The DOI matches its Crossref record; 2 of the 2 references it cites were found in a registry or an index.
Intermediate-Term Hematopoietic Stem Cells with Extended but Time-Limited Reconstitution Potential
Abstract
Sustained blood cell production depends on divisions by hematopoietic stem cells (HSCs) that yield both differentiating progeny as well as new HSCs via self-renewal. Differentiating progeny remain capable of self-renewal, but only HSCs sustain self-renewal through successive divisions securely enough to maintain clones that persist life-long. Until recently, the first identified next stage consisted of "short-term" reconstituting cells able to sustain clones of differentiating cells for only 4-6 weeks. Here we expand evidence for a numerically dominant "intermediate-term" multipotent HSC stage in mice whose clones persist for 6-8 months before becoming extinct and that are separable from both short-term as well as permanently reconstituting "long-term" HSCs. The findings suggest that the first step in stem cell differentiation consists not in loss of initial capacity for serial self-renewal divisions, but rather in loss of mechanisms that stabilize self-renewing behavior throughout successive future stem cell divisions.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
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?
In the citing paper
“Similar approaches, including paired daughter cell assays (Suda et al, 1984;Suda et al, 1984;Leary et al, 1985;Ema et al, 2005;Kent et al, 2008;Weinreb et al, 2020;Wehling et al, 2022) and HSPC split cultures (Benveniste et al, 2010;Naik et al, 2013;Lin et al, 2018;Tian et al, 2021) have been restricted to clonal tracking for describing cellular or molecular outputs, assuming substantial uniform”
From A scalable in vitro cell competition model identifies preleukemic super competitor clones (2026) · cites this paper as Benveniste et al, 2010
Citations
Cites
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
Dai, X.-M., Ryan, G. R., Hapel, A. J., Dominguez, M. G., Russell, R. G., Kapp, S., Sylvestre, V., & Stanley, E. R. (2002) · Blood · doi:10.1182/blood.v99.1.111 · Cited by 1,184
Research works printed but not linked: 38
- Adolfsson, 2001, Upregulation of Flt3 expression within the bone marrow Lin(-)Sca1(+)c-kit(+) stem cell compartment is accompanied by loss of self-renewal capacity, Immunity, 15, 659, 10.1016/S1074-7613(01)00220-5 · DOI
- Adolfsson, 2005, Identification of Flt3+ lympho-myeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment, Cell, 121, 295, 10.1016/j.cell.2005.02.013 · DOI
- Arai, 2004, Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche, Cell, 118, 149, 10.1016/j.cell.2004.07.004 · DOI
- Benveniste, 2003, Hematopoietic stem cells engraft in mice with absolute efficiency, Nat. Immunol., 4, 708, 10.1038/ni940 · DOI
- Christensen, 2001, Flk-2 is a marker in hematopoietic stem cell differentiation: A simple method to isolate long-term stem cells, Proc. Natl. Acad. Sci. USA, 98, 14541, 10.1073/pnas.261562798 · DOI
- Dykstra, 2007, Long-term propagation of distinct hematopoietic differentiation programs in vivo, Cell Stem Cell, 1, 218, 10.1016/j.stem.2007.05.015 · DOI · Paper page
- Ema, 2005, Quantification of self-renewal capacity in single hematopoietic stem cells from normal and Lnk-deficient mice, Dev. Cell, 8, 907, 10.1016/j.devcel.2005.03.019 · DOI
- Forsberg, 2006, New evidence supporting megakaryocyte-erythrocyte potential of flk2/flt3+ multipotent hematopoietic progenitors, Cell, 126, 415, 10.1016/j.cell.2006.06.037 · DOI
- Foudi, 2009, Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells, Nat. Biotechnol., 27, 84, 10.1038/nbt.1517 · DOI · Paper page
- Harrison, 1991, Lymphoid and erythroid repopulation in B6 W-anemic mice: A new unirradiated recipient, Exp. Hematol., 19, 374
- Hasumura, 2003, Expression change of Flk-2/Flt-3 on murine hematopoietic stem cells in an activating state, Exp. Hematol., 31, 1331, 10.1016/j.exphem.2003.09.004 · DOI
- Haug, 2008, N-cadherin expression level distinguishes reserved versus primed states of hematopoietic stem cells, Cell Stem Cell, 2, 367, 10.1016/j.stem.2008.01.017 · DOI
- Iscove, 1997, Hematopoietic stem cells expand during serial transplantation in vivo without apparent exhaustion, Curr. Biol., 7, 805, 10.1016/S0960-9822(06)00341-1 · DOI
- Iscove, 2002, Representation is faithfully preserved in global cDNA amplified exponentially from sub-picogram quantities of mRNA, Nat. Biotechnol., 20, 940, 10.1038/nbt729 · DOI
- Kent, 2009, Prospective isolation and molecular characterization of hematopoietic stem cells with durable self-renewal potential, Blood, 113, 6342, 10.1182/blood-2008-12-192054 · DOI
- Kiel, 2005, SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells, Cell, 121, 1109, 10.1016/j.cell.2005.05.026 · DOI · Paper page
- Li, 1995, Murine hematopoietic stem and progenitor cells: I. Enrichment and biologic characterization, Blood, 85, 1472, 10.1182/blood.V85.6.1472.bloodjournal8561472 · DOI
- Morrison, 1994, The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype, Immunity, 1, 661, 10.1016/1074-7613(94)90037-X · DOI
- Morshead, 2002, Hematopoietic competence is a rare property of neural stem cells that may depend on genetic and epigenetic alterations, Nat. Med., 8, 268, 10.1038/nm0302-268 · DOI
- Muro, 2008, Identification of gene 3′ ends by automated EST cluster analysis, Proc. Natl. Acad. Sci. USA, 105, 20286, 10.1073/pnas.0807813105 · DOI
- Nakauchi, 1999, Further characterization of CD34-low/negative mouse hematopoietic stem cells, Ann. N Y Acad. Sci., 872, 57, 10.1111/j.1749-6632.1999.tb08453.x · DOI
- Nibley, 1998, Primitive stem cells alone mediate rapid marrow recovery and multilineage engraftment after transplantation, Bone Marrow Transplant., 21, 345, 10.1038/sj.bmt.1701097 · DOI
- Nocka, 1990, Molecular bases of dominant negative and loss of function mutations at the murine c-kit/white spotting locus: W37, Wv, W41 and W, EMBO J., 9, 1805, 10.1002/j.1460-2075.1990.tb08305.x · DOI
- Osawa, 1996, Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell, Science, 273, 242, 10.1126/science.273.5272.242 · DOI
- Pawliuk, 1996, Evidence of both ontogeny and transplant dose-regulated expansion of hematopoietic stem cells in vivo, Blood, 88, 2852, 10.1182/blood.V88.8.2852.bloodjournal8882852 · DOI
- Perez-Iratxeta, 2005, Study of stem cell function using microarray experiments, FEBS Lett., 579, 1795, 10.1016/j.febslet.2005.02.020 · DOI
- Porter, 2007, StemBase: A resource for the analysis of stem cell gene expression data, Methods Mol. Biol., 407, 137, 10.1007/978-1-59745-536-7_11 · DOI
- Ramsfjell, 1999, Distinct requirements for optimal growth and in vitro expansion of human CD34(+)CD38(-) bone marrow long-term culture-initiating cells (LTC-IC), extended LTC-IC, and murine in vivo long-term reconstituting stem cells, Blood, 94, 4093, 10.1182/blood.V94.12.4093 · DOI
- Sieburg, 2006, The hematopoietic stem compartment consists of a limited number of discrete stem cell subsets, Blood, 107, 2311, 10.1182/blood-2005-07-2970 · DOI
- Till, 1964, A stochastic model of stem cell proliferation, based on the growth of spleen colony-forming cells, Proc. Natl. Acad. Sci. USA, 51, 29, 10.1073/pnas.51.1.29 · DOI
- Trevisan, 1995, Phenotypic analysis of murine long-term hemopoietic reconstituting cells quantitated competitively in vivo and comparison with more advanced colony-forming progeny, J. Exp. Med., 181, 93, 10.1084/jem.181.1.93 · DOI
- Trevisan, 1996, Cycle initiation and colony formation in culture by murine marrow cells with long-term reconstituting potential in vivo, Blood, 88, 4149, 10.1182/blood.V88.11.4149.bloodjournal88114149 · DOI
- Uchida, 2003, Different in vivo repopulating activities of purified hematopoietic stem cells before and after being stimulated to divide in vitro with the same kinetics, Exp. Hematol., 31, 1338, 10.1016/j.exphem.2003.09.001 · DOI
- Wagers, 2006, Differential expression of alpha2 integrin separates long-term and short-term reconstituting Lin-/loThy1.1(lo)c-kit+ Sca-1+ hematopoietic stem cells, Stem Cells, 24, 1087, 10.1634/stemcells.2005-0396 · DOI
- Wagers, 2002, Changes in integrin expression are associated with altered homing properties of Lin(-/lo)Thy1.1(lo)Sca-1(+)c-kit(+) hematopoietic stem cells following mobilization by cyclophosphamide/granulocyte colony-stimulating factor, Exp. Hematol., 30, 176, 10.1016/S0301-472X(01)00777-9 · DOI
- Yang, 2005, Identification of Lin(-)Sca1(+)kit(+)CD34(+)Flt3- short-term hematopoietic stem cells capable of rapidly reconstituting and rescuing myeloablated transplant recipients, Blood, 105, 2717, 10.1182/blood-2004-06-2159 · DOI
- Zhao, 2000, Murine hematopoietic stem cell characterization and its regulation in BM transplantation, Blood, 96, 3016, 10.1182/blood.V96.9.3016 · DOI
- Zhong, 2005, Gene expression profile of murine long-term reconstituting vs. short-term reconstituting hematopoietic stem cells, Proc. Natl. Acad. Sci. USA, 102, 2448, 10.1073/pnas.0409459102 · DOI
Cited by
Isolation of Single Human Hematopoietic Stem Cells Capable of Long-Term Multilineage Engraftment
Notta, F., Doulatov, S., Laurenti, E., Poeppl, A., Jurisica, I., & Dick, J. E. (2011) · Science · doi:10.1126/science.1201219 · Cited by 919
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
Kowalczyk, M. S., Tirosh, I., Heckl, D., Rao, T. N., Dixit, A., Haas, B. J., Schneider, R. K., Wagers, A. J., Ebert, B. L., & Regev, A. (2015) · Genome Research · doi:10.1101/gr.192237.115 · Cited by 778
Pietras, E. M., Reynaud, D., Kang, Y.-A., Carlin, D., Calero-Nieto, F. J., Leavitt, A. D., Stuart, J. M., Göttgens, B., & Passegué, E. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.05.003 · Cited by 723
Reynaud, D., Pietras, E., Barry-Holson, K., Mir, A., Binnewies, M., Jeanne, M., Sala-Torra, O., Radich, J. P., & Passegué, E. (2011) · Cancer Cell · doi:10.1016/j.ccr.2011.10.012 · Cited by 335
Metadata
- Authors
- Benveniste, P., Frelin, C., Janmohamed, S., Barbara, M., Herrington, R., Hyam, D., & Iscove, N. N.
- Venue
- Cell Stem Cell
- Publisher
- Elsevier BV
- Published
- 2010-01
- Volume
- 6
- Issue
- 1
- Pages
- 48-58
- ISSN
- 1934-5909
- Cited by
- 216
- References
- 2
- Language
- en
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1329 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
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
How to cite
Cite CoChat for the checks on this page, and the paper for its own findings.
- This page
- CoChat. (2026). Citation check: Intermediate-Term Hematopoietic Stem Cells with Extended but Time-Limited Reconstitution Potential. https://app.cochat.ai/papers/10.1016/j.stem.2009.11.014
- The paper
- Benveniste, P., Frelin, C., Janmohamed, S., Barbara, M., Herrington, R., Hyam, D., & Iscove, N. N. (2010). Intermediate-Term Hematopoietic Stem Cells with Extended but Time-Limited Reconstitution Potential. Cell Stem Cell. https://doi.org/10.1016/j.stem.2009.11.014