Hematopoietic Stem Cells Are the Major Source of Multilineage Hematopoiesis in Adult Animals
Open accessAbstract
Hematopoietic stem cells (HSCs) sustain long-term reconstitution of hematopoiesis in transplantation recipients, yet their role in the endogenous steady-state hematopoiesis remains unclear. In particular, recent studies suggested that HSCs provide a relatively minor contribution to immune cell development in adults. We directed transgene expression in a fraction of HSCs that maintained reconstituting activity during serial transplantations. Inducible genetic labeling showed that transgene-expressing HSCs gave rise to other phenotypic HSCs, confirming their top position in the differentiation hierarchy. The labeled HSCs rapidly contributed to committed progenitors of all lineages and to mature myeloid cells and lymphocytes, but not to B-1a cells or tissue macrophages. Importantly, labeled HSCs gave rise to more than two-thirds of all myeloid cells and platelets in adult mice, and this contribution could be accelerated by an induced interferon response. Thus, classically defined HSCs maintain immune cell development in the steady state and during systemic cytokine responses.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Direct fluorescent labeling of mouse HSCs under steady state conditions illustrated a significant and continued contribution of HSCs to nearly all steady state hematopoiesis.
“Similarly, direct fluorescent labeling of mouse HSCs under steady state conditions illustrated a significant and continued contribution of HSCs to nearly all steady state hematopoiesis (Chapple et al., 2018; Sawai et al., 2016; Säwen et al., 2018).”
From Unraveling Hematopoiesis through the Lens of Genomics (2020) · cites this paper as Sawai et al., 2016
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
A robust and high-throughput Cre reporting and characterization system for the whole mouse brain
Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., Ng, L. L., Palmiter, R. D., Hawrylycz, M. J., Jones, A. R., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2467 · Cited by 6,907 · see citing works
Kiel, M. J., Yilmaz, Ö. H., Iwashita, T., Yilmaz, O. H., Terhorst, C., & Morrison, S. J. (2005) · Cell · doi:10.1016/j.cell.2005.05.026 · Cited by 3,168 · see citing works
Development of Monocytes, Macrophages, and Dendritic Cells
Geissmann, F., Manz, M. G., Jung, S., Sieweke, M. H., Merad, M., & Ley, K. (2010) · Science · doi:10.1126/science.1178331 · Cited by 3,049 · see citing works
Purification and Characterization of Mouse Hematopoietic Stem Cells
Spangrude, G. J., Heimfeld, S., & Weissman, I. L. (1988) · Science · doi:10.1126/science.2898810 · Cited by 2,889 · see citing works
Wilson, A., Laurenti, E., Oser, G., van der Wath, R. C., Blanco-Bose, W., Jaworski, M., Offner, S., Dunant, C. F., Eshkind, L., Bockamp, E., et al. (2008) · Cell · doi:10.1016/j.cell.2008.10.048 · Cited by 1,908 · see citing works
Monocytes and macrophages: developmental pathways and tissue homeostasis
Ginhoux, F., & Jung, S. (2014) · Nature Reviews Immunology · doi:10.1038/nri3671 · Cited by 1,840 · see citing works
IFNα activates dormant haematopoietic stem cells in vivo
Essers, M. A. G., Offner, S., Blanco-Bose, W. E., Waibler, Z., Kalinke, U., Duchosal, M. A., & Trumpp, A. (2009) · Nature · doi:10.1038/nature07815 · Cited by 1,368 · see citing works
Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches
Ding, L., & Morrison, S. J. (2013) · Nature · doi:10.1038/nature11885 · Cited by 1,286 · see citing works
Arteriolar niches maintain haematopoietic stem cell quiescence
Kunisaki, Y., Bruns, I., Scheiermann, C., Ahmed, J. U., Pinho, S., Zhang, D., Mizoguchi, T., Wei, Q., Lucas, D., Ito, K., et al. (2013) · Nature · doi:10.1038/nature12612 · Cited by 1,236 · see citing works
Morrison, S. J., & Weissman, I. L. (1994) · Immunity · doi:10.1016/1074-7613(94)90037-x · Cited by 1,116 · see citing works
Cheshier, S. H., Morrison, S. J., Liao, X., & Weissman, I. L. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.6.3120 · Cited by 858 · see citing works
Clonal dynamics of native haematopoiesis
Sun, J., Ramos, A., Chapman, B., Johnnidis, J. B., Le, L., Ho, Y.-J., Klein, A. M., Hofmann, O., & Camargo, F. D. (2014) · Nature · doi:10.1038/nature13824 · Cited by 803 · see citing works
Causes, consequences, and reversal of immune system aging
Montecino-Rodriguez, E., Berent-Maoz, B., & Dorshkind, K. (2013) · Journal of Clinical Investigation · doi:10.1172/jci64096 · Cited by 793 · see citing works
Fundamental properties of unperturbed haematopoiesis from stem cells in vivo
Busch, K., Klapproth, K., Barile, M., Flossdorf, M., Holland-Letz, T., Schlenner, S. M., Reth, M., Höfer, T., & Rodewald, H.-R. (2015) · Nature · doi:10.1038/nature14242 · Cited by 769 · see citing works
Yamamoto, R., Morita, Y., Ooehara, J., Hamanaka, S., Onodera, M., Rudolph, K. L., Ema, H., & Nakauchi, H. (2013) · Cell · doi:10.1016/j.cell.2013.08.007 · Cited by 745 · see citing works
Deep imaging of bone marrow shows non-dividing stem cells are mainly perisinusoidal
Acar, M., Kocherlakota, K. S., Murphy, M. M., Peyer, J. G., Oguro, H., Inra, C. N., Jaiyeola, C., Zhao, Z., Luby‐Phelps, K., & Morrison, S. J. (2015) · Nature · doi:10.1038/nature15250 · Cited by 702 · see citing works
Oguro, H., Ding, L., & Morrison, S. J. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.05.014 · Cited by 657 · see citing works
Platelet-biased stem cells reside at the apex of the haematopoietic stem-cell hierarchy
Sanjuán-Pla, A., Macaulay, I. C., Jensen, C. T., Woll, P. S., Luis, T. C., Mead, A. J., Moore, S., Carella, C., Matsuoka, S., Jones, T., et al. (2013) · Nature · doi:10.1038/nature12495 · Cited by 653 · see citing works
Passegué, E., Wagers, A. J., Giuriato, S., Anderson, W. C., & Weissman, I. L. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20050967 · Cited by 646 · see citing works
Ikuta, K., & Weissman, I. L. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.4.1502 · Cited by 637 · see citing works
Long-Term Propagation of Distinct Hematopoietic Differentiation Programs In Vivo
Dykstra, B. J., Kent, D. G., Bowie, M. B., McCaffrey, L., Hamilton, M. J., Lyons, K., Lee, S.-J., Brinkman, R. R., & Eaves, C. J. (2007) · Cell stem cell · doi:10.1016/j.stem.2007.05.015 · Cited by 632 · see citing works
Exit from dormancy provokes DNA-damage-induced attrition in haematopoietic stem cells
Walter, D., Lier, A., Geiselhart, A., Thalheimer, F. B., Huntscha, S., Sobotta, M. C., Moehrle, B., Brocks, D., Bayindir, I., Kaschutnig, P., et al. (2015) · Nature · doi:10.1038/nature14131 · Cited by 619 · see citing works
Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells
Foudi, A., Hochedlinger, K., Van Buren, D., Schindler, J. W., Jaenisch, R., Carey, V., & Hock, H. (2009) · Nature Biotechnology · doi:10.1038/nbt.1517 · Cited by 586 · see citing works
Distinct Hematopoietic Stem Cell Subtypes Are Differentially Regulated by TGF-β1
Challen, G. A., Boles, N. C., Chambers, S. M., & Goodell, M. A. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.02.002 · Cited by 580 · see citing works
Hematopoietic stem cells: concepts, definitions, and the new reality
Eaves, C. J. (2015) · Blood · doi:10.1182/blood-2014-12-570200 · Cited by 550 · see citing works
Wilson, N. K., Kent, D. G., Buettner, F., Shehata, M., Macaulay, I. C., Calero-Nieto, F. J., Sánchez Castillo, M., Oedekoven, C. A., Diamanti, E., Schulte, R., et al. (2015) · Cell Stem Cell · doi:10.1016/j.stem.2015.04.004 · Cited by 466 · see citing works
Heterogeneity and hierarchy within the most primitive hematopoietic stem cell compartment
Morita, Y., Ema, H., & Nakauchi, H. (2010) · The Journal of Experimental Medicine · doi:10.1084/jem.20091318 · Cited by 456 · see citing works
Haematopoietic stem cells do not asymmetrically segregate chromosomes or retain BrdU
Kiel, M. J., He, S., Ashkenazi, R., Gentry, S. N., Teta, M., Kushner, J. A., Jackson, T. L., & Morrison, S. J. (2007) · Nature · doi:10.1038/nature06115 · Cited by 417 · see citing works
Oestrogen increases haematopoietic stem-cell self-renewal in females and during pregnancy
Nakada, D., Oguro, H., Levi, B. P., Ryan, N., Kitano, A., Saitoh, Y., Takeichi, M., Wendt, G. R., & Morrison, S. J. (2014) · Nature · doi:10.1038/nature12932 · Cited by 409 · see citing works
Making sense of hematopoietic stem cell niches.
Boulais, P., & Frenette, P. (2015) · Blood · doi:10.1182/blood-2014-09-570192 · Cited by 397 · see citing works
B-1 B Cell Development in the Fetus and Adult
Montecino‐Rodriguez, E., & Dorshkind, K. A. (2012) · Immunity · doi:10.1016/j.immuni.2011.11.017 · Cited by 353 · see citing works
Cabezas-Wallscheid, N., Klimmeck, D., Hansson, J., Lipka, D., Reyes, A., Wang, Q., Weichenhan, D., Lier, A., von Paleske, L., Renders, S., et al. (2014) · Cell Stem Cell · doi:10.1016/j.stem.2014.07.005 · Cited by 352 · see citing works
Hoxb5 marks long-term haematopoietic stem cells and reveals a homogenous perivascular niche
Chen, J. Y., Miyanishi, M., Wang, S. K., Yamazaki, S., Sinha, R., Kao, K. S., Seita, J., Sahoo, D., Nakauchi, H., & Weissman, I. L. (2016) · Nature · doi:10.1038/nature16943 · Cited by 345 · see citing works
Shizuru, J. A., Negrin, R. S., & Weissman, I. L. (2002) · Annual Review of Medicine · doi:10.1146/annurev.med.54.101601.152334 · Cited by 337 · see citing works
Kent, D. G., Copley, M. R., Benz, C., Wöhrer, S., Dykstra, B. J., Ma, E., Cheyne, J., Zhao, Y., Bowie, M. B., Zhao, Y. S., et al. (2009) · Blood · doi:10.1182/blood-2008-12-192054 · Cited by 336 · see citing works
Bagger, F. O., Sasivarevic, D., Sohi, S. H., Laursen, L. G., Pundhir, S., Sønderby, C. K., Winther, O., Rapin, N., & Porse, B. T. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1101 · Cited by 330 · see citing works
Balazs, A. B., Fabian, A. J., Esmon, C. T., & Mulligan, R. C. (2005) · Blood · doi:10.1182/blood-2005-06-2249 · Cited by 329 · see citing works
Pietras, E. M., Lakshminarasimhan, R., Techner, J.-M., Fong, S., Flach, J., Binnewies, M., & Passegué, E. (2014) · Journal of Experimental Medicine · doi:10.1084/jem.20131043 · Cited by 323 · see citing works
Benz, C., Copley, M. R., Kent, D. G., Wöhrer, S., Cortés, A., Aghaeepour, N., Ma, E., Mader, H., Rowe, K. M., Day, C. W., et al. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.02.007 · Cited by 322 · see citing works
Differential Expression of Novel Potential Regulators in Hematopoietic Stem Cells
Forsberg, E. C., Prohaska, S. S., Katzman, S. J., Heffner, G. C., Stuart, J. M., & Weissman, I. L. (2005) · PLoS Genetics · doi:10.1371/journal.pgen.0010028 · Cited by 284 · see citing works
Tissue macrophage identity and self‐renewal
Gentek, R., Molawi, K., & Sieweke, M. H. (2014) · Immunological Reviews · doi:10.1111/imr.12224 · Cited by 277 · see citing works
Living and dying for inflammation: neutrophils, eosinophils, basophils
Geering, B., Stoeckle, C., Conus, S., & Simon, H. (2013) · Trends in Immunology · doi:10.1016/j.it.2013.04.002 · Cited by 257 · see citing works
Biasco, L., Pellin, D., Scala, S., Dionisio, F., Basso-Ricci, L., Leonardelli, L., Scaramuzza, S., Baricordi, C., Ferrua, F., Cicalese, M. P., et al. (2016) · Cell stem cell · doi:10.1016/j.stem.2016.04.016 · Cited by 243 · see citing works
Fgd5 identifies hematopoietic stem cells in the murine bone marrow
Gazit, R., Mandal, P. K., Ebina, W., Ben‐Zvi, A., Nombela‐Arrieta, C., Silberstein, L. E., & Rossi, D. J. (2014) · The Journal of Experimental Medicine · doi:10.1084/jem.20130428 · Cited by 194 · see citing works
Kataoka, K., Sato, T., Yoshimi, A., Goyama, S., Tsuruta-Kishino, T., Kobayashi, H., Shimabe, M., Arai, S., Nakagawa, M. M., Imai, Y., et al. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20110447 · Cited by 192 · see citing works
Aging-Induced Stem Cell Mutations as Drivers for Disease and Cancer
Adams, P. D., Jasper, H., & Rudolph, K. L. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.05.002 · Cited by 179 · see citing works
Sánchez-Aguilera, A., Arranz, L., Martı́n-Pérez, D., García-García, A., Stavropoulou, V., Kubovcakova, L., Isern, J., Martín-Salamanca, S., Langa, X., Skoda, R., et al. (2014) · Cell Stem Cell · doi:10.1016/j.stem.2014.11.002 · Cited by 128 · see citing works
Molecular Signatures of Quiescent, Mobilized and Leukemia-Initiating Hematopoietic Stem Cells
Forsberg, E. C., Passegué, E., Prohaska, S. S., Wagers, A. J., Koeva, M., Stuart, J. M., & Weissman, I. L. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008785 · Cited by 127 · see citing works
Serial bone marrow sampling for long-term follow up of human hematopoiesis in NOD/SCID mice.
Verlinden, S. F. F., van Es, H. H. G., & van Bekkum, D. W. (1998) · PubMed · Cited by 62 · see citing works
Stem cell origin of myelodysplastic syndromes
Elias, H. K., Schinke, C., Bhattacharyya, S., Will, B., Verma, A. K., & Steidl, U. G. (2013) · Oncogene · doi:10.1038/onc.2013.520 · Cited by 39 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Diversity, Mechanisms, and Significance of Macrophage Plasticity
Locati, M., Curtale, G., & Mantovani, A. (2020) · Annual Review of Pathology: Mechanisms of Disease · doi:10.1146/annurev-pathmechdis-012418-012718 · Cited by 2,199 · see citing works
Haematopoietic stem cell activity and interactions with the niche
Pinho, S., & Frenette, P. S. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0103-9 · Cited by 990 · see citing works
Developmental and Functional Heterogeneity of Monocytes
Guilliams, M., Mildner, A., & Yona, S. (2018) · Immunity · doi:10.1016/j.immuni.2018.10.005 · Cited by 973 · see citing works
From haematopoietic stem cells to complex differentiation landscapes
Laurenti, E., & Göttgens, B. (2018) · Nature · doi:10.1038/nature25022 · Cited by 830 · see citing works
Clonal hematopoiesis, with and without candidate driver mutations, is common in the elderly
Zink, F., Stacey, S. N., Norddahl, G. L., Frigge, M. L., Magnusson, O. T., Jonsdottir, I., Thorgeirsson, T. E., Sigurdsson, A., Gudjonsson, S. A., Gudmundsson, J., et al. (2017) · Blood · doi:10.1182/blood-2017-02-769869 · Cited by 777 · see citing works
Adult haematopoietic stem cell niches
Crane, G. M., Jeffery, E., & Morrison, S. J. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2017.53 · Cited by 712 · see citing works
Plasmacytoid Dendritic Cells: Development, Regulation, and Function
Reizis, B. (2019) · Immunity · doi:10.1016/j.immuni.2018.12.027 · Cited by 679 · see citing works
Population dynamics of normal human blood inferred from somatic mutations
Lee-Six, H., Øbro, N. F., Shepherd, M. S., Grossmann, S., Dawson, K., Belmonte, M., Osborne, R. J., Huntly, B. J. P., Martincorena, I., Anderson, E., et al. (2018) · Nature · doi:10.1038/s41586-018-0497-0 · Cited by 604 · see citing works
Tissue-resident macrophages provide a pro-tumorigenic niche to early NSCLC cells
Casanova-Acebes, M., Dalla, E., Leader, A. M., Bérichel, J. L., Nikolić, J., Morales, B. M., Brown, M. K., Chang, C., Troncoso, L., Chen, S. T., et al. (2021) · Nature · doi:10.1038/s41586-021-03651-8 · Cited by 599 · see citing works
Clonal analysis of lineage fate in native haematopoiesis
Rodriguez-Fraticelli, A. E., Wolock, S. L., Weinreb, C. S., Panero, R., Patel, S. H., Jankovic, M., Sun, J., Calogero, R. A., Klein, A. M., & Camargo, F. D. (2018) · Nature · doi:10.1038/nature25168 · Cited by 596 · see citing works
Macrophages and lipid metabolism
Remmerie, A., & Scott, C. L. (2018) · Cellular Immunology · doi:10.1016/j.cellimm.2018.01.020 · Cited by 385 · see citing works
Polylox barcoding reveals haematopoietic stem cell fates realized in vivo
Pei, W., Feyerabend, T. B., Rößler, J., Wang, X., Postrach, D., Busch, K., Rode, I., Klapproth, K., Dietlein, N., Quedenau, C., et al. (2017) · Nature · doi:10.1038/nature23653 · Cited by 412 · see citing works
Does niche competition determine the origin of tissue-resident macrophages?
Guilliams, M., & Scott, C. L. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2017.42 · Cited by 409 · see citing works
Fetal monocytes and the origins of tissue-resident macrophages
Hoeffel, G., & Ginhoux, F. (2018) · Cellular Immunology · doi:10.1016/j.cellimm.2018.01.001 · Cited by 393 · see citing works
Hierarchically related lineage-restricted fates of multipotent haematopoietic stem cells
Carrelha, J., Meng, Y., Kettyle, L. M., Luis, T. C., Norfo, R., Alcolea, V., Boukarabila, H., Grasso, F., Gambardella, A. R., Grover, A., et al. (2018) · Nature · doi:10.1038/nature25455 · Cited by 385 · see citing works
Niches for Hematopoietic Stem Cells and Their Progeny
Wei, Q., & Frenette, P. S. (2018) · Immunity · doi:10.1016/j.immuni.2018.03.024 · Cited by 379 · see citing works
Dasari, A. N., Morris, V. K., Allegra, C. J., Atreya, C. E., Benson, A. B., Boland, P. M., Chung, K., Copur, M. S., Corcoran, R. B., Deming, D. A., et al. (2020) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-020-0392-0 · Cited by 374 · see citing works
Hematopoietic progenitor cells as integrative hubs for adaptation to and fine-tuning of inflammation
Chavakis, T., Mitroulis, I., & Hajishengallis, G. (2019) · Nature Immunology · doi:10.1038/s41590-019-0402-5 · Cited by 319 · see citing works
Niches that regulate stem cells and hematopoiesis in adult bone marrow
Comazzetto, S., Shen, B., & Morrison, S. J. (2021) · Developmental Cell · doi:10.1016/j.devcel.2021.05.018 · Cited by 290 · see citing works
Ural, B. B., Yeung, S. T., Damani‐Yokota, P., Devlin, J. C., de Vries, M., Vera‐Licona, P., Samji, T., Sawai, C. M., Jang, G., Perez, O. A., et al. (2020) · Science Immunology · doi:10.1126/sciimmunol.aax8756 · Cited by 281 · see citing works
New paradigms on hematopoietic stem cell differentiation
Cheng, H., Zheng, Z., & Cheng, T. (2019) · Protein & Cell · doi:10.1007/s13238-019-0633-0 · Cited by 275 · see citing works
Single-cell analysis reveals the continuum of human lympho-myeloid progenitor cells
Karamitros, D., Stoilova, B., Aboukhalil, Z., Hamey, F., Reinisch, A., Samitsch, M., Quek, L. S., Otto, G., Repapi, E., Doondeea, J. B., et al. (2017) · Nature Immunology · doi:10.1038/s41590-017-0001-2 · Cited by 247 · see citing works
Schneider, C., Lee, J., Koga, S., Ricardo-González, R. R., Nussbaum, J. C., Smith, L. K., Villeda, S., Liang, H.-E., & Locksley, R. M. (2019) · Immunity · doi:10.1016/j.immuni.2019.04.019 · Cited by 256 · see citing works
Developmental and Functional Control of Natural Killer Cells by Cytokines
Wu, Y., Tian, Z., & Wei, H. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00930 · Cited by 269 · see citing works
Pattern of human monocyte subpopulations in health and disease
Ożańska, A., Szymczak, D., & Rybka, J. (2020) · Scandinavian Journal of Immunology · doi:10.1111/sji.12883 · Cited by 247 · see citing works
Does tissue imprinting restrict macrophage plasticity?
Guilliams, M., & Svedberg, F. R. (2021) · Nature Immunology · doi:10.1038/s41590-020-00849-2 · Cited by 232 · see citing works
Heterogeneous Responses of Hematopoietic Stem Cells to Inflammatory Stimuli Are Altered with Age
Mann, M., Mehta, A., de Boer, C. G., Kowalczyk, M. S., Lee, K., Haldeman, P., Rogel, N., Knecht, A. R., Farouq, D., Regev, A., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.11.056 · Cited by 188 · see citing works
Hematopoiesis and Cardiovascular Disease
Poller, W. C., Nahrendorf, M., & Świrski, F. K. (2020) · Circulation Research · doi:10.1161/circresaha.120.315895 · Cited by 183 · see citing works
Dysregulated haematopoietic stem cell behaviour in myeloid leukaemogenesis
Yamashita, M., Dellorusso, P. V., Olson, O. C., & Passegue, E. A. (2020) · Nature reviews. Cancer · doi:10.1038/s41568-020-0260-3 · Cited by 182 · see citing works
Pei, W., Shang, F., Wang, X., Fanti, A.-K., Greco, A., Busch, K., Klapproth, K., Zhang, Q., Quedenau, C., Sauer, S., et al. (2020) · Cell stem cell · doi:10.1016/j.stem.2020.07.018 · Cited by 174 · see citing works
Hematopoietic Hierarchy – An Updated Roadmap
Zhang, Y., Gao, S., Xia, J., & Liu, F. (2018) · Trends in Cell Biology · doi:10.1016/j.tcb.2018.06.001 · Cited by 167 · see citing works
Emerging Principles in Myelopoiesis at Homeostasis and during Infection and Inflammation
Schultze, J. L., Mass, E., & Schlitzer, A. (2019) · Immunity · doi:10.1016/j.immuni.2019.01.019 · Cited by 168 · see citing works
Independent origins of fetal liver haematopoietic stem and progenitor cells
Yokomizo, T., Ideue, T., Morino‐Koga, S., Tham, C. Y., Sato, T., Takeda, N., Kubota, Y., Kurokawa, M., Komatsu, N., Ogawa, M., et al. (2022) · Nature · doi:10.1038/s41586-022-05203-0 · Cited by 160 · see citing works
Unraveling Hematopoiesis through the Lens of Genomics
Liggett, L. A., & Sankaran, V. G. (2020) · Cell · doi:10.1016/j.cell.2020.08.030 · Cited by 163 · see citing works
Barrier-tissue macrophages: functional adaptation to environmental challenges
Mowat, A. M., Scott, C. L., & Bain, C. C. (2017) · Nature Medicine · doi:10.1038/nm.4430 · Cited by 155 · see citing works
Haematopoietic stem cells: past, present and future
Ng, A. P., & Alexander, W. S. (2017) · Cell Death Discovery · doi:10.1038/cddiscovery.2017.2 · Cited by 154 · see citing works
Deciphering cell states and genealogies of human haematopoiesis
Weng, C., Yu, F., Yang, D., Poeschla, M., Liggett, L. A., Jones, M. G., Qiu, X., Wahlster, L., Caulier, A., Hussmann, J. A., et al. (2024) · Nature · doi:10.1038/s41586-024-07066-z · Cited by 150 · see citing works
Plasmacytoid dendritic cell biology and its role in immune‐mediated diseases
Ye, Y., Gaugler, B., Mohty, M., & Malard, F. (2020) · Clinical & Translational Immunology · doi:10.1002/cti2.1139 · Cited by 147 · see citing works
Ca2+–mitochondria axis drives cell division in hematopoietic stem cells
Umemoto, T., Hashimoto, M., Matsumura, T., Nakamura‐Ishizu, A., & Suda, T. (2018) · The Journal of Experimental Medicine · doi:10.1084/jem.20180421 · Cited by 148 · see citing works
Expansible residence decentralizes immune homeostasis
Wijeyesinghe, S. P., Beura, L., Pierson, M. J., Stolley, J., Adam, O. A., Ruscher, R., Steinert, E. M., Rosato, P. C., Vezys, V., & Masopust, D. (2021) · Nature · doi:10.1038/s41586-021-03351-3 · Cited by 113 · see citing works
Palis, J. (2016) · FEBS Letters · doi:10.1002/1873-3468.12459 · Cited by 132 · see citing works
Granulopoiesis and Neutrophil Homeostasis: A Metabolic, Daily Balancing Act
Yvan‐Charvet, L., & Ng, L. G. (2019) · Trends in Immunology · doi:10.1016/j.it.2019.05.004 · Cited by 130 · see citing works
Haematopoiesis in the era of advanced single-cell technologies
Jacobsen, S. E. W., & Nerlov, C. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0227-8 · Cited by 127 · see citing works
Hepatic Macrophages in Liver Injury
Shan, Z., & Ju, C. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00322 · Cited by 132 · see citing works
Losing Sense of Self and Surroundings: Hematopoietic Stem Cell Aging and Leukemic Transformation
Verovskaya, E. V., Dellorusso, P. V., & Passegue, E. A. (2019) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2019.04.006 · Cited by 122 · see citing works
Immunology of the ageing kidney
Sato, Y., & Yanagita, M. (2019) · Nature Reviews Nephrology · doi:10.1038/s41581-019-0185-9 · Cited by 126 · see citing works
Säwen, P., Eldeeb, M., Erlandsson, E., Kristiansen, T. A., Laterza, C., Kokaia, Z., Karlsson, G., Yuan, J., Soneji, S., Mandal, P. K., et al. (2018) · eLife · doi:10.7554/elife.41258 · Cited by 120 · see citing works
Human Dendritic Cell Subsets, Ontogeny, and Impact on HIV Infection
Rhodes, J. W., Tong, O., Harman, A. N., & Turville, S. G. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01088 · Cited by 117 · see citing works
Niche-specific functional heterogeneity of intestinal resident macrophages
Viola, M. F., & Boeckxstaens, G. E. (2020) · Gut · doi:10.1136/gutjnl-2020-323121 · Cited by 120 · see citing works
Scala, S., Ricci, L. B., Dionisio, F., Pellin, D., Giannelli, S., Salerio, F. A., Leonardelli, L., Cicalese, M. P., Ferrua, F., Aiuti, A., et al. (2018) · Nature Medicine · doi:10.1038/s41591-018-0195-3 · Cited by 111 · see citing works
Epidermal γδ T cells originate from yolk sac hematopoiesis and clonally self-renew in the adult
Gentek, R., Ghigo, C., Hoeffel, G., Jorquera, A., Msallam, R., Wienert, S., Klauschen, F., Ginhoux, F., & Bajénoff, M. (2018) · The Journal of Experimental Medicine · doi:10.1084/jem.20181206 · Cited by 111 · see citing works
Structural organization of the bone marrow and its role in hematopoiesis
Lucas, D. (2020) · Current Opinion in Hematology · doi:10.1097/moh.0000000000000621 · Cited by 108 · see citing works
Clonal lineage tracing reveals shared origin of conventional and plasmacytoid dendritic cells
Feng, J., Pucella, J. N., Jang, G., Alcántara‐Hernández, M., Upadhaya, S., Adams, N. M., Khodadadi‐Jamayran, A., Lau, C. M., Stoeckius, M., Hao, S. P., et al. (2022) · Immunity · doi:10.1016/j.immuni.2022.01.016 · Cited by 106 · see citing works
Non-alcoholic steatohepatitis induces transient changes within the liver macrophage pool
Devisscher, L., Scott, C. L., Lefere, S., Raevens, S., Bogaerts, E., Paridaens, A., Verhelst, X., Geerts, A. M., Guilliams, M., & Vlierberghe, H. V. (2017) · Cellular Immunology · doi:10.1016/j.cellimm.2017.10.006 · Cited by 104 · see citing works
Akinduro, O., Weber, T., Ang, H. Y.-K., Haltalli, M. L. R., Ruivo, N., Duarte, D., Rashidi, N. M., Hawkins, E. D., Duffy, K. R., & Celso, C. L. (2018) · Nature Communications · doi:10.1038/s41467-017-02376-5 · Cited by 95 · see citing works
Bhlhe40 and Bhlhe41 Transcription Factors Regulate Alveolar Macrophage Self‐renewal and Identity
Rauschmeier, R., Gustafsson, C., Reinhardt, A., A‐Gonzalez, N., Tortola, L., Cansever, D., Subramanian, S., Taneja, R., Rossner, M. J., Sieweke, M. H., et al. (2019) · The EMBO Journal · doi:10.15252/embj.2018101233 · Cited by 102 · see citing works
Mechanosensing in macrophages and dendritic cells in steady-state and disease
Lee, M., Du, H., Winer, D. A., Clemente-Casares, X., & Tsai, S. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.1044729 · Cited by 99 · see citing works
Made to order: emergency myelopoiesis and demand-adapted innate immune cell production
Swann, J. W., Olson, O. C., & Passegue, E. A. (2024) · Nature reviews. Immunology · doi:10.1038/s41577-024-00998-7 · Cited by 99 · see citing works
An ERK-Dependent Feedback Mechanism Prevents Hematopoietic Stem Cell Exhaustion
Baumgärtner, C., Toifl, S., Farlik, M., Halbritter, F., Scheicher, R., Fischer, I., Sexl, V., Bock, C., & Baccarini, M. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.05.003 · Cited by 93 · see citing works
Differentiation-based model of hematopoietic stem cell functions and lineage pathways
Höfer, T., & Rodewald, H.-R. (2018) · Blood · doi:10.1182/blood-2018-03-791517 · Cited by 94 · see citing works
Hematopoietic stem cell fate through metabolic control
Ito, K., & Ito, K. (2018) · Experimental Hematology · doi:10.1016/j.exphem.2018.05.005 · Cited by 93 · see citing works
Do haematopoietic stem cells age?
Dorshkind, K. A., Höfer, T., Montecino‐Rodriguez, E., Pioli, P. D., & Rodewald, H.-R. (2019) · Nature reviews. Immunology · doi:10.1038/s41577-019-0236-2 · Cited by 92 · see citing works
Chapple, R. H., Tseng, Y.-J., Hu, T., Kitano, A., Takeichi, M., Hoegenauer, K. A., & Nakada, D. (2018) · Blood Advances · doi:10.1182/bloodadvances.2018016295 · Cited by 90 · see citing works
Grinenko, T., Eugster, A., Thielecke, L., Ramasz, B., Krüger, A., Dietz, S., Glauche, I., Gerbaulet, A., Bonin, M. V., Başak, O., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-04188-7 · Cited by 87 · see citing works
Harnessing Hematopoietic Stem Cell Low Intracellular Calcium Improves Their Maintenance In Vitro
Luchsinger, L. L., Strikoudis, A., Danzl, N. M., Bush, E. C., Finlayson, M. O., Satwani, P., Sykes, M., Yazawa, M., & Snoeck, H. (2019) · Cell stem cell · doi:10.1016/j.stem.2019.05.002 · Cited by 88 · see citing works
Kinetics of adult hematopoietic stem cell differentiation in vivo
Upadhaya, S., Sawai, C. M., Papalexi, E., Rashidfarrokhi, A., Jang, G., Chattopadhyay, P. K., Satija, R., & Reizis, B. (2018) · The Journal of Experimental Medicine · doi:10.1084/jem.20180136 · Cited by 83 · see citing works
Cosgrove, J., Hustin, L., de Boer, R. J., & Perié, L. (2021) · Trends in Immunology · doi:10.1016/j.it.2021.10.006 · Cited by 88 · see citing works
The extracellular matrix of hematopoietic stem cell niches
Lee‐Thedieck, C., Schertl, P., & Klein, G. (2021) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2021.114069 · Cited by 87 · see citing works
Polycomb complexes PRC1 and their function in hematopoiesis
Vidal, M., & Starowicz, K. (2017) · Experimental Hematology · doi:10.1016/j.exphem.2016.12.006 · Cited by 83 · see citing works
Developmental control of macrophage function
Bonnardel, J., & Guilliams, M. (2017) · Current Opinion in Immunology · doi:10.1016/j.coi.2017.12.001 · Cited by 84 · see citing works
Epigenetic Regulators as the Gatekeepers of Hematopoiesis
Rodrigues, C. P., Shvedunova, M., & Akhtar, A. (2020) · Trends in Genetics · doi:10.1016/j.tig.2020.09.015 · Cited by 85 · see citing works
Numerous niches for hematopoietic stem cells remain empty during homeostasis
Shimoto, M., Sugiyama, T., & Nagasawa, T. (2017) · Blood · doi:10.1182/blood-2016-09-740563 · Cited by 82 · see citing works
Lee, J.-M., Govindarajah, V., Goddard, B., Hinge, A. S., Muench, D. E., Filippi, M., Aronow, B. J., Cancelas, J. A., Salomonis, N., Grimes, H. L., et al. (2017) · The Journal of Experimental Medicine · doi:10.1084/jem.20170690 · Cited by 81 · see citing works
Metabolism as master of hematopoietic stem cell fate
Ito, K., Bonora, M., & Ito, K. (2018) · International Journal of Hematology · doi:10.1007/s12185-018-2534-z · Cited by 80 · see citing works
Origin and Heterogeneity of Tissue Myeloid Cells: A Focus on GMP-Derived Monocytes and Neutrophils
Ng, L. G., Liu, Z., Kwok, I., & Ginhoux, F. (2023) · Annual Review of Immunology · doi:10.1146/annurev-immunol-081022-113627 · Cited by 85 · see citing works
Lai, S. M., Sheng, J., Gupta, P., Rénia, L., Duan, K., Zolezzi, F., Karjalainen, K., Newell, E. W., & Ruedl, C. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.11.059 · Cited by 80 · see citing works
Molecular and cellular mechanisms of aging in hematopoietic stem cells and their niches
Zhang, L., Mack, R. M., Breslin, P., & Zhang, J. (2020) · Journal of Hematology & Oncology · doi:10.1186/s13045-020-00994-z · Cited by 78 · see citing works
B-1a cells acquire their unique characteristics by bypassing the pre-BCR selection stage
Wong, J. B., Hewitt, S. L., Heltemes-Harris, L. M., Mandal, M., Johnson, K., Rajewsky, K., Koralov, S. B., Clark, M. R., Farrar, M. A., & Skok, J. A. (2019) · Nature Communications · doi:10.1038/s41467-019-12824-z · Cited by 79 · see citing works
Differentiation route determines the functional outputs of adult megakaryopoiesis
Li, J., Liu, J., Li, Y., Chen, L. V., Cheng, H., Li, Y., Cheng, T., Wang, Q., & Zhou, B. O. (2024) · Immunity · doi:10.1016/j.immuni.2024.02.006 · Cited by 80 · see citing works
Myelopoiesis in the Context of Innate Immunity
Mitroulis, I., Kalafati, L., Hajishengallis, G., & Chavakis, T. (2018) · Journal of Innate Immunity · doi:10.1159/000489406 · Cited by 75 · see citing works
Intravital Imaging Reveals Motility of Adult Hematopoietic Stem Cells in the Bone Marrow Niche
Upadhaya, S., Krichevsky, O., Akhmetzyanova, I., Sawai, C. M., Fooksman, D., & Reizis, B. (2020) · Cell stem cell · doi:10.1016/j.stem.2020.06.003 · Cited by 74 · see citing works
T Cell Development by the Numbers
Krueger, A., Ziętara, N., & Łyszkiewicz, M. (2016) · Trends in Immunology · doi:10.1016/j.it.2016.10.007 · Cited by 71 · see citing works
Ganuza, M., Hall, T., Finkelstein, D., Wang, Y., Chabot, A., Kang, G., Bi, W., Wu, G., & McKinney‐Freeman, S. (2019) · Blood · doi:10.1182/blood-2018-09-873059 · Cited by 71 · see citing works
Hematopoietic stem cell-independent hematopoiesis and the origins of innate-like B lymphocytes
Ghosn, E., Yoshimoto, M., Nakauchi, H., Weissman, I. L., & Herzenberg, L. A. (2019) · Development · doi:10.1242/dev.170571 · Cited by 68 · see citing works
Genetics and epidemiology of mutational barcode-defined clonal hematopoiesis
Stacey, S., Zink, F., Halldorsson, G. H., Stefánsdóttir, L., Gudjonsson, S. A., Einarsson, G., Hjörleifsson, G., Eiriksdottir, T., Helgadóttir, A., Björnsdóttir, G., et al. (2023) · Nature Genetics · doi:10.1038/s41588-023-01555-z · Cited by 68 · see citing works
Leung, G., Cool, T., Valencia, C. H., Worthington, A. K., Beaudin, A. E., & Forsberg, E. C. (2019) · Development · doi:10.1242/dev.176180 · Cited by 67 · see citing works
Fate mapping of hematopoietic stem cells reveals two pathways of native thrombopoiesis
Morcos, M. N. F., Li, C., Munz, C. M., Greco, A., Dressel, N., Reinhardt, S., Sameith, K., Dahl, A., Becker, N. B., Roers, A., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-31914-z · Cited by 65 · see citing works
Chen, Z., Soni, N., Piñero, G., Giotti, B., Eddins, D. J., Lindblad, K. E., Ross, J., Vallcorba, M. P., Joshi, T. V., Angione, A., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-37361-8 · Cited by 65 · see citing works
HSC-independent definitive hematopoiesis persists into adult life
Kobayashi, M., Wei, H., Yamanashi, T., Portilho, N. A., Cornelius, S. A., Valiente, N., Nishida, C., Cheng, H., Latorre, A., Zheng, W. J., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112239 · Cited by 68 · see citing works
The Bone Marrow Microenvironment for Hematopoietic Stem Cells
Lucas, D. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-69194-7_2 · Cited by 61 · see citing works
Lin, X., Zhou, Q., Zhao, C., Lin, G., Xu, J., & Wen, Z. (2019) · Developmental Cell · doi:10.1016/j.devcel.2019.03.028 · Cited by 57 · see citing works
SCA-1 Expression Level Identifies Quiescent Hematopoietic Stem and Progenitor Cells
Morcos, M. N. F., Schoedel, K. B., Hoppe, A., Behrendt, R., Başak, O., Clevers, H. C., Roers, A., & Gerbaulet, A. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.04.012 · Cited by 60 · see citing works
Differences in Cell Cycle Status Underlie Transcriptional Heterogeneity in the HSC Compartment
Lauridsen, F. K. B., Jensen, T. L., Rapin, N., Aslan, D., Wilhelmson, A. S., Pundhir, S., Rehn, M., Paul, F., Giladi, A., Hasemann, M. S., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.06.057 · Cited by 55 · see citing works
Macrophage Subsets in Obesity, Aligning the Liver and Adipose Tissue
Remmerie, A., Martens, L., & Scott, C. L. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00259 · Cited by 56 · see citing works
The DNA methylation landscape of hematological malignancies: an update
Blecua, P., Martinez‐Verbo, L., & Esteller, M. (2020) · Molecular Oncology · doi:10.1002/1878-0261.12744 · Cited by 57 · see citing works
A Common Origin for B-1a and B-2 Lymphocytes in Clonal Pre- Hematopoietic Stem Cells
Hadland, B., Varnum‐Finney, B., Mandal, P. K., Rossi, D. J., Poulos, M. G., Butler, J. M., Rafii, S., Yöder, M. C., Yoshimoto, M., & Bernstein, I. D. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.04.007 · Cited by 55 · see citing works
Hadland, B., & Yoshimoto, M. (2017) · Experimental Hematology · doi:10.1016/j.exphem.2017.12.008 · Cited by 54 · see citing works
In Situ Modification of Tissue Stem and Progenitor Cell Genomes
Goldstein, J. M., Tabebordbar, M., Zhu, K., Wang, L. D., Messemer, K. A., Peacker, B. L., Kakhki, S. A., Gonzalez-Celeiro, M., Shwartz, Y., Cheng, J. K. W., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.03.105 · Cited by 53 · see citing works
The Source and Dynamics of Adult Hematopoiesis: Insights from Lineage Tracing
Pucella, J. N., Upadhaya, S., & Reizis, B. (2020) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-020520-114601 · Cited by 53 · see citing works
Self-citationModern Concepts in Cardiovascular Disease: Inflamm-Aging
Puspitasari, Y. M., Ministrini, S., Schwarz, L., Karch, C., Liberale, L., & Camici, G. G. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.882211 · Cited by 54 · see citing works
- Authors
- Sawai, C. M., Babovic, S., Upadhaya, S., Knapp, D. J. H. F., Lavin, Y., Lau, C. M., Goloborodko, A., Feng, J., Fujisaki, J., Ding, L., Mirny, L. A., Merad, M., Eaves, C. J., & Reizis, B.
- Affiliations
- NYU Langone Health (US)
- BC Cancer Agency (CA)
- Columbia University Irving Medical Center (US)
- Tisch Cancer Institute (US)
- Massachusetts Institute of Technology (US)
- Corresponding author
- Sawai, Catherine M.
- Reizis, Boris
- ORCID
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2016-09
- Volume
- 45
- Issue
- 3
- Pages
- 597-609
- ISSN
- 1074-7613 (ISSN-L)
- PMC
- PMC5054720
- OpenAlex
- W2517782886
- Cited by
- 381
- References
- 50
- Citations by year
- 2026: 13 · 2025: 22 · 2024: 33 · 2023: 35 · 2022: 45 · 2021: 36 · 2020: 55 · 2019: 54 · 2018: 49 · 2017: 33 · 2016: 6
- FWCI
- 45.00
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Immunity (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-nd)
- PMC
- Funders
- National Institutes of Health
- Canadian Institutes of Health Research
- National Institute on Aging (R01AG049074)
- National Heart, Lung, and Blood Institute (R21HL113678, R01HL132074, R01HL129506)
- National Cancer Institute (R01CA173861, R01CA190400, R01CA154947, P30CA016087)
- National Institute of General Medical Sciences (T32GM008224)
- National Institute of Allergy and Infectious Diseases (R01AI072571, R21AI115382, T32AI100853, R37AI072571)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32HD055165)
- Topics
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Blood disorders and treatments
- Keywords
- hematopoietic stem cells, multilineage hematopoiesis, steady-state hematopoiesis, myeloid cell development, lymphocyte development, megakaryopoiesis, interferon response, serial transplantation, B-1a cells, tissue macrophages
- MeSH terms
- Animals, B-Lymphocytes, Blood Platelets, Cell Differentiation, Hematopoiesis, Hematopoietic Stem Cells, Interferons, Macrophages, Mice, Inbred C57BL, Hematopoietic Stem Cell Transplantation, Cell Lineage, Myeloid Cells, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
