The replication rate of human hematopoietic stem cells in vivo
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Hematopoietic stem cells (HSCs) replicate (self-renew) to create 2 daughter cells with capabilities equivalent to their parent, as well as differentiate, and thus can both maintain and restore blood cell production. Cell labeling with division-sensitive markers and competitive transplantation studies have been used to estimate the replication rate of murine HSCs in vivo. However, these methods are not feasible in humans and surrogate assays are required. In this report, we analyze the changing ratio with age of maternal/paternal X-chromosome phenotypes in blood cells from females and infer that human HSCs replicate on average once every 40 weeks (range, 25-50 weeks). We then confirm this estimate with 2 independent approaches, use the estimate to simulate human hematopoiesis, and show that the simulations accurately reproduce marrow transplantation data. Our simulations also provide evidence that the number of human HSCs increases from birth until adolescence and then plateaus, and that the ratio of contributing to quiescent HSCs in humans significantly differs from mouse. In addition, they suggest that human marrow failure, such as the marrow failure that occurs after umbilical cord blood transplantation and with aplastic anemia, results from insufficient numbers of early progenitor cells, and not the absence of HSCs.
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There are approximately 10,000 HSCs in humans.
“current estimates that there are approximately 10,000 HSCs in humans12”
From Role of TP53 mutations in the origin and evolution of therapy-related acute myeloid leukaemia (2015) · cites this paper as [12]
Cites
STATISTICAL METHODS FOR ASSESSING AGREEMENT BETWEEN TWO METHODS OF CLINICAL MEASUREMENT
Martin Bland, J., & Altman, D. (1986) · The Lancet · doi:10.1016/s0140-6736(86)90837-8 · Cited by 47,965 · see citing works
Beckett, A. H., Rowland, M., & TURNER, P. (1965) · The Lancet · doi:10.1016/s0140-6736(65)91037-8 · Cited by 16,917 · see citing works
The serial cultivation of human diploid cell strains
Hayflick, L., & Moorhead, P. S. (1961) · Experimental Cell Research · doi:10.1016/0014-4827(61)90192-6 · Cited by 8,508 · see citing works
Hematopoiesis: An Evolving Paradigm for Stem Cell Biology
Orkin, S. H., & Zon, L. I. (2008) · Cell · doi:10.1016/j.cell.2008.01.025 · Cited by 2,570 · 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
Lectures on the Coupling Method
Lindvall, T. (1992) · CERN Document Server (European Organization for Nuclear Research) · Cited by 1,160 · see citing works
Evidence for a mitotic clock in human hematopoietic stem cells: loss of telomeric DNA with age.
Vaziri, H., Dragowska, W., Allsopp, R. C., Thomas, T. E., Harley, C. B., & Lansdorp, P. M. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.21.9857 · Cited by 1,132 · 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
Delaney, C. S., Heimfeld, S., Brashem‐Stein, C., Voorhies, H., Manger, R. L., & Bernstein, I. D. (2010) · Nature Medicine · doi:10.1038/nm.2080 · Cited by 769 · see citing works
Age-Associated Characteristics of Murine Hematopoietic Stem Cells
Sudo, K., Ema, H., Morita, Y., & Nakauchi, H. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.192.9.1273 · Cited by 722 · see citing works
Rufer, N., Brümmendorf, T. H., Kolvraa, S., Bischoff, C., Christensen, K., Wadsworth, L., Schulzer, M., & Lansdorp, P. M. (1999) · The Journal of Experimental Medicine · doi:10.1084/jem.190.2.157 · Cited by 709 · see citing works
Intra-individual Change Over Time in DNA Methylation With Familial Clustering
Bjornsson, H. T. (2008) · JAMA · doi:10.1001/jama.299.24.2877 · Cited by 702 · see citing works
The application of molecular genetic approaches to the study of human evolution
Cavalli-Sforza, L. L., & Feldman, M. W. (2003) · Nature Genetics · doi:10.1038/ng1113 · Cited by 671 · see citing works
Quiescence, cycling, and turnover in the primitive hematopoietic stem cell compartment.
Bradford, G. B., Williams, B., Rossi, R., & Bertoncello, I. (1997) · PubMed · Cited by 419 · 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
Signaling pathways governing stem-cell fate
Blank, U., Karlsson, G., & Karlsson, S. (2007) · Blood · doi:10.1182/blood-2007-07-075168 · Cited by 350 · see citing works
Evidence that hematopoiesis may be a stochastic process in vivo
Abkowitz, J. L., Catlin, S. N., & Guttorp, P. M. (1996) · Nature Medicine · doi:10.1038/nm0296-190 · Cited by 246 · see citing works
Self-citationStochastic Modeling of Scientific Data
Guttorp, P. M. (1995) · Springer eBooks · doi:10.1007/978-1-4899-4449-8 · Cited by 245 · see citing works
Self-citationEvidence that the number of hematopoietic stem cells per animal is conserved in mammals
Abkowitz, J. L., Catlin, S. N., McCallie, M. T., & Guttorp, P. M. (2002) · Blood · doi:10.1182/blood-2002-03-0822 · Cited by 233 · see citing works
Self-citationGale, R. E., Fielding, A. K., Harrison, C. N., & Linch, D. C. (1997) · British Journal of Haematology · doi:10.1046/j.1365-2141.1997.2573078.x · Cited by 228 · see citing works
Self-citationIn vivo kinetics of murine hemopoietic stem cells
Abkowitz, J. L., Golinelli, D., Harrison, D. E., & Guttorp, P. M. (2000) · Blood · doi:10.1182/blood.v96.10.3399 · Cited by 152 · see citing works
Self-citationHematopoietic stem cells engraft in mice with absolute efficiency
Benveniste, P. M., Cantin, C., Hyam, D., & Iscove, N. N. (2003) · Nature Immunology · doi:10.1038/ni940 · Cited by 141 · see citing works
Leukocyte telomere dynamics and human hematopoietic stem cell kinetics during somatic growth
Sidorov, I., Kimura, M., Yashin, A., & Aviv, A. (2009) · Experimental Hematology · doi:10.1016/j.exphem.2008.11.009 · Cited by 135 · see citing works
X-linked genetic factors regulate hematopoietic stem-cell kinetics in females
Christensen, K., Kristiansen, M. B., Hagen-Larsen, H., Skytthe, A., Bathum, L., Jeune, B., Andersen‐Ranberg, K., Vaupel, J. W., & Ørstavik, K. H. (2000) · Blood · doi:10.1182/blood.v95.7.2449 · Cited by 121 · see citing works
No evidence that skewing of X chromosome inactivation patterns is transmitted to offspring in humans
Bolduc, V., Chagnon, P., Provost, S., Dubé, M., Bélisle, C., Gingras, M., Mollica, L. R., & Busque, L. (2007) · Journal of Clinical Investigation · doi:10.1172/jci33166 · Cited by 114 · see citing works
Self-citationKim, H. J., Tisdale, J. F., Wu, T., Takatoku, M., Sellers, S. E., Zickler, P., Metzger, M. E., Agricola, B. A., Malley, J. D., Kato, I., et al. (2000) · Blood · doi:10.1182/blood.v96.1.1 · Cited by 109 · see citing works
Hematopoietic Stem Cell Heterogeneity: Subtypes, Not Unpredictable Behavior
Schroeder, T. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.02.006 · Cited by 109 · see citing works
Estimating human hematopoietic stem cell kinetics using granulocyte telomere lengths
Shepherd, B. E., Guttorp, P. M., Lansdorp, P. M., & Abkowitz, J. L. (2004) · Experimental Hematology · doi:10.1016/j.exphem.2004.07.023 · Cited by 98 · see citing works
Self-citationRowe, J. M., Ciobanu, N., Ascensao, J., Stadtmauer, E. A., Weiner, R. S., Schenkein, D. P., McGlave, P., Lazarus, H. M., & and Eastern Cooperative Oncology Group. (1994) · Annals of Internal Medicine · doi:10.7326/0003-4819-120-2-199401150-00008 · Cited by 96 · see citing works
O’Brien, S. J., Johnson, W. E., Driscoll, C. A., Pontius, J. U., Pecon‐Slattery, J., & Menotti-Raymond, M. A. (2008) · Trends in Genetics · doi:10.1016/j.tig.2008.03.004 · Cited by 94 · see citing works
An X chromosome gene regulates hematopoietic stem cell kinetics
Abkowitz, J. L., Taboada, M. R., Shelton, G. H., Catlin, S. N., Guttorp, P. M., & Kiklevich, J. V. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.7.3862 · Cited by 90 · see citing works
Self-citationUnbalanced X‐chromosome inactivation in haemopoietic cells from normal women
Tonon, L., Bergamaschi, G., Dellavecchia, C., Rosti, V., Lucotti, C., Malabarba, L., Novella, A., Vercesi, E., Frassoni, F., & Cazzola, M. (1998) · British Journal of Haematology · doi:10.1046/j.1365-2141.1998.00867.x · Cited by 87 · see citing works
Hematopoietic stem-cell behavior in nonhuman primates
Shepherd, B. E., Kiem, H., Lansdorp, P. M., Dunbar, C. E., Aubert, G., Larochelle, A., Seggewiss, R., Guttorp, P. M., & Abkowitz, J. L. (2007) · Blood · doi:10.1182/blood-2007-02-075382 · Cited by 87 · see citing works
Self-citationBuescher, E. S., Alling, D. W., & Gallin, J. I. (1985) · Journal of Clinical Investigation · doi:10.1172/jci112140 · Cited by 85 · see citing works
Busque, L., Paquette, Y., Provost, S., Roy, D., Levine, R. L., Mollica, L. R., & Gilliland, D. G. (2009) · Blood · doi:10.1182/blood-2008-12-195677 · Cited by 85 · see citing works
Self-citationEvolving concepts on the microenvironmental niche for hematopoietic stem cells
Raaijmakers, M. H. G. P., & Scadden, D. T. (2008) · Current Opinion in Hematology · doi:10.1097/moh.0b013e328303e14c · Cited by 81 · see citing works
Barrett, A. J., Ringdén, O. T. H., Zhang, M., Bashey, A., Cahn, J.-Y. Y., Cairo, M. S., Gale, R. P., Gratwohl, A. A., Locatelli, F., Martino, R., et al. (2000) · PubMed · doi:10.1182/blood.v95.11.3323 · Cited by 79 · see citing works
Self-citationWilson, A., Osee, G., van der Wath, R. C., Blanco-Bose, W. E., Laurenti, E., Dunant, C. F., Lio, P. M., MacDonald, H. R., & Trumpp, A. (2008) · Infoscience (Ecole Polytechnique Fédérale de Lausanne) · Cited by 71 · see citing works
Assessment of mechanism of acquired skewed X inactivation by analysis of twins
Vickers, M. A., McLeod, E., Spector, T. D., & Wilson, I. (2001) · Blood · doi:10.1182/blood.v97.5.1274 · Cited by 61 · see citing works
Gale, R. E., Bunch, C., Moir, D. J., Patterson, K. G., Goldstone, A. H., & Linch, D. C. (1996) · British Journal of Haematology · doi:10.1046/j.1365-2141.1996.4751014.x · Cited by 35 · see citing works
Self-citationAcquired skewing of Lyonization remains stable for a prolonged period in healthy blood donors
van Dijk, J., Heuver, L. H. H., Stevens-Linders, E., Jansen, J., Mensink, E. J. B. M., Raymakers, R. A. P., & de Witte, T. (2002) · Leukemia · doi:10.1038/sj.leu.2402379 · Cited by 29 · see citing works
Mehta, J., Powles, R. L., Horton, C., Treleaven, J. G., & Singhal, S. (1996) · PubMed · Cited by 19 · see citing works
CELLULARITY AND CELL PROLIFERATION RATES IN HUMAN BONE MARROW
Skårberg, K. O. (1974) · Acta Medica Scandinavica · doi:10.1111/j.0954-6820.1974.tb08140.x · Cited by 18 · see citing works
Statistical Inference in a Two‐Compartment Model for Hematopoiesis
Catlin, S. N., Abkowitz, J. L., & Guttorp, P. M. (2001) · Biometrics · doi:10.1111/j.0006-341x.2001.00546.x · Cited by 17 · see citing works
Self-citationZubair, A. C., Zahrieh, D., Daley, H., Schott, D., Gribben, J. G., Freedman, A. S., & Ritz, J. (2003) · Transfusion · doi:10.1046/j.1537-2995.2003.00369.x · Cited by 16 · see citing works
Bayesian inference in a hidden stochastic two-compartment model for feline hematopoiesis
Golinelli, D., Guttorp, P. M., & Abkowitz, J. A. (2006) · Mathematical Medicine and Biology A Journal of the IMA · doi:10.1093/imammb/dql008 · Cited by 13 · see citing works
Self-citationFong, Y., Guttorp, P. M., & Abkowitz, J. L. (2009) · The Annals of Applied Statistics · doi:10.1214/09-aoas269 · Cited by 11 · see citing works
Self-citationHematopoiesis as a competitive exclusion process: Estimation of a stem cell selective advantage
Catlin, S. N., Guttorp, P. M., McCallie, M. T., & Abkowitz, J. L. (2004) · Journal of Agricultural Biological and Environmental Statistics · doi:10.1198/1085711043550 · Cited by 4 · see citing works
Self-citation
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The origin and evolution of mutations in acute myeloid leukemia
Welch, J. S., Ley, T. J., Link, D. C., Miller, C. A., Larson, D. E., Koboldt, D. C., Wartman, L. D., Lamprecht, T. L., Liu, F., Xia, J., et al. (2012) · Cell · doi:10.1016/j.cell.2012.06.023 · Cited by 1,575 · see citing works
Role of TP53 mutations in the origin and evolution of therapy-related acute myeloid leukaemia
Wong, T. N., Ramsingh, G., Young, A. L., Miller, C. A., Touma, W., Welch, J. S., Lamprecht, T. L., Shen, D., Hundal, J., Fulton, R. S., et al. (2015) · Nature · doi:10.1038/nature13968 · Cited by 892 · see citing works
Hematopoiesis: a human perspective
Doulatov, S., Notta, F., Laurenti, E., & Dick, J. E. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.01.006 · Cited by 895 · 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
Clonal haematopoiesis harbouring AML-associated mutations is ubiquitous in healthy adults
Young, A. L., Challen, G. A., Birmann, B. M., & Druley, T. E. (2016) · Nature Communications · doi:10.1038/ncomms12484 · Cited by 692 · 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
Telomeres shorten at equivalent rates in somatic tissues of adults
Daniali, L., Benetos, A., Susser, E., Kark, J. D., Labat, C., Kimura, M., Desai, K. K., Granick, M., & Aviv, A. (2013) · Nature Communications · doi:10.1038/ncomms2602 · Cited by 601 · see citing works
Clonal dynamics of haematopoiesis across the human lifespan
Mitchell, E., Chapman, M. S., Williams, N., Dawson, K. J., Mende, N., Calderbank, E. F., Jung, H., Mitchell, T. J., Coorens, T. H. H., Spencer, D. H., et al. (2022) · Nature · doi:10.1038/s41586-022-04786-y · Cited by 501 · see citing works
Cell cycle regulation in hematopoietic stem cells
Pietras, E. M., Warr, M. R., & Passegué, E. (2011) · Journal of Cell Biology · doi:10.1083/jcb.201102131 · Cited by 447 · see citing works
Winkler, I. G., Barbier, V., Nowlan, B., Jacobsen, R. N., Forristal, C. E., Patton, J. T., Magnani, J. L., & Lévesque, J.-P. (2012) · Nature Medicine · doi:10.1038/nm.2969 · Cited by 439 · see citing works
Goodell, M. A., & Rando, T. A. (2015) · Science · doi:10.1126/science.aab3388 · Cited by 347 · see citing works
CDK6 Levels Regulate Quiescence Exit in Human Hematopoietic Stem Cells
Laurenti, E., Frelin, C., Xie, S. Z.-J., Ferrari, R., Dunant, C. F., Zandi, S., Neumann, A. L., Plumb, I., Doulatov, S. R., Chen, J., et al. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.01.017 · Cited by 340 · see citing works
Regulation of hematopoietic stem cells by bone marrow stromal cells
Anthony, B. A., & Link, D. C. (2013) · Trends in Immunology · doi:10.1016/j.it.2013.10.002 · Cited by 301 · see citing works
Ivanovs, A., Александрович, Р. С., Welch, L. A., Anderson, R. A., Turner, M. L., & Medvinsky, A. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20111688 · Cited by 289 · see citing works
Human haematopoietic stem cell development: from the embryo to the dish
Ivanovs, A., Александрович, Р. С., Ng, E. S., Stanley, E. G., Elefanty, A. G., & Medvinsky, A. (2017) · Development · doi:10.1242/dev.134866 · Cited by 267 · see citing works
Increased stem cell proliferation in atherosclerosis accelerates clonal hematopoiesis
Heyde, A., Rohde, D., McAlpine, C. S., Zhang, S., Hoyer, F. F., Gerold, J. M., Cheek, D., Iwamoto, Y., Schloss, M. J., Vandoorne, K., et al. (2021) · Cell · doi:10.1016/j.cell.2021.01.049 · Cited by 267 · see citing works
Somatic Mutations Reveal Lineage Relationships and Age-Related Mutagenesis in Human Hematopoiesis
Osorio, F. G., Huber, A. R., Oka, R., Verheul, M., Patel, S. H., Hasaart, K., de la Fonteijne, L., Varela, I., Camargo, F. D., & van Boxtel, R. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.11.014 · Cited by 237 · see citing works
Vannini, N., Campos, V., Girotra, M., Trachsel, V., Rojas-Sutterlin, S., Tratwal, J., Ragusa, S., Stefanidis, E., Ryu, D., Rainer, P. Y., et al. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2019.02.012 · Cited by 218 · see citing works
Van Egeren, D., Escabi, J., Nguyen, M., Liu, S., Reilly, C. R., Patel, S., Kamaz, B., Kalyva, M., DeAngelo, D. J., Galinsky, I., et al. (2021) · Cell Stem Cell · doi:10.1016/j.stem.2021.02.001 · Cited by 206 · see citing works
Wu, C., Li, B., Lu, R., Koelle, S., Yang, Y., Jares, A., Krouse, A. E., Metzger, M. E., Liang, F., Loré, K., et al. (2014) · Cell stem cell · doi:10.1016/j.stem.2014.01.020 · Cited by 186 · 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
Acute myeloid leukaemia: a paradigm for the clonal evolution of cancer?
Grove, C. S., & Vassiliou, G. S. (2014) · Disease Models & Mechanisms · doi:10.1242/dmm.015974 · Cited by 182 · 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
Telomeropathies: An emerging spectrum disorder
Holohan, B., Wright, W. E., & Shay, J. W. (2014) · Journal of Cell Biology · doi:10.1083/jcb.201401012 · Cited by 175 · see citing works
Hematopoietic Stem Cell Heterogeneity Takes Center Stage
Copley, M. R., Beer, P. A., & Eaves, C. J. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.05.006 · Cited by 174 · see citing works
Holstege, H., Pfeiffer, W., Sie, D., Hulsman, M., Nicholas, T. J., Lee, C. C., Ross, T., Lin, J., Miller, M. A., Ylstra, B., et al. (2014) · Genome Research · doi:10.1101/gr.162131.113 · Cited by 152 · 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
Forristal, C. E., Winkler, I. G., Nowlan, B., Barbier, V., Walkinshaw, G., & Lévesque, J.-P. (2012) · Blood · doi:10.1182/blood-2012-02-408419 · Cited by 133 · see citing works
Cruickshank, M. N., Oshlack, A., Theda, C., Davis, P. G., Martino, D., Sheehan, P. M., Dai, Y., Saffery, R., Doyle, L. W., & Craig, J. M. (2013) · Genome Medicine · doi:10.1186/gm500 · Cited by 132 · see citing works
Rozhok, A. I., & DeGregori, J. V. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1501713112 · Cited by 115 · see citing works
Itkin, T., Ludin, A., Gradus, B., Gur‐Cohen, S., Kalinkovich, A., Schajnovitz, A., Ovadya, Y., Kollet, Ó., Canaani, J., Shezen, E., et al. (2012) · Blood · doi:10.1182/blood-2011-11-394692 · Cited by 120 · see citing works
Role of bone marrow macrophages in controlling homeostasis and repair in bone and bone marrow niches
Kaur, S., Raggatt, L. J., Batoon, L., Hume, D. A., Lévesque, J.-P., & Pettit, A. R. (2016) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2016.08.009 · Cited by 118 · see citing works
Clonal fate mapping quantifies the number of haematopoietic stem cells that arise during development
Henninger, J. E., Santoso, B., Hans, S., Durand, E. M., Moore, J. L., Mosimann, C., Brand, M., Traver, D. J., & Zon, L. I. (2016) · Nature Cell Biology · doi:10.1038/ncb3444 · Cited by 113 · see citing works
Li, H., Slone, J. D., Fei, L., & Huang, T. (2019) · Cells · doi:10.3390/cells8060608 · Cited by 103 · see citing works
An evolutionary perspective on chronic myelomonocytic leukemia
Itzykson, R., & Solary, É. (2013) · Leukemia · doi:10.1038/leu.2013.100 · Cited by 102 · see citing works
New Insights from Studies of Clonal Hematopoiesis
Gibson, C. J., & Steensma, D. P. (2018) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-17-3044 · Cited by 94 · see citing works
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Gillespie, M. S., Ward, C. M., & Davies, C. C. (2023) · Cancers · doi:10.3390/cancers15061897 · Cited by 96 · see citing works
A Potential Mechanism for ADC-Induced Neutropenia: Role of Neutrophils in Their Own Demise
Zhao, H., Gulesserian, S., Malinao, M. C., Ganesan, S. K., Song, J., Chang, M. S., Williams, M. M., Zeng, Z., Mattie, M. D., Mendelsohn, B. A., et al. (2017) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-17-0133 · Cited by 90 · see citing works
Niwa, O., Barcellos‐Hoff, M. H., Globus, R. K., Harrison, J. D., Hendry, J. H., Jacob, P., Martin, M. T., Seed, T. M., Shay, J. W., Story, M. D., et al. (2015) · Annals of the ICRP · doi:10.1177/0146645315595585 · Cited by 90 · 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
Murine foetal liver supports limited detectable expansion of life-long haematopoietic progenitors
Ganuza, M., Hall, T., Myers, J., Nevitt, C. D., Sánchez‐Lanzas, R., Chabot, A., Ding, J., Kooienga, E., Caprio, C., Finkelstein, D., et al. (2022) · Nature Cell Biology · doi:10.1038/s41556-022-00999-5 · Cited by 87 · see citing works
Switching roles: the functional plasticity of adult tissue stem cells
Wabik, A., & Jones, P. H. (2015) · The EMBO Journal · doi:10.15252/embj.201490386 · Cited by 81 · see citing works
Reduced Lymphoid Lineage Priming Promotes Human Hematopoietic Stem Cell Expansion
van Galen, P., Kreso, A., Wienholds, E., Laurenti, E., Eppert, K., Lechman, E. R., Mbong, N., Hermans, K. G., Dobson, S. M., April, C., et al. (2014) · Cell stem cell · doi:10.1016/j.stem.2013.11.021 · Cited by 78 · see citing works
Normal Hematopoiesis Is a Balancing Act of Self-Renewal and RegenerationPreprint
Olson, O. C., Kang, Y.-A., & Passegue, E. A. (2020) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a035519 · Cited by 78 · see citing works
Clonal dynamics of haematopoiesis across the human lifespanPreprint
Mitchell, E., Chapman, M. S., Williams, N., Dawson, K. J., Mende, N., Calderbank, E. F., Jung, H., Mitchell, T. J., Coorens, T. H. H., Spencer, D. H., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.08.16.456475 · Cited by 74 · see citing works
A generalized theory of age-dependent carcinogenesis
Rozhok, A. I., & DeGregori, J. V. (2019) · eLife · doi:10.7554/elife.39950 · Cited by 73 · see citing works
Koelle, S., Espinoza, D. A., Wu, C., Xu, J., Lu, R., Li, B., Donahue, R. E., & Dunbar, C. E. (2017) · Blood · doi:10.1182/blood-2016-07-728691 · Cited by 61 · see citing works
Six, E. M., Guilloux, A., Denis, A., Lecoules, A., Magnani, A., Vilette, R., Male, F., Cagnard, N., Delville, M., Magrin, E., et al. (2020) · Blood · doi:10.1182/blood.2019002350 · Cited by 65 · see citing works
Recent advances in understanding clonal haematopoiesis in aplastic anaemia
Stanley, N. L., Olson, T. S., & Babushok, D. V. (2017) · British Journal of Haematology · doi:10.1111/bjh.14510 · Cited by 64 · see citing works
Resilient and resourceful: Genome maintenance strategies in hematopoietic stem cells
Bakker, S. T., & Passegue, E. A. (2013) · Experimental Hematology · doi:10.1016/j.exphem.2013.09.007 · Cited by 63 · see citing works
Effect of Dedifferentiation on Time to Mutation Acquisition in Stem Cell-Driven Cancers
Jilkine, A., & Gutenkunst, R. N. (2013) · PLoS Comput. Biol. · doi:10.1371/journal.pcbi.1003481 · Cited by 64 · see citing works
Transit-Amplifying Cells in the Fast Lane from Stem Cells towards Differentiation
Rangel‐Huerta, E., & Maldonado, E. (2017) · Stem Cells International · doi:10.1155/2017/7602951 · Cited by 62 · see citing works
Higham, C. F., Morales, F., Cobbold, C. A., Haydon, D. T., & Monckton, D. G. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds059 · Cited by 56 · see citing works
Huang, X., Zhu, B., Wang, X., Xiao, R., & Wang, C. (2016) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2016.2712 · Cited by 57 · see citing works
Aging of human hematopoietic stem cells is linked to changes in Cdc42 activity
Amoah, A., Keller, A., Emini, R., Hoenicka, M., Liebold, A., Vollmer, A., Eiwen, K., Soller, K., Sakk, V., Zheng, Y., et al. (2021) · Haematologica · doi:10.3324/haematol.2020.269670 · Cited by 56 · see citing works
Antiviral treatment causes a unique mutational signature in cancers of transplantation recipients
de Kanter, J. K., Peci, F., Bertrums, E. J. M., Huber, A. R., van Leeuwen, A. J. C. N., van Roosmalen, M. J., Manders, F., Verheul, M., Oka, R., Brandsma, A. M., et al. (2021) · Cell stem cell · doi:10.1016/j.stem.2021.07.012 · Cited by 51 · see citing works
Rozhok, A. I., Salstrom, J. L., & DeGregori, J. V. (2014) · Aging · doi:10.18632/aging.100707 · Cited by 54 · see citing works
Origin of the hematopoietic system in the human embryo
Julien, E., Omar, R. E., & Tavian, M. (2016) · FEBS Letters · doi:10.1002/1873-3468.12389 · Cited by 55 · see citing works
Developmental and temporal characteristics of clonal sperm mosaicism
Yang, X., Breuss, M. W., Xu, X., Antaki, D., James, K. N., Stanley, V., Ball, L., George, R. D., Wirth, S. A., Cao, B., et al. (2021) · Cell · doi:10.1016/j.cell.2021.07.024 · 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
Yadav, V. K., DeGregori, J. V., & De, S. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw086 · Cited by 48 · see citing works
Advances in stem cell transplantation and gene therapy in the β-hemoglobinopathies
Payen, E., & Leboulch, P. (2012) · Hematology · doi:10.1182/asheducation.v2012.1.276.3807841 · Cited by 49 · see citing works
Shinriki, S., Hirayama, M., Nagamachi, A., Yokoyama, A., Kawamura, T., Kanai, A., Kawai, H., Iwakiri, J., Liu, R., Maeshiro, M., et al. (2022) · Leukemia · doi:10.1038/s41375-022-01708-9 · Cited by 48 · see citing works
Biechonski, S., Yassin, M., & Milyavsky, M. (2017) · Carcinogenesis · doi:10.1093/carcin/bgx002 · Cited by 47 · see citing works
Reduced hematopoietic stem cell frequency predicts outcome in acute myeloid leukemia
Wang, W., Stiehl, T., Raffel, S., Hoang, V. T., Hoffmann, I., Poisa-Beiro, L., Saeed, B. R., Blume, R., Manta, L., Eckstein, V., et al. (2017) · Haematologica · doi:10.3324/haematol.2016.163584 · Cited by 47 · see citing works
In vivo dynamics of human hematopoietic stem cells: novel concepts and future directions
Scala, S., & Aiuti, A. (2019) · Blood Advances · doi:10.1182/bloodadvances.2019000039 · Cited by 47 · see citing works
The impact of aging on primate hematopoiesis as interrogated by clonal tracking
Yu, K.-R., Espinoza, D. A., Wu, C., Truitt, L., Shin, T.-H., Chen, S., Fan, X., Yabe, I. M., Panch, S., Hong, S. G., et al. (2018) · Blood · doi:10.1182/blood-2017-08-802033 · Cited by 47 · see citing works
Changing mutational and adaptive landscapes and the genesis of cancer
Liggett, L. A., & DeGregori, J. V. (2017) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2017.01.005 · Cited by 45 · see citing works
Ion Channels in Hematopoietic and Mesenchymal Stem Cells
Pillozzi, S., & Becchetti, A. (2012) · Stem Cells International · doi:10.1155/2012/217910 · Cited by 43 · see citing works
Modeling Human Hematopoietic Stem Cell Biology in the Mouse
Sykes, S. M., & Scadden, D. T. (2013) · Seminars in Hematology · doi:10.1053/j.seminhematol.2013.03.029 · Cited by 39 · see citing works
Epigenetics of hematopoietic stem cell aging and disease
Oshima, M., & Iwama, A. (2014) · International Journal of Hematology · doi:10.1007/s12185-014-1647-2 · Cited by 39 · see citing works
A Critical Examination of the “Bad Luck” Explanation of Cancer Risk
Rozhok, A. I., Wahl, G. M., & DeGregori, J. V. (2015) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-15-0229 · Cited by 39 · see citing works
Prolonged persistence of mutagenic DNA lesions in somatic cells
Chapman, M. S., Mitchell, E., Yoshida, K., Williams, N., Fabre, M. A., Ranzoni, A. M., Robinson, P. S., Kregar, L. D., Wilk, C. M., Boettcher, S., et al. (2025) · Nature · doi:10.1038/s41586-024-08423-8 · Cited by 37 · see citing works
Non‐genetic heterogeneity, altered cell fate and differentiation therapy
Lewis, A. C., & Kats, L. M. (2021) · EMBO Molecular Medicine · doi:10.15252/emmm.202012670 · Cited by 36 · see citing works
Fibroblast growth factor signaling promotes physiological bone remodeling and stem cell self-renewal
Itkin, T., Kaufmann, K. B., Gur‐Cohen, S., Ludin, A., & Lapidot, T. (2013) · Current Opinion in Hematology · doi:10.1097/moh.0b013e3283606162 · Cited by 35 · see citing works
Updates on the pathophysiology and treatment of aplastic anemia: a comprehensive review
Boddu, P. C., & Kadia, T. M. (2017) · Expert Review of Hematology · doi:10.1080/17474086.2017.1313700 · Cited by 36 · see citing works
Goyal, S., Kim, S., Chen, I. S. Y., & Chou, T. (2015) · BMC Biology · doi:10.1186/s12915-015-0191-8 · Cited by 31 · see citing works
Mitchell, K., & Steidl, U. G. (2019) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a036251 · Cited by 34 · see citing works
Clonal dominance and transplantation dynamics in hematopoietic stem cell compartments
Ashcroft, P., Manz, M. G., & Bonhoeffer, S. (2017) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1005803 · Cited by 34 · see citing works
Huo, Y., Wu, L., Pang, A., Li, Q., Hong, F., Zhu, C., Yang, Z., Dai, W., Zheng, Y., Meng, Q., et al. (2023) · Science Immunology · doi:10.1126/sciimmunol.abn6429 · Cited by 35 · see citing works
Kumar, R., Shah, S. R., & Stiehl, T. (2024) · Applied Mathematical Modelling · doi:10.1016/j.apm.2024.01.048 · Cited by 45 · see citing works
Melo, J. V., & Ross, D. M. (2011) · Hematology · doi:10.1182/asheducation-2011.1.136 · Cited by 31 · see citing works
A decade with whole exome sequencing in haematology
Hansen, M. H., Haferlach, T., & Nyvold, C. G. (2019) · British Journal of Haematology · doi:10.1111/bjh.16249 · Cited by 31 · see citing works
Autophagy regulates the cell cycle of murine HSPCs in a nutrient-dependent manner
Cao, Y., Zhang, A., Cai, J., Yuan, N., Lin, W., Liu, S., Xu, F., Song, L., Li, X., Fang, Y., et al. (2014) · Experimental Hematology · doi:10.1016/j.exphem.2014.11.002 · Cited by 31 · see citing works
Quantitative modeling of chronic myeloid leukemia: insights from radiobiology
Radivoyevitch, T., Hlatky, L., Landaw, J., & Sachs, R. K. (2012) · Blood · doi:10.1182/blood-2011-09-381855 · Cited by 31 · see citing works
Rozhok, A. I., Salstrom, J. L., & DeGregori, J. V. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1509333113 · Cited by 27 · see citing works
Differentiation of leukemic blasts is not completely blocked in acute myeloid leukemia
Agarwal, A., Bolosky, W. J., Wilson, D. B., Eide, C. A., Olson, S. B., Fan, G., & Druker, B. J. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1904091116 · Cited by 29 · see citing works
Paul, K. C., Binder, A. M., Horvath, S., Kusters, C., Yan, Q. J., Rosario, I. D., Yu, Y., Bronstein, J. M., & Ritz, B. R. (2021) · BMC Genomics · doi:10.1186/s12864-021-08009-y · Cited by 27 · see citing works
Cell Adhesion Molecules in Normal and Malignant Hematopoiesis: from Bench to Bedside
Lévesque, J.-P., & Winkler, I. G. (2016) · Current Stem Cell Reports · doi:10.1007/s40778-016-0066-0 · Cited by 26 · see citing works
The biology of hematopoietic stem cells and its clinical implications
Skulimowska, I., Sośniak, J., Gońka, M., Szade, A., Józkowicz, A., & Szade, K. (2021) · FEBS Journal · doi:10.1111/febs.16192 · Cited by 26 · see citing works
CD133-targeted Gene Transfer Into Long-term Repopulating Hematopoietic Stem Cells
Brendel, C., Goebel, B., Abriss, D., Brugman, M. H., Kneissl, S., Schwäble, J., Kaufmann, K. B., Müller-Kuller, U., Kunkel, H., Chen-Wichmann, L., et al. (2014) · Molecular Therapy · doi:10.1038/mt.2014.173 · Cited by 25 · see citing works
Tracking hematopoietic stem cells and their progeny using whole-genome sequencing
Lee-Six, H., & Kent, D. G. (2020) · Experimental Hematology · doi:10.1016/j.exphem.2020.01.004 · Cited by 26 · see citing works
Mossner, M., Nolte, F., Hütter, G., Reins, J., Klaumuenzer, M., Nowak, V., Obländer, J., Ackermann, K., Will, S., Röhl, H., et al. (2013) · Journal of Medical Genetics · doi:10.1136/jmedgenet-2012-101093 · Cited by 24 · see citing works
Replication stress in hematopoietic stem cells in mouse and man
Flach, J., & Milyavsky, M. (2017) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2017.10.001 · Cited by 23 · see citing works
Stem Cells, Hematopoiesis and Lineage Tracing: Transplantation-Centric Views and Beyond
Konturek-Cieśla, A., & Bryder, D. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.903528 · Cited by 22 · see citing works
Park, D. S., Akuffo, A. A., Muench, D. E., Grimes, H. L., Epling‐Burnette, P. K., Maini, P. K., Anderson, A. R. A., & Bonsall, M. B. (2019) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1006913 · Cited by 23 · see citing works
HEMATOPOIETIC STEM CELL GENE THERAPY: ASSESSING THE RELEVANCE OF PRE-CLINICAL MODELS
Larochelle, A., & Dunbar, C. (2013) · Seminars in hematology (Print) · doi:10.1053/j.seminhematol.2013.03.025 · Cited by 22 · see citing works
CHIPing away the progression potential of CHIP: A new reality in the making
Xie, Z., & Zeidan, A. M. (2022) · Blood Reviews · doi:10.1016/j.blre.2022.101001 · Cited by 21 · see citing works
Cruz, L. J., Rezaei, S., Grosveld, F. G., Philipsen, S., & Eich, C. (2022) · Frontiers in Genome Editing · doi:10.3389/fgeed.2022.1030285 · Cited by 22 · see citing works
- Authors
- Catlin, S. N., Busque, L., Gale, R. E., Guttorp, P., & Abkowitz, J. L.
- Affiliations
- University of Nevada, Las Vegas (US)
- Hôpital Maisonneuve-Rosemont (CA)
- University College London (GB)
- Norwegian Computing Center (NO)
- University of Washington (US)
- Venue
- Blood
- Publisher
- American Society of Hematology
- Published
- 2011-04-28
- Volume
- 117
- Issue
- 17
- Pages
- 4460-4466
- ISSN
- 0006-4971 (ISSN-L)
- 1528-0020
- PMC
- PMC3099568
- OpenAlex
- W2072193332
- Cited by
- 259
- References
- 48
- Citations by year
- 2026: 12 · 2025: 16 · 2024: 20 · 2023: 14 · 2022: 18 · 2021: 28 · 2020: 22 · 2019: 17 · 2018: 18 · 2017: 19 · 2016: 15 · 2015: 11 · 2014: 16 · 2013: 18 · 2012: 12
- FWCI
- 10.72
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Blood (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- National Institutes of Health
- National Heart, Lung, and Blood Institute (R01HL046598, R01HL082933, R01-HL46598)
- National Center for Research Resources (UL1RR025014)
- 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, HSC self-renewal, X chromosome inactivation, bone marrow transplantation, HSC quiescence, cord blood transplantation, aplastic anemia, bone marrow failure
- MeSH terms
- Bone Marrow Failure Disorders, Adolescent, Adult, Aging, Anemia, Aplastic, Animals, Bone Marrow Diseases, Cats, Cell Division, Child, Child, Preschool, Computer Simulation, Female, Hematopoiesis, Hematopoietic Stem Cells, Hemoglobinuria, Paroxysmal, Humans, Infant, Infant, Newborn, Models, Biological, Phenotype, Species Specificity, Stochastic Processes, Cord Blood Stem Cell Transplantation, X Chromosome Inactivation, Mice, Young Adult
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