Enhanced Apoptotic Cell Clearance Capacity and B Cell Survival Factor Production by IL-10-Activated Macrophages: Implications for Burkitt’s Lymphoma

Ogden, Carol Anne; Pound, John D; Batth, Balvinder K; Owens, Sarah; Johannessen, Ingolfur; Wood, Katrina; Gregory, Christopher D

doi:10.4049/jimmunol.174.5.3015

Cited by 147Phagocytosis and Immune RegulationImmune cells in cancerLymphoma Diagnosis and Treatment

Enhanced Apoptotic Cell Clearance Capacity and B Cell Survival Factor Production by IL-10-Activated Macrophages: Implications for Burkitt’s Lymphoma

Ogden, Carol Anne, Pound, John D, Batth, Balvinder K, Owens, Sarah, Johannessen, Ingolfur, Wood, Katrina, Gregory, Christopher D·2005·The Journal of Immunology

DOI 10.4049/jimmunol.174.5.3015

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Abstract

Burkitt’s lymphoma (BL) is typified by frequent tumor cell apoptosis and significant macrophage infiltration. Since BL cells have an inherent tendency to undergo apoptosis at a high rate, we reasoned that macrophages in BL are functionally enhanced in at least two activities that have implications for tumor pathogenesis: 1) engulfment of apoptotic cells, an anti-inflammatory process known to suppress immune responses, and 2) production of BL cell survival factors that limit the extent of tumor cell apoptosis. In this study, we show that the microenvironment of BL is rich in the pleiotropic cytokine IL-10, which can be produced by both tumor cells and macrophages, and that IL-10-activated human macrophages have enhanced capacity to engulf apoptotic cells in vitro. This was found to be dependent on the macrophage tethering receptor of apoptotic cells, CD14. Furthermore, IL-10-activated macrophages were found to produce markedly higher levels of the B cell survival factor, B cell-activating factor of the TNF family/B lymphocyte stimulator (BAFF/BLyS) than macrophages matured in the absence of IL-10. Coculture of macrophages with BL cells further enhanced BAFF secretion. Significantly, we show that enhancement of BL cell survival by IL-10-activated macrophages is mediated by a BAFF-dependent component and that BAFF is produced at high levels by tumor-associated macrophages in situ. These results indicate that macrophages, regulated by IL-10, have the potential to promote BL pathogenesis, first, through suppression of antitumor immunity following enhanced engulfment of apoptotic tumor cells and, second, through increased production of tumor cell growth/survival factors.

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Authors: Ogden, C. A., Pound, J. D., Batth, B. K., Owens, S., Johannessen, I., Wood, K., & Gregory, C. D.
Affiliations: Centre for Inflammation Research (GB)
Laboratory for Clinical and Molecular Virology, University of Edinburgh College of Medicine and Veterinary Medicine , Edinburgh ,
Royal Victoria Infirmary (GB)
ORCID: Gregory, Christopher D
Venue: The Journal of Immunology
Publisher: Oxford University Press (OUP)
Published: 2005-03-01
Volume: 174
Issue: 5
Pages: 3015-3023
ISSN: 0022-1767 (ISSN-L)
1550-6606
DOI: 10.4049/jimmunol.174.5.3015
OpenAlex: W1818791232
Cited by: 147
References: 65
Citations by year: 2026: 3 · 2025: 3 · 2024: 2 · 2023: 5 · 2022: 3 · 2021: 8 · 2020: 7 · 2019: 6 · 2018: 2 · 2017: 6 · 2016: 2 · 2015: 7 · 2014: 8 · 2013: 7 · 2012: 10
FWCI: 4.51
Type: journal article
Language: en
Open access: closed
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
Locations: The Journal of Immunology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
Health Sciences › Medicine › Pathology and Forensic Medicine › Lymphoma Diagnosis and Treatment
Keywords: Burkitt lymphoma, IL-10, macrophages, efferocytosis, CD14, BAFF, B lymphocyte stimulator, tumor-associated macrophages, tumor microenvironment, antitumor immunity, macrophage activation
MeSH terms: Adjuvants, Immunologic, Animals, B-Lymphocytes, Burkitt Lymphoma, Cell Movement, Cell Survival, Cells, Cultured, Humans, Macrophage Activation, Macrophages, Membrane Proteins, Mice, Inbred BALB C, Phagocytosis, Tumor Cells, Cultured, Tumor Necrosis Factor-alpha, Mice, SCID, Interleukin-10, Apoptosis, Coculture Techniques, Lipopolysaccharide Receptors, Cell Line, Tumor, Mice, B-Cell Activating Factor

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Enhanced Apoptotic Cell Clearance Capacity and B Cell Survival Factor Production by IL-10-Activated Macrophages: Implications for Burkitt’s Lymphoma

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