The DOI matches its Crossref record; 49 of the 49 references it cites were found in a registry or an index.
Human bone marrow hematopoietic stem cells are increased in frequency and myeloid-biased with age
Open accessAbstract
In the human hematopoietic system, aging is associated with decreased bone marrow cellularity, decreased adaptive immune system function, and increased incidence of anemia and other hematological disorders and malignancies. Recent studies in mice suggest that changes within the hematopoietic stem cell (HSC) population during aging contribute significantly to the manifestation of these age-associated hematopoietic pathologies. Though the mouse HSC population has been shown to change both quantitatively and functionally with age, changes in the human HSC and progenitor cell populations during aging have been incompletely characterized. To elucidate the properties of an aged human hematopoietic system that may predispose to age-associated hematopoietic dysfunction, we evaluated immunophenotypic HSC and other hematopoietic progenitor populations from healthy, hematologically normal young and elderly human bone marrow samples. We found that aged immunophenotypic human HSC increase in frequency, are less quiescent, and exhibit myeloid-biased differentiation potential compared with young HSC. Gene expression profiling revealed that aged immunophenotypic human HSC transcriptionally up-regulate genes associated with cell cycle, myeloid lineage specification, and myeloid malignancies. These age-associated alterations in the frequency, developmental potential, and gene expression profile of human HSC are similar to those changes observed in mouse HSC, suggesting that hematopoietic aging is an evolutionarily conserved process.
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
“Although the number of peripheral B cells decreases with age, a more pronounced decrease of B cells in AD was observed, suggesting that ongoing disease may exacerbate ageing effects [88,89].”
From Is there a role for B cells in Alzheimer's disease? (2026) · cites this paper as [89]
In the citing paper
“This shift has been correlated with increased expression of myeloid lineage genes and downregulation of those specifying a lymphoid lineage fate (11,17).”
From Causes, consequences, and reversal of immune system aging (2013) · cites this paper as [17]
In the citing paper
“From an immunologic perspective, the most profound effect of stem cell aging in both mice (11,18) and humans (17) is a decreased capacity to produce lymphocytes and an increase in myeloid potential.”
From Causes, consequences, and reversal of immune system aging (2013) · cites this paper as [17]
In the citing paper
“The age-related increase in expression of myeloid lineage genes in the studies noted above (11,17) likely resulted from the accumulation of myeloid-biased HSCs, as these analyses were performed on unseparated pools of HSCs.”
From Causes, consequences, and reversal of immune system aging (2013) · cites this paper as [17]
In the citing paper
“HSCs exhibit multiple age-related changes that include impaired adherence to stromal cells and, in some strains of mice (15,16) and elderly humans (17), an increase in number.”
From Causes, consequences, and reversal of immune system aging (2013) · cites this paper as [17]
In the citing paper
“an age-dependent increase in the frequency of putative stem cells, coinciding with impaired functionality and reduced lymphoid potential, has also been in the human system.”
From Aging of hematopoietic stem cells (2018) · cites this paper as [28]
In the citing paper
“As humans age, they typically experience an increase in total phenotypic HSC numbers as the cell pool grows with time (de Haan and Van Zant, 1999; Pang et al., 2011; Sudo et al., 2000).”
From Unraveling Hematopoiesis through the Lens of Genomics (2020) · cites this paper as Pang et al., 2011
Citations
Cites
In silico prediction of protein-protein interactions in human macrophages
Souiai, O., Guerfali, F. Z., Miled, S. B., Brun, C., & Benkahla, A. (2014) · BMC Research Notes · doi:10.1186/1756-0500-7-157 · Cited by 10,785
Significance analysis of microarrays applied to the ionizing radiation response
Tusher, V. G., Tibshirani, R., & Chu, G. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.091062498 · Cited by 10,568
Guralnik, J. M., Eisenstaedt, R. S., Ferrucci, L., Klein, H. G., & Woodman, R. C. (2004) · Blood · doi:10.1182/blood-2004-05-1812 · Cited by 1,450
McCune, J. M., Namikawa, R., Kaneshima, H., Shultz, L. D., Lieberman, M., & Weissman, I. L. (1988) · Science · doi:10.1126/science.2971269 · Cited by 1,404
Self-citationAge-related changes in lymphocyte development and function
Linton, P. J., & Dorshkind, K. A. (2004) · Nature Immunology · doi:10.1038/ni1033 · Cited by 1,199
Cell intrinsic alterations underlie hematopoietic stem cell aging
Rossi, D. J., Bryder, D., Zahn, J. M., Ahlenius, H., Sonu, R., Wagers, A. J., & Weissman, I. L. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503280102 · Cited by 1,152 · cited 3×
“Notably, the results from our functional analysis and gene expression profiling of young and elderly human HSC significantly parallel the data we and others have generated on young and elderly mouse HSC (2, 6, 36).”
BackgroundResultSelf-citationIsolation of a candidate human hematopoietic stem-cell population.
Baum, C. M., Weissman, I. L., Tsukamoto, A. S., Buckle, A., & Péault, B. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.7.2804 · Cited by 1,084
Self-citationDevelopment of functional human blood and immune systems in NOD/SCID/IL2 receptor γ chainnull mice
Ishikawa, F., Yasukawa, M., Lyons, B. L., Yoshida, S., Miyamoto, T., Yoshimoto, G., Watanabe, T., Akashi, K., Shultz, L. D., & Harada, M. (2005) · Blood · doi:10.1182/blood-2005-02-0516 · Cited by 933
The aging of hematopoietic stem cells
Morrison, S. J., Wandycz, A. M., Akashi, K., Globerson, A., & Weissman, I. L. (1996) · Nature Medicine · doi:10.1038/nm0996-1011 · Cited by 853
Self-citationPurification of primitive human hematopoietic cells capable of repopulating immune-deficient mice
Bhatia, M., Wang, J. C. Y., Kapp, U., Bonnet, D. A., & Dick, J. E. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.10.5320 · Cited by 849
Cited by
Sorted by citations
Variation in cancer risk among tissues can be explained by the number of stem cell divisions
Tomasetti, C., & Vogelstein, B. (2015) · Science · doi:10.1126/science.1260825 · Cited by 1,927
Single-cell RNA sequencing to explore immune cell heterogeneity
Papalexi, E., & Satija, R. (2018) · Nature Reviews Immunology · doi:10.1038/nri.2017.76 · Cited by 1,806
Inflammation and aging: signaling pathways and intervention therapies
Li, X., Li, C., Zhang, W., Wang, Y., Qian, P., & Huang, H. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01502-8 · Cited by 1,443
“This leads to a reduction in the number of precursors for T and B cells with increasing age.(108,109) Taken together, with aging, the number of HSCs increases, while their function including self-renewal and clonogenicity, decreases.”
BackgroundMass Cytometry: Single Cells, Many Features
Spitzer, M. H., & Nolan, G. P. (2016) · Cell · doi:10.1016/j.cell.2016.04.019 · Cited by 1,199
Age-dependent dysregulation of innate immunity
Shaw, A. C., Goldstein, D. R., & Montgomery, R. R. (2013) · Nature Reviews Immunology · doi:10.1038/nri3547 · Cited by 1,061
Immunosenescence: molecular mechanisms and diseases
Liu, Z., Liang, Q., Ren, Y., Guo, C., Ge, X., Wang, L., Cheng, Q., Luo, P., Zhang, Y., & Han, X. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01451-2 · Cited by 1,082
Understanding immunosenescence to improve responses to vaccines
Goronzy, J. J., & Weyand, C. M. (2013) · Nature Immunology · doi:10.1038/ni.2588 · Cited by 827
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
Measuring biological aging in humans: a quest
Ferrucci, L., Gonzalez‐Freire, M., Fabbri, E., Simonsick, E., Tanaka, T., Moore, Z., Salimi, S., Sierra, F., & de Cabo, R. (2020) · Aging Cell · doi:10.1111/acel.13080 · Cited by 781
Distinct routes of lineage development reshape the human blood hierarchy across ontogeny
Notta, F., Zandi, S., Takayama, N., Dobson, S., Gan, O. I., Wilson, G., Kaufmann, K. B., McLeod, J., Laurenti, E., Dunant, C. F., et al. (2016) · Science · doi:10.1126/science.aab2116 · Cited by 780
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
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
The ageing haematopoietic stem cell compartment
Geiger, H., de Haan, G., & Florian, M. C. (2013) · Nature Reviews Immunology · doi:10.1038/nri3433 · Cited by 604
Immunosenescence and inflammaging in the aging process: age-related diseases or longevity?
Santoro, A., Bientinesi, E., & Monti, D. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101422 · Cited by 603
Cancer stem cell–immune cell crosstalk in tumour progression
Bayık, D., & Lathia, J. D. (2021) · Nature reviews. Cancer · doi:10.1038/s41568-021-00366-w · Cited by 564
Immunosenescence and human vaccine immune responses
Crooke, S. N., Ovsyannikova, I. G., Poland, G. A., & Kennedy, R. B. (2019) · Immunity & Ageing · doi:10.1186/s12979-019-0164-9 · Cited by 530
Xist RNA Is a Potent Suppressor of Hematologic Cancer in Mice
Yildirim, E., Kirby, J. E., Brown, D. E., Mercier, F., Sadreyev, R. I., Scadden, D. T., & Lee, J. T. (2013) · Cell · doi:10.1016/j.cell.2013.01.034 · Cited by 532
Senescent cell clearance by the immune system: Emerging therapeutic opportunities
Prata, L. G. P. L., Ovsyannikova, I. G., Tchkonia, T., & Kirkland, J. L. (2018) · Seminars in Immunology · doi:10.1016/j.smim.2019.04.003 · Cited by 497
Beerman, I., Bock, C., Garrison, B. S., Smith, Z. D., Gu, H., Meissner, A., & Rossi, D. J. (2013) · Cell Stem Cell · doi:10.1016/j.stem.2013.01.017 · Cited by 485
Self-citationCheng, C., Adams, G. B., Perin, L., Wei, M., Zhou, X., Lam, B. S., Sacco, S. D., Mirisola, M. G., Quinn, D. I., Dorff, T. B., et al. (2014) · Cell stem cell · doi:10.1016/j.stem.2014.04.014 · Cited by 491
Clonal Hematopoiesis and Evolution to Hematopoietic Malignancies
Bowman, R. L., Busque, L., & Levine, R. L. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.01.011 · Cited by 448
Beerman, I., Seita, J., Inlay, M. A., Weissman, I. L., & Rossi, D. J. (2014) · Cell Stem Cell · doi:10.1016/j.stem.2014.04.016 · Cited by 445
Self-citationContributions of Age-Related Thymic Involution to Immunosenescence and Inflammaging
Thomas, R., Wang, W., & Su, D.-M. (2020) · Immunity & Ageing · doi:10.1186/s12979-020-0173-8 · Cited by 442
Aging of hematopoietic stem cells
de Haan, G., & Lazare, S. S. (2018) · Blood · doi:10.1182/blood-2017-06-746412 · Cited by 432
Vaccination in the elderly: The challenge of immune changes with aging
Ciabattini, A., Nardini, C., Santoro, F., Garagnani, P., Franceschi, C., & Medaglini, D. (2018) · Seminars in Immunology · doi:10.1016/j.smim.2018.10.010 · Cited by 411
DNA damage checkpoints in stem cells, ageing and cancer
Sperka, T., Wang, J., & Rudolph, K. L. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3420 · Cited by 393
Aged skeletal stem cells generate an inflammatory degenerative niche
Ambrosi, T. H., Marecic, O., McArdle, A., Sinha, R., Gulati, G. S., Tong, X., Wang, Y., Steininger, H. M., Hoover, M. Y., Koepke, L. S., et al. (2021) · Nature · doi:10.1038/s41586-021-03795-7 · Cited by 392
Self-citationBao, H., Cao, J., Chen, M., Min, C., Chen, W., Chen, X., Chen, Y., Chen, Y., Chen, Y., Chen, Z., et al. (2023) · Science China Life Sciences · doi:10.1007/s11427-023-2305-0 · Cited by 402
Aging and the immune system: An overview
Akha, A. A. S. (2018) · Journal of Immunological Methods · doi:10.1016/j.jim.2018.08.005 · Cited by 403
Alcohol and endogenous aldehydes damage chromosomes and mutate stem cells
Garaycoechea, J. I., Crossan, G. P., Langevin, F., Mulderrig, L., Louzada, S., Yang, F., Guilbaud, G., Park, N., Roerink, S. F., Nik‐Zainal, S., et al. (2018) · Nature · doi:10.1038/nature25154 · Cited by 397
Buscarlet, M., Provost, S., Zada, Y. F., Barhdadi, A., Bourgoin, V., Lépine, G., Mollica, L., Szuber, N., Dubé, M.-P., & Busque, L. (2017) · Blood · doi:10.1182/blood-2017-04-777029 · Cited by 383
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 386
Inflamm-aging of hematopoiesis, hematopoietic stem cells, and the bone marrow microenvironment
Kovtonyuk, L. V., Fritsch, K., Feng, X., Manz, M. G., & Takizawa, H. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00502 · Cited by 371
Adrover, J. M., McDowell, S. A. C., He, X., Quail, D. F., & Egeblad, M. (2023) · Cancer Cell · doi:10.1016/j.ccell.2023.02.001 · Cited by 365
Human Hemato-Lymphoid System Mice: Current Use and Future Potential for Medicine
Rongvaux, A., Takizawa, H., Strowig, T., Willinger, T., Eynon, E. E., Flavell, R. A., & Manz, M. G. (2013) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032712-095921 · Cited by 359
Single-cell transcriptomics reveals expansion of cytotoxic CD4 T cells in supercentenarians
Hashimoto, K., Kouno, T., Ikawa, T., Hayatsu, N., Miyajima, Y., Yabukami, H., Terooatea, T., Sasaki, T., Suzuki, T., Valentine, M., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1907883116 · Cited by 343
Grover, A., Sanjuán-Pla, A., Thongjuea, S., Carrelha, J., Giustacchini, A., Gambardella, A. R., Macaulay, I. C., Mancini, E., Luis, T. C., Mead, A. J., et al. (2016) · Nature Communications · doi:10.1038/ncomms11075 · Cited by 361
Neutrophil phenotypes and functions in cancer: A consensus statement
Quail, D. F., Amulic, B., Aziz, M., Barnes, B. J., Eruslanov, E. B., Fridlender, Z. G., Goodridge, H. S., Granot, Z., Hidalgo, A., Huttenlocher, A., et al. (2022) · The Journal of Experimental Medicine · doi:10.1084/jem.20220011 · Cited by 347
Age-associated epigenetic drift: implications, and a case of epigenetic thrift?
Teschendorff, A. E., West, J., & Beck, S. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt375 · Cited by 330
Ho, Y.-H., del Toro, R., Rivera-Torres, J., Rak, J., Korn, C., García-García, A., Macías, D., González-Gómez, C., del Monte, A., Wittner, M., et al. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2019.06.007 · Cited by 315
Interconnections between Inflammageing and Immunosenescence during Ageing
Teissier, T., Boulanger, É., & Cox, L. S. (2022) · Cells · doi:10.3390/cells11030359 · Cited by 323
Aging, inflammation, immunity and periodontal disease
Ebersole, J. L., Graves, C. L., González, O. A., Dawson, D. R., Morford, L. A., Emecen‐Huja, P., Hartsfield, J. K., Huja, S. S., Pandruvada, S. N. M., & Wallet, S. M. (2016) · Periodontology 2000 · doi:10.1111/prd.12135 · Cited by 315
The total mass, number, and distribution of immune cells in the human body
Sender, R., Weiss, Y., Navon, Y., Milo, I., Azulay, N., Keren, L., Fuchs, S., Ben-Zvi, D., Noor, E., & Milo, R. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2308511120 · Cited by 300
Caiado, F., Pietras, E. M., & Manz, M. G. (2021) · Journal of Experimental Medicine · doi:10.1084/jem.20201541 · Cited by 289
Hematopoietic stem cells count and remember self-renewal divisions
Bernitz, J. M., Kim, H. S., MacArthur, B., Sieburg, H., & Moore, K. (2016) · Cell · doi:10.1016/j.cell.2016.10.022 · Cited by 285
Niche heterogeneity in the bone marrow
Birbrair, A., & Frenette, P. S. (2016) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13016 · Cited by 313
Hematopoietic stem cell and progenitor cell mechanisms in myelodysplastic syndromes
Pang, W. W., Pluvinage, J. V., Price, E. A., Sridhar, K., Arber, D. A., Greenberg, P. L., Schrier, S. L., Park, C. Y., & Weissman, I. L. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1222861110 · Cited by 277
Self-citationHuman bone marrow assessment by single-cell RNA sequencing, mass cytometry, and flow cytometry
Oetjen, K. A., Lindblad, K. E., Goswami, M., Gui, G., Dagur, P. K., Lai, C., Dillon, L. W., McCoy, J. P., & Hourigan, C. S. (2018) · JCI Insight · doi:10.1172/jci.insight.124928 · Cited by 272
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
Markers of T Cell Senescence in Humans
Xu, W., & Larbi, A. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18081742 · Cited by 261
The Human Cell Atlas bone marrow single-cell interactive web portal
Hay, S. B., Ferchen, K., Chetal, K., Grimes, H. L., & Salomonis, N. (2018) · Experimental Hematology · doi:10.1016/j.exphem.2018.09.004 · Cited by 256
Cell Therapy: Types, Regulation, and Clinical Benefits
El-Kadiry, A. E.-H., Rafei, M., & Shammaa, R. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.756029 · Cited by 256
Mosaicism in health and disease — clones picking up speed
Forsberg, L. A., Gisselsson, D., & Dumanski, J. P. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2016.145 · Cited by 261
Platelet factors attenuate inflammation and rescue cognition in ageing
Schroer, A. B., Ventura, P. B., Sucharov, J., Misra, R., Chui, M. K. K., Bieri, G., Horowitz, A. M., Smith, L. K., Encabo, K., Tenggara, I., et al. (2023) · Nature · doi:10.1038/s41586-023-06436-3 · Cited by 252
Regulation of hematopoietic and leukemic stem cells by the immune system
Riether, C., Schürch, C. M., & Ochsenbein, A. F. (2014) · Cell Death and Differentiation · doi:10.1038/cdd.2014.89 · Cited by 253
Loss of Dnmt3a Immortalizes Hematopoietic Stem Cells In Vivo
Jeong, M., Park, H. J., Celik, H., Ostrander, E. L., Reyes, J. M., Guzman, A., Rodriguez, B., Lei, Y., Lee, Y., Ding, L., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.03.025 · Cited by 243
Depleting myeloid-biased haematopoietic stem cells rejuvenates aged immunity
Ross, J., Myers, L. M., Noh, J. J., Collins, M. M., Carmody, A., Messer, R. J., Dhuey, E., Hasenkrug, K. J., & Weissman, I. L. (2024) · Nature · doi:10.1038/s41586-024-07238-x · Cited by 245
Self-citationIBD across the age spectrum—is it the same disease?
Ruel, J., Ruane, D., Mehandru, S., Gower‐Rousseau, C., & Colombel, J. (2013) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2013.240 · Cited by 244
Rps14 haploinsufficiency causes a block in erythroid differentiation mediated by S100A8 and S100A9
Schneider, R. K., Schenone, M., Ferreira, M. S. V., Kramann, R., Joyce, C. E., Hartigan, C. R., Beier, F., Brümmendorf, T. H., Germing, U., Platzbecker, U., et al. (2016) · Nature Medicine · doi:10.1038/nm.4047 · Cited by 246
Shin, J. Y., Hu, W., Naramura, M., & Park, C. Y. (2014) · The Journal of Experimental Medicine · doi:10.1084/jem.20131128 · Cited by 234
Bacos, K., Gillberg, L., Volkov, P., Olsson, A. H., Hansen, T. F., Pedersen, O. B., Gjesing, A. P., Eiberg, H., Tuomilehto, J., Almgren, P., et al. (2016) · Nature Communications · doi:10.1038/ncomms11089 · Cited by 242
Targeting immune dysfunction in aging
Borgoni, S., Kudryashova, K. S., Burka, K., & de Magalhães, J. P. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101410 · Cited by 232
Chronic immune response dysregulation in MDS pathogenesis
Barreyro, L., Chlon, T. M., & Starczynowski, D. T. (2018) · Blood · doi:10.1182/blood-2018-03-784116 · Cited by 226
Circulating hematopoietic stem and progenitor cells are myeloid-biased in cancer patients
Wu, W., Sun, H.-W., Chen, H., Liang, J., Yu, X.-J., Wu, C., Wang, Z., & Zheng, L. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1320753111 · Cited by 231
Retinal stem cell transplantation: Balancing safety and potential
Singh, M. S., Park, S. S., Albini, T. A., Canto-Soler, M. V., Klassen, H. J., MacLaren, R. E., Takahashi, M., Nagiel, A., Schwartz, S. D., & Bharti, K. (2019) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2019.100779 · Cited by 228
Adelman, E. R., Huang, H.-T., Roisman, A., Olsson, A., Colaprico, A., Qin, T., Lindsley, R. C., Bejar, R. L., Salomonis, N., Grimes, H. L., et al. (2019) · Cancer Discovery · doi:10.1158/2159-8290.cd-18-1474 · Cited by 234
Myocardial Infarction Activates CCR2+ Hematopoietic Stem and Progenitor Cells
Dutta, P., Sager, H. B., Stengel, K. R., Naxerova, K., Courties, G., Sáez, B., Silberstein, L., Heidt, T., Sebas, M., Sun, Y., et al. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.04.008 · Cited by 226
Decline in IGF1 in the bone marrow microenvironment initiates hematopoietic stem cell aging
Young, K., Eudy, E., Bell, R., Loberg, M. A., Stearns, T., Sharma, D., Velten, L., Haas, S., Filippi, M.-D., & Trowbridge, J. J. (2021) · Cell Stem Cell · doi:10.1016/j.stem.2021.03.017 · Cited by 216
Immunosenescence, aging and successful aging
Wang, Y., Chen, D., Han, Y., Gu, Z., & Sun, C. C. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.942796 · Cited by 237
Impact of genomic damage and ageing on stem cell function
Behrens, A., van Deursen, J. M., Rudolph, K. L., & Schumacher, B. (2014) · Nature Cell Biology · doi:10.1038/ncb2928 · Cited by 207
Understanding intrinsic hematopoietic stem cell aging
Mejía-Ramírez, E., & Florian, M. C. (2019) · Haematologica · doi:10.3324/haematol.2018.211342 · Cited by 206
Immune checkpoint inhibitors and elderly people: A review
Daste, A., Domblides, C., Gross‐Goupil, M., Chakiba, C., Quivy, A., Cochin, V., de Monès, E., Larmonier, N., Soubeyran, P., & Ravaud, A. (2017) · European Journal of Cancer · doi:10.1016/j.ejca.2017.05.044 · Cited by 194
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
ADAR1 promotes malignant progenitor reprogramming in chronic myeloid leukemia
Jiang, Q., Crews, L. A., Barrett, C. L., Chun, H.-J. E., Court, A. C., Isquith, J. M., Zipeto, M., Goff, D. J., Minden, M. D., Sadarangani, A., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1213021110 · Cited by 189
Human immune diversity: from evolution to modernity
Liston, A., Humblet-Baron, S., Duffy, D., & Goris, A. (2021) · Nature Immunology · doi:10.1038/s41590-021-01058-1 · Cited by 187
Immunosenescence, Inflammaging, and Frailty: Role of Myeloid Cells in Age-Related Diseases
Bleve, A., Motta, F., Durante, B., Pandolfo, C., Selmi, C., & Sica, A. (2022) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-021-08909-7 · Cited by 185
Mitochondrial Potentiation Ameliorates Age-Related Heterogeneity in Hematopoietic Stem Cell Function
Mansell, E., Sigurðsson, V., Deltcheva, E. M., Brown, J., James, C. T., Miharada, K., Soneji, S., Larsson, J. T., & Enver, T. (2020) · Cell stem cell · doi:10.1016/j.stem.2020.09.018 · Cited by 187
Aging, Clonality, and Rejuvenation of Hematopoietic Stem Cells
Akunuru, S., & Geiger, H. (2016) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2016.06.003 · Cited by 178
Chichili, G. R., Huang, L., Li, H., Burke, S., He, L., Tang, Q., Jin, L. X., Gorlatov, S. N., Ciccarone, V. C., Chen, F., et al. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.aaa5693 · Cited by 173
Kotini, A. G., Chang, C.-J., Boussaad, I., Delrow, J. J., Dolezal, E. K., Nagulapally, A. B., Perna, F., Fishbein, G. A., Klimek, V. M., Hawkins, R. D., et al. (2015) · Nature Biotechnology · doi:10.1038/nbt.3178 · Cited by 171
B cell maintenance and function in aging
Kogut, I., Scholz, J. L., Cancro, M. P., & Cambier, J. C. (2012) · Seminars in Immunology · doi:10.1016/j.smim.2012.04.004 · Cited by 166
IL-1 mediates microbiome-induced inflammaging of hematopoietic stem cells in mice
Kovtonyuk, L. V., Caiado, F., Garcia-Martin, S., Manz, E.-M., Helbling, P., Takizawa, H., Boettcher, S., Al-Shahrour, F., Nombela-Arrieta, C., Slack, E., et al. (2022) · Blood · doi:10.1182/blood.2021011570 · Cited by 166
Hematopoietic Stem Cells and Their Roles in Tissue Regeneration
Lee, J. Y., & Hong, S.-H. (2020) · International Journal of Stem Cells · doi:10.15283/ijsc19127 · Cited by 165
Stem cell heterogeneity: implications for aging and regenerative medicine
Müller‐Sieburg, C. E., Sieburg, H. B., Bernitz, J. M., & Cattarossi, G. (2012) · Blood · doi:10.1182/blood-2011-12-376749 · Cited by 164
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
Aged marrow macrophages expand platelet-biased hematopoietic stem cells via interleukin-1B
Frisch, B. J., Hoffman, C. M., Latchney, S. E., LaMere, M. W., Myers, J., Ashton, J., Li, A. J., Saunders, J., Palis, J., Perkins, A. S., et al. (2019) · JCI Insight · doi:10.1172/jci.insight.124213 · Cited by 160
Cell size is a determinant of stem cell potential during aging
Lengefeld, J., Cheng, C., Maretich, P., Blair, M., Hagen, H. R., McReynolds, M. R., Sullivan, E. J., Majors, K., Roberts, C., Kang, J. H., et al. (2021) · Science Advances · doi:10.1126/sciadv.abk0271 · Cited by 165
The NLRP3 inflammasome triggers sterile neuroinflammation and Alzheimer’s disease
Milner, M. T., Maddugoda, M. P., Götz, J., Burgener, S. S., & Schroder, K. (2020) · Current Opinion in Immunology · doi:10.1016/j.coi.2020.10.011 · Cited by 162
Immunosenescence and inflammaging: Mechanisms and role in diseases
Ajoolabady, A., Praticò, D., Tang, D., Zhou, S., Franceschi, C., & Ren, J. T. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102540 · Cited by 172
Zeng, X., Li, X., Li, X., Wei, C., Shi, C., Hu, K., Kong, D., Luo, Q., Xu, Y., Shan, W., et al. (2023) · Blood · doi:10.1182/blood.2022017514 · Cited by 157
Immunosenescence: signaling pathways, diseases and therapeutic targets
Fu, Y., Wang, B., Alu, A., Hong, W., Hong, L., He, X., Shi, H., Cheng, P., & Yang, X. (2025) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02371-z · Cited by 168
Sceneay, J., Goreczny, G. J., Wilson, K., Morrow, S., DeCristo, M. J., Ubellacker, J. M., Qin, Y., Laszewski, T., Stover, D. G., Barrera, V., et al. (2019) · Cancer Discovery · doi:10.1158/2159-8290.cd-18-1454 · Cited by 156
Salminen, A., Kaarniranta, K., & Kauppinen, A. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03048-x · Cited by 156
Rimmelé, P., Bigarella, C. L., Liang, R. H.-S., Izac, B., Dieguez‐Gonzalez, R., Barbet, G., Donovan, M. J., Brugnara, C., Blander, J. M., Sinclair, D. A., et al. (2014) · Stem Cell Reports · doi:10.1016/j.stemcr.2014.04.015 · Cited by 154
Activation of immunosuppressive network in the aging process
Salminen, A. (2019) · Ageing Research Reviews · doi:10.1016/j.arr.2019.100998 · Cited by 155
Nilsson, A. R., Soneji, S., Adolfsson, S., Bryder, D., & Pronk, C. J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0158369 · Cited by 161
Aging-associated inflammation promotes selection for adaptive oncogenic events in B cell progenitors
Henry, C. J., Casás-Selves, M., Kim, J., Zaberezhnyy, V., Aghili, L., Daniel, A. E., Jimenez, L., Azam, T., McNamee, E. N., Clambey, E. T., et al. (2015) · Journal of Clinical Investigation · doi:10.1172/jci83024 · Cited by 148
Musashi-2 controls cell fate, lineage bias, and TGF-β signaling in HSCs
Park, S., Deering, R. P., Lu, Y., Tivnan, P., Lianoglou, S., Al‐Shahrour, F., Ebert, B. L., Hacohen, N., Leslie, C. S., Daley, G. Q., et al. (2014) · The Journal of Experimental Medicine · doi:10.1084/jem.20130736 · Cited by 147
Organ-on-a-chip model of vascularized human bone marrow niches
Glaser, D. E., Curtis, M. B., Sariano, P. A., Rollins, Z. A., Shergill, B. S., Anand, A., Deely, A. M., Shirure, V. S., Anderson, L., Lowen, J. M., et al. (2022) · Biomaterials · doi:10.1016/j.biomaterials.2021.121245 · Cited by 146
Neutrophils in aging and aging‐related pathologies
Avondt, K. V., Strecker, J., Tulotta, C., Minnerup, J., Schulz, C., & Soehnlein, O. (2022) · Immunological Reviews · doi:10.1111/imr.13153 · Cited by 155
Metadata
- Authors
- Pang, W. W., Price, E. A., Sahoo, D., Beerman, I., Maloney, W. J., Rossi, D. J., Schrier, S. L., & Weissman, I. L.
- Affiliations
- Institute for Stem Cell Biology and Regenerative Medicine (IN)
- Department of Internal Medicine, Division of Hematology, and
- Harvard University (US)
- Stanford Medicine (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2011-11-28
- Volume
- 108
- Issue
- 50
- Pages
- 20012-20017
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3250139
- OpenAlex
- W2028815852
- Cited by
- 991
- References
- 49
- Citations by year
- 2026: 79 · 2025: 79 · 2024: 93 · 2023: 87 · 2022: 85 · 2021: 91 · 2020: 83 · 2019: 55 · 2018: 59 · 2017: 54 · 2016: 51 · 2015: 49 · 2014: 63 · 2013: 36 · 2012: 26
- FWCI
- 27.35
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Aging (R01AG029124)
- National Cancer Institute (R01CA086065, K99CA151673)
- 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 › Acute Myeloid Leukemia Research
- Keywords
- hematopoietic stem cells, aging, bone marrow, myeloid differentiation, HSC quiescence, hematopoietic progenitor cells, gene expression profiling, immunophenotype, myeloid neoplasms
- MeSH terms
- Adult, Aged, Aged, 80 and over, Aging, Animals, Bone Marrow Cells, Cell Count, Cell Differentiation, Gene Expression Regulation, Hematopoietic Stem Cells, Humans, Middle Aged, Cell Lineage, Gene Expression Profiling, Myeloid Cells, Mice, Young Adult
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