Aging-associated inflammation promotes selection for adaptive oncogenic events in B cell progenitors
Open accessAbstract
The incidence of cancer is higher in the elderly; however, many of the underlying mechanisms for this association remain unexplored. Here, we have shown that B cell progenitors in old mice exhibit marked signaling, gene expression, and metabolic defects. Moreover, B cell progenitors that developed from hematopoietic stem cells (HSCs) transferred from young mice into aged animals exhibited similar fitness defects. We further demonstrated that ectopic expression of the oncogenes BCR-ABL, NRAS(V12), or Myc restored B cell progenitor fitness, leading to selection for oncogenically initiated cells and leukemogenesis specifically in the context of an aged hematopoietic system. Aging was associated with increased inflammation in the BM microenvironment, and induction of inflammation in young mice phenocopied aging-associated B lymphopoiesis. Conversely, a reduction of inflammation in aged mice via transgenic expression of α-1-antitrypsin or IL-37 preserved the function of B cell progenitors and prevented NRAS(V12)-mediated oncogenesis. We conclude that chronic inflammatory microenvironments in old age lead to reductions in the fitness of B cell progenitor populations. This reduced progenitor pool fitness engenders selection for cells harboring oncogenic mutations, in part due to their ability to correct aging-associated functional defects. Thus, modulation of inflammation--a common feature of aging--has the potential to limit aging-associated oncogenesis.
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The theory of adaptive oncogenesis stipulates that environmental factors associated with tissue decline, such as inflammation, are crucial drivers of oncogenesis by selecting for emergent phenotypes, such as increased proliferation, self-renewal, or survival, that are linked to cancer-associated mutations.
“the theory of adaptive oncogenesis, which stipulates that environmental factors associated with tissue decline, such as inflammation, are crucial drivers of oncogenesis by selecting for emergent phenotypes, such as increased proliferation, self-renewal, or survival, that are linked cancer-associated mutations (Henry et al., 2015; Laconi et al., 2020).”
From PU.1 enforces quiescence and limits hematopoietic stem cell expansion during inflammatory stress (2021) · cites this paper as Henry et al., 2015
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- Authors
- 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., Klawitter, J., Serkova, N. J., Tan, A. C., Dinarello, C. A., & DeGregori, J.
- Affiliations
- National Jewish Health (US)
- University of Colorado Anschutz (US)
- Radboud University Medical Center (NL)
- Corresponding author
- Henry, Curtis J.
- DeGregori, James
- ORCID
- Venue
- Journal of Clinical Investigation
- Published
- 2015-11-09
- Volume
- 125
- Issue
- 12
- Pages
- 4666-4680
- ISSN
- 0021-9738 (ISSN-L)
- 1558-8238
- PMC
- PMC4665776
- OpenAlex
- W2139864776
- Cited by
- 148
- References
- 72
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 16 · 2023: 10 · 2022: 16 · 2021: 14 · 2020: 12 · 2019: 25 · 2018: 10 · 2017: 18 · 2016: 13 · 2015: 2
- FWCI
- 11.27
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Maynooth University ePrints and eTheses Archive (Maynooth University) (acceptedVersion)
- Radboud Repository (Radboud University) (submittedVersion, other-oa)
- Radboud Repository (Radboud University) (submittedVersion)
- Funders
- Interleukin Foundation for Medical Research
- National Institutes of Health (CA-04-6934, UL1TR001082, AI‐15614, RR025780, AG000279, R01 AI15614, P 30CA046934)
- University of California, San Francisco
- National Institute on Aging (T32AG000279)
- National Cancer Institute (R01CA180175, K01CA160798, P30CA046934)
- National Institute of Allergy and Infectious Diseases (R01 AI15614, R01AI015614)
- National Center for Research Resources (RR-025780, UL1RR025780)
- National Center for Advancing Translational Sciences
- Colorado Clinical and Translational Sciences Institute
- Topics
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Health Sciences › Medicine › Hematology › Acute Myeloid Leukemia Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Keywords
- aging, inflammation, B cell progenitors, hematopoietic stem cells, leukemogenesis, BCR-ABL, c-Myc, bone marrow microenvironment, B cell development, alpha-1-antitrypsin, IL-37
- MeSH terms
- Aging, Animals, Bone Marrow, Cell Transformation, Neoplastic, Inflammation, Mice, Inbred BALB C, Mice, Transgenic, Fusion Proteins, bcr-abl, Proto-Oncogene Proteins c-myc, Mice, Precursor Cells, B-Lymphoid, Stem Cell Niche
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.
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