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Etoposide Selectively Ablates Activated T Cells To Control the Immunoregulatory Disorder Hemophagocytic Lymphohistiocytosis
Open accessAbstract
Hemophagocytic lymphohistiocytosis (HLH) is an inborn disorder of immune regulation caused by mutations affecting perforin-dependent cytotoxicity. Defects in this pathway impair negative feedback between cytotoxic lymphocytes and APCs, leading to prolonged and pathologic activation of T cells. Etoposide, a widely used chemotherapeutic drug that inhibits topoisomerase II, is the mainstay of treatment for HLH, although its therapeutic mechanism remains unknown. We used a murine model of HLH, involving lymphocytic choriomeningitis virus infection of perforin-deficient mice, to study the activity and mechanism of etoposide for treating HLH and found that it substantially alleviated all symptoms of murine HLH and allowed prolonged survival. This therapeutic effect was relatively unique among chemotherapeutic agents tested, suggesting distinctive effects on the immune response. We found that the therapeutic mechanism of etoposide in this model system involved potent deletion of activated T cells and efficient suppression of inflammatory cytokine production. This effect was remarkably selective; etoposide did not exert a direct anti-inflammatory effect on macrophages or dendritic cells, and it did not cause deletion of quiescent naive or memory T cells. Finally, etoposide’s immunomodulatory effects were similar in wild-type and perforin-deficient animals. Thus, etoposide treats HLH by selectively eliminating pathologic, activated T cells and may have usefulness as a novel immune modulator in a broad array of immunopathologic disorders.
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“Cyclophosphamide and etoposide, which are broadly cytotoxic but particularly effective at eliminating activated CD8+ T cells, are often effective in patients with primary HLH, secondary HLH (including macrophage activation syndrome), and corresponding models.75”
From Cytokine storm (2020) · cites this paper as [75]
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Metadata
- Authors
- Johnson, T. S., Terrell, C. E., Millen, S. H., Katz, J. D., Hildeman, D. A., & Jordan, M. B.
- Affiliations
- Augusta University (US)
- Cincinnati Children's Hospital Medical Center (US)
- Corresponding author
- Jordan, Michael B
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-01-01
- Volume
- 192
- Issue
- 1
- Pages
- 84-91
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- PMC
- PMC4177106
- OpenAlex
- W2105957247
- Cited by
- 203
- References
- 48
- Citations by year
- 2026: 7 · 2025: 13 · 2024: 29 · 2023: 19 · 2022: 17 · 2021: 20 · 2020: 28 · 2019: 18 · 2018: 12 · 2017: 19 · 2016: 8 · 2015: 8 · 2014: 4
- FWCI
- 5.02
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Heart, Lung, and Blood Institute (R01HL091769)
- National Institute of Allergy and Infectious Diseases (U54AI082973)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK081175)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (P30AR047363)
- Topics
- Health Sciences › Medicine › Hematology › Autoimmune and Inflammatory Disorders Research
- Life Sciences › Immunology and Microbiology › Immunology › Immunodeficiency and Autoimmune Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
- Keywords
- hemophagocytic lymphohistiocytosis, etoposide, perforin deficiency, topoisomerase II inhibition, cytotoxic T lymphocytes, lymphocytic choriomeningitis virus, inflammatory cytokines, immunomodulation, innate immune regulation
- MeSH terms
- Animals, Dendritic Cells, Disease Models, Animal, DNA-Binding Proteins, Etoposide, Interferon-gamma, Lymphocyte Activation, Lymphocytic choriomeningitis virus, Macrophage Activation, Macrophages, T-Lymphocytes, Apoptosis, Antigen Presentation, Mice, Knockout, Lymphohistiocytosis, Hemophagocytic, Mice, Topoisomerase II Inhibitors
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