Clearance of apoptotic neutrophils and resolution of inflammation

Greenlee‐Wacker, Mallary C.

doi:10.1111/imr.12453

Cited by 478Phagocytosis and Immune RegulationCell death mechanisms and regulationNeutrophil, Myeloperoxidase and Oxidative Mechanisms

Clearance of apoptotic neutrophils and resolution of inflammation

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Greenlee‐Wacker, Mallary C.·2016·Immunological Reviews

DOI 10.1111/imr.12453PMC PMC5000862

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Abstract

Summary: The engulfment of apoptotic cells by phagocytes, a process referred to as efferocytosis, is essential for maintenance of normal tissue homeostasis and a prerequisite for the resolution of inflammation. Neutrophils are the predominant circulating white blood cell in humans, and contain an arsenal of toxic substances that kill and degrade microbes. Neutrophils are short‐lived and spontaneously die by apoptosis. This review will highlight how the engulfment of apoptotic neutrophils by human phagocytes occurs, how heterogeneity of phagocyte populations influences efferocytosis signaling, and downstream consequences of efferocytosis. The efferocytosis of apoptotic neutrophils by macrophages promotes anti‐inflammatory signaling, prevents neutrophil lysis, and dampens immune responses. Given the immunomodulatory properties of efferocytosis, understanding pathways that regulate and enhance efferocytosis could be harnessed to combat infection and chronic inflammatory conditions.

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Mature neutrophils circulate in the bloodstream for 10-24 h before migrating to tissues, where they remain for 1-2 days before undergoing apoptosis and being cleared by macrophages.
“Mature neutrophils are released into the bloodstream, where they circulate for 10–24 h before migrating to tissues, where they remain for the next 1–2 days before undergoing apoptosis and being cleared by macrophages [211].”
From Superoxide Anion Chemistry—Its Role at the Core of the Innate Immunity (2023) · cites this paper as [211]

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Macrophage activation and polarization: nomenclature and experimental guidelines
Murray, P. J., Allen, J. E., Biswas, S. K., Fisher, E. A., Gilroy, D. W., Goerdt, S., Gordon, S., Hamilton, J. A., Ivashkiv, L. B., Lawrence, T., et al. (2014) · Immunity · doi:10.1016/j.immuni.2014.06.008 · Cited by 6,337 · see citing works
Monocyte and macrophage heterogeneity
Gordon, S., & Taylor, P. R. (2005) · Nature Reviews Immunology · doi:10.1038/nri1733 · Cited by 5,190 · see citing works
Cytokine-mediated regulation of CXCR4 expression in human neutrophils
Nagase, H., Miyamasu, M., Yamaguchi, M., Imanishi, M., Tsuno, N. H., Matsushima, K., Yamamoto, K., Morita, Y., & Hirai, K. (2002) · Journal of Leukocyte Biology · doi:10.1189/jlb.71.4.711 · Cited by 4,713 · see citing works
Tissue Destruction by Neutrophils
Epstein, F. H., & Weiss, S. J. (1989) · New England Journal of Medicine · doi:10.1056/nejm198902093200606 · Cited by 3,950 · see citing works
Tissue Destruction by Neutrophils
(1989) · New England Journal of Medicine · doi:10.1056/nejm198908033210513 · Cited by 3,634 · see citing works
Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages
Fadok, V. A., Voelker, D. R., Campbell, P. A., Cohen, J., Bratton, D. L., & Henson, P. M. (1992) · The Journal of Immunology · doi:10.4049/jimmunol.148.7.2207 · Cited by 3,321 · see citing works
Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF.
Fadok, V. A., Bratton, D. L., Konowal, A., Freed, P. W., Westcott, J. Y., & Henson, P. M. (1998) · Journal of Clinical Investigation · doi:10.1172/jci1112 · Cited by 3,166 · see citing works
Macrophage activation and polarization
Martinez, F. O. (2008) · Frontiers in Bioscience · doi:10.2741/2692 · Cited by 3,160 · see citing works
Mechanisms of phagocytosis in macrophages
Aderem, A., & Underhill, D. M. (1999) · Annual Review of Immunology · doi:10.1146/annurev.immunol.17.1.593 · Cited by 2,854 · see citing works
Points of control in inflammation
Nathan, C. (2002) · Nature · doi:10.1038/nature01320 · Cited by 2,738 · see citing works
Apoptosis: controlled demolition at the cellular level
Taylor, R. C., Cullen, S. P., & Martin, S. J. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2312 · Cited by 2,617 · see citing works
Immunosuppressive effects of apoptotic cells
Voll, R. E., Herrmann, M., Roth, E. A., Stach, C., Kalden, J. R., & Girkontaite, I. (1997) · Nature · doi:10.1038/37022 · Cited by 1,787 · see citing works
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
Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages.
Savill, J. S., Wyllie, A. H., Henson, J. E., Walport, M. J., Henson, P. M., & Haslett, C. (1989) · Journal of Clinical Investigation · doi:10.1172/jci113970 · Cited by 1,536 · see citing works
Cell-Surface Calreticulin Initiates Clearance of Viable or Apoptotic Cells through trans-Activation of LRP on the Phagocyte
Gardai, S. J., McPhillips, K. A., Frasch, S. C., Janssen, W. J., Starefeldt, A., Murphy-Ullrich, J. E., Bratton, D. L., Oldenborg, P.-A., Michalak, M., & Henson, P. M. (2005) · Cell · doi:10.1016/j.cell.2005.08.032 · Cited by 1,473 · 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
Consequences of Cell Death
Sauter, B., Albert, M. L., Francisco, L. M., Larsson, M., Somersan, S., & Bhardwaj, N. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.191.3.423 · Cited by 1,357 · see citing works
Immature Dendritic Cells Phagocytose Apoptotic Cells via αvβ5 and CD36, and Cross-present Antigens to Cytotoxic T Lymphocytes
Albert, M. L., Pearce, S. F. A., Francisco, L. M., Sauter, B., Roy, P., Silverstein, R. L., & Bhardwaj, N. (1998) · The Journal of Experimental Medicine · doi:10.1084/jem.188.7.1359 · Cited by 1,234 · see citing works
Phagocytosis and clearance of apoptotic cells is mediated by MER
Scott, R. S., McMahon, E. J., Pop, S. M., Reap, E. A., Caricchio, R., Cohen, P. L., Earp, H. S., & Matsushima, G. K. (2001) · Nature · doi:10.1038/35075603 · Cited by 1,215 · see citing works
The Induction of Tolerance by Dendritic Cells That Have Captured Apoptotic Cells
Steinman, R. M., Turley, S. J., Mellman, I., & Inaba, K. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.191.3.411 · Cited by 1,172 · see citing works
Modulation of granulocyte survival and programmed cell death by cytokines and bacterial products
Colotta, F., Re, F., Polentarutti, N., Sozzani, S., & Mantovani, A. (1992) · Blood · doi:10.1182/blood.v80.8.2012.2012 · Cited by 1,158 · see citing works
C1q and Mannose Binding Lectin Engagement of Cell Surface Calreticulin and Cd91 Initiates Macropinocytosis and Uptake of Apoptotic Cells
Ogden, C. A., deCathelineau, A. M., Hoffmann, P. R., Bratton, D. L., Ghebrehiwet, B., Fadok, V. A., & Henson, P. M. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.194.6.781 · Cited by 1,148 · see citing works
Phagocytosis of Apoptotic Neutrophils Regulates Granulopoiesis via IL-23 and IL-17
Stark, M. A., Huo, Y., Burcin, T. L., MORRIS, M. A., Olson, T. S., & Ley, K. F. (2005) · Immunity · doi:10.1016/j.immuni.2005.01.011 · Cited by 945 · see citing works
Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo
Lämmermann, T., Afonso, P. V., Angermann, B., Wang, J. M., Kastenmüller, W., Parent, C. A., & Germain, R. N. (2013) · Nature · doi:10.1038/nature12175 · Cited by 937 · see citing works
Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis
Savill, J., Dransfield, I., Hogg, N., & Haslett, C. (1990) · Nature · doi:10.1038/343170a0 · Cited by 846 · see citing works
In Vivo Imaging Reveals an Essential Role for Neutrophils in Leishmaniasis Transmitted by Sand Flies
Peters, N. C., Egen, J. G., Secundino, N. F. C., Debrabant, A., Kimblin, N., Kamhawi, S., Lawyer, P. G., Fay, M. P., Germain, R. N., & Sacks, D. L. (2008) · Science · doi:10.1126/science.1159194 · Cited by 837 · see citing works
Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis.
Savill, J., Hogg, N., Ren, Y., & Haslett, C. (1992) · Journal of Clinical Investigation · doi:10.1172/jci116019 · Cited by 813 · see citing works
Complement-dependent Clearance of Apoptotic Cells by Human Macrophages
Mevorach, D., Mascarenhas, J., Gershov, D., & Elkon, K. (1998) · Journal of Experimental Medicine · doi:10.1084/jem.188.12.2313 · Cited by 776 · see citing works
Chemokines Acting via CXCR2 and CXCR4 Control the Release of Neutrophils from the Bone Marrow and Their Return following Senescence
Martin, C., Burdon, P. C. E., Bridger, G. J., Gutierrez-Ramos, J.-C., Williams, T. J., & Rankin, S. M. (2003) · Immunity · doi:10.1016/s1074-7613(03)00263-2 · Cited by 770 · see citing works
Inhibition of apoptosis and prolongation of neutrophil functional longevity by inflammatory mediators
Lee, A., Whyte, M. K. B., & Haslett, C. (1993) · Journal of Leukocyte Biology · doi:10.1002/jlb.54.4.283 · Cited by 714 · see citing works
Homeostatic Regulation of the Immune System by Receptor Tyrosine Kinases of the Tyro 3 Family
Lu, Q., & Lemke, G. (2001) · Science · doi:10.1126/science.1061663 · Cited by 699 · see citing works
Loss of Phospholipid Asymmetry and Surface Exposure of Phosphatidylserine Is Required for Phagocytosis of Apoptotic Cells by Macrophages and Fibroblasts*
Fadok, V., de Cathelineau, A., Daleke, D. L., Henson, P., & Bratton, D. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m003649200 · Cited by 689 · see citing works
Phagocytosis
Stuart, L. M., & Ezekowitz, R. A. B. (2005) · Immunity · doi:10.1016/j.immuni.2005.05.002 · Cited by 667 · see citing works
A family of proteins that inhibit signalling through tyrosine kinase receptors
Kharitonenkov, A., Chen, Z., Sures, I., Wang, H., Schilling, J., & Ullrich, A. (1997) · Nature · doi:10.1038/386181a0 · Cited by 662 · see citing works
Efficient Clearance of Early Apoptotic Cells by Human Macrophages Requires M2c Polarization and MerTK Induction
Zizzo, G., Hilliard, B. A., Monestier, M., & Cohen, P. L. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1200662 · Cited by 650 · see citing works
LEUKOKINETIC STUDIES. IV. THE TOTAL BLOOD, CIRCULATING AND MARGINAL GRANULOCYTE POOLS AND THE GRANULOCYTE TURNOVER RATE IN NORMAL SUBJECTS*
Athens, J. W., Haab, O. P., RAAB, S. O., Mauer, A. M., Ashenbrucker, H., Cartwright, G. E., & Wintrobe, M. M. (1961) · Journal of Clinical Investigation · doi:10.1172/jci104338 · Cited by 639 · see citing works
Cutting Edge: Lipoxins Rapidly Stimulate Nonphlogistic Phagocytosis of Apoptotic Neutrophils by Monocyte-Derived Macrophages
Godson, C., Mitchell, S., Harvey, K., Petasis, N. A., Hogg, N., & Brady, H. R. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.164.4.1663 · Cited by 638 · 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
Different populations of macrophages use either the vitronectin receptor or the phosphatidylserine receptor to recognize and remove apoptotic cells
Fadok, V. A., Savill, J., Haslett, C., Bratton, D. L., Doherty, D. E., Campbell, P. A., & Henson, P. M. (1992) · The Journal of Immunology · doi:10.4049/jimmunol.149.12.4029 · Cited by 596 · see citing works
The resolution code of acute inflammation: Novel pro-resolving lipid mediators in resolution
Serhan, C. N., Chiang, N., & Dalli, J. (2015) · Seminars in Immunology · doi:10.1016/j.smim.2015.03.004 · Cited by 583 · see citing works
Phagocytosis and antigen presentation in dendritic cells
Savina, A., & Amigorena, S. (2007) · Immunological Reviews · doi:10.1111/j.1600-065x.2007.00552.x · Cited by 562 · see citing works
Specific lipid mediator signatures of human phagocytes: microparticles stimulate macrophage efferocytosis and pro-resolving mediators
Dalli, J., & Serhan, C. N. (2012) · Blood · doi:10.1182/blood-2012-04-423525 · Cited by 556 · see citing works
Find-me and eat-me signals in apoptotic cell clearance: progress and conundrums
Ravichandran, K. S. (2010) · The Journal of Experimental Medicine · doi:10.1084/jem.20101157 · Cited by 547 · see citing works
Phosphatidylserine (PS) induces PS receptor–mediated macropinocytosis and promotes clearance of apoptotic cells
Hoffmann, P. R., deCathelineau, A. M., Ogden, C. A., Leverrier, Y., Bratton, D. L., Daleke, D. L., Ridley, A. J., Fadok, V. A., & Henson, P. M. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.200108080 · Cited by 541 · see citing works
Role of Surfactant Proteins A, D, and C1q in the Clearance of Apoptotic Cells In Vivo and In Vitro: Calreticulin and CD91 as a Common Collectin Receptor Complex
Vandivier, R. W., Ogden, C. A., Fadok, V. A., Hoffmann, P. R., Brown, K. K., Botto, M., Walport, M. J., Fisher, J. H., Henson, P. M., & Greene, K. E. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.7.3978 · Cited by 517 · see citing works
Clearing the Dead: Apoptotic Cell Sensing, Recognition, Engulfment, and Digestion
Hochreiter-Hufford, A., & Ravichandran, K. S. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a008748 · Cited by 503 · see citing works
Burying the Dead
Vandivier, R. W., Henson, P. M., & Douglas, I. S. (2006) · CHEST Journal · doi:10.1378/chest.129.6.1673 · Cited by 450 · see citing works
Human neutrophils lose their surface Fc gamma RIII and acquire Annexin V binding sites during apoptosis in vitro
Homburg, C., de Haas, M., Borne, A. E. G. K. V. D., Verhoeven, A. J., Reutelingsperger, C. P. M., & Roos, D. (1995) · Blood · doi:10.1182/blood.v85.2.532.532 · Cited by 431 · see citing works
Molecular definition of distinct cytoskeletal structures involved in complement- and Fc receptor-mediated phagocytosis in macrophages.
Allen, L. H., & Aderem, A. A. (1996) · The Journal of Experimental Medicine · doi:10.1084/jem.184.2.627 · Cited by 431 · see citing works
Cutting Edge: Neutrophil Granulocyte Serves as a Vector for <i>Leishmania</i> Entry into Macrophages
van Zandbergen, G., Klinger, M., Mueller, A., Dannenberg, S., Gebert, A., Solbach, W., & Laskay, T. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.11.6521 · Cited by 430 · see citing works
Oxidized phosphatidylserine–CD36 interactions play an essential role in macrophage-dependent phagocytosis of apoptotic cells
Greenberg, M. E., Sun, M., Zhang, R., Febbraio, M., Silverstein, R., & Hazen, S. L. (2006) · The Journal of Experimental Medicine · doi:10.1084/jem.20060370 · Cited by 430 · see citing works
CD36 is required for phagocytosis of apoptotic cells by human macrophages that use either a phosphatidylserine receptor or the vitronectin receptor (alpha v beta 3).
Fadok, V. A., Warner, M. L., Bratton, D. L., & Henson, P. M. (1998) · PubMed · Cited by 406 · see citing works
Apoptosis disables CD31-mediated cell detachment from phagocytes promoting binding and engulfment
Brown, S., Heinisch, I., Ross, E., Shaw, K., Buckley, C. D., & Savill, J. (2002) · Nature · doi:10.1038/nature00811 · Cited by 390 · see citing works
Differential Effects of Apoptotic Versus Lysed Cells on Macrophage Production of Cytokines: Role of Proteases
Fadok, V. A., Bratton, D. L., Guthrie, L. A., & Henson, P. M. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.11.6847 · Cited by 368 · see citing works
CD36 Is Required for Phagocytosis of Apoptotic Cells by Human Macrophages That Use Either a Phosphatidylserine Receptor or the Vitronectin Receptor (αvβ3)
Fadok, V. A., Warner, M. L., Bratton, D. L., & Henson, P. M. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.161.11.6250 · Cited by 353 · see citing works
Neutrophil apoptosis pathways and their modifications in inflammation
Simon, H. (2003) · Immunological Reviews · doi:10.1034/j.1600-065x.2003.00038.x · Cited by 350 · see citing works
Apoptosis: The importance of being eaten
Ren, Y., & Savill, J. (1998) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400407 · Cited by 347 · see citing works
Modulation of Macrophage Efferocytosis in Inflammation
Johnson, D. K., Frasch, S. C., Fernandez-Boyanapalli, R. F., Henson, P. M., & Bratton, D. L. (2011) · Frontiers in Immunology · doi:10.3389/fimmu.2011.00057 · Cited by 346 · see citing works
Identification of a phenotypically and functionally distinct population of long-lived neutrophils in a model of reverse endothelial migration
Buckley, C. D., Ross, E. A., McGettrick, H. M., Osborne, C., Haworth, O., Schmutz, C., Stone, P. C., Salmon, M., Matharu, N. M., Vohra, R. K., et al. (2005) · Journal of Leukocyte Biology · doi:10.1189/jlb.0905496 · Cited by 340 · see citing works
Bacterial pathogens modulate an apoptosis differentiation program in human neutrophils
Kobayashi, S. D., Braughton, K. R., Whitney, A. R., Voyich, J. M., Schwan, T. G., Musser, J. M., & DeLeo, F. R. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1833375100 · Cited by 336 · see citing works
Neutrophil apoptosis is associated with a reduction in CD16 (Fc gamma RIII) expression.
Dransfield, I., Buckle, A., Savill, J., McDowall, A., Haslett, C., & Hogg, N. (1994) · The Journal of Immunology · doi:10.4049/jimmunol.153.3.1254 · Cited by 329 · see citing works
Phagocytosis of senescent neutrophils by human monocyte-derived macrophages and rabbit inflammatory macrophages.
Newman, S. L., Henson, J. E., & Henson, P. M. (1982) · The Journal of Experimental Medicine · doi:10.1084/jem.156.2.430 · Cited by 321 · see citing works
Are bloodstream leukocytes Trojan Horses for the metastasis of Staphylococcus aureus?
Thwaites, G. E., & Gant, V. A. (2011) · Nature Reviews Microbiology · doi:10.1038/nrmicro2508 · Cited by 319 · see citing works
Peculiarities of cell death mechanisms in neutrophils
Geering, B., & Simon, H.-U. (2011) · Cell Death and Differentiation · doi:10.1038/cdd.2011.75 · Cited by 301 · see citing works
What's your age again? Determination of human neutrophil half-lives revisited
Tak, T., Tesselaar, K., Pillay, J., Borghans, J. A. M., & Koenderman, L. (2013) · Journal of Leukocyte Biology · doi:10.1189/jlb.1112571 · Cited by 294 · see citing works
Homeostatic Regulation of Blood Neutrophil Counts
von Vietinghoff, S., & Ley, K. F. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.8.5183 · Cited by 293 · see citing works
Regulation of Human Neutrophil Apoptosis and Lifespan in Health and Disease
McCracken, J., & Allen, L. H. (2014) · Journal of Cell Death · doi:10.4137/jcd.s11038 · Cited by 292 · see citing works
Phagocytosis of aged human neutrophils by macrophages is mediated by a novel "charge-sensitive" recognition mechanism.
Savill, J., Henson, P. M., & Haslett, C. (1989) · Journal of Clinical Investigation · doi:10.1172/jci114328 · Cited by 291 · see citing works
Annexin-1 and Peptide Derivatives Are Released by Apoptotic Cells and Stimulate Phagocytosis of Apoptotic Neutrophils by Macrophages
Scannell, M., Flanagan, M. B., deStefani, A., Wynne, K. J., Cagney, G., Godson, C., & MADERNA, P. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.7.4595 · Cited by 282 · see citing works
The final step in programmed cell death: phagocytes carry apoptotic cells to the grave
deCathelineau, A. M., & Henson, P. M. (2003) · Essays in Biochemistry · doi:10.1042/bse0390105 · Cited by 282 · see citing works
Regulation of Interleukin-12 by Complement Receptor 3 Signaling
Marth, T., & Kelsall, B. L. (1997) · The Journal of Experimental Medicine · doi:10.1084/jem.185.11.1987 · Cited by 281 · see citing works
Phagocytosis of apoptotic neutrophils does not induce macrophage release of thromboxane B2
MEAGHER, L. C., Savill, J., Baker, A. J., Fuller, R. W., & Haslett, C. (1992) · Journal of Leukocyte Biology · doi:10.1002/jlb.52.3.269 · Cited by 280 · see citing works
Indium-111-labeled leukocytes for the localization of abscesses: preparation, analysis, tissue distribution, and comparison with gallium-67 citrate in dogs.
Thakur, M. L., Coleman, R. E., & Mj, W. (1977) · PubMed · Cited by 274 · see citing works
Azithromycin Improves Macrophage Phagocytic Function and Expression of Mannose Receptor in Chronic Obstructive Pulmonary Disease
Hodge, S. J., Hodge, G. L., Jersmann, H. P. A., Matthews, G. M., Ahern, J., Holmes, M., & Reynolds, P. N. (2008) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200711-1666oc · Cited by 258 · see citing works
Calreticulin Functions as a Molecular Chaperone in the Biosynthesis of Myeloperoxidase
Nauseef, W. M., McCormick, S. J., & Clark, R. A. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.9.4741 · Cited by 255 · see citing works
Human monocyte-derived macrophage phagocytosis of senescent eosinophils undergoing apoptosis. Mediation by alpha v beta 3/CD36/thrombospondin recognition mechanism and lack of phlogistic response.
Stern, M., Savill, J., & Haslett, C. (1996) · Europe PMC (PubMed Central) · Cited by 239 · see citing works
Receptor Tyrosine Kinases, TYRO3, AXL, and MER, Demonstrate Distinct Patterns and Complex Regulation of Ligand-induced Activation
Tsou, W., Nguyen, K.-Q. N., Calarese, D. A., Garforth, S., Lewis-Antes, A., Sv, S., Almo, S. C., Birge, R. B., & Kotenko, S. V. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.569020 · Cited by 237 · see citing works
Saturated‐efferocytosis generates pro‐resolving CD11b low macrophages: Modulation by resolvins and glucocorticoids
Schif‐Zuck, S., Gross, N., Assi, S., Rostoker, R., Serhan, C. N., & Ariel, A. (2010) · European Journal of Immunology · doi:10.1002/eji.201040801 · Cited by 236 · see citing works
Lipopolysaccharide Induces Rapid Production of IL-10 by Monocytes in the Presence of Apoptotic Neutrophils
Byrne, A. M., & Reen, D. J. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.168.4.1968 · Cited by 228 · see citing works
Macrophage phagocytosis of apoptotic neutrophils is critically regulated by the opposing actions of pro‐inflammatory and anti‐inflammatory agents: key role for TNF‐α
Michlewska, S., Dransfield, I., Megson, I. L., & Rossi, A. G. (2008) · The FASEB Journal · doi:10.1096/fj.08-121228 · Cited by 228 · see citing works
Macrolide antibiotics as immunomodulatory medications: Proposed mechanisms of action
Shinkai, M., Henke, M. O., & Rubin, B. K. (2008) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2007.11.001 · Cited by 228 · see citing works
Global changes in gene expression by human polymorphonuclear leukocytes during receptor-mediated phagocytosis: Cell fate is regulated at the level of gene expression
Kobayashi, S. D., Voyich, J. M., Buhl, C. L., Stahl, R. M., & DeLeo, F. R. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.092148299 · Cited by 225 · see citing works
Guidelines on the use of extracorporeal photopheresis
Knobler, R., Berlin, G., Calzavara‐Pinton, P., Greinix, H., Jaksch, P., Laroche, L., Ludvigsson, J., Quaglino, P., Reinisch, W., Scarisbrick, J. J., et al. (2013) · Journal of the European Academy of Dermatology and Venereology · doi:10.1111/jdv.12311 · Cited by 219 · see citing works
Lovastatin Enhances Clearance of Apoptotic Cells (Efferocytosis) with Implications for Chronic Obstructive Pulmonary Disease
Morimoto, K., Janssen, W. J., Fessler, M. B., McPhillips, K. A., Borges, V. M., Bowler, R. P., Xiao, Y., Kench, J. A., Henson, P. M., & Vandivier, R. W. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.12.7657 · Cited by 215 · see citing works
Apoptotic neutrophils are phagocytosed by fibroblasts with participation of the fibroblast vitronectin receptor and involvement of a mannose/fucose-specific lectin.
Hall, S. E., Savill, J., Henson, P. M., & Haslett, C. (1994) · The Journal of Immunology · doi:10.4049/jimmunol.153.7.3218 · Cited by 207 · see citing works
Apoptotic cell recognition receptors and scavenger receptors
Penberthy, K. K., & Ravichandran, K. S. (2015) · Immunological Reviews · doi:10.1111/imr.12376 · Cited by 202 · see citing works
Macrophages use different internalization mechanisms to clear apoptotic and necrotic cells
Krysko, D. V., Denecker, G., Festjens, N., Gabriëls, S., Parthoens, E., D'Herde, K. G. M. A., & Vandenabeele, P. (2006) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401900 · Cited by 197 · see citing works
Heterogeneity in Neutrophil Microparticles Reveals Distinct Proteome and Functional Properties
Dalli, J., Montero‐Melendez, T., Norling, L. V., Yin, X., Hinds, C., Haskard, D. O., Mayr, M., & Perretti, M. (2013) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m113.028589 · Cited by 197 · see citing works
Mycobacterium tuberculosis Inhibits Neutrophil Apoptosis, Leading to Delayed Activation of Naive CD4 T cells
Blomgran, R., Desvignes, L., Briken, V., & Ernst, J. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2011.11.012 · Cited by 193 · see citing works
Modulation of Phagocytosis of Apoptotic Neutrophils by Supernatant from Dexamethasone-Treated Macrophages and Annexin-Derived Peptide Ac2–26
MADERNA, P., Yona, S., Perretti, M., & Godson, C. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.6.3727 · Cited by 190 · see citing works
Human CD300a binds to phosphatidylethanolamine and phosphatidylserine, and modulates the phagocytosis of dead cells
Simhadri, V. R., Andersen, J. F., Calvo, E., Choi, S., Coligan, J. E., & Borrego, F. (2012) · Blood · doi:10.1182/blood-2011-08-372425 · Cited by 189 · see citing works
Macrophage Recognition of ICAM-3 on Apoptotic Leukocytes
Moffatt, O., Devitt, A., Bell, E. D., Simmons, D. L., & Gregory, C. D. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.162.11.6800 · Cited by 185 · see citing works
High Mobility Group Protein-1 Inhibits Phagocytosis of Apoptotic Neutrophils through Binding to Phosphatidylserine
Liu, G., Wang, J., Park, Y.-J., Tsuruta, Y., Lorne, E., Zhao, X., & Abraham, E. H. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.6.4240 · Cited by 185 · see citing works
Phagocytosis of Staphylococcus aureus by Human Neutrophils Prevents Macrophage Efferocytosis and Induces Programmed Necrosis
Greenlee‐Wacker, M. C., Rigby, K. M., Kobayashi, S. D., Porter, A. R., DeLeo, F. R., & Nauseef, W. M. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1302692 · Cited by 185 · see citing works
Self-citation
Role of the liver in regulating numbers of circulating neutrophils
Shi, J., Gilbert, G. E., Kokubo, Y., & Ohashi, T. (2001) · Blood · doi:10.1182/blood.v98.4.1226 · Cited by 178 · see citing works
Macrophages clean up: efferocytosis and microbial control
Martin, C. J., Peters, K. N., & Behar, S. M. (2013) · Current Opinion in Microbiology · doi:10.1016/j.mib.2013.10.007 · Cited by 177 · see citing works
The matricellular protein CCN1 mediates neutrophil efferocytosis in cutaneous wound healing
Jun, J.-I., Kim, K.-H., & Lau, L. F. (2015) · Nature Communications · doi:10.1038/ncomms8386 · Cited by 173 · see citing works
Staphylococcus aureus Panton-Valentine leukocidin induces an inflammatory response in human phagocytes via the NLRP3 inflammasome
Holzinger, D., Gieldon, L., Mysore, V., Nippe, N., Taxman, D. J., Duncan, J. A., Broglie, P. M., Marketon, K., Austermann, J., Vogl, T., et al. (2012) · Journal of Leukocyte Biology · doi:10.1189/jlb.0112014 · Cited by 170 · see citing works
Glucocorticoid Augmentation of Macrophage Capacity for Phagocytosis of Apoptotic Cells Is Associated with Reduced p130Cas Expression, Loss of Paxillin/pyk2 Phosphorylation, and High Levels of Active Rac
Giles, K. M., Ross, K. A., Rossi, A. G., Hotchin, N. A., Haslett, C., & Dransfield, I. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.167.2.976 · Cited by 165 · see citing works
Galectin-3 functions as an opsonin and enhances the macrophage clearance of apoptotic neutrophils
Karlsson, A., Christenson, K., Matlak, M., Björstad, Å., Brown, K. L., Telemo, E., Salomonsson, E., Leffler, H., & Bylund, J. (2008) · Glycobiology · doi:10.1093/glycob/cwn104 · Cited by 163 · see citing works
Efferocytosis impairs pulmonary macrophage and lung antibacterial function via PGE2/EP2 signaling
de Medeiros, A. I., Serezani, C. H., Lee, S. P., & Peters-Golden, M. L. (2009) · The Journal of Experimental Medicine · doi:10.1084/jem.20082058 · Cited by 160 · see citing works
Dying and Necrotic Neutrophils Are Anti-Inflammatory Secondary to the Release of α-Defensins
Miles, K., Clarke, D. J., Lu, W., Sibinska, Z., Beaumont, P. E., Davidson, D. J., Barr, T. A., Campopiano, D. J., & Gray, M. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0804187 · Cited by 160 · see citing works
Complement binding is an early feature of necrotic and a rather late event during apoptotic cell death
Gaipl, U. S., Kuenkele, S., Voll, R. E., Beyer, T. D., Kolowos, W., Heyder, P., Kalden, J. R., & i, M. H. (2001) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400826 · Cited by 159 · see citing works
Regulation of cell adhesion molecule expression and function associated with neutrophil apoptosis
Dransfield, I., Stocks, S. C., & Haslett, C. (1995) · Blood · doi:10.1182/blood.v85.11.3264.bloodjournal85113264 · Cited by 156 · see citing works
Rapid Neutrophil Destruction following Phagocytosis of Staphylococcus aureus
Kobayashi, S. D., Braughton, K. R., Palazzolo‐Ballance, A. M., Kennedy, A. D., Sampaio, E. P., Kristosturyan, E., Whitney, A. R., Sturdevant, D. E., Dorward, D. W., Holland, S. M., et al. (2010) · Journal of Innate Immunity · doi:10.1159/000317134 · Cited by 154 · see citing works
Neutrophil maturation and activation determine anatomic site of clearance from circulation
Suratt, B. T., Young, S. K., Lieber, J. G., et al. (2001) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.2001.281.4.l913 · Cited by 152 · see citing works
Regulation of Macrophage Phagocytosis of Apoptotic Cells by cAMP
Rossi, A. G., McCutcheon, J. C., Roy, N., Chilvers, E. R., Haslett, C., & Dransfield, I. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.160.7.3562 · Cited by 150 · see citing works
Differential regulation of phagosome maturation in macrophages and dendritic cells mediated by Rho GTPases and ezrin–radixin–moesin (ERM) proteins
Erwig, L., McPhillips, K. A., Wynes, M. W., Ívetic, A., Ridley, A. J., & Henson, P. M. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605331103 · Cited by 150 · see citing works
Neutrophil-macrophage cooperation in the host defence against mycobacterial infections
Silva, M. T., Silva, M. N., & Appelberg, R. (1989) · Microbial Pathogenesis · doi:10.1016/0882-4010(89)90079-x · Cited by 148 · see citing works
PPARγ‐dependent regulation of human macrophages in phagocytosis of apoptotic cells
Majai, G. E., Sarang, Z., Csomós, K., Zahuczky, G., & Fésüs, L. (2007) · European Journal of Immunology · doi:10.1002/eji.200636398 · Cited by 146 · see citing works
Molecular characterization of the surface of apoptotic neutrophils: Implications for functional downregulation and recognition by phagocytes
Hart, S. P., Ross, J. A., Ross, K., Haslett, C., & Dransfield, I. (2000) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400680 · Cited by 137 · see citing works
Glucocorticoids Induce Protein S-Dependent Phagocytosis of Apoptotic Neutrophils by Human Macrophages
McColl, A., Bournazos, S., Franz, S., Perretti, M., Morgan, B. P., Haslett, C., & Dransfield, I. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0803503 · Cited by 135 · see citing works
Pathogen-Induced Apoptotic Neutrophils Express Heat Shock Proteins and Elicit Activation of Human Macrophages
Zheng, L., He, M. Y., Long, M., Blomgran, R., & Stendahl, O. I. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.10.6319 · Cited by 130 · see citing works
HMGB1 inhibits macrophage activity in efferocytosis through binding to the αvβ3-integrin
Friggeri, A., Yang, Y., Banerjee, S., Park, Y.-J., Liu, G., & Abraham, E. H. (2010) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00152.2010 · Cited by 128 · see citing works
The kinetics of 111Indium distribution following injection of 111Indium labelled autologous granulocytes in man
Saverymuttu, S. H., Peters, A. M., Keshavarzian, A., Reavy, H. J., & Lavender, J. P. (1985) · British Journal of Haematology · doi:10.1111/j.1365-2141.1985.tb02882.x · Cited by 126 · see citing works
Neutrophils in Barth syndrome (BTHS) avidly bind annexin-V in the absence of apoptosis.
Kuijpers, T., Maianski, N., Tool, A., Becker, K., Plecko, B., Valianpour, F., Wanders, R., Pereira, R., Hove, J. V. V., Verhoeven, A., et al. (2004) · Blood · doi:10.1182/blood-2003-11-3940 · Cited by 117 · see citing works
NADPH Oxidase-dependent Generation of Lysophosphatidylserine Enhances Clearance of Activated and Dying Neutrophils via G2A
Frasch, S. C., Berry, K. A. Z., Fernandez-Boyanapalli, R. F., Jin, H.-S., Leslie, C. C., Henson, P. M., Murphy, R. C., & Bratton, D. L. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m807047200 · Cited by 113 · see citing works
Phospholipid Flip-Flop and Phospholipid Scramblase 1 (PLSCR1) Co-localize to Uropod Rafts in Formylated Met-Leu-Phe-stimulated Neutrophils
Frasch, S. C., Henson, P. M., Nagaosa, K., Fessler, M. B., Borregaard, N., & Bratton, D. L. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m313414200 · Cited by 113 · see citing works
PAI-1 inhibits neutrophil efferocytosis
Park, Y.-J., Liu, G., Lorne, E., Zhao, X., Wang, J., Tsuruta, Y., Zmijewski, J. W., & Abraham, E. H. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0801394105 · Cited by 110 · see citing works
TNF-α Inhibits Macrophage Clearance of Apoptotic Cells via Cytosolic Phospholipase A2 and Oxidant-Dependent Mechanisms
McPhillips, K. A., Janssen, W. J., Ghosh, M., Byrne, A. M., Gardai, S. J., Remigio, L. K., Bratton, D. L., Kang, J. L., & Henson, P. M. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.12.8117 · Cited by 106 · see citing works
Nonphlogistic Clearance of Late Apoptotic Neutrophils by Macrophages: Efficient Phagocytosis Independent of β2 Integrins
Ren, Y., Stuart, L. M., Lindberg, F. P., Rosenkranz, A. R., Chen, Y., Mayadas, T. N., & Savill, J. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.7.4743 · Cited by 105 · see citing works
Antigen presentation by macrophages is enhanced by the uptake of necrotic, but not apoptotic, cells
Barker, R. N., Erwig, L.-P., Hill, K., Devine, A., Pearce, W. P., & Rees, A. J. (2002) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.2002.01774.x · Cited by 104 · see citing works
Apoptosis is associated with reduced expression of complement regulatory molecules, adhesion molecules and other receptors on polymorphonuclear leucocytes: functional relevance and role in inflammation.
Jones, J. R., & Morgan, B. P. (1995) · PubMed Central · Cited by 99 · see citing works
Apoptotic Cell Recognition: Will the Real Phosphatidylserine Receptor(s) Please Stand up?
Bratton, D. L., & Henson, P. M. (2008) · Current Biology · doi:10.1016/j.cub.2007.11.024 · Cited by 99 · see citing works
Lipoxin A4 Redistributes Myosin IIA and Cdc42 in Macrophages: Implications for Phagocytosis of Apoptotic Leukocytes
Reville, K., Crean, J. K. G., Vivers, S., Dransfield, I., & Godson, C. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.3.1878 · Cited by 94 · see citing works
The PPAR-γ antagonist GW9662 elicits differentiation of M2c-like cells and upregulation of the MerTK/Gas6 axis: a key role for PPAR-γ in human macrophage polarization
Zizzo, G., & Cohen, P. (2015) · Journal of Inflammation · doi:10.1186/s12950-015-0081-4 · Cited by 94 · see citing works
CD300b regulates the phagocytosis of apoptotic cells via phosphatidylserine recognition
Murakami, Y., Tian, L., Voss, O. H., Margulies, D. H., Krzewski, K., & Coligan, J. E. (2014) · Cell Death and Differentiation · doi:10.1038/cdd.2014.86 · Cited by 94 · see citing works
The prototypic tissue pentraxin PTX3, in contrast to the short pentraxin serum amyloid P, inhibits phagocytosis of late apoptotic neutrophils by macrophages
van Rossum, A. P., Fazzini, F., Limburg, P. C., Manfredi, A. A., Rovere, P. Q., Mantovani, A., & Kallenberg, C. G. M. (2004) · Arthritis & Rheumatism · doi:10.1002/art.20370 · Cited by 89 · see citing works
Fourteen-Member Macrolides Promote the Phosphatidylserine Receptor-Dependent Phagocytosis of Apoptotic Neutrophils by Alveolar Macrophages
Yamaryo, T., Oishi, K., Yoshimine, H., et al. (2002) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.47.1.48-53.2003 · Cited by 88 · see citing works
Complement Component C1q Regulates Macrophage Expression of Mer Tyrosine Kinase To Promote Clearance of Apoptotic Cells
Galvan, M. D., Foreman, D. B., Zeng, E., Tan, J. C., & Bohlson, S. S. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1102920 · Cited by 82 · see citing works
Phagocytosis of apoptotic cells
Hart, S. P., Dransfield, I., & Rossi, A. G. (2008) · Methods · doi:10.1016/j.ymeth.2007.11.009 · Cited by 81 · see citing works
Monocyte Induction of IL-10 and Down-Regulation of IL-12 by iC3b Deposited in Ultraviolet-Exposed Human Skin
Yoshida, Y., Kang, K., Berger, M., Chen, G., Gilliam, A. C., Moser, A., Wu, L., Hammerberg, C., & Cooper, K. D. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.161.11.5873 · Cited by 80 · see citing works
Chlamydia pneumoniae Hides inside Apoptotic Neutrophils to Silently Infect and Propagate in Macrophages
Rupp, J., Pfleiderer, L., Jugert, C., Möller, S., Klinger, M. H. F., Dalhoff, K., Solbach, W., Stenger, S., Laskay, T., & van Zandbergen, G. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006020 · Cited by 78 · see citing works
Viable, apoptotic and necrotic monocytes expose phosphatidylserine: cooperative binding of the ligand Annexin V to dying but not viable cells and implications for PS-dependent clearance
Appelt, U., Sheriff, A., Gaipl, U. S., et al. (2004) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401527 · Cited by 78 · see citing works
Dendritic cell uptake of human apoptotic and necrotic neutrophils inhibits CD40, CD80, and CD86 expression and reduces allogeneic T cell responses: Relevance to systemic vasculitis
Clayton, A. R., Prue, R. L., Harper, L., Drayson, M. T., & Savage, C. O. S. (2003) · Arthritis & Rheumatism · doi:10.1002/art.11130 · Cited by 76 · see citing works
N-Acetylcysteine Inhibits RhoA and Promotes Apoptotic Cell Clearance during Intense Lung Inflammation
Moon, C., Lee, Y.-J., Park, H.-J., Chong, Y. H., & Kang, J. L. (2009) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200907-1061oc · Cited by 74 · see citing works
Proteinase 3, the Autoantigen in Granulomatosis with Polyangiitis, Associates with Calreticulin on Apoptotic Neutrophils, Impairs Macrophage Phagocytosis, and Promotes Inflammation
Gabillet, J., Millet, A., Pederzoli-Ribeil, M., Tacnet‐Delorme, P., Guillevin, L., Mouthon, L., Frachet, P., & Witko‐Sarsat, V. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1200600 · Cited by 74 · see citing works
Yersinia pestissurvival and replication within human neutrophil phagosomes and uptake of infected neutrophils by macrophages
Spinner, J. L., Winfree, S., Starr, T., et al. (2013) · Journal of Leukocyte Biology · doi:10.1189/jlb.1112551 · Cited by 73 · see citing works
Mechanisms regulating neutrophil survival and cell death
Gabelloni, M. L., Trevani, A. S., Sabatté, J., & Geffner, J. R. (2013) · Seminars in Immunopathology · doi:10.1007/s00281-013-0364-x · Cited by 68 · see citing works
Intracellular HMGB1 Negatively Regulates Efferocytosis
Banerjee, S., de Freitas, A., Friggeri, A., Zmijewski, J. W., Liu, G., & Abraham, E. H. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1101500 · Cited by 68 · see citing works
Participation of the urokinase receptor in neutrophil efferocytosis
Park, Y.-J., Liu, G., Tsuruta, Y., Lorne, E., & Abraham, E. H. (2009) · Blood · doi:10.1182/blood-2008-12-193524 · Cited by 62 · see citing works
Macrophage Vitronectin Receptor, CD36, and Thrombospondin Cooperate in Recognition of Neutrophils Undergoing Programmed Cell Death
Savill, J., Hogg, N., & Haslett, C. (1991) · CHEST Journal · doi:10.1378/chest.99.3_supplement.6s-a · Cited by 60 · see citing works
Membrane Trafficking and Phagosome Maturation During the Clearance of Apoptotic Cells
Lü, N., & Zhou, Z. (2012) · International review of cytology · doi:10.1016/b978-0-12-394304-0.00013-0 · Cited by 60 · see citing works
Extracellular Histones Inhibit Efferocytosis
Friggeri, A., Banerjee, S., Xie, N., Cui, H., de Freitas, A., Zerfaoui, M., Dupont, H., Abraham, E. H., & Liu, G. (2012) · Molecular Medicine · doi:10.2119/molmed.2012.00005 · Cited by 52 · see citing works
Apoptotic cell clearance of Leishmania major-infected neutrophils by dendritic cells inhibits CD8+ T-cell priming in vitro by Mer tyrosine kinase-dependent signaling
Ribeiro-Gomes, F. L., Romano, A., Lee, S., Roffê, E., Peters, N. C., Debrabant, A., & Sacks, D. L. (2015) · Cell Death and Disease · doi:10.1038/cddis.2015.351 · Cited by 52 · 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
Adjunctive Therapy in Community-Acquired Pneumonia
Wunderink, R. G. (2009) · Seminars in Respiratory and Critical Care Medicine · doi:10.1055/s-0029-1202933 · Cited by 44 · see citing works
Antigen-Specific Immunity and Cross-Priming by Epithelial Ovarian Carcinoma-Induced CD11b+Gr-1+ Cells
Tomihara, K., Guo, M., Shin, T., Sun, X., Ludwig, S. M., Brumlik, M. J., Zhang, B., Curiel, T. J., & Shin, T. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0903519 · Cited by 44 · see citing works
Spontaneous or Mycobacterium tuberculosis‐induced apoptotic neutrophils exert opposite effects on the dendritic cell‐mediated immune response
Alemán, M., de la Barrera, S., Schierloh, P., Yokobori, N. K., Baldini, M., Musella, R. M., Abbate, E. H., & Sasiain, M. D. C. (2007) · European Journal of Immunology · doi:10.1002/eji.200636771 · Cited by 40 · see citing works
Impaired efferocytosis in human chronic granulomatous disease is reversed by pioglitazone treatment
Fernandez-Boyanapalli, R. F., Falcone, E. L., Zerbe, C. S., Marciano, B. E., Frasch, S. C., Henson, P. M., Holland, S. M., & Bratton, D. L. (2015) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2015.07.034 · Cited by 38 · see citing works
A Systematic Approach to Identify Markers of Distinctly Activated Human Macrophages
Zhanbolat, B., Wacker, M. A., Wilson, M. E., & Graff, J. W. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00253 · Cited by 35 · see citing works
Vitronectin Inhibits Efferocytosis through Interactions with Apoptotic Cells as well as with Macrophages
Bae, H., Tadié, J., Jiang, S., Park, D. W., Bell, C. P., Thompson, L. C., Peterson, C. B., Thannickal, V. J., Abraham, E. H., & Zmijewski, J. W. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1200625 · Cited by 34 · see citing works
Dendritic Cells Take up and Present Antigens from Viable and Apoptotic Polymorphonuclear Leukocytes
Alfaro, C., Suárez, N., Oñate, C., Perez‐Gracia, J. L., Martínez‐Forero, I., Hervás‐Stubbs, S., Rodríguez, I., Pérez, G., Bolaños, E., Palazón, A., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0029300 · Cited by 32 · see citing works
Activation of dendritic cells by polymorphonuclear neutrophils
Boudaly, S. (2009) · Frontiers in bioscience · doi:10.2741/3326 · Cited by 26 · see citing works
Adjunctive Therapy in Community-Acquired Pneumonia
Wunderink, R. G., & Mandell, L. A. (2012) · Seminars in Respiratory and Critical Care Medicine · doi:10.1055/s-0032-1315643 · Cited by 26 · see citing works
Sequestration patterns of transfused rat neutrophilic granulocytes under normal and inflammatory conditions
Løvås, K., Knudsen, E., Iversen, P. O., & Benestad, H. B. (1996) · European Journal Of Haematology · doi:10.1111/j.1600-0609.1996.tb01933.x · Cited by 25 · see citing works
CD31 delays phagocyte membrane repolarization to promote efficient binding of apoptotic cells
Vernon-Wilson, E. F., Aurade, F., Tian, L., Rowe, I. C. M., Shipston, M. J., Savill, J., & Brown, S. B. (2007) · Journal of Leukocyte Biology · doi:10.1189/jlb.0507283 · Cited by 25 · see citing works
Characterization of the Effects of Cross-Linking of Macrophage CD44 Associated with Increased Phagocytosis of Apoptotic PMN
Hart, S. P., Rossi, A. G., Haslett, C., & Dransfield, I. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033142 · Cited by 24 · see citing works
PPARγ modulated inflammatory response of human dendritic cell subsets to engulfed apoptotic neutrophils
Majai, G. E., Gogolák, P., Temesszentandrási‐Ambrus, C., Vereb, G., Hodrea, J., Fésüs, L., & Rajnavölgyi, É. (2010) · Journal of Leukocyte Biology · doi:10.1189/jlb.0310144 · Cited by 21 · see citing works
Phosphatidylserine receptors: what is the new RAGE?
Armstrong, A. J., & Ravichandran, K. S. (2011) · EMBO Reports · doi:10.1038/embor.2011.41 · Cited by 18 · see citing works
Neutrophils: dead or effete? Cell surface phenotype and implications for phagocytic clearance
Dransfield, I., Rossi, A. G., Brown, S. B., et al. (2005) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401695 · Cited by 17 · see citing works

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Neutrophil: A Cell with Many Roles in Inflammation or Several Cell Types?
Rosales, C. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00113 · Cited by 1,334 · see citing works
Macrophage Phenotypes Regulate Scar Formation and Chronic Wound Healing
Hesketh, M., Sahin, K. B., West, Z. E., & Murray, R. Z. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18071545 · Cited by 852 · see citing works
Neutrophils at the crossroads of innate and adaptive immunity
Rosales, C. (2020) · Journal of Leukocyte Biology · doi:10.1002/jlb.4mir0220-574rr · Cited by 372 · 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
Is there a role for N1-N2 neutrophil phenotypes in bone regeneration? A systematic review
Lu, F., Verleg, S. M. N. E., Groven, R. V. M., Poeze, M., van Griensven, M., & Blokhuis, T. J. (2024) · Bone · doi:10.1016/j.bone.2024.117021 · Cited by 25 · see citing works
MicroRNAs as Regulators of Phagocytosis
Gierlikowski, W., & Gierlikowska, B. (2022) · Cells · doi:10.3390/cells11091380 · Cited by 25 · see citing works

PHAGOCYTOSIS OF STAPHYLOCOCCUS AUREUS BY HUMAN LEUKOCYTES: QUANTITATION BY A FLOW CYTOMETRIC AND A MICROBIOLOGICAL METHOD
Bassøe, C., & SOLBERG, C. O. (2009) · Acta Pathologica Microbiologica Scandinavica Section C Immunology · doi:10.1111/j.1699-0463.1984.tb00050.x · Cited by 29 · see citing works
Efferocytosis and Atherosclerosis: Regulation of Phagocyte Function by MicroRNAs.
Tajbakhsh, A., Bianconi, V., Pirro, M., Hayat, S. G. G., Johnston, T., & Sahebkar, A. (2019) · Trends in endocrinology and metabolism · doi:10.1016/j.tem.2019.07.006 · Cited by 55 · see citing works
[The significance of phagocytosis for cellular defense. II. Disorders in phagocyte function].
Jw, V. D. M., & van Furth, R. (1976) · PubMed
Efferocytosis of Pathogen-Infected Cells
Karaji, N., & Sattentau, Q. J. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01863 · Cited by 61 · see citing works
Phagocytosis of Bacteria by Human Leukocytes Measured by Flow Cytometry
e, C.-F. B., Lærum, O. D., SOLBERG, C. O., et al. (1983) · Experimental Biology and Medicine · doi:10.3181/00379727-174-41722 · Cited by 58 · see citing works

Authors: Greenlee‐Wacker, M. C.
Affiliations: University of Iowa (US)
Corresponding author: Greenlee‐Wacker, Mallary C.
ORCID: Greenlee‐Wacker, Mallary C.
Venue: Immunological Reviews
Publisher: Wiley
Published: 2016-08-25
Volume: 273
Issue: 1
Pages: 357-370
ISSN: 0105-2896 (ISSN-L)
1600-065X
DOI: 10.1111/imr.12453
PMC: PMC5000862
OpenAlex: W2516344353
Cited by: 478
References: 161
Citations by year: 2026: 58 · 2025: 66 · 2024: 58 · 2023: 56 · 2022: 48 · 2021: 43 · 2020: 48 · 2019: 43 · 2018: 35 · 2017: 20 · 2016: 3
FWCI: 3.25
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Immunological Reviews (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (AI070958, AI044642)
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 › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
Keywords: efferocytosis, apoptotic neutrophils, inflammation resolution, phagocytes, macrophages, anti-inflammatory signaling, immunomodulation, neutrophil lysis, tissue homeostasis, chronic inflammation
MeSH terms: Animals, Humans, Immunity, Innate, Inflammation, Macrophages, Neutrophils, Phagocytosis, Signal Transduction, Apoptosis, Immunomodulation

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