NADPH oxidase controls phagosomal pH and antigen cross-presentation in human dendritic cells
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The phagocyte NADPH oxidase (NOX2) is critical for the bactericidal activity of phagocytic cells and plays a major role in innate immunity. We showed recently that NOX2 activity in mouse dendritic cells (DCs) prevents acidification of phagosomes, promoting antigen cross-presentation. Inorder to investigate the role of NOX2 in the regulation of the phagosomal pH in human DCs, we analyzed the production of reactive oxygen species (ROS) and the phagosomal/endosomal pH in monocyte-derived DCs and macrophages (MØs) from healthy donors or patients with chronic granulomatous disease (CGD). As expected, we found that human MØs acidify their phagosomes more efficiently than human DCs. Accordingly, the expression of the vacuolar proton ATPase (V-H+-ATPase) was higher in MØs than in DCs. Phagosomal ROS production, however, was also higher in MØs than in DCs, due to higher levels of gp91phox expression and recruitment to phagosomes. In contrast, in the absence of active NOX2, the phagosomal and endosomal pH decreased. Both in the presence of a NOX2 inhibitor and in DCs derived from patients with CGD, the cross-presentation of 2 model tumor antigens was impaired. We conclude that NOX2 activity participates in the regulation of the phagosomal and endosomal pH in human DCs, and is required for efficient antigen cross-presentation.
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Dendritic cells express little NOX2 and consequently have lower O2•− and ROS production after activation.
“Dendritic cells (DC) express little NOX2 and consequently have a lower O2•− and ROS production after activation [179].”
From Superoxide Anion Chemistry—Its Role at the Core of the Innate Immunity (2023) · cites this paper as [179]
Cites
Meijer, L., Nelson, D. J., Riazanski, V., Gabdoulkhakova, A. G., Héry-Arnaud, G., Berre, R. L., Loaëc, N., Oumata, N., Galons, H., Nowak, E., et al. (2016) · Journal of Innate Immunity · doi:10.1159/000444256 · Cited by 4,992 · see citing works
Apetoh, L., Ghiringhelli, F., Tesniere, A., Obeid, M., Ortiz, C., Criollo, A., Mignot, G., Maiuri, M. C., Ullrich, E., Saulnier, P., et al. (2007) · Nature Medicine · doi:10.1038/nm1622 · Cited by 3,056 · see citing works
Self-citationSavina, A., Jancic, C. C., Hugues, S., Guermonprez, P., Vargas, P., Moura, I. C., Lennon‐Duménil, A., Seabra, M. C., Raposo, G., & Amigorena, S. (2006) · Cell · doi:10.1016/j.cell.2006.05.035 · Cited by 896 · see citing works
Self-citationCross-Presentation, Dendritic Cells, Tolerance and Immunity
Heath, W. R., & Carbone, F. R. (2001) · Annual Review of Immunology · doi:10.1146/annurev.immunol.19.1.47 · Cited by 882 · see citing works
Differential Lysosomal Proteolysis in Antigen-Presenting Cells Determines Antigen Fate
Delamarre, L., Pack, M., Chang, H. C., Mellman, I., & Trombetta, E. S. (2005) · Science · doi:10.1126/science.1108003 · Cited by 776 · see citing works
ER–phagosome fusion defines an MHC class I cross-presentation compartment in dendritic cells
Guermonprez, P., Saveanu, L., Kleijmeer, M. J., Davoust, J. M., Endert, P. V., & Amigorena, S. (2003) · Nature · doi:10.1038/nature01911 · Cited by 753 · see citing works
Self-citationRodrı́guez, A., Régnault, A., Kleijmeer, M. J., Ricciardi‐Castagnoli, P., & Amigorena, S. (1999) · Nature Cell Biology · doi:10.1038/14058 · Cited by 552 · see citing works
Self-citationCFTR regulates phagosome acidification in macrophages and alters bactericidal activity
Di, A., Brown, M. E., Deriy, L. V., Li, C., Szeto, F. L., Chen, Y., Huang, P. C., Tong, J., Naren, A. P., Bindokas, V. P., et al. (2006) · Nature Cell Biology · doi:10.1038/ncb1456 · Cited by 494 · see citing works
The NADPH oxidase of professional phagocytes—prototype of the NOX electron transport chain systems
Cross, A. R., & Segal, A. W. (2004) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2004.03.008 · Cited by 489 · see citing works
T cells express a phagocyte-type NADPH oxidase that is activated after T cell receptor stimulation
Jackson, S. H., Devadas, S., Kwon, J., Pinto, L. A., & Williams, M. S. (2004) · Nature Immunology · doi:10.1038/ni1096 · Cited by 457 · see citing works
Cross‐presentation: underlying mechanisms and role in immune surveillance
Rock, K. L., & Shen, L. (2005) · Immunological Reviews · doi:10.1111/j.0105-2896.2005.00301.x · Cited by 449 · see citing works
Heyworth, P. G., Cross, A. R., & Curnutte, J. T. (2003) · Current Opinion in Immunology · doi:10.1016/s0952-7915(03)00109-2 · Cited by 396 · see citing works
(2012) · SpringerReference · doi:10.1007/springerreference_172807 · Cited by 360 · see citing works
Clemens, D. L., Lee, B., & Horwitz, M. A. (2004) · Infection and Immunity · doi:10.1128/iai.72.6.3204-3217.2004 · Cited by 349 · see citing works
Rab27a regulates phagosomal pH and NADPH oxidase recruitment to dendritic cell phagosomes
Jancic, C. C., Savina, A., Wasmeier, C., Tolmachova, T., Benna, J. E., Dang, P. M., Pascolo, S., Gougerot-Pocidalo, M.-A., Raposo, G., Seabra, M. C., et al. (2007) · Nature Cell Biology · doi:10.1038/ncb1552 · Cited by 250 · see citing works
Self-citationChloroquine enhances human CD8 + T cell responses against soluble antigens in vivo
Accapezzato, D., Visco, V., Francavilla, V., Molette, C., Donato, T., Paroli, M., Mondelli, M. U., Doria, M., Torrisi, M. R., & Barnaba, V. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20051106 · Cited by 219 · see citing works
Phagocyte NADPH oxidase: a multicomponent enzyme essential for host defenses.
Benna, J. E., Dang, P. M., Gougerot‐Pocidalo, M., & Elbim, C. (2005) · PubMed · Cited by 212 · see citing works
Determinants of the Phagosomal pH in Neutrophils
Jankowski, A. W., Scott, C. C., & Grinstein, S. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m110059200 · Cited by 181 · see citing works
Regulation of Phagosomal Acidification
Hackam, D. J., Rotstein, O. D., Zhang, W.-J., Demaurex, N., Woodside, M. J., Tsai, O., & Grinstein, S. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.47.29810 · Cited by 161 · see citing works
Inflammatory Manifestations in Chronic Granulomatous Disease (CGD)
Rosenzweig, S. D. (2008) · Journal of Clinical Immunology · doi:10.1007/s10875-007-9160-5 · Cited by 130 · see citing works
Self-citationToll Receptor-Mediated Regulation of NADPH Oxidase in Human Dendritic Cells
Vulcano, M., Dusi, S., Lissandrini, D., Badolato, R., Mazzi, P., Riboldi, E., Borroni, E. M., Calleri, A., Donini, M., Plebani, A., et al. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.9.5749 · Cited by 124 · see citing works
Vascotto, F., Lankar, D., Faure-André, G., Vargas, P., Diaz, J., Roux, D. L., Yuseff, M.-I., Sibarita, J., Boes, M. L., Raposo, G., et al. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200611147 · Cited by 115 · see citing works
van de Loo, F. A. J., Bennink, M. B., Arntz, O. J., Smeets, R. L., Lubberts, E., Joosten, L. A. B., van Lent, P. L. E. M., Roo, C. J. J. C., Cuzzocrea, S., Segal, B. H., et al. (2003) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)63509-2 · Cited by 95 · see citing works
Chronic Granulomatous Disease and Other Disorders of Phagocyte Function
Dinauer, M. C. (2005) · Hematology · doi:10.1182/asheducation-2005.1.89 · Cited by 94 · see citing works
Steinberg, B. E., Touret, N., Vargas‐Caballero, M., & Grinstein, S. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0700783104 · Cited by 84 · see citing works
Sanford, A. N., Suriano, A. R., Herche, D., Dietzmann, K., & Sullivan, K. E. (2005) · Lara D. Veeken · doi:10.1093/rheumatology/kei135 · Cited by 68 · see citing works
Donini, M., Zenaro, E., Tamassia, N., & Dusi, S. (2007) · European Journal of Immunology · doi:10.1002/eji.200636532 · Cited by 55 · see citing works
Dufour, E., Carcelain, G., Gaudin, C., Flament, C., Avril, M.-F., & Faure, F. (1997) · The Journal of Immunology · doi:10.4049/jimmunol.158.8.3787 · Cited by 48 · see citing works
Self-citationHultqvist, M. H., & Holmdahl, R. (2005) · Cellular Immunology · doi:10.1016/j.cellimm.2005.04.008 · Cited by 45 · see citing works
T Cell-Dependent Activation of Dendritic Cells Requires IL-12 and IFN-γ Signaling in T Cells
Miró‐Mur, F., Nobile, C., Blanchard, N., Lind, M., Filipe‐Santos, O., Fieschi, C., Chapgier, A. L. A., Vogt, G., de Beaucoudrey, L., Kumararatne, D. S., et al. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.6.3625 · Cited by 42 · see citing works
Self-citationChronic Granulomatous Disease Associated with Atypical Kawasaki Disease
Yamazaki‐Nakashimada, M. A., Ramírez-Vargas, N. G., & Rubens-Figueroa, J. D. (2007) · Pediatric Cardiology · doi:10.1007/s00246-007-9011-4 · Cited by 19 · see citing works
["Pseudo-lupus" eruptions in a mother carrying X chromosome-linked chronic septic granulomatosis].
Cuny, J.-F., Chauvel, F., Schmutz, J. ‐., Bordigoni, P., Weber, M., & Beurey, J. (1990) · PubMed · Cited by 10 · see citing works
Destructive T cells lured by lipids
Epps, H. L. V. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem2021iti2 · Cited by 5 · see citing works
More mature and more promiscuous
Epps, H. L. V. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem2021iti1 · Cited by 2 · see citing works
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Cross-presentation by dendritic cells
Joffre, O. P., Segura, É., Savina, A., & Amigorena, S. (2012) · Nature reviews. Immunology · doi:10.1038/nri3254 · Cited by 1,646 · see citing works
Self-citationReactive oxygen species and mitochondria: A nexus of cellular homeostasis
Dunn, J. D., Álvarez, L., Zhang, X., & Soldati, T. (2015) · Redox Biology · doi:10.1016/j.redox.2015.09.005 · Cited by 1,199 · see citing works
The Cell Biology of Phagocytosis
Flannagan, R. S., Jaumouillé, V., & Grinstein, S. (2011) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-011811-132445 · Cited by 1,018 · see citing works
Redox regulation of the immune response
Morris, G., Gevezova, M., Sarafian, V. S., & Maes, M. H. J. (2022) · Cellular and Molecular Immunology · doi:10.1038/s41423-022-00902-0 · Cited by 600 · see citing works
Are Reactive Oxygen Species Always Detrimental to Pathogens?
Paiva, C. N., & Bozza, M. T. (2013) · Antioxidants and Redox Signaling · doi:10.1089/ars.2013.5447 · Cited by 559 · see citing works
Activation of antibacterial autophagy by NADPH oxidases
Huang, J., Canadien, V., Lam, G. Y., Steinberg, B. E., Dinauer, M. C., Magalhaes, M. A. O., Glogauer, M., Grinstein, S., & Brumell, J. H. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811045106 · Cited by 556 · see citing works
Reactive Oxygen Species in the Immune System
Yang, Y., Bazhin, A. V., Werner, J., & Karakhanova, S. (2013) · International Reviews of Immunology · doi:10.3109/08830185.2012.755176 · Cited by 508 · see citing works
Current Concepts of Antigen Cross-Presentation
Embgenbroich, M., & Burgdorf, S. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01643 · Cited by 403 · see citing works
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Pidwill, G. R., Gibson, J. F., Cole, J., Renshaw, S. A., & Foster, S. J. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.620339 · Cited by 341 · see citing works
Superoxide Anion Chemistry—Its Role at the Core of the Innate Immunity
Andrés, C. M. C., Pérez de la Lastra, J. M., Andrés Juan, C., Plou, F. J., & Pérez-Lebeña, E. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24031841 · Cited by 342 · see citing works
Reactive Oxygen Species Regulate T Cell Immune Response in the Tumor Microenvironment
Chen, X., Song, M., Zhang, B., & Zhang, Y. (2016) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2016/1580967 · Cited by 326 · see citing works
The life cycle of phagosomes: formation, maturation, and resolution
Levin‐Konigsberg, R., Grinstein, S., & Canton, J. (2016) · Immunological Reviews · doi:10.1111/imr.12439 · Cited by 307 · see citing works
Xu, M. M., Yang, P., Han, D., Shi, Y., Cao, X., Liang, H. L., Chen, X., Li, X.-D., Deng, L., Chen, Z. J., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.07.016 · Cited by 315 · see citing works
Savina, A., Peres, A., Cebrián, I., Carmo, N., Moita, C. F., Hacohen, N., Moita, L. F., & Amigorena, S. (2009) · Immunity · doi:10.1016/j.immuni.2009.01.013 · Cited by 306 · see citing works
Self-citationThe Biology and Underlying Mechanisms of Cross-Presentation of Exogenous Antigens on MHC-I Molecules
Cruz, F. M., Colbert, J. D., Merino, E., Kriegsman, B. A., & Rock, K. L. (2017) · Annual Review of Immunology · doi:10.1146/annurev-immunol-041015-055254 · Cited by 302 · see citing works
Oxidative Stress in the Tumor Microenvironment and Its Relevance to Cancer Immunotherapy
Aboelella, N. S., Brandle, C., Kim, T., Ding, Z., & Zhou, G. (2021) · Cancers · doi:10.3390/cancers13050986 · Cited by 295 · see citing works
Segura, É., Durand, M., & Amigorena, S. (2013) · The Journal of Experimental Medicine · doi:10.1084/jem.20121103 · Cited by 287 · see citing works
Self-citationNanoparticle Drug Delivery Systems Designed to Improve Cancer Vaccines and Immunotherapy
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Acid Resistance inMycobacterium tuberculosis
Vandal, O. H., Nathan, C., & Ehrt, S. (2009) · Journal of Bacteriology · doi:10.1128/jb.00305-09 · Cited by 261 · see citing works
Presentation of Phagocytosed Antigens by MHC Class I and II
Mantegazza, A. R., Magalhaes, J. G., Amigorena, S., & Marks, M. S. (2012) · Traffic · doi:10.1111/tra.12026 · Cited by 254 · see citing works
Self-citationAntigen Cross-Presentation by Macrophages
Muntjewerff, E. M., Meesters, L. D., & van den Bogaart, G. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01276 · Cited by 262 · see citing works
Induction of regulatory T cells by macrophages is dependent on production of reactive oxygen species
Kraaij, M. D., Savage, N. D. L., van der Kooij, S. W., Koekkoek, K. M., Wang, J., van den Berg, J. M., Ottenhoff, T. H. M., Kuijpers, T. W., Holmdahl, R., van Kooten, C., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1012016107 · Cited by 253 · see citing works
Intracellular mechanisms of antigen cross presentation in dendritic cells
Amigorena, S., & Savina, A. (2010) · Current Opinion in Immunology · doi:10.1016/j.coi.2010.01.022 · Cited by 246 · see citing works
Self-citationThe many roles of NOX2 NADPH oxidase-derived ROS in immunity
Lam, G. Y., Huang, J., & Brumell, J. H. (2010) · Seminars in Immunopathology · doi:10.1007/s00281-010-0221-0 · Cited by 243 · see citing works
Ulfig, A., & Leichert, L. I. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03591-y · Cited by 239 · see citing works
The protective role of ROS in autoimmune disease
Hultqvist, M. H., Olsson, L. M., Gelderman, K. A., & Holmdahl, R. (2009) · Trends in Immunology · doi:10.1016/j.it.2009.03.004 · Cited by 224 · see citing works
Contrasting phagosome pH regulation and Maturation in Human M1 and M2 macrophages
Canton, J., Khezri, R., Glogauer, M., & Grinstein, S. (2014) · Molecular Biology of the Cell · doi:10.1091/mbc.e14-05-0967 · Cited by 221 · see citing works
The Influence of Gut Microbiota on Oxidative Stress and the Immune System
Kunst, C., Schmid, S. A., Michalski, M., Tümen, D., Buttenschoen, J., Müller, M., & Gülow, K. (2023) · Biomedicines · doi:10.3390/biomedicines11051388 · Cited by 223 · see citing works
NOX2-dependent regulation of inflammation
Singel, K. L., & Segal, B. H. (2016) · Clinical Science · doi:10.1042/cs20150660 · Cited by 214 · see citing works
Sokolovska, A., Becker, C., Ip, W., Rathinam, V. A. K., Brudner, M., Paquette, N., Tanne, A. J., Vanaja, S. K., Moore, K. J., Fitzgerald, K. A., et al. (2013) · Nature Immunology · doi:10.1038/ni.2595 · Cited by 205 · see citing works
Regulation of the NADPH Oxidase and Associated Ion Fluxes During Phagocytosis
Nunes, P., Demaurex, N., & Dinauer, M. C. (2013) · Traffic · doi:10.1111/tra.12115 · Cited by 204 · see citing works
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Cohn, L. B., Chatterjee, B., Esselborn, F., Smed‐Sörensen, A., Nakamura, N., Chalouni, C. M., Lee, B.-C., Vandlen, R. A., Keler, T., Lauer, P., et al. (2013) · The Journal of Experimental Medicine · doi:10.1084/jem.20121251 · Cited by 200 · see citing works
Antigen processing and presentation
(2019) · International Review of Cell and Molecular Biology · doi:10.1016/bs.ircmb.2019.07.005 · Cited by 194 · see citing works
Regulation of the Cell Biology of Antigen Cross-Presentation
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V-ATPase is a universal regulator of LC3-associated phagocytosis and non-canonical autophagy
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Alloatti, A., Kotsias, F., Pauwels, A.-M., Carpier, J.-M., Jouve, M. J., Timmerman, E., Pace, L., Vargas, P., Maurin, M., Gehrmann, U., et al. (2015) · Immunity · doi:10.1016/j.immuni.2015.11.006 · Cited by 189 · see citing works
Self-citationJacob, C. O., Eisenstein, M., Dinauer, M. C., Ming, W., Liu, Q., John, S. K., Quismorio, F. P., Reiff, A. O., Myones, B. L., Kaufman, K. M., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113251108 · Cited by 184 · see citing works
Targeting dendritic cells: a promising strategy to improve vaccine effectiveness
Macri, C., Dumont, C., Johnston, A. P. R., & Mintern, J. D. (2016) · Clinical & Translational Immunology · doi:10.1038/cti.2016.6 · Cited by 181 · see citing works
Durgan, J., & Florey, O. (2022) · Science Advances · doi:10.1126/sciadv.abo1274 · Cited by 176 · see citing works
Cross-presentation of cell-associated antigens by MHC class I in dendritic cell subsets
Gutiérrez-Martínez, E. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00363 · Cited by 177 · see citing works
The role of NADPH oxidases in infectious and inflammatory diseases
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Wheeler, M. L., & DeFranco, A. L. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1201433 · Cited by 171 · see citing works
Roles of reactive oxygen species in inflammation and cancer
Yu, Y., Liu, S., Yang, L., Song, P., Liu, Z., Liu, X., Yan, X., & Dong, Q. (2024) · MedComm · doi:10.1002/mco2.519 · Cited by 170 · see citing works
Leishmania promastigotes: building a safe niche within macrophages
Moradin, N., & Descoteaux, A. (2012) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2012.00121 · Cited by 157 · see citing works
Lipid peroxidation causes endosomal antigen release for cross-presentation
Dingjan, I., Verboogen, D. R. J., Paardekooper, L. M., Revelo, N. H., Sittig, S. P., Visser, L. J., von Mollard, G. F., Henriet, S., Figdor, C. G., ter Beest, M., et al. (2016) · Scientific Reports · doi:10.1038/srep22064 · Cited by 153 · see citing works
Reactive Oxygen Species and Antitumor Immunity—From Surveillance to Evasion
Kotsafti, A., Scarpa, M., Castagliuolo, I., & Scarpa, M. (2020) · Cancers · doi:10.3390/cancers12071748 · Cited by 157 · see citing works
Rybicka, J. M., Balce, D. R., Khan, M. F., Krohn, R. M., & Yates, R. M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914867107 · Cited by 153 · see citing works
Dendritic Cell-Based Vaccines: Barriers and Opportunities
Cintolo, J. A., Datta, J., Mathew, S., & Czerniecki, B. J. (2012) · Future Oncology · doi:10.2217/fon.12.125 · Cited by 153 · see citing works
Spadaro, F., Lapenta, C., Donati, S., Abalsamo, L., Barnaba, V., Belardelli, F., Santini, S. M., & Ferrantini, M. (2011) · Blood · doi:10.1182/blood-2011-06-363564 · Cited by 150 · see citing works
Phagosomal proteolysis in dendritic cells is modulated by NADPH oxidase in a pH‐independent manner
Rybicka, J. M., Balce, D. R., Chaudhuri, S., Allan, E. R. O., & Yates, R. M. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.440 · Cited by 141 · see citing works
Santos, C. X. C., Nabeebaccus, A., Shah, A. M., Camargo, L. L., Filho, S. V., & Lopes, L. R. (2013) · Antioxidants and Redox Signaling · doi:10.1089/ars.2013.5262 · Cited by 140 · see citing works
Kotsias, F., Hoffmann, E., Amigorena, S., & Savina, A. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.4557 · Cited by 139 · see citing works
Self-citationPrecise modulation and use of reactive oxygen species for immunotherapy
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Freeman, S. A., Grinstein, S., & Orlowski, J. (2022) · Physiological Reviews · doi:10.1152/physrev.00009.2022 · Cited by 127 · see citing works
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Baker, K., Räth, T., Pyzik, M., & Blumberg, R. S. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00408 · Cited by 123 · see citing works
Cross-Presentation in Mouse and Human Dendritic Cells
Segura, É., & Amigorena, S. (2015) · Advances in immunology · doi:10.1016/bs.ai.2015.03.002 · Cited by 117 · see citing works
Self-citationDAMPs and inflammatory processes: the role of redox in the different outcomes
Carta, S., Castellani, P., Delfino, L., Tassi, S., Venè, R., & Rubartelli, A. (2009) · Journal of Leukocyte Biology · doi:10.1189/jlb.1008598 · Cited by 112 · see citing works
Pizzolla, A., Hultqvist, M., Nilson, B., Grimm, M. J., Eneljung, T., Jonsson, I.-M., Verdrengh, M., Kelkka, T., Gjertsson, I., Segal, B. H., et al. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1103430 · Cited by 108 · see citing works
Targeting the C-type Lectins-Mediated Host-Pathogen Interactions with Dextran
Pustylnikov, S., Sagar, D., Jain, P., & Khan, Z. K. (2014) · Journal of Pharmacy & Pharmaceutical Sciences · doi:10.18433/j3n590 · Cited by 105 · see citing works
Hydroxychloroquine inhibits proinflammatory signalling pathways by targeting endosomal NADPH oxidase
Müller‐Calleja, N., Manukyan, D., Canisius, A., Strand, D. J., & Lackner, K. J. (2016) · Annals of the Rheumatic Diseases · doi:10.1136/annrheumdis-2016-210012 · Cited by 107 · see citing works
Lysosome remodelling and adaptation during phagocyte activation
Hipolito, V. E. B., Escobar, E. O., & Botelho, R. J. (2018) · Cellular Microbiology · doi:10.1111/cmi.12824 · Cited by 98 · see citing works
Mycobacteria and the Intraphagosomal Environment: Take It With a Pinch of Salt(s)!
Soldati, T., & Neyrolles, O. (2012) · Traffic · doi:10.1111/j.1600-0854.2012.01358.x · Cited by 106 · see citing works
Metabolic adaptation supports enhanced macrophage efferocytosis in limited-oxygen environments
Wang, Y., Trzeciak, A. J., Rojas, W. S., Saavedra, P. H. V., Chen, Y., Chirayil, R., Etchegaray, J. I., Lucas, C. D., Puleston, D. J., Keshari, K. R., et al. (2022) · Cell Metabolism · doi:10.1016/j.cmet.2022.12.005 · Cited by 107 · see citing works
Phagosome maturation in polarized macrophages
Canton, J. (2014) · Journal of Leukocyte Biology · doi:10.1189/jlb.1mr0114-021r · Cited by 100 · see citing works
Allan, E. R. O., Tailor, P., Balce, D. R., Pirzadeh, P., McKenna, N. T., Renaux, B., Warren, A. L., Jirik, F. R., & Yates, R. M. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1302896 · Cited by 95 · see citing works
MHC molecules and microbial antigen processing in phagosomes
Ramachandra, L., Simmons, D. P., & Harding, C. V. (2009) · Current Opinion in Immunology · doi:10.1016/j.coi.2009.01.001 · Cited by 95 · see citing works
The Plasma Membrane: A Platform for Intra- and Intercellular Redox Signaling
Nordzieke, D. E., & Medraño-Fernandez, I. (2018) · Antioxidants · doi:10.3390/antiox7110168 · Cited by 90 · see citing works
Staphylococcus aureus, phagocyte NADPH oxidase and chronic granulomatous disease
Buvelot, H., Posfay-Barbe, K. M., Linder, P., Schrenzel, J., & Krause, K. (2016) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuw042 · Cited by 88 · see citing works
Segovia, M., Louvet, C., Charnet, P., Savina, A., Tilly, G., Gautreau‐Rolland, L., Carretero-Iglesia, L., Bériou, G., Cebrián, I., Cens, T., et al. (2014) · American Journal of Transplantation · doi:10.1111/ajt.12708 · Cited by 88 · see citing works
Self-citationOxygen in the tumor microenvironment: effects on dendritic cell function
Paardekooper, L. M., de Vos, W., & van den Bogaart, G. (2019) · Oncotarget · doi:10.18632/oncotarget.26608 · Cited by 87 · see citing works
Phagocyte NADPH oxidase and specific immunity
Cachat, J., Deffert, C., Hugues, S., & Krause, K. (2015) · Clinical Science · doi:10.1042/cs20140635 · Cited by 85 · see citing works
Gengenbacher, M., Nieuwenhuizen, N. E., Vogelzang, A., Liu, H., Kaiser, P., Schuerer, S., Lazar, D., Wagner, I., Mollenkopf, H., & Kaufmann, S. H. E. (2016) · mBio · doi:10.1128/mbio.00679-16 · Cited by 84 · see citing works
Mantegazza, A. R., Guttentag, S. H., Benna, J. E., Sasai, M., Iwasaki, A., Shen, H., Laufer, T. M., & Marks, M. S. (2012) · Immunity · doi:10.1016/j.immuni.2012.02.018 · Cited by 81 · see citing works
Self-citationNADPH oxidase activation regulates apoptotic neutrophil clearance by murine macrophages
Bagaitkar, J., Huang, J., Zeng, M. Y., Pech, N. K., Monlish, D. A., Perez‐Zapata, L. J., Miralda, I., Schuettpelz, L. G., & Dinauer, M. C. (2018) · Blood · doi:10.1182/blood-2017-09-809004 · Cited by 82 · see citing works
Mechanisms by Which Dendritic Cells Present Tumor Microparticle Antigens to CD8+ T Cells
Ma, J., Wei, K., Zhang, H., Tang, K., Li, F., Zhang, T., Liu, J., Xu, P., Yu, Y., Sun, W., et al. (2018) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-17-0716 · Cited by 78 · see citing works
Quantum Sensing of Free Radicals in Primary Human Dendritic Cells
Nie, L., Nusantara, A. C., Damle, V. G., Baranov, M. V., Chipaux, M., Reyes-San-Martin, C., Hamoh, T., Epperla, C. P., Guricova, M., Cígler, P., et al. (2021) · Nano Letters · doi:10.1021/acs.nanolett.1c03021 · Cited by 78 · see citing works
Luca, A. D., Iannitti, R. G., Bozza, S., Beau, R., Casagrande, A., D’Angelo, C., Moretti, S., Cunha, C., Giovannini, G., Massi-Benedetti, C., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci60862 · Cited by 77 · see citing works
Reactive oxygen species in immune cells: A new antitumor target
Wang, L., Kuang, Z., Zhang, D., Gao, Y., Ying, M., & Wang, T. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110978 · Cited by 78 · see citing works
Sarantis, H., & Gray‐Owen, S. D. (2011) · Infection and Immunity · doi:10.1128/iai.05702-11 · Cited by 74 · see citing works
Naqvi, A. R., Fordham, J. B., Ganesh, B. B., & Nares, S. (2016) · Scientific Reports · doi:10.1038/srep32925 · Cited by 77 · see citing works
Spel, L., Boelens, J. J., Nierkens, S., & Boes, M. L. (2013) · OncoImmunology · doi:10.4161/onci.26403 · Cited by 74 · see citing works
A Modular and Combinatorial View of the Antigen Cross‐Presentation Pathway in Dendritic Cells
Segura, É., & Villadangos, J. A. (2011) · Traffic · doi:10.1111/j.1600-0854.2011.01254.x · Cited by 73 · see citing works
Human Intestinal Mononuclear Phagocytes in Health and Inflammatory Bowel Disease
Caër, C., & Wick, M. J. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00410 · Cited by 73 · see citing works
Antigen Presentation in the Lung
Kawasaki, T., Ikegawa, M., & Kawai, T. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.860915 · Cited by 73 · see citing works
Inflammatory consequences of inherited disorders affecting neutrophil function
Dinauer, M. C. (2019) · Blood · doi:10.1182/blood-2018-11-844563 · Cited by 69 · see citing works
Meinderts, S. M., Baker, G., van Wijk, S. W., Beuger, B. M., Geissler, J., Jansen, M. H., Saris, A., ten Brinke, A., Kuijpers, T. W., van den Berg, T. K., et al. (2019) · Blood Advances · doi:10.1182/bloodadvances.2018028753 · Cited by 68 · see citing works
Li, L.-S., Yang, L., Zhuang, L., Ye, Z.-Y., Zhao, W.-G., & Gong, W. (2023) · Military Medical Research · doi:10.1186/s40779-023-00490-8 · Cited by 77 · see citing works
Paardekooper, L. M., Dingjan, I., Linders, P. T. A., Staal, A. H. J., Cristescu, S. M., Verberk, W. C. E. P., & van den Bogaart, G. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01216 · Cited by 69 · see citing works
de Geus, E. D., Jansen, C. A., & Vervelde, L. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1200092 · Cited by 68 · see citing works
Perforin-2 is a pore-forming effector of endocytic escape in cross-presenting dendritic cells
Rodríguez-Silvestre, P., Laub, M., Krawczyk, P. A., Davies, A. K., Schessner, J. P., Parveen, R., Tuck, B. J., McEwan, W. A., Borner, G. H. H., & Kozik, P. (2023) · Science · doi:10.1126/science.adg8802 · Cited by 67 · see citing works
Redox signaling in innate immunity and inflammation: focus on macrophages and neutrophils
Braunstein, I., Motohashi, H., Dallenga, T. K., Schaible, U. E., & Benhar, M. (2025) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2025.06.006 · Cited by 72 · see citing works
Pathways of MHC I cross-presentation of exogenous antigens
Cruz, F. M., Chan, A., & Rock, K. L. (2023) · Seminars in Immunology · doi:10.1016/j.smim.2023.101729 · Cited by 66 · see citing works
Protein Disulfide Isomerase and Host-Pathogen Interaction
Stolf, B. S., Smyrnias, I., Lopes, L. R., Gatti, A. V., Goto, H., Laurindo, F. R. M., Shah, A. M., & Santos, C. X. C. (2011) · The Scientific World JOURNAL · doi:10.1100/2011/289182 · Cited by 66 · see citing works
- Authors
- Mantegazza, A. R., Savina, A., Vermeulen, M., Pérez, L., Geffner, J., Hermine, O., Rosenzweig, S. D., Faure, F., & Amigorena, S.
- Affiliations
- Inserm (FR)
- Instituto de Investigaciones Hematológicas, Academia Nacional de Medicina, Buenos Aires, Argentina;
- Garrahan Hospital (AR)
- Academia Nacional de Medicina (AR)
- Hôpital Necker-Enfants Malades (FR)
- ORCID
- Venue
- Blood
- Publisher
- American Society of Hematology
- Published
- 2008-12-01
- Volume
- 112
- Issue
- 12
- Pages
- 4712-4722
- ISSN
- 0006-4971 (ISSN-L)
- 1528-0020
- PMC
- PMC2597138
- OpenAlex
- W2093168274
- Cited by
- 329
- References
- 34
- Citations by year
- 2026: 14 · 2025: 16 · 2024: 17 · 2023: 26 · 2022: 23 · 2021: 22 · 2020: 28 · 2019: 17 · 2018: 22 · 2017: 18 · 2016: 15 · 2015: 18 · 2014: 8 · 2013: 15 · 2012: 28
- FWCI
- 5.84
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Blood (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- CONICET Digital (CONICET) (submittedVersion, cc-by-nc-sa)
- Funders
- Institut National de la Santé et de la Recherche Médicale
- Consejo Nacional de Investigaciones Científicas y Técnicas
- National Institutes of Health
- Directorate for Biological Sciences
- Fogarty International Center (R01TW006644)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Keywords
- NADPH oxidase, NOX2, dendritic cells, phagosomal pH, cross-presentation, reactive oxygen species, gp91phox, vacuolar ATPase, chronic granulomatous disease, monocyte-derived macrophages, endosomal pH, innate immunity
- MeSH terms
- NADPH Oxidase 2, Acid-Base Equilibrium, Adolescent, Adult, Cells, Cultured, Child, Child, Preschool, Dendritic Cells, Humans, Hydrogen-Ion Concentration, Macrophages, Membrane Glycoproteins, Phagosomes, Antigen Presentation, NADPH Oxidases, Cross-Priming, Young Adult
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