A novel method to determine the engulfment of apoptotic cells by macrophages using pHrodo succinimidyl ester
Open accessAbstract
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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pHrodo only fluoresces once it enters acidic compartments of lysosomes, so pHrodo-positive fluorescence within microglia confirms phagocytosis of RGC inputs.
“Because pHrodo only fluoresces once it enters acidic compartments of lysosomes, any pHrodo-positive fluorescence within a microglia confirms phagocytosis of RGC inputs.”
From Microglia Sculpt Postnatal Neural Circuits in an Activity and Complement-Dependent Manner (2012) · cites this paper as Miksa et al., 2009
The Results (page not provided) show that pHrodo-labeled cells become much brighter after macrophage engulfment as phagosomes acidify. But the paper also reports dim fluorescence before engulfment, so “only fluoresces once” is too absolute; it tests macrophages engulfing apoptotic cells, not microglia engulfing RGC inputs. (LLM, conf=0.88)
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Cites
A blast from the past: clearance of apoptotic cells regulates immune responses
Savill, J., Dransfield, I., Gregory, C. D., & Haslett, C. (2002) · Nature reviews. Immunology · doi:10.1038/nri957 · Cited by 1,574 · see citing works
Identification of a factor that links apoptotic cells to phagocytes
Hanayama, R., Tanaka, M., Miwa, K., Shinohara, A., Iwamatsu, A., & Nagata, S. (2002) · Nature · doi:10.1038/417182a · Cited by 1,401 · see citing works
Huynh, M.-L. N., Fadok, V., & Henson, P. (2002) · Journal of Clinical Investigation · doi:10.1172/jci11638 · Cited by 1,333 · see citing works
Autoimmune Disease and Impaired Uptake of Apoptotic Cells in MFG-E8-Deficient Mice
Hanayama, R., Tanaka, M., Miyasaka, K., Aozasa, K., Koike, M., Uchiyama, Y., & Nagata, S. (2004) · Science · doi:10.1126/science.1094359 · Cited by 992 · see citing works
Regulation of Phagosome Maturation by Signals from Toll-Like Receptors
Blander, J. M., & Medzhitov, R. (2004) · Science · doi:10.1126/science.1096158 · Cited by 991 · see citing works
Huynh, M.-L. N., Fadok, V. A., & Henson, P. M. (2002) · Journal of Clinical Investigation · doi:10.1172/jci0211638 · Cited by 957 · see citing works
Engulfment of apoptotic cells: signals for a good meal
Ravichandran, K. S., & Lorenz, U. M. (2007) · Nature reviews. Immunology · doi:10.1038/nri2214 · Cited by 634 · see citing works
Bacterial strategies for overcoming host innate and adaptive immune responses
Hornef, M. W., Wick, M. J., Rhen, M., & Normark, S. J. (2002) · Nature Immunology · doi:10.1038/ni1102-1033 · Cited by 505 · see citing works
Phagocytosis and comparative innate immunity: learning on the fly
Stuart, L. M., & Ezekowitz, R. A. B. (2008) · Nature reviews. Immunology · doi:10.1038/nri2240 · Cited by 288 · see citing works
Asano, K., Miwa, M., Miwa, K., Hanayama, R., Nagase, H., Nagata, S., & Tanaka, M. (2004) · The Journal of Experimental Medicine · doi:10.1084/jem.20040342 · Cited by 268 · see citing works
Lactadherin Deficiency Leads to Apoptotic Cell Accumulation and Accelerated Atherosclerosis in Mice
Ait-Oufella, H., Kinugawa, K., Zoll, J., Simon, T., Boddaert, J., Heeneman, S., Blanc-Brude, O., Barateau, V., Potteaux, S., Merval, R., et al. (2007) · Circulation · doi:10.1161/circulationaha.106.662080 · Cited by 255 · see citing works
Bu, H., Zuo, X.-L., Wang, X., Ensslin, M. A., Koti, V., Hsueh, W., Raymond, A. S., Shur, B. D., & Tan, X. (2007) · Journal of Clinical Investigation · doi:10.1172/jci31841 · Cited by 210 · see citing works
A co-stimulatory signal through ICAM-β2 integrin-binding potentiates neutrophil phagocytosis
Schnitzler, N., Haase, G., Podbielski, A., Lütticken, R., & Schweizer, K. G. (1999) · Nature Medicine · doi:10.1038/5597 · Cited by 63 · see citing works
The Bell Tolls for Phagosome Maturation
Watts, C. K. W. (2004) · Science · doi:10.1126/science.1098573 · Cited by 18 · see citing works
100 years of the phagocytosis doctrine (Ilya Ilyich Mechnikov).
Nn, K. (1983) · PubMed · Cited by 1 · see citing works
Flagged first, then by citations
1 of the 16 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Microglia Sculpt Postnatal Neural Circuits in an Activity and Complement-Dependent Manner
Schafer, D. P., Lehrman, E. K., Kautzman, A. G., Koyama, R., Mardinly, A. R., Yamasaki, R., Ransohoff, R. M., Greenberg, M. E., Barres, B. A., & Stevens, B. (2012) · Neuron · doi:10.1016/j.neuron.2012.03.026 · Cited by 4,089 · see citing works
“To further validate that microglia phagocytose RGC inputs, pHrodo-dextran, an anterograde tracer and pH-sensitive dye, was used to label RGC inputs (Figures S1A and S1B; Deriy et al., 2009; Miksa et al., 2009).”
Fluorescent Indicators for Intracellular pH
Han, J., & Burgess, K. (2009) · Chemical Reviews · doi:10.1021/cr900249z · Cited by 1,623 · see citing works
CD24 signalling through macrophage Siglec-10 is a target for cancer immunotherapy
Barkal, A. A., Brewer, R. E., Markovic, M., Kowarsky, M., Barkal, S. A., Zaro, B. W., Krishnan, V., Hatakeyama, J., Dorigo, O., Barkal, L. J., et al. (2019) · Nature · doi:10.1038/s41586-019-1456-0 · Cited by 1,391 · see citing works
Apoptosis and Clearance of Apoptotic Cells
Nagata, S. (2018) · Annual Review of Immunology · doi:10.1146/annurev-immunol-042617-053010 · Cited by 1,107 · see citing works
Sellgren, C. M., Gracias, J., Watmuff, B., Biag, J. D., Thanos, J. M., Whittredge, P. B., Fu, T., Worringer, K. A., Brown, H. E., Wang, J. P., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-018-0334-7 · Cited by 784 · see citing works
TAM receptors regulate multiple features of microglial physiology
Fourgeaud, L., Través, P. G., Tufail, Y., Leal-Bailey, H., Lew, E. D., Burrola, P. G., Callaway, P., Zagórska, A., Rothlin, C. V., Nimmerjahn, A., et al. (2016) · Nature · doi:10.1038/nature17630 · Cited by 600 · see citing works
Caspase-mediated cleavage of phospholipid flippase for apoptotic phosphatidylserine exposure
Segawa, K., Kurata, S., Yanagihashi, Y., Brummelkamp, T. R., Matsuda, F., & Nagata, S. (2014) · Science · doi:10.1126/science.1252809 · Cited by 528 · see citing works
Cancer across the tree of life: cooperation and cheating in multicellularity
Aktipis, C. A., Boddy, A. M., Jansen, G., Hibner, U., Hochberg, M. E., Maley, C. C., & Wilkinson, G. S. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0219 · Cited by 466 · see citing works
Diversification of TAM receptor tyrosine kinase function
Zagórska, A., Través, P. G., Lew, E. D., Dransfield, I., & Lemke, G. (2014) · Nature Immunology · doi:10.1038/ni.2986 · Cited by 430 · see citing works
VISTA is a checkpoint regulator for naïve T cell quiescence and peripheral tolerance
ElTanbouly, M. A., Zhao, Y., Nowak, E. C., Li, J., Schaafsma, E., Mercier, I. L., Ceeraz, S., Lines, J. L., Peng, C., Carrière, C., et al. (2020) · Science · doi:10.1126/science.aay0524 · Cited by 299 · see citing works
Mesenchymal stromal cell apoptosis is required for their therapeutic function
Pang, S. H. M., D’Rozario, J., Mendonca, S., Bhuvan, T., Payne, N. L., Zheng, D., Hisana, A., Wallis, G., Barugahare, A., Powell, D., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-26834-3 · Cited by 245 · see citing works
Organelle-targeting surface-enhanced Raman scattering (SERS) nanosensors for subcellular pH sensing
Shen, Y., Liang, L., Zhang, S., Huang, D., Zhang, J., Xu, S., Liang, C., & Xu, W. (2017) · Nanoscale · doi:10.1039/c7nr08636a · Cited by 253 · see citing works
Two‐Color Probe to Monitor a Wide Range of pH Values in Cells
Lee, M. H., Han, J. H., Lee, J. H., Park, N., Kumar, R., Kang, C., & Kim, J. S. (2013) · Angewandte Chemie International Edition · doi:10.1002/anie.201301894 · Cited by 252 · see citing works
Pacak, C. A., Preble, J. M., Kondo, H., Seibel, P., Levitsky, S., del Nido, P. J., Cowan, D. B., & McCully, J. D. (2015) · Biology Open · doi:10.1242/bio.201511478 · Cited by 212 · see citing works
Characterization of the mononuclear phagocyte system in zebrafish
Wittamer, V., Bertrand, J. Y., Gutschow, P., & Traver, D. J. (2011) · Blood · doi:10.1182/blood-2010-11-321448 · Cited by 206 · see citing works
Two‐Color Probe to Monitor a Wide Range of pH Values in Cells
Lee, M. H., Han, J. H., Lee, J. H., Park, N., Kumar, R., Kang, C., & Kim, J. S. (2013) · Angewandte Chemie · doi:10.1002/ange.201301894 · Cited by 206 · see citing works
EGFET-Based Sensors for Bioanalytical Applications: A Review
Pullano, S. A., Critello, C. D., Mahbub, I., Tasneem, N. T., Shamsir, S., Islam, S. K., Greco, M., & Fiorillo, A. S. (2018) · Sensors · doi:10.3390/s18114042 · Cited by 197 · see citing works
Cain, D. W., O’Koren, E. G., Kan, M. J., Womble, M. A., Sempowski, G. D., Hopper, K., Gunn, M. D., & Kelsoe, G. H. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1300581 · Cited by 187 · see citing works
SLAM is a microbial sensor that regulates bacterial phagosome functions in macrophages
Berger, S. B., Ros, X. R., Ma, C., Wang, G., Faubion, W. A., Liao, G., Compeer, E. B., Keszei, M., Rameh, L. E., Wang, N., et al. (2010) · Nature Immunology · doi:10.1038/ni.1931 · Cited by 182 · see citing works
Galectin-3 is a new MerTK-specific eat-me signal
Caberoy, N. B., Alvarado, G., Bigcas, J., & Li, W. (2012) · Journal of Cellular Physiology · doi:10.1002/jcp.22955 · Cited by 176 · see citing works
Karpowicz, R. J., Haney, C. M., Mihaila, T. S., Frasier, R. M., Petersson, E. J., & Lee, V. M. ‐. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.780296 · Cited by 165 · see citing works
Patient-specific models of microglia-mediated engulfment of synapses and neural progenitors
Sellgren, C. M., Sheridan, S. D., Gracias, J., Xuan, D., Fu, T., & Perlis, R. H. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.220 · Cited by 157 · see citing works
Tim4- and MerTK-Mediated Engulfment of Apoptotic Cells by Mouse Resident Peritoneal Macrophages
Nishi, C., Toda, S., Segawa, K., & Nagata, S. (2014) · Molecular and Cellular Biology · doi:10.1128/mcb.01394-13 · Cited by 157 · see citing works
Niu, G., Zhang, P., Liu, W., Wang, M., Zhang, H., Wu, J., Zhang, L., & Wang, P. (2017) · Analytical Chemistry · doi:10.1021/acs.analchem.6b04417 · Cited by 150 · see citing works
Self-citationYang, S., Shim, M. K., Kim, W. J., Choi, J., Nam, G., Kim, J., Kim, J., Moon, Y., Kim, H. Y., Park, J., et al. (2021) · Biomaterials · doi:10.1016/j.biomaterials.2021.120791 · Cited by 145 · see citing works
Engulfing Astrocytes Protect Neurons from Contact-Induced Apoptosis following Injury
Lööv, C., Hillered, L., Ebendal, T., & Erlandsson, A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033090 · Cited by 144 · see citing works
The Axl receptor tyrosine kinase is a discriminator of macrophage function in the inflamed lung
Fujimori, T., Grabiec, A. M., Kaur, M., Bell, T. J., Fujino, N., Cook, P. C., Svedberg, F. R., MacDonald, A. S., Maciewicz, R. A., Singh, D., et al. (2015) · Mucosal Immunology · doi:10.1038/mi.2014.129 · Cited by 130 · see citing works
Two-Step Engulfment of Apoptotic Cells
Toda, S., Hanayama, R., & Nagata, S. (2011) · Molecular and Cellular Biology · doi:10.1128/mcb.05993-11 · Cited by 124 · see citing works
The role of the FPR2/ALX receptor in atherosclerosis development and plaque stability
Petri, M. H., Laguna-Fernández, A., Gonzalez-Diez, M., Paulsson-Berne, G., Hansson, G. K., & Bäck, M. (2015) · Cardiovascular Research · doi:10.1093/cvr/cvu224 · Cited by 125 · see citing works
Zhou, T. G., Li, Y., Li, X., Zeng, F., Rao, Y., He, Y., Wang, Y., Liu, M., Li, D., Xu, Z., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-33932-3 · Cited by 122 · see citing works
Mer receptor tyrosine kinase mediates both tethering and phagocytosis of apoptotic cells
Dransfield, I., Zagórska, A., Lew, E. D., Michail, K., & Lemke, G. (2015) · Cell Death and Disease · doi:10.1038/cddis.2015.18 · Cited by 122 · see citing works
Shuang, E., Mao, Q.-X., Yuan, X., Kong, X.-L., Chen, X., & Wang, J. (2018) · Nanoscale · doi:10.1039/c8nr03453b · Cited by 124 · see citing works
Suresh Babu, S., Thandavarayan, R. A., Joladarashi, D., Jeyabal, P., Krishnamurthy, S., Bhimaraj, A., Youker, K. A., & Krishnamurthy, P. (2016) · Scientific Reports · doi:10.1038/srep36207 · Cited by 119 · see citing works
Esmann, L., Idel, C., Sarkar, A., Hellberg, L., Behnen, M., Möller, S., van Zandbergen, G., Klinger, M. H. F., Köhl, J., Bussmeyer, U., et al. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0900564 · Cited by 114 · see citing works
Han, J., Kang, Y. J., Shin, C., Ra, J.-S., Shin, H., Hong, S. Y., Do, Y., & Kang, S. (2013) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2013.11.003 · Cited by 116 · see citing works
Cho, E., Nam, G., Hong, Y., Kim, Y. K., Kim, D., Yang, Y., & Kim, I. (2018) · Journal of Controlled Release · doi:10.1016/j.jconrel.2018.04.037 · Cited by 114 · see citing works
Zhang, B., Sun, J., Wang, Y., Ji, D., Yuan, Y., Li, S., Sun, Y., Hou, Y., Li, P., Zhao, L., et al. (2021) · Nature Biomedical Engineering · doi:10.1038/s41551-021-00797-8 · Cited by 114 · see citing works
Nam, G., Lee, E. J., Kim, Y. K., Hong, Y., Choi, Y., Ryu, M., Woo, J., Cho, Y., Ahn, D. J., Yang, Y., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-04607-9 · Cited by 113 · see citing works
Pan, W., Wang, H., Yang, L., Yu, Z., Li, N., & Tang, B. (2016) · Analytical Chemistry · doi:10.1021/acs.analchem.6b01010 · Cited by 111 · see citing works
Avalos, C. R., Price, S. L., Forsyth, E. R., Pin, J. N., Shirk, E. N., Bullock, B. T., Queen, S. E., Li, M., Gellerup, D. D., O’Connor, S. L., et al. (2016) · Journal of Virology · doi:10.1128/jvi.00290-16 · Cited by 107 · see citing works
Genomic instability in mutant p53 cancer cells upon entotic engulfment
Mackay, H. L., Moore, D. A., Hall, C., Birkbak, N. J., Jamal‐Hanjani, M., Karim, S. A., Phatak, V. M., Piñon, L., Morton, J. P., Swanton, C., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-05368-1 · Cited by 107 · see citing works
Zhang, Q. Q., Yang, T., Li, R. S., Zou, H. Y., Li, Y. F., Guo, J. W., Liu, X. D., & Huang, C. Z. (2018) · Nanoscale · doi:10.1039/c8nr03212b · Cited by 104 · see citing works
Choi, B., Moon, H., Hong, S. J., Shin, C., Do, Y., Ryu, S., & Kang, S. (2016) · ACS Nano · doi:10.1021/acsnano.5b08084 · Cited by 98 · see citing works
Wang, H., Yang, Y., Sun, X., Tian, F., Guo, S., Wang, W., Tian, Z., Jin, H. H., Zhang, Z., & Tian, Y. (2018) · Theranostics · doi:10.7150/thno.26193 · Cited by 95 · see citing works
Exosomal CD47 Plays an Essential Role in Immune Evasion in Ovarian Cancer
Shimizu, A., Sawada, K., Kobayashi, M., Yamamoto, M., Yagi, T., Kinose, Y., Kodama, M., Hashimoto, K., & Kimura, T. (2021) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-20-0956 · Cited by 96 · see citing works
Rhodamine-based fluorescent probe for direct bio-imaging of lysosomal pH changes
Shi, X., Mao, G., Zhang, X., Liu, H., Gong, Y., Wu, Y., Zhou, L., Zhang, J., & Tan, W. (2014) · Talanta · doi:10.1016/j.talanta.2014.07.030 · Cited by 90 · see citing works
A novel nanogel-based fluorescent probe for ratiometric detection of intracellular pH values
Cao, L., Li, X., Wang, S., Li, S., Li, Y., & Yang, G. (2014) · Chemical Communications · doi:10.1039/c4cc03716b · Cited by 90 · see citing works
MafB is a critical regulator of complement component C1q
Tran, M. T., Hamada, M., Jeon, H., Shiraishi, R., Asano, K., Hattori, M., Nakamura, M., Imamura, Y., Tsunakawa, Y., Fujii, R., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-01711-0 · Cited by 89 · see citing works
The Prototypic Cyclotide Kalata B1 Has a Unique Mechanism of Entering Cells
Henriques, S. T., Huang, Y., Chaousis, S., Sani, M., Poth, A. G., Separovic, F., & Craik, D. J. (2015) · Chemistry & Biology · doi:10.1016/j.chembiol.2015.07.012 · Cited by 87 · see citing works
Apoptotic cells suppress mast cell inflammatory responses via the CD300a immunoreceptor
Nakahashi-Oda, C., Tahara‐Hanaoka, S., Shoji, M., Okoshi, Y., Nakano-Yokomizo, T., Ohkohchi, N., Yasui, T., Kikutani, H., Honda, S.-I., Shibuya, K., et al. (2012) · The Journal of Experimental Medicine · doi:10.1084/jem.20120096 · Cited by 87 · see citing works
Fan, L., Liu, Q., Lu, D., Shi, H., Yang, Y., Li, Y., Dong, C., & Shuang, S. (2013) · Journal of Materials Chemistry B · doi:10.1039/c3tb20547a · Cited by 84 · see citing works
Milk Fat Globule-EGF Factor VIII in Sepsis and Ischemia-Reperfusion Injury
Matsuda, A., Jacob, A., Wu, R., Zhou, M., Nicastro, J. M., Coppa, G. F., & Wang, P. (2010) · Molecular Medicine · doi:10.2119/molmed.2010.00135 · Cited by 83 · see citing works
Self-citationMerTK-mediated engulfment of pyrenocytes by central macrophages in erythroblastic islands
Toda, S., Segawa, K., & Nagata, S. (2014) · Blood · doi:10.1182/blood-2014-01-547976 · Cited by 80 · see citing works
Cheung, T. S., Galleu, A., Bonin, M. V., Bornhäuser, M., & Dazzi, F. (2019) · Haematologica · doi:10.3324/haematol.2018.214767 · Cited by 80 · see citing works
Transmembrane TNF-dependent uptake of anti-TNF antibodies
Deora, A. B., Hegde, S., Lee, J. R. E., Choi, C.-H., Chang, Q., Lee, C. Q. E., Eaton, L. J., Tang, H., Wang, D., Lee, D., et al. (2017) · mAbs · doi:10.1080/19420862.2017.1304869 · Cited by 81 · see citing works
A fluorogenic cyclic peptide for imaging and quantification of drug-induced apoptosis
Barth, N. D., Subirós‐Funosas, R., Mendive‐Tapia, L., Duffin, R., Shields, M. A., Cartwright, J. A., Henriques, S. T., Sot, J., Goñi, F. M., Lavilla, R., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-17772-7 · Cited by 78 · see citing works
Novel Therapeutic Targets for Sepsis: Regulation of Exaggerated Inflammatory Responses
Matsuda, A., Jacob, A., Wu, R., Aziz, M., Yang, W.-L., Matsutani, T., Suzuki, H., Furukawa, K., Uchida, E., & Wang, P. (2012) · Journal of Nippon Medical School · doi:10.1272/jnms.79.4 · Cited by 72 · see citing works
Self-citationProtective Role of the MER Tyrosine Kinase via Efferocytosis in Rheumatoid Arthritis Models
Waterborg, C. E. J., Beermann, S., Broeren, M. G. A., Bennink, M. B., Koenders, M. I., van Lent, P. L. E. M., van den Berg, W. B., van der Kraan, P. M., & van de Loo, F. A. J. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00742 · Cited by 73 · see citing works
Slow degradation in phagocytic astrocytes can be enhanced by lysosomal acidification
Lööv, C., Mitchell, C. H., Simonsson, M., & Erlandsson, A. (2015) · Glia · doi:10.1002/glia.22873 · Cited by 69 · see citing works
Identification and isolation of splenic tissue-resident macrophage sub-populations by flow cytometry
Fujiyama, S., Nakahashi-Oda, C., Abe, F., Wang, Y., Satoh, K., & Shibuya, A. (2018) · International Immunology · doi:10.1093/intimm/dxy064 · Cited by 68 · see citing works
Pivotal Advance: Characterization of mouse liver phagocytic B cells in innate immunity
Nakashima, M., Kinoshita, M., Nakashima, H., Habu, Y., Miyazaki, H., Shono, S., Hiroi, S., Shinomiya, N., Nakanishi, K., & Seki, S. (2011) · Journal of Leukocyte Biology · doi:10.1189/jlb.0411214 · Cited by 66 · see citing works
Nanoparticle‐based luminescent probes for intracellular sensing and imaging of pH
Schäferling, M. (2015) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.1366 · Cited by 64 · see citing works
Nakahashi-Oda, C., Fujiyama, S., Nakazawa, Y., Kanemaru, K., Wang, Y., Lyu, W., Shichita, T., Kitaura, J., Abe, F., & Shibuya, A. (2021) · Science Immunology · doi:10.1126/sciimmunol.abe7915 · Cited by 61 · see citing works
Jiang, D., Burger, C. A., Akhanov, V., Liang, J. H., Mackin, R. D., Albrecht, N. E., Andrade, P., Schafer, D. P., & Samuel, M. A. (2022) · Immunity · doi:10.1016/j.immuni.2022.10.018 · Cited by 62 · see citing works
Phagocytosis Assays with Different pH-Sensitive Fluorescent Particles and Various Readouts
Lindner, B., Burkard, T., & Schuler, M. J. (2020) · BioTechniques · doi:10.2144/btn-2020-0003 · Cited by 61 · see citing works
Myc‐nick promotes efferocytosis through M2 macrophage polarization during resolution of inflammation
Zhong, X., Lee, H., Kim, S. H., Park, S., Kim, W., Cha, Y., & Surh, Y. (2018) · The FASEB Journal · doi:10.1096/fj.201800223r · Cited by 62 · see citing works
Subbarayalu, P., Viswanadhapalli, S., Abdelfattah, N., Onyeagucha, B. C., Timilsina, S., Mohammad, T. A., Chen, Y., Drake, M. T., Vuori, K., Kumar, T. R., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-00590-9 · Cited by 60 · see citing works
Prosser, A., Hibbert, J., Strunk, T., Kok, C. H., Simmer, K. N., Richmond, P., Burgner, D. P., & Currie, A. J. (2013) · Pediatric Research · doi:10.1038/pr.2013.145 · Cited by 59 · see citing works
Sun, M., Du, L., Yu, H., Zhang, K., Liu, Y., & Wang, S. (2016) · Talanta · doi:10.1016/j.talanta.2016.10.012 · Cited by 59 · see citing works
Xiong, W., Han, Z., Ding, S., Wang, H., Du, Y., Cui, W., & Zhang, M. (2024) · Advanced Science · doi:10.1002/advs.202400345 · Cited by 57 · see citing works
A novel method for determining antibody-dependent cellular phagocytosis
Kamen, L. A., Myneni, S., Langsdorf, C., Kho, E., Ordonia, B., Thakurta, T. G., Zheng, K., Song, A., & Chung, S. (2019) · Journal of Immunological Methods · doi:10.1016/j.jim.2019.03.001 · Cited by 57 · see citing works
H-Rubies, a new family of red emitting fluorescent pH sensors for living cells
Despras, G., Ильгизовна, З. А., Dardevet, L., Tisseyre, C., Magalhaes, J. G., Garner, C., WAARD, M. M. D., Amigorena, S., Feltz, A., Mallet, J., et al. (2015) · Chemical Science · doi:10.1039/c5sc01113b · Cited by 56 · see citing works
Yang, M., Zhang, X., Liu, H., Kang, H., Zhu, Z., Yang, W. J., & Tan, W. (2015) · Analytical Chemistry · doi:10.1021/acs.analchem.5b01233 · Cited by 55 · see citing works
Zebrafish as a Novel Vertebrate Model To Dissect Enterococcal Pathogenesis
Prajsnar, T. K., Renshaw, S. A., Ogryzko, N. V., Foster, S. J., Serror, P., & Mesnage, S. (2013) · Infection and Immunity · doi:10.1128/iai.00976-13 · Cited by 52 · see citing works
Protein Corona Inhibits Endosomal Escape of Functionalized DNA Nanostructures in Living Cells
Smolková, B., MacCulloch, T., Rockwood, T., Liu, M., Henry, S. J. W., Frtús, A., Uzhytchak, M., Lunová, M., Hof, M., Jurkiewicz, P., et al. (2021) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.1c14401 · Cited by 53 · see citing works
The Complement System Is Essential for the Phagocytosis of Mesenchymal Stromal Cells by Monocytes
Gavin, C., Meinke, S., Heldring, N., Heck, K. A., Achour, A., Iacobaeus, E., Höglund, P., Blanc, K. L., & Kadri, N. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02249 · Cited by 53 · see citing works
Motani, K., Ito, S., & Nagata, S. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1402705 · Cited by 48 · see citing works
Das, S., Sarkar, A., Ryan, K. A., Fox, S., Berger, A. H., Juncadella, I. J., Bimczok, D., Smythies, L. E., Harris, P. R., Ravichandran, K. S., et al. (2014) · The FASEB Journal · doi:10.1096/fj.13-243238 · Cited by 48 · see citing works
Essential Role of mTORC1 in Self-Renewal of Murine Alveolar Macrophages
Deng, W., Yang, J., Lin, X., Shin, J., Gao, J., & Zhong, X. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1501845 · Cited by 47 · see citing works
Upconversion Luminescence Sensitized pH-Nanoprobes
Mahata, M. K., Bae, H., & Lee, K. N. (2017) · Molecules · doi:10.3390/molecules22122064 · Cited by 49 · see citing works
Ma, Y., Qin, P., Zhang, L., Lu, J., Shui, T., Chen, J., Shi, C., Yang, J. H., Smith, M., Liu, Y., et al. (2018) · Europe PMC (PubMed Central) · Cited by 48 · see citing works
Ligand-dependent kinase activity of MERTK drives efferocytosis in human iPSC-derived macrophages
Wanke, F., Gutbier, S., Rümmelin, A., Steinberg, M., Hughes, L. D., Koenen, M., Komuczki, J., Regan-Komito, D., Wagage, S., Hesselmann, J., et al. (2021) · Cell Death and Disease · doi:10.1038/s41419-021-03770-0 · Cited by 47 · see citing works
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) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00498-5 · Cited by 48 · see citing works
Di, A., Kiya, T., Gong, H., Gao, X., & Malik, A. B. (2017) · Journal of Cell Science · doi:10.1242/jcs.196014 · Cited by 49 · see citing works
The adipokine NimrodB5 regulates peripheral hematopoiesis in Drosophila
Ramond, E. J., Petrignani, B., Dudzic, J. P., Boquete, J., Poidevin, M., Kondo, S., & Lemaître, B. (2020) · FEBS Journal · doi:10.1111/febs.15237 · Cited by 47 · see citing works
Neaga, A., Lefor, J., Lich, K. E., Liparoto, S. F., & Xiao, Y. Q. (2011) · Journal of Immunological Methods · doi:10.1016/j.jim.2011.06.027 · Cited by 47 · see citing works
Novel role of ICAM3 and LFA-1 in the clearance of apoptotic neutrophils by human macrophages
Kristóf, E., Zahuczky, G., Katona, K., Doró, Z., Nagy, É., & Fésüs, L. (2013) · APOPTOSIS · doi:10.1007/s10495-013-0873-z · Cited by 48 · see citing works
He, L., Yang, X., Zhao, F., Wang, K., Wang, Q., Liu, J., Huang, J. L., Li, W., & Yang, M. (2015) · Analytical Chemistry · doi:10.1021/ac504458r · Cited by 46 · see citing works
A single pH fluorescent probe for biosensing and imaging of extreme acidity and extreme alkalinity
Chao, J., Wang, H., Zhang, Y., Li, Z., Liu, Y., Huo, F., Yin, C., Shi, Y., & Wang, J.-J. (2017) · Analytica Chimica Acta · doi:10.1016/j.aca.2017.04.020 · Cited by 46 · see citing works
Tubby regulates microglial phagocytosis through MerTK
Caberoy, N. B., Alvarado, G., & Li, W. (2012) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2012.07.009 · Cited by 44 · see citing works
Murphy, M., Xiong, Y., Pattabiraman, G., Qiu, F., & Medvedev, A. E. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.640128 · Cited by 45 · see citing works
Study on various fluorescein derivatives as pH sensors
Kim, H. N., Swamy, K. M. K., & Yoon, J. (2011) · Tetrahedron Letters · doi:10.1016/j.tetlet.2011.02.076 · Cited by 45 · see citing works
Protein kinase Cδ is a critical component of Dectin-1 signaling in primary human monocytes
Elsori, D. H., Yakubenko, V. P., Roome, T., Thiagarajan, P. S., Bhattacharjee, A., Yadav, S. P., & Cathcart, M. K. (2011) · Journal of Leukocyte Biology · doi:10.1189/jlb.0610376 · Cited by 45 · see citing works
MerTK is a mediator of alpha-synuclein fibril uptake by human microglia
Dorion, M., Yaqubi, M., Senkevich, K. A., Kieran, N. W., MacDonald, A., Chen, C. X. ‐., Luo, W., Wallis, A., Shlaifer, I., Hall, J. A., et al. (2023) · Brain · doi:10.1093/brain/awad298 · Cited by 43 · see citing works
Hendrickx, D. A. E., Schuurman, K. G., van Draanen, M., Hamann, J., & Huitinga, I. (2014) · Journal of Neuroinflammation · doi:10.1186/1742-2094-11-64 · Cited by 43 · see citing works
Lenzo, J. C., O’brien-simpson, N. M., Orth, R., Mitchell, H. L., Dashper, S. G., & Reynolds, E. C. (2016) · Infection and Immunity · doi:10.1128/iai.01500-15 · Cited by 43 · see citing works
Inactivation of Rab11a GTPase in Macrophages Facilitates Phagocytosis of Apoptotic Neutrophils
Jiang, C., Liu, Z., Hu, R., Bo, L., Minshall, R. D., Malik, A. B., & Hu, G. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1601495 · Cited by 43 · see citing works
Ye, Y., Huang, X., Zhang, Y., Lai, X., Wu, X., Zeng, X., Tang, X., & Zeng, Y. (2011) · International Immunopharmacology · doi:10.1016/j.intimp.2011.12.011 · Cited by 43 · see citing works
Simons, E. R. (2010) · Current Protocols in Cytometry · doi:10.1002/0471142956.cy0931s51 · Cited by 43 · see citing works
Ying, L.-Q., & Branchaud, B. P. (2011) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2011.04.137 · Cited by 42 · see citing works
- Authors
- Miksa, M., Komura, H., Wu, R., Shah, K. G., & Wang, P.
- Affiliations
- Feinstein Institute for Medical Research (US)
- Corresponding author
- 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)
- 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
- 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
- Health Sciences › Medicine › Epidemiology › 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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