Genetic analysis of hemopoietic cell cycling in mice suggests its involvement in organismal life span

de Haan, Gerald; van Zant, Gary

doi:10.1096/fasebj.13.6.707

Cited by 87Genetics, Aging, and Longevity in Model OrganismsTelomeres, Telomerase, and SenescenceHematopoietic Stem Cell Transplantation

Genetic analysis of hemopoietic cell cycling in mice suggests its involvement in organismal life span

de Haan, Gerald, van Zant, Gary·1999·The FASEB Journal

DOI 10.1096/fasebj.13.6.707

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Abstract

Normal somatic cells undergo replicative senescence in vitro but the significance of this process in organismic aging remains controversial. We have shown previously that hemopoietic stem cells of common inbred strains of mice vary widely in cycling activity and that this parameter is inversely correlated with strain-dependent mean life span. To assess whether cell cycling and life span are causally related, we searched for quantitative trait loci (QTLs) that contributed to variation of these traits in BXH and BXD recombinant inbred mice. Two QTLs, mapping to exactly the same intervals on chromosomes 7 and 11, were identified that were associated with variation of both cell cycling and life span. The locus on chromosome 11 mapped to the cytokine cluster, a segment that shows synteny with human chromosome 5q, in which deletions are strongly associated with myelodysplastic syndrome. These data indicate that steady-state cell turn-over, here measured in hemopoietic progenitor cells, may have a significant effect on the mean life span of mammals.

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From Aging of hematopoietic stem cells (2018) · cites this paper as [30]

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
The limited in vitro lifetime of human diploid cell strains
Hayflick, L. (1965) · Experimental Cell Research · doi:10.1016/0014-4827(65)90211-9 · Cited by 5,876 · see citing works
Genetic dissection of complex traits: guidelines for interpreting and reporting linkage results
Lander, E. S., & Kruglyak, L. (1995) · Nature Genetics · doi:10.1038/ng1195-241 · Cited by 5,196 · see citing works
Extension of Life-Span by Introduction of Telomerase into Normal Human Cells
Bodnar, A. G., Ouellette, M., Frolkis, M., Holt, S. E., Chiu, C.-P., Morin, G. B., Harley, C. B., Shay, J. W., Lichtsteiner, S., & Wright, W. E. (1998) · Science · doi:10.1126/science.279.5349.349 · Cited by 4,975 · see citing works
Empirical threshold values for quantitative trait mapping.
Churchill, G. A., & Doerge, R. W. (1994) · Genetics · doi:10.1093/genetics/138.3.963 · Cited by 4,950 · see citing works
Telomere length predicts replicative capacity of human fibroblasts.
Allsopp, R. C., Vaziri, H., Patterson, C., Goldstein, S., Younglai, E. V., Futcher, A. B., Greider, C. W., & Harley, C. B. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.21.10114 · Cited by 2,200 · see citing works
Biology of the Laboratory Mouse
Heston, W. E. (1967) · Journal of Heredity · doi:10.1093/oxfordjournals.jhered.a107528 · Cited by 1,396 · 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
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 · see citing works
Replicative Senescence: Implications for in Vivo Aging and Tumor Suppression
Smith, J. R., & Pereira-Smith, O. M. (1996) · Science · doi:10.1126/science.273.5271.63 · Cited by 547 · see citing works
A Macintosh program for storage and analysis of experimental genetic mapping data
Manly, K. F. (1993) · Mammalian Genome · doi:10.1007/bf00357089 · Cited by 502 · see citing works
Replicative Senescence: An Old Lives' Tale?
Campisi, J. (1996) · Cell · doi:10.1016/s0092-8674(00)81023-5 · Cited by 434 · see citing works
Ontogeny-related changes in proliferative potential of human hematopoietic cells.
Lansdorp, P. M., Dragowska, W. H., & Mayani, H. (1993) · The Journal of Experimental Medicine · doi:10.1084/jem.178.3.787 · Cited by 384 · see citing works
Deletion of IRF-1 , Mapping to Chromosome 5q31.1, in Human Leukemia and Preleukemic Myelodysplasia
Willman, C. L., Sever, C. E., Pallavicini, M. G., Harada, H., Tanaka, N., Slovak, M. L., Yamamoto, H., Harada, K., Meeker, T. C., List, A. F., et al. (1993) · Science · doi:10.1126/science.8438156 · Cited by 380 · see citing works
A Genomic Scan for Selection Reveals Candidates for Genes Involved in the Evolution of Cultivated Sunflower (Helianthus annuus)
Chapman, M. A., Pashley, C. H., Wenzler, J., Hvala, J., Tang, S., Knapp, S. J., & Burke, J. M. (2008) · The Plant Cell · doi:10.1105/tpc.108.059808 · Cited by 361 · see citing works
Evidence for a relationship between longevity of mammalian species and life spans of normal fibroblasts in vitro and erythrocytes in vivo
Röhme, D. (1981) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.78.8.5009 · Cited by 351 · see citing works
Mouse Strain-Dependent Changes in Frequency and Proliferation of Hematopoietic Stem Cells During Aging: Correlation Between Lifespan and Cycling Activity
de Haan, G., NIJHOF, W., & Zant, G. E. V. (1997) · Blood · doi:10.1182/blood.v89.5.1543 · Cited by 300 · see citing works
Use of limiting-dilution type long-term marrow cultures in frequency analysis of marrow-repopulating and spleen colony-forming hematopoietic stem cells in the mouse
Ploemacher, R., der Sluijs, J. V., van Beurden, C., Baert, M., & Chan, P. (1991) · Blood · doi:10.1182/blood.v78.10.2527.2527 · Cited by 261 · see citing works
Rapid accumulation of genome rearrangements in liver but not in brain of old mice
Dollé, M. E. T., Giese, H., Hopkins, C. L., Martus, H., Hausdorff, J. M., & Vijg, J. (1997) · Nature Genetics · doi:10.1038/ng1297-431 · Cited by 248 · see citing works
The 5q-syndrome
Boultwood, J., Lewis, S. M., & Wainscoat, J. S. (1994) · Blood · doi:10.1182/blood.v84.10.3253.3253 · Cited by 244 · see citing works
Cytogenetic and molecular delineation of the smallest commonly deleted region of chromosome 5 in malignant myeloid diseases.
Beau, M. M. L., Espinosa, R., Neuman, W. L., Stock, W., Roulston, D., Larson, R. A., Keinänen, M., & Westbrook, C. A. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.12.5484 · Cited by 238 · see citing works
Accelerated telomere shortening in young recipients of allogeneic bone-marrow transplants
Wynn, R. F., Cross, M. A., Hatton, C. E., Will, A., Lashford, L. S., Dexter, T. M., & Testa, N. G. (1998) · The Lancet · doi:10.1016/s0140-6736(97)08256-1 · Cited by 228 · see citing works
Cell aging in vivo and in vitro
Rubin, H. (1997) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(97)00067-5 · Cited by 226 · see citing works
Studies of hematopoietic stem cells spared by 5-fluorouracil.
Zant, G. V. (1984) · The Journal of Experimental Medicine · doi:10.1084/jem.159.3.679 · Cited by 210 · see citing works
Dynamic Changes in Mouse Hematopoietic Stem Cell Numbers During Aging
de Haan, G., & Van Zant, G. (1999) · Blood · doi:10.1182/blood.v93.10.3294.410k07_3294_3301 · Cited by 208 · see citing works
In vivo telomere dynamics of human hematopoietic stem cells
Notaro, R., Cimmino, A., Tabarini, D., Rotoli, B., & Luzzatto, L. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.25.13782 · Cited by 196 · see citing works
ORGANIZATION OF HAEMOPOIETIC STEM CELLS: THE GENERATION‐AGE HYPOTHESIS
Rosendaal, M., HODGSON, G. S., & Bradley, T. R. (1979) · Cell Proliferation · doi:10.1111/j.1365-2184.1979.tb00110.x · Cited by 176 · see citing works
Murine chromosomal regions correlated with longevity.
Gelman, R. S., Watson, A., Bronson, R. T., & Yunis, E. J. (1988) · Genetics · doi:10.1093/genetics/118.4.693 · Cited by 156 · see citing works
Molecular delineation of the smallest commonly deleted region of chromosome 5 in malignant myeloid diseases to 1–1.5 Mb and preparation of a PAC-based physical map
Zhao, N., Stoffel, A., Wang, P. W., Eisenbart, J. D., Espinosa, R., Larson, R. A., & Beau, M. M. L. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.13.6948 · Cited by 150 · see citing works
Intrinsic and extrinsic control of hemopoietic stem cell numbers: mapping of a stem cell gene
Haan, G. D., & Zant, G. V. (1997) · The Journal of Experimental Medicine · doi:10.1084/jem.186.4.529 · Cited by 134 · cited 4× · see citing works
“activity that is inversely correlated with organismal life span (5, 6).”
BackgroundInfluential
Long-term erythropoietic repopulating ability of old, young, and fetal stem cells.
Harrison, D. E. (1983) · The Journal of Experimental Medicine · doi:10.1084/jem.157.5.1496 · Cited by 123 · see citing works
Natural Variation in Neuron Number in Mice Is Linked to a Major Quantitative Trait Locus on Chr 11
Williams, R. W., Strom, R. C., & Goldowitz, D. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-01-00138.1998 · Cited by 120 · see citing works
Genetic control of the frequency of hematopoietic stem cells in mice: mapping of a candidate locus to chromosome 1.
Müller‐Sieburg, C. E., & Riblet, R. J. (1996) · The Journal of Experimental Medicine · doi:10.1084/jem.183.3.1141 · Cited by 109 · see citing works
Transient and permanent engraftment potential of murine hematopoietic stem cell subsets: differential effects of host conditioning with gamma radiation and cytotoxic drugs.
Jd, D., & Ploemacher, R. (1993) · PubMed · Cited by 108 · see citing works
Genotype-restricted growth and aging patterns in hematopoietic stem cell populations of allophenic mice
Van Zant, G., Holland, B. P., Eldridge, P. W., & Chen, J. J. (1990) · The Journal of Experimental Medicine · doi:10.1084/jem.171.5.1547 · Cited by 99 · cited 2× · see citing works
“the maximal life span of that strain (7).”
Background
Molecular Mapping of Uncharacteristically Small 5q Deletions in Two Patients with the 5q- Syndrome: Delineation of the Critical Region on 5q and Identification of a 5q- Breakpoint
Boultwood, J., Fidler, C., Lewis, S. M., Kelly, S., Sheridan, H., Littlewood, T. J., Buckle, V. J., & Wainscoat, J. S. (1994) · Genomics · doi:10.1006/geno.1994.1090 · Cited by 87 · see citing works
Genetic control of hematopoietic kinetics revealed by analyses of allophenic mice and stem cell suicide
Zant, G. E. V., Eldridge, P. W., Behringer, R. R., & Dewey, M. J. (1983) · Cell · doi:10.1016/0092-8674(83)90096-x · Cited by 75 · see citing works
Wheat germ agglutinin affinity of murine hemopoietic stem cell subpopulations is an inverse function of their long-term repopulating ability in vitro and in vivo.
Ploemacher, R., van der Loo, J. C. M., Beurden, C. A. J. V. D. L.-V., & Baert, M. R. M. (1993) · PubMed · Cited by 68 · see citing works
Lifespan and aging patterns.
Russell, E. S. (1966) · The Mouseion at the JAXlibrary (Jackson Laboratory) · Cited by 67 · see citing works
Physical mapping of the minimal region of loss in 5q- chromosome.
Fairman, J., Chumakov, I. M., Chinault, A. C., Nowell̀, P. C., & Nagarajan, L. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.16.7406 · Cited by 66 · see citing works
Ponce d'elegans: Genetic Quest for the Fountain of Youth
Kenyon, C. J. (1996) · Cell · doi:10.1016/s0092-8674(00)81024-7 · Cited by 59 · see citing works
Synergistic effects of interleukin-11 with other growth factors on the expansion of murine hematopoietic progenitors and maintenance of stem cells in liquid culture.
Neben, S., Donaldson, D. D., Sieff, C. A., Mauch, P. M., Bodine, D., Ferrara, J. L. M., Yetz-Aldape, J., & Turner, K. (1994) · PubMed · Cited by 56 · see citing works
Normal Function of Transplanted Mouse Erythrocyte Precursors for 21 Months beyond Donor Life Spans
Harrison, D. E. (1972) · Nature New Biology · doi:10.1038/newbio237220a0 · Cited by 53 · see citing works
A putative gene causes variability in lifespan among genotypically identical mice
de Haan, G., Gelman, R. S., Watson, A., Yunis, E. J., & Zant, G. E. V. (1998) · Nature Genetics · doi:10.1038/465 · Cited by 50 · see citing works
Alternatives to stem cell renewal from a developmental viewpoint.
Zant, G. V., de Haan, G., & Rich, I. N. (1997) · PubMed · Cited by 48 · see citing works
Genetic analysis of aging in Saccharomyces cerevisiae
Kennedy, B. K., & Guarente, L. (1996) · Trends in Genetics · doi:10.1016/s0168-9525(96)80018-7 · Cited by 27 · see citing works
Mechanisms of cellular senescence
Smeal, T., & Guarente, L. (1997) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(97)80139-6 · Cited by 26 · see citing works
Prophylactic pretreatment of mice with hematopoietic growth factors induces expansion of primitive cell compartments and results in protection against 5-fluorouracil-induced toxicity
de Haan, G., Donte, B., Engel, C., Loeffler, M., & NIJHOF, W. (1996) · Blood · doi:10.1182/blood.v87.11.4581.bloodjournal87114581 · Cited by 23 · see citing works
Novel Genes Mapping to the Critical Region of the 5q− Syndrome
Boultwood, J., Fidler, C., Soularue, P., Strickson, A., Kostrzewa, M., Jaju, R. J., Cotter, F. E., Fairweather, N. D., Monaco, A. P., Müller, U., et al. (1997) · Genomics · doi:10.1006/geno.1997.4899 · Cited by 19 · see citing works
Prospects for quantitative trait locus methodology in gerontology
McClearn, G. E. (1997) · Experimental Gerontology · doi:10.1016/s0531-5565(96)00066-6 · Cited by 14 · see citing works
An RI QTL cooperative data bank for recombinant inbred quantitative trait loci analyses
Plomin, R. J., McClearn, G. E., Gora-Maslak, G., & Neiderhiser, J. M. (1991) · Behavior Genetics · doi:10.1007/bf01066329 · Cited by 12 · see citing works

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Mitonuclear protein imbalance as a conserved longevity mechanism
Houtkooper, R. H., Mouchiroud, L., Ryu, D., Moullan, N., Katsyuba, E., Knott, G., Williams, R. W., & Auwerx, J. (2013) · Nature · doi:10.1038/nature12188 · Cited by 1,035 · see citing works
The aging of the immune system
Weiskopf, D., Weinberger, B., & Grubeck-Loebenstein, B. (2009) · Transplant International · doi:10.1111/j.1432-2277.2009.00927.x · Cited by 908 · see citing works
Aging of hematopoietic stem cells
de Haan, G., & Lazare, S. S. (2018) · Blood · doi:10.1182/blood-2017-06-746412 · Cited by 432 · see citing works
The Genetics of Aging
Finch, C. E., & Ruvkun, G. (2001) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev.genom.2.1.435 · Cited by 446 · see citing works
Uncovering regulatory pathways that affect hematopoietic stem cell function using 'genetical genomics'
Bystrykh, L. V., Weersing, E., Dontje, B., Sutton, S., Pletcher, M. T., Wiltshire, T., Su, A. I., Vellenga, E., Wang, J., Manly, K. F., et al. (2005) · Nature Genetics · doi:10.1038/ng1497 · Cited by 390 · see citing works
“In previous studies, we used a genetic approach to identify loci associated with variation in attributes of HSC population”
Method
T cells and aging january 2002 update
Pawelec, G. (2002) · Frontiers in bioscience · doi:10.2741/a831 · Cited by 368 · see citing works
The aging of the immune system
Grubeck-Loebenstein, B., & Wick, G. (2002) · Advances in immunology · doi:10.1016/s0065-2776(02)80017-7 · Cited by 235 · see citing works
The aging of lympho-hematopoietic stem cells
Geiger, H., & Van Zant, G. (2002) · Nature Immunology · doi:10.1038/ni0402-329 · Cited by 233 · see citing works
Metabolic networks of longevity
Houtkooper, R. H., Williams, R. W., & Auwerx, J. (2010) · Cell · doi:10.1016/j.cell.2010.06.029 · Cited by 217 · see citing works
Dynamic Changes in Mouse Hematopoietic Stem Cell Numbers During Aging
de Haan, G., & Van Zant, G. (1999) · Blood · doi:10.1182/blood.v93.10.3294.410k07_3294_3301 · Cited by 208 · see citing works
The role of stem cells in aging
Zant, G. E. V., & Liang, Y. (2003) · Experimental Hematology · doi:10.1016/s0301-472x(03)00088-2 · Cited by 194 · see citing works
“Secondly, it has become clear in recent years that there is not only considerable mouse strain variation in longevity, but in properties of the stem cell compartment [101, 102].”
Background
A novel dynamic model of hematopoietic stem cell organization based on the concept of within-tissue plasticity
Roeder, I., & Loeffler, M. (2002) · Experimental Hematology · doi:10.1016/s0301-472x(02)00832-9 · Cited by 178 · see citing works
“First, DBA/2 cells are given a shorter average turnover time � c than C57BL/6 cells, implying an elevated cycling activity as previously reported [ 39 ].”
Result
Does p53 affect organismal aging?
Donehower, L. A. (2002) · Journal of Cellular Physiology · doi:10.1002/jcp.10104 · Cited by 155 · see citing works
“One hypothesis is that senescence in mouse cells is a result of their higher sensitivity to the stresses of in vitro culture conditions (Sherr and DePinho, 2000).”
Background
A Limited Role for p21Cip1/Waf1 in Maintaining Normal Hematopoietic Stem Cell Functioning
van Os, R. P., Kamminga, L. M., Ausema, A., Bystrykh, L. V., Draijer, D. P., van Pelt, K., Dontje, B., & de Haan, G. (2006) · Stem Cells · doi:10.1634/stemcells.2006-0631 · Cited by 118 · see citing works
The aryl hydrocarbon receptor has a normal function in the regulation of hematopoietic and other stem/progenitor cell populations
Singh, K. P., Casado, F. L., Opanashuk, L. A., & Gasiewicz, T. A. (2008) · Biochemical Pharmacology · doi:10.1016/j.bcp.2008.10.001 · Cited by 118 · see citing works
Hematopoietic stem cell aging and self-renewal
Dykstra, B. J., & de Haan, G. (2007) · Cell and Tissue Research · doi:10.1007/s00441-007-0529-9 · Cited by 106 · see citing works
Age- and stage-specific regulation patterns in the hematopoietic stem cell hierarchy
Geiger, H., True, J. M., de Haan, G., & Zant, G. E. V. (2001) · Blood · doi:10.1182/blood.v98.10.2966 · Cited by 103 · see citing works
Hemopoiesis in healthy old people and centenarians: well-maintainedresponsiveness of CD34+ cells to hemopoietic growth factors and remodelingof cytokine network
Bagnara, G. P., Bonsi, L., Strippoli, P., Bonifazi, F., Tonelli, R., D’Addato, S., Paganelli, R., Scala, E., Fagiolo, U., Monti, D., et al. (2000) · The Journals of Gerontology Series A · doi:10.1093/gerona/55.2.b61 · Cited by 100 · see citing works
“These parameters appear to have a strong genetic basis in mice (23, 24 ).”
Background
Stem cells, aging, and cancer: inevitabilities and outcomes
Bell, D. R., & Zant, G. E. V. (2004) · Oncogene · doi:10.1038/sj.onc.1207949 · Cited by 99 · see citing works
Aging in the lympho-hematopoietic stem cell compartment
Geiger, H., & Rudolph, K. L. (2009) · Trends in Immunology · doi:10.1016/j.it.2009.03.010 · Cited by 97 · see citing works
The quantitative trait gene latexin influences the size of the hematopoietic stem cell population in mice
Liang, Y., Jansen, M., Aronow, B. J., Geiger, H., & Zant, G. E. V. (2007) · Nature Genetics · doi:10.1038/ng1938 · Cited by 97 · see citing works
The biology of hematopoietic stem cells
Szilvassy, S. J. (2003) · Archives of Medical Research · doi:10.1016/j.arcmed.2003.06.004 · Cited by 90 · see citing works
Evidence for a continuous decline in haemopoietic cell function from birth: application to evaluating bone marrow failure in children
Marley, Lewis, Davidson, Roberts, Dokal, I. S., Goldman, & Gordon (1999) · British Journal of Haematology · doi:10.1046/j.1365-2141.1999.01477.x · Cited by 90 · see citing works
A genetic and genomic analysis identifies a cluster of genes associated with hematopoietic cell turnover
de Haan, G., Bystrykh, L. V., Weersing, E., Dontje, B., Geiger, H., Ivanova, N. B., Lemischka, I. R., Vellenga, E., & Zant, G. E. V. (2002) · Blood · doi:10.1182/blood-2002-03-0808 · Cited by 69 · see citing works
The Convergence of Systems and Reductionist Approaches in Complex Trait Analysis
Williams, E. G., & Auwerx, J. H. (2015) · Cell · doi:10.1016/j.cell.2015.06.024 · Cited by 67 · see citing works
Complex Adaptive Systems, Aging and Longevity
Mangel, M. (2001) · Journal of Theoretical Biology · doi:10.1006/jtbi.2001.2431 · Cited by 63 · see citing works
Does functional depletion of stem cells drive aging?
Schlessinger, D., & Zant, G. E. V. (2001) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(01)00299-8 · Cited by 62 · see citing works
The aryl hydrocarbon receptor has an important role in the regulation of hematopoiesis: Implications for benzene-induced hematopoietic toxicity
Gasiewicz, T. A., Singh, K. P., & Casado, F. L. (2009) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2009.10.019 · Cited by 61 · see citing works
Concise Review: Hematopoietic Stem Cell Aging, Life Span, and Transplantation
Zant, G. E. V., & Liang, Y. (2012) · Stem Cells Translational Medicine · doi:10.5966/sctm.2012-0033 · Cited by 61 · see citing works
Age-dependent effects of <i>Igf2bp2</i> on gene regulation, function, and aging of hematopoietic stem cells in mice
Suo, M., Rommelfanger, M. K., Chen, Y., Amro, E. M., Han, B., Chen, Z., Szafranski, K., Chakkarappan, S. R., Boehm, B. O., MacLean, A. L., et al. (2022) · Blood · doi:10.1182/blood.2021012197 · Cited by 57 · see citing works
Multiomic profiling of the liver across diets and age in a diverse mouse population
Williams, E. G., Pfister, N., Roy, S., Statzer, C., Haverty, J., Ingels, J. F., Bohl, C. J., Hasan, M., Čuklina, J., Bühlmann, P., et al. (2021) · Cell Systems · doi:10.1016/j.cels.2021.09.005 · Cited by 55 · see citing works
Gene-by-environment modulation of lifespan and weight gain in the murine BXD family
Roy, S., Sleiman, M. S. B., Jha, P., Ingels, J. F., Chapman, C. J., McCarty, M. S., Ziebarth, J. D., Hook, M., Sun, A., Zhao, W., et al. (2021) · Nature Metabolism · doi:10.1038/s42255-021-00449-w · Cited by 52 · see citing works
Quantitative genetic variation in the hematopoietic stem cell and progenitor cell compartment and in lifespan are closely linked at multiple loci in BXD recombinant inbred mice
Henckaerts, E., Langer, J., & Snoeck, H. (2004) · Blood · doi:10.1182/blood-2003-12-4304 · Cited by 52 · see citing works
Distinct functional properties of highly purified hematopoietic stem cells from mouse strains differing in stem cell numbers
de Haan, G., Szilvassy, S. J., Meyerrose, T. E., Dontje, B., Grimes, B. A., & Zant, G. E. V. (2000) · Blood · doi:10.1182/blood.v96.4.1374 · Cited by 52 · see citing works
Aging stem cells, latexin, and longevity
Liang, Y., & Zant, G. E. V. (2008) · Experimental Cell Research · doi:10.1016/j.yexcr.2008.01.032 · Cited by 42 · see citing works
Epigenetic Control of Hematopoietic Stem Cell Aging The Case of Ezh2
de Haan, G., & GERRITS, A. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1392.008 · Cited by 40 · see citing works
Significant increase of self-renewal in hematopoietic cells after forced expression of EVI1
Laricchia‐Robbio, L., & Nucifora, G. (2007) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2007.07.012 · Cited by 40 · see citing works
Body weight and high‐fat diet are associated with epigenetic aging in female members of the BXD murine family
Sandoval-Sierra, J. V., Helbing, A. H. B., Williams, E. G., Ashbrook, D. G., Roy, S., Williams, R. W., & Mozhui, K. (2020) · Aging Cell · doi:10.1111/acel.13207 · Cited by 37 · see citing works
The Relationships of Animal Age and Caloric Intake to Cellular Replication In Vivo and In Vitro: A Review
Wolf, N. S., & Pendergrass, W. (1999) · The Journals of Gerontology Series A · doi:10.1093/gerona/54.11.b502 · Cited by 37 · see citing works
PML a target of translocations in APL is a regulator of cellular senescence
Ferbeyre, G. (2002) · Leukemia · doi:10.1038/sj.leu.2402722 · Cited by 35 · see citing works
The Positive Regulatory Effect of TGF-β2 on Primitive Murine Hemopoietic Stem and Progenitor Cells Is Dependent on Age, Genetic Background, and Serum Factors
Henckaerts, E., Langer, J., Orenstein, J., & Snoeck, H. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.4.2486 · Cited by 28 · see citing works
Genetic Control of Stem Cells: Implications for Aging
Zant, G. E. V. (2003) · International Journal of Hematology · doi:10.1007/bf02982600 · Cited by 28 · see citing works
“Moreover, QTL affecting the fraction of progenitor cells killed by the cell cycle‐specific drug hydroxyurea also comap to the same markers as QTL affecting life span [ 69 ].”
Background
Autonomous behavior of hematopoietic stem cells
Kamminga, L. M., Akkerman, I., Weersing, E., Ausema, A., Dontje, B., Zant, G. E. V., & de Haan, G. (2000) · Experimental Hematology · doi:10.1016/s0301-472x(00)00543-9 · Cited by 26 · see citing works
Quantitative Trait Loci (QTL) analysis of longevity in C57BL/6J by DBA/2J (BXD) recombinant inbred mice
Lang, D. H., Gerhard, G. S., Griffith, J. W., Vogler, G. P., Vandenbergh, D. J., Blizard, D. A., Stout, J. T., Lakoski, J. M., & McClearn, G. E. (2010) · Aging Clinical and Experimental Research · doi:10.1007/bf03324809 · Cited by 25 · see citing works
Osteoblast progenitor fate and age-related bone loss.
Jilka, R. L. (2002) · PubMed · Cited by 24 · see citing works
The Cobblestone-Area-Forming Cell Assay
de Haan, G., & Ploemacher, R. (2003) · Humana Press eBooks · doi:10.1385/1-59259-140-x:143 · Cited by 23 · see citing works
Age-related change in thymic T-cell development is associated with genetic loci on mouse chromosomes 1, 3, and 11
Hsu, H., Mountz, J. D., Williams, R. W., Shelton, B. J., Yang, P., Matsuki, Y., Xu, X., Dodd, C. H., Li, L., Geiger, H., et al. (2002) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(02)00004-0 · Cited by 23 · see citing works
Isolation and Analysis of Hematopoietic Stem Cells from Mouse Embryos
Dzierzak, E. A., & Bruijn, M. F. T. R. D. (2003) · Humana Press eBooks · doi:10.1385/1-59259-140-x:001 · Cited by 22 · see citing works
Genetic control of lifespan: studies from animal models
Zant, G. E. V., & de Haan, G. (1999) · Expert Reviews in Molecular Medicine · doi:10.1017/s1462399499001441 · Cited by 20 · see citing works
Mitochondrial cross-compartmental signalling to maintain proteostasis and longevity
Molenaars, M., Daniels, E. G., Meurs, A., Janssens, G. E., & Houtkooper, R. H. (2020) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2019.0414 · Cited by 16 · see citing works
“The lifespan of BXD mouse strains ranges from approximately 365 to 900 days [15].”
Background
Combining transcriptional profiling and genetic linkage analysis to uncover gene networks operating in hematopoietic stem cells and their progeny
Gerrits, A., Dykstra, B. J., Otten, M., Bystrykh, L. V., & de Haan, G. (2008) · Immunogenetics · doi:10.1007/s00251-008-0305-3 · Cited by 16 · see citing works
Quantitative Trait Locus (QTL) Mapping in Aging Systems
Hsu, H., Lu, L., Yi, N., Zant, G. E. V., Williams, R. W., & Mountz, J. D. (2007) · Methods in molecular biology · doi:10.1007/978-1-59745-361-5_23 · Cited by 16 · see citing works
Gene-specific sex effects on eosinophil infiltration in leishmaniasis
Slapničková, M., Volkova, V., Čepičková, M., Kobets, T., Šíma, M., Svobodová, M., Démant, P., & Lipoldová, M. (2016) · Biology of Sex Differences · doi:10.1186/s13293-016-0117-3 · Cited by 14 · see citing works
Genetic Dissection of Age‐Related Changes of Immune Function in Mice
Mountz, J. D., Zant, G. E. V., Zhang, H., Grizzle, W. E., Ahmed, R., Williams, R. W., & Hsu, H. (2001) · Scandinavian Journal of Immunology · doi:10.1046/j.1365-3083.2001.00943.x · Cited by 14 · see citing works
“7 and 11, are important in regulating the rate of proliferation of haematopoietic progenitor cells [ 17 ].”
Background
Hematopoietic Stem Cells: Self-Renewing or Aging?
de Haan, G. (2002) · Cells Tissues Organs · doi:10.1159/000057689 · Cited by 13 · see citing works
Quantitative trait mapping reveals a regulatory axis involving peroxisome proliferator-activated receptors, PRDM16, transforming growth factor-β2 and FLT3 in hematopoiesis
Avagyan, S., Aguiló, F., Kamezaki, K., & Snoeck, H. (2011) · Blood · doi:10.1182/blood-2011-07-365080 · Cited by 12 · see citing works
Natural Genetic Diversity as a Means to Uncover Stem Cell Regulatory Pathways
Zant, G. E. V., & Liang, Y. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04567.x · Cited by 12 · see citing works
Stem Cells and Genetics in the Study of Development, Aging, and Longevity
Zant, G. E. V. (2000) · Results and problems in cell differentiation · doi:10.1007/978-3-540-48003-7_11 · Cited by 12 · see citing works
Changes in the frequencies of human hematopoietic stem and progenitor cells with age and site
Farrell, T. L., McGuire, T. R., Bilek, L. D., Brusnahan, S. K., Jackson, J. D., Lane, J. T., Garvin, K. L., O'Kane, B. J., Berger, A. M., Tuljapurkar, S. R., et al. (2013) · Experimental Hematology · doi:10.1016/j.exphem.2013.11.003 · Cited by 11 · see citing works
QTL influencing baseline hematocrit in the C57BL/6J and DBA/2J lineage: age-related effects
Johannes, F. M., Blizard, D. A., Lionikas, A., Lang, D., Vandenbergh, D. J., Stout, J. T., Strauss, J. A., McClearn, G. E., & Vogler, G. P. (2006) · Mammalian Genome · doi:10.1007/s00335-006-0009-7 · Cited by 11 · see citing works
Hematopoiesis during development, aging, and disease
Jung, J., Buisman, S. C., & de Haan, G. (2016) · Experimental Hematology · doi:10.1016/j.exphem.2016.05.007 · Cited by 10 · see citing works
“In a series of elegant experiments, partly published in Experimental Hematology, Gary Van Zant and his co-workers reported that, in fact, hematopoietic stem cells do age [2]; the rate of aging is related to their (strain-dependent) proliferative activity [3]; and stem cell quiescence is reversible [4].”
Background
Lifespan-Associated Gene Expression Signatures of Recombinant BXD Mice Implicates Coro7 and Set in Longevity
Vitiello, D., Dakhovnik, A., Statzer, C., & Ewald, C. Y. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.694033 · Cited by 9 · see citing works
Mouse bone marrow and peripheral blood erythroid cell counts are regulated by different autosomal genetic loci
Jawad, M., Giotopoulos, G., Fitch, S. R., Cole, C., Plumb, M., & Talbot, C. J. (2006) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2006.10.009 · Cited by 9 · see citing works
“Similarly, QTL have been identified that determine mouse stem, progenitor and mature white blood cell numbers [10-18].”
Background
A Quantitative Trait Locus on Chromosome 4 Affects Cycling of Hematopoietic Stem and Progenitor Cells through Regulation of TGF-β2 Responsiveness
Avagyan, S., Glouchkova, L., Choi, J., & Snoeck, H. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.9.5904 · Cited by 8 · see citing works
Mechanisms of Stem Cell Ageing
Waterstrat, A., Oakley, E. J., Miller, A. R., Swiderski, C. F., Liang, Y., & Zant, G. E. V. (2007) · Springer eBooks · doi:10.1007/978-3-540-73709-4_6 · Cited by 8 · see citing works
Polycomb group proteins in hematopoietic stem cell aging and malignancies
Klauke, K., & de Haan, G. (2011) · International Journal of Hematology · doi:10.1007/s12185-011-0857-0 · Cited by 7 · see citing works
Identification of quantitative trait loci regulating haematopoietic parameters in B6AKRF2 mice
van Os, R. P., Ausema, A., Noach, E. J. K., van Pelt, K., Dontje, B., Vellenga, E., & de Haan, G. (2005) · British Journal of Haematology · doi:10.1111/j.1365-2141.2005.05835.x · Cited by 7 · see citing works
E3 ubiquitin ligase on the biological properties of hematopoietic stem cell
Zhan, Q., Wang, J., Zhang, H., & Zhang, L. (2023) · Journal of Molecular Medicine · doi:10.1007/s00109-023-02315-6 · Cited by 5 · see citing works
Beneficial influences of systemic cooperation and sociological behavior on longevity
Mountz, J. D., Zant, G. E. V., Allison, D. B., Zhang, H., & Hsu, H. (2002) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(02)00034-9 · Cited by 5 · see citing works
Analysis of expansion of myeloid progenitors in mice to identify leukemic susceptibility genes
Sollars, V. E., Pequignot, E., Rothstein, J. L., & Buchberg, A. M. (2006) · Mammalian Genome · doi:10.1007/s00335-006-0017-7 · Cited by 5 · see citing works
Engineering the In Vitro Cellular Microenvironment for the Control and Manipulation of Adult Stem Cell Responses
Khademhosseini, A., & Zandstra, P. W. (2004) · doi:10.1007/978-1-59259-732-1_15 · Cited by 4 · see citing works
Body weight at young adulthood and association with epigenetic aging and lifespan in the BXD murine familyPreprint
Sandoval-Sierra, J. V., Helbing, A. H. B., Williams, E. G., Ashbrook, D. G., Roy, S., Williams, R. W., & Mozhui, K. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/791582 · Cited by 4 · see citing works
Stem cells from birth to death: The history and the future
de Haan, G., & Zant, G. E. V. (2002) · AGE · doi:10.1007/s11357-002-0006-z · Cited by 3 · see citing works
Lebensdauer: Genetische Determinierung und lebensverlängernde Strategien
Niedermüller, H., & Hofecker, G. (2004) · Springer eBooks · doi:10.1007/978-3-642-18741-4_2 · Cited by 3 · see citing works
Hematopoietic stem cells and aging
Zant, G. E. V., Manning, E., & Geiger, H. (2002) · Advances in cell aging and gerontology · doi:10.1016/s1566-3124(02)09042-9 · Cited by 2 · see citing works
Basal and induced granulopoiesis in outbred, F 1 hybrid and inbred mice: can inbreeding depression influence the experimental practice?
Hofer, M., Pospíšil, M., Dušek, L., Hòlá, J., Hoferová, Z., & Weiterová, L. (2010) · Experimental Biology and Medicine · doi:10.1258/ebm.2010.010032 · Cited by 1 · see citing works
Hematopoietic Stem Cells, Aging, and Cancer
Bell, D. R., & Zant, G. E. V. (2005) · Elsevier eBooks · doi:10.1016/b978-012088387-5/50007-8 · Cited by 1 · see citing works
THE ROLE OF STEM CELL ANTIGEN-1(Sca-1) IN MUSCLE AGING
Richards-Malcolm, S. A. (2008) · UKnowledge (University of Kentucky)
THE GENETIC REGULATION OF THE RESPONSE OF HEMATOPOIETIC STEM/PROGENITOR CELLS TO THE CYTOSTATIC AGENT HYDROXYUREA
Yates, J. L. (2006) · UKnowledge (University of Kentucky)
GENETIC REGULATION OF HEMATOPOIETIC STEM CELL NUMBERS IN MICE
Liang, Y. (2005) · UKnowledge (University of Kentucky)
Hematopoietic Stem Cell Aging and Fate Decision
Illing, A., & Ju, Z. (2010) · Else Kröner-Fresenius Symposia · doi:10.1159/000312645
Molecular and Endocrine Mechanisms Underlying the Stem Cell Theory of Aging
Coutu, D. L., & Galipeau, J. (2013) · Stem cell biology and regenerative medicine · doi:10.1007/978-1-4614-9569-7_17
Aging, Nutrients, and Endogenous Stem Cell Populations
Zuba‐Surma, E. K., Elias, H. K., & Dawn, B. (2013) · CRC Press eBooks · doi:10.1201/b14663-12
The Role of Cbx Proteins in Human Benign and Malignant Hematopoiesis
Jung, J., Schepers, H., Lazare, S., Buisman, S. C., Weersing, E., Dethmers-Ausema, B., Klauke, K., Bystrykh, L., & de Haan, G. (2016) · Blood · doi:10.1182/blood.v128.22.2651.2651
A Limited Role for p21 in Maintaining Normal Hematopoietic Stem Cell Functioning
Kamminga, L. M., Ausema, A., Bystrykh, L. V., & Draijer, D. P. (2007)
Patent Highlights
Mucke, H. A. (2013) · Pharmaceutical Patent Analyst · doi:10.4155/ppa.13.19
The role of DNA methylation in stem cell ageing
Taiwo, O. S. (2013) · UCL Discovery (University College London)

Quantitative genetic variation in the hematopoietic stem cell and progenitor cell compartment and in lifespan are closely linked at multiple loci in BXD recombinant inbred mice
Henckaerts, E., Langer, J., & Snoeck, H. (2004) · Blood · doi:10.1182/blood-2003-12-4304 · Cited by 52 · see citing works
Of mice, genes and aging
DeGregori, J. V. (2020) · Haematologica · doi:10.3324/haematol.2019.238683 · Cited by 1 · see citing works
The lifespan quantitative trait locus gene Securin controls hematopoietic progenitor cell function
Brown, A., Schuetz, D., Han, Y., Daria, D., Nattamai, K., Eiwen, K., Sakk, V., Pospiech, J., Saller, T., Zant, G. E. V., et al. (2019) · Haematologica · doi:10.3324/haematol.2018.213009 · Cited by 4 · see citing works
PTTG1/securin as a quantitative trait locus candidate gene controlling progenitor cell survival and organismal lifespan
Schütz, D., Brown, A., Geiger, H., & Nattamai, K. (2017) · Experimental Hematology · doi:10.1016/j.exphem.2017.06.130
Genetic Regulation of Life Span, Metabolism, and Body Weight in Pohn, a New Wild-Derived Mouse Strain
Yuan, R., Flurkey, K., Meng, Q., Astle, M. C., & Harrison, D. E. (2012) · The Journals of Gerontology Series A · doi:10.1093/gerona/gls104 · Cited by 17 · see citing works

Authors: de Haan, G., & van Zant, G.
Affiliations: Blood and Marrow Transplant Program Division of Hematology/Oncology University of Kentucky Medical Center Lexington Kentucky 40536-0093 USA
Venue: The FASEB Journal
Publisher: Wiley
Published: 1999-04
Volume: 13
Issue: 6
Pages: 707-713
ISSN: 0892-6638 (ISSN-L)
1530-6860
DOI: 10.1096/fasebj.13.6.707
OpenAlex: W1558342973
Cited by: 87
References: 51
Citations by year: 2023: 1 · 2022: 1 · 2021: 3 · 2020: 2 · 2019: 1 · 2017: 1 · 2016: 3 · 2015: 1 · 2013: 6 · 2012: 1
FWCI: 3.04
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: The FASEB Journal (publishedVersion)
PubMed (publishedVersion)
University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
Funders: Lucille P. Markey Charitable Trust
University of Kentucky
Department of Internal Medicine, University of Nebraska Medical Center
Netherlands Organization for International Cooperation in Higher Education
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
Keywords: hematopoietic stem cells, cell cycling, replicative senescence, biological aging, lifespan, quantitative trait loci, BXD recombinant inbred mice, chromosome 11, chromosome 7, cell turnover, myelodysplastic syndrome, inbred mouse strains
MeSH terms: Aging, Animals, Cell Cycle, Chromosome Mapping, Female, Multigene Family, Hematopoietic Stem Cells, Mice, Inbred C3H, Mice, Inbred C57BL, Mice, Inbred DBA, Species Specificity, Cytokines, Cellular Senescence, Quantitative Trait, Heritable, Mice

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Genetic analysis of hemopoietic cell cycling in mice suggests its involvement in organismal life span

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