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B Cell Maintenance in Aged Mice Reflects Both Increased B Cell Longevity and Decreased B Cell Generation
Abstract
In aged mice the population of mature peripheral B cells is maintained despite a severalfold decrease in the population of bone marrow B cell progenitors. The analysis of the rate of accumulation of 5′-bromo-2-deoxyuridine (BrdU)-labeled splenic B cells in mice fed BrdU for 8 days to 8 wk demonstrated a severalfold increase in the half-life of mature B cells in aged mice. Consistent with a role for decreased B cell turnover in maintaining the mature B cell population of aged mice, several findings indicate that fewer newly generated B cells enter the spleen from the bone marrow in aged vs young adult mice. These include 1) a fourfold decrease in the population of relatively immature splenic B cells, defined as cells that express high levels of heat-stable Ag and accumulate BrdU within 8 wk of labeling; and 2) an equivalent decrease in the population of bone marrow cells representative of later stages of B cell maturation (sIgD−sIgMint-high). Surprisingly, despite a four- to sixfold decrease in pre-B cells, the population of least mature bone marrow B cells (IgD−sIgMvery low) remains intact. Because this population accumulates BrdU-labeled cells more slowly in aged mice than in younger mice, and bone marrow B cells at more mature developmental stages are diminished, it appears that in aged mice B cell development beyond the sIgMvery low stage may be retarded and that cells, therefore, accumulate within this population.
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“In mice, the turnover of mature spleen B cells also decreases with age [143, 144].”
From Immunosenescence: a key player in cancer development (2020) · cites this paper as [144]
Citations
Cites
Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow.
Hardy, R. R., Carmack, C. E., Shinton, S. A., Kemp, J. D., & Hayakawa, K. (1991) · The Journal of Experimental Medicine · doi:10.1084/jem.173.5.1213 · Cited by 1,604
Handbook of the Biology of Aging
Finch, C. E., & Schneider, E. L. (1990) · DigitalGeorgetown (Georgetown University Library) · Cited by 1,210
Receptor editing in self-reactive bone marrow B cells.
Tiegs, S. L., Russell, D. M., & Nemazee, D. A. (1993) · The Journal of Experimental Medicine · doi:10.1084/jem.177.4.1009 · Cited by 1,033
Clonal deletion of B lymphocytes in a transgenic mouse bearing anti-MHC class I antibody genes
Nemazee, D. A., & Bürki, K. (1989) · Nature · doi:10.1038/337562a0 · Cited by 1,019
A monoclonal antibody discriminating between subsets of T and B cells.
BRUCE, J. S., Symington, F. W., McKearn, T. J., & Sprent, J. (1981) · The Journal of Immunology · doi:10.4049/jimmunol.127.6.2496 · Cited by 542
Hartley, S. B., Cooke, M. P., Fulcher, D. A., Harris, A. W., Cory, S., Basten, A., & Goodnow, C. C. (1993) · Cell · doi:10.1016/0092-8674(93)90111-3 · Cited by 509
Allman, D., Ferguson, S. E., Lentz, V. M., & Cancro, M. P. (1993) · The Journal of Immunology · doi:10.4049/jimmunol.151.9.4431 · Cited by 408
Lymphocyte life-span and memory
Sprent, J., & Tough, D. F. (1994) · Science · doi:10.1126/science.8073282 · Cited by 398
Protein Splicing of Inteins and Hedgehog Autoproteolysis: Structure, Function, and Evolution
Perler, F. B. (1998) · Cell · doi:10.1016/s0092-8674(00)80892-2 · Cited by 370
Transitional B cells are the target of negative selection in the B cell compartment.
Carsetti, R., Köhler, G., & Lamers, M. C. (1995) · The Journal of Experimental Medicine · doi:10.1084/jem.181.6.2129 · Cited by 358
Flagged first, then by citations
Research works printed but not linked: 43
- 1977, Cell. Immunol., 26
- 1997, Immunol. Rev., 79
- 1997, Immunol. Rev., 55
- 1981, J. Exp. Med., 547
- 1982, Cell. Immunol., 34
- 1980, Nature, 164
- 1983, J. Exp. Med., 1300
- 1986, Cell. Immunol., 452
- 1976, J. Exp. Med., 1037
- 1997, Immunol. Rev., 103
- 1986, J. Immunol., 368
- 1989, J. Immunol., 3798
- 1991, J. Immunol., 2750
- 1994, J. Immunol., 2214
- 1993, J. Cell. Biochem., F404
- 1986, Immunol. Rev., 159
- 1993, Curr. Opin. Immunol., 433
- 1975, Cell Tissue Kinet., 97
- 1997, Eur. J. Immunol., 1188
- 1982, Immunol. Rev., 81
- 1988, J. Immunol., 1863
- 1991, Clin. Immunol. Immunopathol., 301
- 1993, Blood, 2290
- 1993, Curr. Opin. Immunol., 207
- 1996, Int. Immunol., 509
- 1992, J. Immunol., 2533
- 1993, J. Immunol., 4431
- 1981, J. Immunol., 2496
- 1994, Science, 1395
- 1992, J. Immunol. Methods, 225
- 1995, Methods Companion Methods Enzymol., 3
- 1991, J. Exp. Med., 1213
- 1981, J. Immunol., 2027
- 1995, J. Exp. Med., 2129
- 1989, Nature, 562
- 1993, Cell, 325
- 1993, J. Exp. Med., 1009
- 1998, Cell, 1
- 1997, Immunity, 97
- 1991, J. Exp. Med., 717
- 1997, Eur. J. Immunol., 1801
- 1998, J. Immunol., 4472
- 1989, J. Immunol., 3833
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Zeitlin, L., Segev, E., Fried, A. I., & Wientroub, S. (2003) · Journal of Cellular Biochemistry · doi:10.1002/jcb.10620 · Cited by 16
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Cortegano, I., Rodríguez, M., Martín, I., Prado, C., Ruíz, C., Hortigüela, R., Alía, M., Vilar, M., Mira, H., Cano, E., et al. (2017) · Cell Death and Disease · doi:10.1038/cddis.2017.351 · Cited by 14
Relative Roles of Somatic and Darwinian Evolution in Shaping the Antibody Response
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Jallah, B. P., & Kuypers, D. R. J. (2024) · Drugs & Aging · doi:10.1007/s40266-024-01100-5 · Cited by 12
Numerical alterations of ageing B lymphocyte subsets (Review)
Ongrádi, J., & Kövesdi, V. (2011) · Acta Physiologica Hungarica · doi:10.1556/aphysiol.98.2011.2.1 · Cited by 13
Evolution of B-cell clonal expansions with age
Szabo, P., Li, F., Matthew, J., Lillvis, J. H., & Weksler, M. E. (2004) · Cellular Immunology · doi:10.1016/j.cellimm.2005.01.002 · Cited by 12
Advancing age and immune cell dysfunction: is it reversible or not?
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He, L., Beghi, F., Baral, V., Dépond, M., Zhang, Y., Joulin, V., Rueda, B. R., Gonin, P., Foudi, A., Wittner, M., et al. (2019) · Stem Cell Reports · doi:10.1016/j.stemcr.2019.06.002 · Cited by 9
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Anver, M. R., & Haines, D. C. (2004) · Elsevier eBooks · doi:10.1016/b978-012336425-8/50074-1 · Cited by 4
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Metadata
- Authors
- Kline, G. H., Hayden, T. A., & Klinman, N. R.
- Affiliations
- Scripps Research Institute (US)
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 1999-03
- Volume
- 162
- Issue
- 6
- Pages
- 3342-3349
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- OpenAlex
- W2156242308
- Cited by
- 170
- References
- 48
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 2 · 2023: 3 · 2022: 3 · 2021: 5 · 2020: 6 · 2019: 9 · 2018: 3 · 2017: 6 · 2016: 3 · 2015: 5 · 2014: 3 · 2013: 5 · 2012: 9
- FWCI
- 1.94
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Aging (P01AG001743, T32AG000080, AG-01743, T32 AG-00080)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Health Sciences › Medicine › Pathology and Forensic Medicine › Lymphoma Diagnosis and Treatment
- Keywords
- B cell aging, splenic B cells, B cell maturation, pre-B cells, CD24, BrdU labeling, immunosenescence
- MeSH terms
- Aging, Animals, B-Lymphocytes, Bone Marrow Cells, Bromodeoxyuridine, Cell Cycle, Cell Differentiation, Cell Survival, Immunoglobulin M, Lymphocyte Activation, Receptors, Antigen, B-Cell, Spleen, Stem Cells, Cell Lineage, Mice
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