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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.
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“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
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Umemoto, T., Hashimoto, M., Matsumura, T., Nakamura‐Ishizu, A., & Suda, T. (2018) · The Journal of Experimental Medicine · doi:10.1084/jem.20180421 · Cited by 158
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ResultImmunology of the ageing kidney
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“In contrast to these findings, recent single-cell tracking studies have reinforced a myeloid developmental pathway for pDCs; lineage tracing of CD115 CDPs shows that most pDCs develop from this myeloid progenitor (86), and pDCs show similar development kinetics to other myeloid cells whereas pDC-biased progenitors ari…”
ResultNiche-specific functional heterogeneity of intestinal resident macrophages
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BackgroundScala, 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 116
Epidermal γδ T cells originate from yolk sac hematopoiesis and clonally self-renew in the adult
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“In the adult, HSCs colonize the bone marrow (BM) and are thought to generate all hematopoietic lineages (Sawai et al., 2016).”
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Bhlhe40 and Bhlhe41 Transcription Factors Regulate Alveolar Macrophage Self‐renewal and Identity
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“Postnatally, nearly all immune cells originate in the bone marrow as hematopoietic stem cells and differentiate through myeloid or lymphoid cell lineages (Sawai et al., 2016).”
BackgroundMade 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 105
“By contrast, data supporting a greater HSC contribution are based on reporters such as Fgd5 and Pdzk1ip1 , which label a greater proportion of more activated HSCs 42–44 .”
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“The production of blood cells depends on the fitness of the hematopoietic stem cell (HSC) compartment, which contributes to multilineage hematopoiesis throughout life (Bernitz et al., 2016; Busch et al., 2015; Sawai et al., 2016; Sun et al., 2014).”
BackgroundDifferentiation-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 97
Hematopoietic stem cell fate through metabolic control
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Do haematopoietic stem cells age?
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“We found that HSCs contributed more robustly to the myeloid lineage than to the lymphoid lineage in steady state, consistent with previous reports.(17,20) Strikingly, platelets received the fastest and most robust influx from labeled HSCs, reaching the labeling efficiency of HSCs and complete equilibrium by 1 year aft…”
ResultGrinenko, 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 94
“HSCs are rare cells that give rise to numerous blood cell types through a series of intermediate progenitors 4 .”
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 100
“As megakaryocytes are hierarchically and temporally the first lineage generated from HSCs (Adolfsson et al., 2005; Notta et al., 2016; Sawai et al., 2016), we monitored appearance of the megakaryocyte marker, CD41.”
BackgroundKinetics 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 89
“Cell populations in the PB were defined as previously described (Sawai et al., 2016).”
InfluentialCosgrove, J., Hustin, L., de Boer, R. J., & Perié, L. (2021) · Trends in Immunology · doi:10.1016/j.it.2021.10.006 · Cited by 101
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 96
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 90
Developmental control of macrophage function
Bonnardel, J., & Guilliams, M. (2017) · Current Opinion in Immunology · doi:10.1016/j.coi.2017.12.001 · Cited by 87
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 99
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
“Furthermore, these results support the idea that cells in the CD34(2)CD48(2)LSK HSC population contribute to the large number of mature blood cells in bone marrow during homeostasis.(8,9) Taken together, our results indicate that the number of empty HSC niches available for engraftment is larger than the number of nic…”
BackgroundResultLee, 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 83
“Contribution of these various HSC subsets to steady-state and emergency hematopoiesis is still a matter of debate (Sun et al., 2014; Busch et al., 2015; Sawai et al., 2016).”
BackgroundMetabolism 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 85
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 91
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
“These organs are known to be seeded under steady-state conditions by embryonic-derived self-renewing tissue-resident macrophages with minimal contribution from adult circulating monocytes (Guilliams and Scott, 2017; Perdiguero and Geissmann, 2016; Sawai et al., 2016; Sheng et al., 2015).”
BackgroundMolecular 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 80
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
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 82
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 83
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
“Notably, our system labels actively contributing HSCs as well as a small subset of HSCs that do not differentiate (Sawai et al., 2016), and therefore is likely to capture the entire spectrum of HSC behavior.”
BackgroundMethodInfluentialT 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
“Recently, the idea that steady-state hematopoiesis relies on nonLT-HSCs has been challenged based on the analysis of a novel genetic model of HSC-specific fate mapping [14].”
BackgroundGanuza, 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 73
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 73
“Hence, despite recent advances in elucidating HSC-independent hematopoiesis (Sawai et al., 2016; Kobayashi et al., 2014; Gomez Perdiguero et al., 2015; Gentek et al., 2018b; McGrath et al., 2015), current limitations in terms of the availability of biomarkers and in vivo models hinder our ability to distinguish the HS…”
BackgroundInfluentialGenetics 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 71
“These cells have high production rates and short time lags from committed progenitor cells, which in turn require continual replenishment from HSC or multipotent progenitors 10 .”
BackgroundLeung, G. A., Cool, T., Valencia, C. H., Worthington, A. K., Beaudin, A. E., & Forsberg, E. C. (2019) · Development · doi:10.1242/dev.176180 · Cited by 69
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 68
“These equations can be rewritten in a simpler form: ṅ1 = −»1n1 ṅi = ̧i−1ni−1 − »ini ; i ≥ 2 (2) using two aggregate parameters: ̧i = 2ȷi + ‚i + —i »i = ȷi + —i + ‹i − ffi (3) where ̧i and »i are the total differentiation rate and net cell loss rate of compartment i , respectively.”
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
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
“Our results of fetal-EC-derived lymphopoiesis in adult mice are also in line with previous reports showing that postnatal HSC labeling showed a gradual increase of HSC-derived-lymphocytes over 32 weeks 18,20–22 , 56 and a A few caveats have to be considered, though.”
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 63
“2014) although these results have been challenged recently (Sawai et al. 2016).”
ResultLin, X., Zhou, Q., Zhao, C., Lin, G., Xu, J., & Wen, Z. (2019) · Developmental Cell · doi:10.1016/j.devcel.2019.03.028 · Cited by 60
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 61
“We speculate that discrepancies between recent studies reporting high (Sawai et al., 2016) or low (Busch et al.”
ResultDifferences 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 56
“This notion was recently challenged, suggesting that HSCs are indeed the main contributor to hematopoietic output even in steady state (Sawai et al., 2016).”
BackgroundMacrophage 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 61
“As there is limited input of HSCs to the microglia pool 46 weeks after tamoxifen administration (13) these LDAMs are suggested to be a population of Res-microglia, suggesting that Res-macs may indeed respond to changes in their local environment as occurs in aging or inflammation.”
BackgroundThe 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
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
“…significantly to the innate B-1a cell compartment, but suggest heteroge- 1568 Stem Cell Reports j Vol. 8 j 1563–1572 j June 6, 2017 neity in the fetal HSC compartment with regard to B-1a cell potential (Beaudin et al., 2016; Ghosn et al., 2012, 2016; Kristiansen et al., 2016; Sawai et al., 2016).”
BackgroundHadland, B., & Yoshimoto, M. (2017) · Experimental Hematology · doi:10.1016/j.exphem.2017.12.008 · Cited by 52
“Parallel evidence from clonal transplantation studies of highly purified adult bone marrow HSC, and more recently from a study using inducible genetic labelling of HSC in situ, confirmed that adult HSC lack efficient contribution to the peritoneal B-1a compartment following transplantation or under physiologic conditi…”
ResultIn 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
“…marrow of secondary recipients 4–5 months post-transplant (Figure 4G), providing functional evidence that AAV-Cre transduced long-term reconstituting HSCs within the initial injected animals, rather than long-lived oligolineage progenitors (Busch et al., 2015; Sawai et al., 2016; Sun et al., 2014).”
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
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 57
Metadata
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Mesenchymal stem cell research
- Health Sciences › Medicine › Hematology › 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
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