Cited by 321Phagocytosis and Immune RegulationCell death mechanisms and regulationAutophagy in Disease and Therapy

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A novel method to determine the engulfment of apoptotic cells by macrophages using pHrodo succinimidyl ester

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Miksa, Michael, Komura, Hidefumi, Wu, Rongqian, Shah, Kavin G., Wang, Ping·2009·Journal of Immunological Methods

DOI 10.1016/j.jim.2008.11.019PMC PMC2675277

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Abstract

Apoptotic cell phagocytosis has recently raised considerable interest, particularly due to its intricate molecular mechanisms and negative immunologic impact of incompetent clearance of apoptotic cells. There is a need for simple and reliable methods to clearly determine the internalization of apoptotic cells. Labeling with pHrodo succinimidyl ester (SE), a pH-sensitive fluorescent dye, makes engulfed apoptotic cells detectable due to the increased post-phagocytic light emission. This is a valuable tool for phagocytosis studies via FACS. We designed an ex vivo assay, using apoptotic pHrodo-labeled lymphocytes as prey and anti-CD11b-labeled tissue macrophages. To demonstrate its validity of detecting internalized apoptotic lymphocytes, we used MFGE8(-/-) macrophages, known to have impaired phagocytic ability. Uptake of apoptotic lymphocytes was accelerated and enhanced in splenic macrophages after stimulation with recombinant MFGE8, while peritoneal macrophages were able to compensate for the delayed uptake. This novel assay is a quick and reliable method to evaluate the internalization of apoptotic cells.

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Wallach, T., Mossmann, Z. J., Szczepek, M., Wetzel, M., Machado, R. S. R., Raden, M., Miladi, M., Kleinau, G., Krüger, C., Dembny, P., et al. (2021) · Figshare · doi:10.6084/m9.figshare.17088344
Additional file 5 of MicroRNA-100-5p and microRNA-298-5p released from apoptotic cortical neurons are endogenous Toll-like receptor 7/8 ligands that contribute to neurodegeneration
Wallach, T., Mossmann, Z. J., Szczepek, M., Wetzel, M., Machado, R. S. R., Raden, M., Miladi, M., Kleinau, G., Krüger, C., Dembny, P., et al. (2021) · Figshare · doi:10.6084/m9.figshare.17088338
Additional file 3 of Overexpression of Toll-like receptor 4 contributes to the internalization and elimination of Escherichia coli in sheep by enhancing caveolae-dependent endocytosis
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Additional file 2 of MicroRNA-100-5p and microRNA-298-5p released from apoptotic cortical neurons are endogenous Toll-like receptor 7/8 ligands that contribute to neurodegeneration
Wallach, T., Mossmann, Z. J., Szczepek, M., Wetzel, M., Machado, R. S. R., Raden, M., Miladi, M., Kleinau, G., Krüger, C., Dembny, P., et al. (2021) · Figshare · doi:10.6084/m9.figshare.17088329
Additional file 5 of An adapted protocol to derive microglia from stem cells and its application in the study of CSF1R-related disorders
Dorion, M.-F., Casas, D., Shlaifer, I., Yaqubi, M., Fleming, P., Karpilovsky, N. C., Chen, C. X. ‐., Nicouleau, M., Piscopo, V. E. C., MacDougall, E. J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26702383
Additional file 1 of An adapted protocol to derive microglia from stem cells and its application in the study of CSF1R-related disorders
Dorion, M.-F., Casas, D., Shlaifer, I., Yaqubi, M., Fleming, P., Karpilovsky, N. C., Chen, C. X. ‐., Nicouleau, M., Piscopo, V. E. C., MacDougall, E. J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25546980
Additional file 3 of An adapted protocol to derive microglia from stem cells and its application in the study of CSF1R-related disorders
Dorion, M.-F., Casas, D., Shlaifer, I., Yaqubi, M., Fleming, P., Karpilovsky, N. C., Chen, C. X. ‐., Nicouleau, M., Piscopo, V. E. C., MacDougall, E. J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26702377
Additional file 2 of An adapted protocol to derive microglia from stem cells and its application in the study of CSF1R-related disorders
Dorion, M.-F., Casas, D., Shlaifer, I., Yaqubi, M., Fleming, P., Karpilovsky, N. C., Chen, C. X. ‐., Nicouleau, M., Piscopo, V. E. C., MacDougall, E. J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25547144
Additional file 3 of MicroRNA-100-5p and microRNA-298-5p released from apoptotic cortical neurons are endogenous Toll-like receptor 7/8 ligands that contribute to neurodegeneration
Wallach, T., Mossmann, Z. J., Szczepek, M., Wetzel, M., Machado, R. S. R., Raden, M., Miladi, M., Kleinau, G., Krüger, C., Dembny, P., et al. (2021) · Figshare · doi:10.6084/m9.figshare.17088332
Additional file 4 of MicroRNA-100-5p and microRNA-298-5p released from apoptotic cortical neurons are endogenous Toll-like receptor 7/8 ligands that contribute to neurodegeneration
Wallach, T., Mossmann, Z. J., Szczepek, M., Wetzel, M., Machado, R. S. R., Raden, M., Miladi, M., Kleinau, G., Krüger, C., Dembny, P., et al. (2021) · Figshare · doi:10.6084/m9.figshare.17088335
Additional file 8 of MicroRNA-100-5p and microRNA-298-5p released from apoptotic cortical neurons are endogenous Toll-like receptor 7/8 ligands that contribute to neurodegeneration
Wallach, T., Mossmann, Z. J., Szczepek, M., Wetzel, M., Machado, R. S. R., Raden, M., Miladi, M., Kleinau, G., Krüger, C., Dembny, P., et al. (2021) · Figshare · doi:10.6084/m9.figshare.17088347
Additional file 11 of MicroRNA-100-5p and microRNA-298-5p released from apoptotic cortical neurons are endogenous Toll-like receptor 7/8 ligands that contribute to neurodegeneration
Wallach, T., Mossmann, Z. J., Szczepek, M., Wetzel, M., Machado, R. S. R., Raden, M., Miladi, M., Kleinau, G., Krüger, C., Dembny, P., et al. (2021) · Figshare · doi:10.6084/m9.figshare.17088317

Authors: Miksa, M., Komura, H., Wu, R., Shah, K. G., & Wang, P.
Affiliations: Feinstein Institute for Medical Research (US)
Corresponding author: Wang, Ping
ORCID: Wu, Rongqian
Shah, Kavin G.
Wang, Ping
Venue: Journal of Immunological Methods
Publisher: Elsevier BV
Published: 2009-03
Volume: 342
Issue: 1-2
Pages: 71-77
ISSN: 0022-1759 (ISSN-L)
DOI: 10.1016/j.jim.2008.11.019
PMC: PMC2675277
OpenAlex: W2100326315
Cited by: 320
References: 16
Citations by year: 2026: 11 · 2025: 14 · 2024: 23 · 2023: 12 · 2022: 17 · 2021: 39 · 2020: 15 · 2019: 19 · 2018: 26 · 2017: 25 · 2016: 23 · 2015: 32 · 2014: 19 · 2013: 15 · 2012: 7
FWCI: 4.31
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Journal of Immunological Methods (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute on Aging (R01AG028352)
National Institute of General Medical Sciences (R01GM053008, R01GM057468)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
Keywords: phagocytosis of apoptotic cells, macrophages, pH-sensitive fluorescent dye, efferocytosis, MFG-E8, splenic macrophages, peritoneal macrophages, lymphocytes
MeSH terms: Animals, Flow Cytometry, Fluorescent Dyes, Male, Mice, Inbred C57BL, Microscopy, Fluorescence, Phagocytosis, Spleen, Succinimides, Thymus Gland, Rats, Sprague-Dawley, Apoptosis, Macrophages, Peritoneal, Mice, Rats

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A novel method to determine the engulfment of apoptotic cells by macrophages using pHrodo succinimidyl ester

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