Genotype-restricted growth and aging patterns in hematopoietic stem cell populations of allophenic mice
Open accessAbstract
We have studied contributions to hematopoiesis of genetically distinct stem cell populations in allophenic mice. Chimeras were made by aggregating embryos of inbred strains known to differ with respect to stem cell population kinetics. One partner strain (DBA/2) has previously been shown to normally have a stem cell (CFU-S) population of which 24% are in S-phase of the cell cycle, whereas the homologous population of the other partner strain (C57BL/6) was characterized by having only 2.6% in cycle (7). Contributions of the chimeric stem cell population to mature blood cell pools were studied throughout the life of the mice and intrinsic differences in stem cell function and aging were reflected in dynamic patterns of blood cell composition. The DBA/2 stem cell population was eclipsed by stem cells of the C57BL/6 genotype and, after 1.5-3 yr, the hemato-lymphoid composition of 22 of 27 mice studied for this long had shifted by at least 25 percentage points toward the C57BL/6 genotype. 8 of the 27 had hematolymphoid populations solely of C57BL/6 origin. To test whether or not a population of stem cells with an inherently higher cycling rate (DBA/2) might have a competitive advantage during repopulation, we engrafted allophenic marrow into lethally irradiated (C57BL/6 x DBA/2)F1 recipients. DBA/2 hematopoiesis was predominant early, far outstripping its representation in the marrow graft. Perhaps as a consequence of inherently greater DBA/2 stem cell proliferation, the populations of developmentally more restricted precursor populations (CFU-E, BFU-E, CFU-GM, CFU-GEMM) showed an overwhelming DBA/2 bias in the first 2-3 mo after engraftment. However, as in the allophenic mice themselves during the aging process, the C57BL/6 genotypic representation was ascendant over the subsequent months. The shift toward C57BL/6 genotype was first documented in the marrow and spleen precursor cell populations and was subsequently reflected in the circulating, mature blood cells. Bone marrow-derived stromal cell cultures from engrafted mice were studied and genotypic analyses showed donor representation in stromal cell populations that reflected donor hematopoietic contributions in the same recipient. Results from these studies involving two in vivo settings (allophenic mice and engraftment by allophenic marrow) are consistent with the notion that a cell autonomous difference in stem cell proliferation confers on one population a competitive repopulating advantage, but at the expense of longevity.
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Aged HSCs transplanted into young mice are functionally worse than young HSCs.
“That aged HSC are functionally impaired compared with their young counterparts upon transplantation in young mice”
From Aging of hematopoietic stem cells (2018) · cites this paper as [11]
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BackgroundInfluentialGenetic 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
The slippery slope of hematopoietic stem cell aging
Wahlestedt, M., & Bryder, D. (2017) · Experimental Hematology · doi:10.1016/j.exphem.2017.09.008 · Cited by 18 · see citing works
Characteristics of the hematopoietic stem cell compartment in adult mice
Spangrude, G. J. (1992) · The International Journal Of Cell Cloning · doi:10.1002/stem.5530100505 · Cited by 18 · see citing works
Hematopoietic stem cell development, aging and functional failure
Chen, J. (2011) · International Journal of Hematology · doi:10.1007/s12185-011-0856-1 · Cited by 16 · see citing works
“In the chimeras, D2 HSC population was eclipsed by HSCs of the B6 genotype over time, and after 1.5‐3 years, the hemato-lymphoid composition significantly skewed toward the B6 genotype with 30% mice had hematolymphoid populations solely of B6 origin, suggesting age-related HSC functional deficiency in D2 mice [ 66 ].”
BackgroundInfluentialSmith, A. L., Ellison, F. M., McCoy, J. P., & Chen, J. (2005) · The Journals of Gerontology Series A · doi:10.1093/gerona/60.4.448 · Cited by 14 · see citing works
“In the B6-D2 allophenic mice, D2 HSCs showed high functionality early in life, but were then eclipsed by HSCs of the B6 genotype (34).”
BackgroundSenescence of Hematopoietic Stem Cells and Bone Marrow Failure
Chen, J. (2005) · International Journal of Hematology · doi:10.1532/ijh97.05094 · Cited by 13 · see citing works
“In B6-D2 allophenic mice, DBA/2 (D2) HSCs had high functionality early, but HSCs of the B6 genotype eclipsed them later in life [ 26 ].”
BackgroundHematopoietic Stem Cells: Self-Renewing or Aging?
de Haan, G. (2002) · Cells Tissues Organs · doi:10.1159/000057689 · Cited by 13 · see citing works
“…has been demonstrated in a series of studies in which stem cells obtained from a mouse strain with a high cell proliferation rate (DBA/2) were competed against stem cells obtained from a mouse strain with a low proliferation rate (C57BL/6) [Van Zant et al., 1990, 1991; Kamminga et al., 2000].”
BackgroundAvagyan, S., Aguiló, F., Kamezaki, K., & Snoeck, H. (2011) · Blood · doi:10.1182/blood-2011-07-365080 · 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
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
“The B6D2F2 animals were genotyped at 96 microsatellite markers distributed throughout the autosomes and the X chromosome at an average spacing of 15 20 cM. Genotyping was performed as described by Vandenbergh et al. (2003).”
BackgroundInfluentialHematopoiesis 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].”
BackgroundIn utero transplantation of haemopoietic stem cells
Flake, A. W. (2001) · Best Practice & Research Clinical Haematology · doi:10.1053/beha.2001.0166 · Cited by 10 · 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
Lynch, M. (2004) · Rejuvenation Research · doi:10.1089/1549168041553008 · 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
The Experimental Basis for Hematopoietic Cell Transplantation for Autoimmune Diseases
Shizuru, J. A. (2015) · doi:10.1002/9781118416426.ch18 · Cited by 7 · see citing works
Mouse Models of Human Blood Cancers
Li, S. (2008) · Springer eBooks · doi:10.1007/978-0-387-69132-9 · Cited by 6 · 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
Genetic factors influencing murine hematopoietic productivity in culture
Phillips, R. L., Couzens, M. S., & Zant, G. E. V. (1995) · Journal of Cellular Physiology · doi:10.1002/jcp.1041640113 · Cited by 3 · see citing works
“…output was greatly increased over that of C57BLi6J in these cultures is in agreement with our earlier in vivo data from allophenic mice (Van Zant et al., 1990; Phillips et al., 1992) indicating that DBAiBJ marrow, because of some inherent kinetic advantage, dominates competitive…”
BackgroundResultLebensdauer: 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
Lympho-Hematopoietic Stem Cells and Their Aging
Geiger, H., & Zant, G. E. V. (2009) · Springer eBooks · doi:10.1007/978-1-4020-9063-9_30 · Cited by 1 · see citing works
“Comparing the engraftment properties of HSCs from various aged mouse inbred strains revealed that there are considerable differences in the rate of which stem cell self-renewal activity is reduced in aged animals, suggesting a strong genetic regulation of stem cell aging ( Van Zant et al. 1990 ; Chen et al. 2000 ; Che…”
BackgroundThe Anemia of Inflammation/Chronic Disease and the Unexplained Anemia of the Elderly
Means, R. T. (2018) · Springer eBooks · doi:10.1007/978-3-319-96487-4_9 · Cited by 1 · see citing works
STEM CELLS AND REPARATIVE REGENERATION IN POSTNATAL ONTOGENESIS OF MAMMALS
Aa, S., Shevlyuk, N. N., Aa, S., & Шевлюк, Н. Н. (2006) · Morphology · doi:10.17816/morph.402516 · Cited by 1 · see citing works
T Lymphocytes of Allophenic Mice Do Not Reject Spleen Colony-Forming Units of the Parental Genotypes
Fedorov, L. M., & Panteleev, E. I. (2000) · Stem Cells and Development · doi:10.1089/152581600419198 · 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
Dietary Restriction: A Model System Probing the Cell Fate Decision Between Cancer and Senescence
Ertl, R. P., & Harrison, D. E. (2008) · Springer eBooks · doi:10.1007/978-0-387-69132-9_6
Yates, J. L. (2006) · UKnowledge (University of Kentucky)
GENETIC REGULATION OF HEMATOPOIETIC STEM CELL NUMBERS IN MICE
Liang, Y. (2005) · UKnowledge (University of Kentucky)
Ziegler, N. (2010) · Loyola eCommons (Loyola University of Chicago)
GENETIC REGULATION OF HEMATOPOIETIC STEM CELL AGING
Oakley, E. J. (2008) · UKnowledge (University of Kentucky)
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
Hematopoietic Stem Cell Aging and Leukemogenesis
Henry, C. J., Rozhok, A. I., & DeGregori, J. V. (2015) · Springer eBooks · doi:10.1007/978-3-7091-1232-8_13
Bystrykh, L. V., Weersing, E., Dontje, B., Geiger, H., Ivanova, N. B., Lemischka, [. V., Vellenga, E., Zant, G. E. V., & de Haan, G. (n.d.) · University of Groningen research database (University of Groningen / Centre for Information Technology)
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
Stem cells and fundamental problems of classical histology
Shevlyuk, N. N., Aa, S., & Umbetov, T. Z. (2020) · Morphology · doi:10.17816/1026-3543-2020-158-6-139-150
Potential Use of Marrow Stromal Cells for Therapy of Osteogenesis Imperfecta and Osteoporosis
Prockop, D. J. (1997) · Springer eBooks · doi:10.1007/978-3-662-03509-2_7
- Authors
- Van Zant, G., Holland, B. P., Eldridge, P. W., & Chen, J. J.
- Affiliations
- Department of Cell Biology and Anatomy, Texas Tech University Health Sciences Center, Lubbock 79430.
- Texas Tech University Health Sciences Center (US)
- Venue
- The Journal of Experimental Medicine
- Publisher
- Rockefeller University Press
- Published
- 1990-05-01
- Volume
- 171
- Issue
- 5
- Pages
- 1547-1565
- ISSN
- 0022-1007 (ISSN-L)
- 1540-9538
- PMC
- PMC2187897
- OpenAlex
- W2166846044
- Cited by
- 99
- References
- 29
- Citations by year
- 2020: 1 · 2019: 1 · 2018: 1 · 2017: 2 · 2016: 2 · 2015: 2 · 2014: 1 · 2013: 1
- FWCI
- 1.99
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Experimental Medicine (publishedVersion)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01ca040575-10)
- National Cancer Institute (CA40575)
- Topics
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Blood disorders and treatments
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Keywords
- hematopoietic stem cells, hematopoietic chimeras, stem cell aging, stem cell proliferation, CFU-S, CFU-E, BFU-E, CFU-GM, CFU-GEMM, hematopoietic recovery, mesenchymal stem cells
- MeSH terms
- Aging, Animals, Cells, Cultured, Chimera, Colony-Forming Units Assay, Embryo, Mammalian, Genotype, Hematopoietic Stem Cells, Mice, Inbred C57BL, Mice, Inbred DBA, Mice, Inbred Strains, Bone Marrow Transplantation, Mice
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