lee, B. et al. Impaired spermatogenesis and fertility in mice carrying a mutation in the Spink2 gene expressed predominantly in testes. J. Biol. Chem. 286, 29108–29117 (2011).
doi: 10.1074/jbc.M111.244905 pubmed: 21705336 pmcid: 3190718
McKinney-Freeman, S. et al. The transcriptional landscape of hematopoietic stem cell ontogeny. Cell Stem Cell 11, 701–714 (2012).
doi: 10.1016/j.stem.2012.07.018 pubmed: 23122293 pmcid: 3545475
Robin, C. et al. An unexpected role for IL-3 in the embryonic development of hematopoietic stem cells. Dev. Cell 11, 171–180 (2006).
doi: 10.1016/j.devcel.2006.07.002 pubmed: 16890157
Copley, M. R. et al. The Lin28b–let-7–Hmga2 axis determines the higher self-renewal potential of fetal haematopoietic stem cells. Nat. Cell Biol. 15, 916–925 (2013).
doi: 10.1038/ncb2783 pubmed: 23811688
Kieusseian, A., Brunet de la Grange, P., Burlen-Defranoux, O., Godin, I. & Cumano, A. Immature hematopoietic stem cells undergo maturation in the fetal liver. Development 139, 3521–3530 (2012).
doi: 10.1242/dev.079210 pubmed: 22899849
Prashad, S. L. et al. GPI-80 defines self-renewal ability in hematopoietic stem cells during human development. Cell Stem Cell 16, 80–87 (2014).
doi: 10.1016/j.stem.2014.10.020 pubmed: 25465114 pmcid: 4520393
Vanuytsel, K. et al. Multi-modal profiling of human fetal liver hematopoietic stem cells reveals the molecular signature of engraftment. Nat. Commun. 13, 1103 (2022).
Chanda, B., Ditadi, A., Iscove, N. N. & Keller, G. Retinoic acid signaling is essential for embryonic hematopoietic stem cell development. Cell 155, 215–227 (2013).
doi: 10.1016/j.cell.2013.08.055 pubmed: 24074870
Ali, S. et al. The dual function cytokine IL-33 interacts with the transcription factor NF-κB to dampen NF-κB-stimulated gene transcription. J. Immunol. 187, 1609–1616 (2011).
doi: 10.4049/jimmunol.1003080 pubmed: 21734074
Motazedian, A. et al. Multipotent RAG1
doi: 10.1038/s41556-019-0445-8 pubmed: 31907413
Uenishi, G. I. et al. NOTCH signaling specifies arterial-type definitive hemogenic endothelium from human pluripotent stem cells. Nat. Commun. 9, 1828–1828 (2018).
doi: 10.1038/s41467-018-04134-7 pubmed: 29739946 pmcid: 5940870
van Dijk, D. et al. Recovering gene interactions from single-cell data using data diffusion. Cell 174, 716–729 (2018).
doi: 10.1016/j.cell.2018.05.061 pubmed: 29961576 pmcid: 6771278
Kuleshov, M. V. et al. Enrichr: a comprehensive gene set enrichment analysis web server 2016 update. Nucleic Acids Res. 44, W90–W97 (2016).
doi: 10.1093/nar/gkw377 pubmed: 27141961 pmcid: 4987924
Kao, T. et al. GAPTrap: a simple expression system for pluripotent stem cells and their derivatives. Stem Cell Rep. 7, 518–526 (2016).
doi: 10.1016/j.stemcr.2016.07.015
Nafria, M., Bonifer, C., Stanley, E. G., Ng, E. S. & Elefanty, A. G. Protocol for the generation of definitive hematopoietic progenitors from human pluripotent stem cells. STAR Protoc. 1, 100130 (2020).
doi: 10.1016/j.xpro.2020.100130 pubmed: 33377024 pmcid: 7757115
Ma, F. & Pellegrini, M. ACTINN: automated identification of cell types in single cell RNA sequencing. Bioinformatics 36, 533–538 (2020).
pubmed: 31359028

Auteurs

Vincenzo Calvanese (V)

Department of Molecular, Cell and Developmental Biology, University of California Los Angeles, Los Angeles, CA, USA. v.calvanese@ucl.ac.uk.
Eli and Edythe Broad Center for Regenerative Medicine and Stem Cell Research, University of California Los Angeles, Los Angeles, CA, USA. v.calvanese@ucl.ac.uk.
Laboratory for Molecular Cell Biology, University College London, London, UK. v.calvanese@ucl.ac.uk.

Sandra Capellera-Garcia (S)

Department of Molecular, Cell and Developmental Biology, University of California Los Angeles, Los Angeles, CA, USA.
Eli and Edythe Broad Center for Regenerative Medicine and Stem Cell Research, University of California Los Angeles, Los Angeles, CA, USA.

Feiyang Ma (F)

Department of Molecular, Cell and Developmental Biology, University of California Los Angeles, Los Angeles, CA, USA.
Eli and Edythe Broad Center for Regenerative Medicine and Stem Cell Research, University of California Los Angeles, Los Angeles, CA, USA.
Chongqing International Institute for Immunology, Chongqing, China.

Iman Fares (I)

Department of Molecular, Cell and Developmental Biology, University of California Los Angeles, Los Angeles, CA, USA.
Eli and Edythe Broad Center for Regenerative Medicine and Stem Cell Research, University of California Los Angeles, Los Angeles, CA, USA.

Simone Liebscher (S)

Institute of Biomedical Engineering, Department for Medical Technologies and Regenerative Medicine, Eberhard Karls University, Tübingen, Germany.

Elizabeth S Ng (ES)

Murdoch Children's Research Institute, The Royal Children's Hospital, Parkville, Victoria, Australia.

Sophia Ekstrand (S)

Department of Molecular, Cell and Developmental Biology, University of California Los Angeles, Los Angeles, CA, USA.
Eli and Edythe Broad Center for Regenerative Medicine and Stem Cell Research, University of California Los Angeles, Los Angeles, CA, USA.

Júlia Aguadé-Gorgorió (J)

Department of Molecular, Cell and Developmental Biology, University of California Los Angeles, Los Angeles, CA, USA.
Eli and Edythe Broad Center for Regenerative Medicine and Stem Cell Research, University of California Los Angeles, Los Angeles, CA, USA.

Anastasia Vavilina (A)

Department of Molecular, Cell and Developmental Biology, University of California Los Angeles, Los Angeles, CA, USA.
Eli and Edythe Broad Center for Regenerative Medicine and Stem Cell Research, University of California Los Angeles, Los Angeles, CA, USA.

Diane Lefaudeux (D)

Signaling Systems Laboratory, Department of Microbiology Immunology and Molecular Genetics (MIMG), University of California Los Angeles, Los Angeles, CA, USA.
Institute for Quantitative and Computational Biosciences (QCB), University of California Los Angeles, Los Angeles, CA, USA.

Brian Nadel (B)

Department of Molecular, Cell and Developmental Biology, University of California Los Angeles, Los Angeles, CA, USA.

Jacky Y Li (JY)

Murdoch Children's Research Institute, The Royal Children's Hospital, Parkville, Victoria, Australia.

Yanling Wang (Y)

Department of Molecular, Cell and Developmental Biology, University of California Los Angeles, Los Angeles, CA, USA.

Lydia K Lee (LK)

Department of Obstetrics and Gynecology, University of California Los Angeles, Los Angeles, CA, USA.

Reza Ardehali (R)

Eli and Edythe Broad Center for Regenerative Medicine and Stem Cell Research, University of California Los Angeles, Los Angeles, CA, USA.
Department of Medicine/Cardiology, CVRL, University of California Los Angeles, Los Angeles, CA, USA.

M Luisa Iruela-Arispe (ML)

Cell and Developmental Biology, Northwestern University, Feinberg School of Medicine, Chicago, IL, USA.

Matteo Pellegrini (M)

Department of Molecular, Cell and Developmental Biology, University of California Los Angeles, Los Angeles, CA, USA.
Eli and Edythe Broad Center for Regenerative Medicine and Stem Cell Research, University of California Los Angeles, Los Angeles, CA, USA.

Ed G Stanley (EG)

Murdoch Children's Research Institute, The Royal Children's Hospital, Parkville, Victoria, Australia.
Department of Paediatrics, Faculty of Medicine, Dentistry and Health Sciences, University of Melbourne, Parkville, Victoria, Australia.
Department of Anatomy and Developmental Biology, Monash University, Clayton, Victoria, Australia.

Andrew G Elefanty (AG)

Murdoch Children's Research Institute, The Royal Children's Hospital, Parkville, Victoria, Australia.
Department of Paediatrics, Faculty of Medicine, Dentistry and Health Sciences, University of Melbourne, Parkville, Victoria, Australia.
Department of Anatomy and Developmental Biology, Monash University, Clayton, Victoria, Australia.

Katja Schenke-Layland (K)

Institute of Biomedical Engineering, Department for Medical Technologies and Regenerative Medicine, Eberhard Karls University, Tübingen, Germany.
Department of Medicine/Cardiology, CVRL, University of California Los Angeles, Los Angeles, CA, USA.
Cluster of Excellence iFIT (EXC 2180) 'Image-Guided and Functionally Instructed Tumor Therapies', Eberhard Karls University Tübingen, Tübingen, Germany.
NMI Natural and Medical Sciences Institute, University Tübingen, Reutlingen, Germany.

Hanna K A Mikkola (HKA)

Department of Molecular, Cell and Developmental Biology, University of California Los Angeles, Los Angeles, CA, USA. hmikkola@mcdb.ucla.edu.
Eli and Edythe Broad Center for Regenerative Medicine and Stem Cell Research, University of California Los Angeles, Los Angeles, CA, USA. hmikkola@mcdb.ucla.edu.

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