Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF.
Open accessAbstract
Apoptosis in vivo is followed almost inevitably by rapid uptake into adjacent phagocytic cells, a critical process in tissue remodeling, regulation of the immune response, or resolution of inflammation. Phagocytosis of apoptotic cells by macrophages has been suggested to be a quiet process that does not lead to production of inflammatory mediators. Here we show that phagocytosis of apoptotic neutrophils (in contrast to immunoglobulin G-opsonized apoptotic cells) actively inhibited the production of interleukin (IL)-1beta, IL-8, IL-10, granulocyte macrophage colony-stimulating factor, and tumor necrosis factor-alpha, as well as leukotriene C4 and thromboxane B2, by human monocyte-derived macrophages. In contrast, production of transforming growth factor (TGF)-beta1, prostaglandin E2, and platelet-activating factor (PAF) was increased. The latter appeared to be involved in the inhibition of proinflammatory cytokine production because addition of exogenous TGF-beta1, prostaglandin E2, or PAF resulted in inhibition of lipopolysaccharide-stimulated cytokine production. Furthermore, anti-TGF-beta antibody, indomethacin, or PAF receptor antagonists restored cytokine production in lipopolysaccharide-stimulated macrophages that had phagocytosed apoptotic cells. These results suggest that binding and/or phagocytosis of apoptotic cells induces active antiinflammatory or suppressive properties in human macrophages. Therefore, it is likely that resolution of inflammation depends not only on the removal of apoptotic cells but on active suppression of inflammatory mediator production. Disorders in either could result in chronic inflammatory diseases.
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Common cytokines used in biomaterial-based research include proinflammatory IFN-γ or IL-4, which are important effectors in steering macrophage phenotypes.
“Some of the more common cytokines used in biomaterial‐based research involves the proinflammatory IFN‐γ or IL‐4, which are important effectors in steering the macrophage phenotypes.[ 103 , 232 , 233 , 234 ]”
From Unraveling and Harnessing the Immune Response at the Cell–Biomaterial Interface for Tissue Engineering Purposes (2024) · cites this paper as [234]
Phagocytosis of neutrophils is a central element to induce phenotype switch of macrophages from M1 to M2.
“Interestingly, phagocytosis of neutrophils is also a central element to induce the phenotype switch of macrophages from pro-inflammatory M1 to a reparative M2 phenotype [73].”
From Transition from inflammation to proliferation: a critical step during wound healing (2016) · cites this paper as [73]
2-AG increases number of phagocytosing macrophages, leading to increased anti-inflammatory cytokines and decreased pro-inflammatory cytokines by macrophages.
“2-AG increases the number of phagocytosing macrophages, which leads to increased production of anti-inflammatory cytokines, e.g., TGF-β1 and decreased output of pro-inflammatory cytokines, e.g., TNF-α by macrophages [73].”
From Transition from inflammation to proliferation: a critical step during wound healing (2016) · cites this paper as [73]
Apoptosis and engulfment of neutrophils by macrophages provides a key signal to the local immune milieu to transition to an anti-inflammatory, pro-repair state.
“Their apoptosis and engulfment by macrophages (efferocytosis) provides a key signal to the local immune milieu, including macrophages, to transition to an anti-inflammatory, pro-repair state”
From Immunology of Wound Healing (2018) · cites this paper as [47]
In physiologic wound repair, neutrophil apoptosis followed by local macrophage uptake of apoptotic neutrophils triggers a transition out of the inflammatory phase.
“In physiologic wound repair, neutrophils undergo apoptosis after carrying out their various functions at the site of injury. Local macrophage uptake of apoptotic neutrophils then triggers a transition out of inflammatory phase [47–49].”
From Immunology of Wound Healing (2018) · cites this paper as [47]
Efferocytosis of apoptotic neutrophils induces macrophages to transition from a pro-inflammatory phenotype to an anti-inflammatory phenotype.
“Macrophages in the wound site are responsible for phagocytosis of apoptotic neutrophils, a process known as efferocytosis [73••]. This action itself induces macrophages to transition from a pro-inflammatory phenotype, to an anti-inflammatory phenotype”
From Immunology of Wound Healing (2018) · cites this paper as [47]
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BackgroundThe clearance of dead cells by efferocytosis
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BackgroundModels of liver fibrosis: exploring the dynamic nature of inflammation and repair in a solid organ
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BackgroundMacrophage activation switching: an asset for the resolution of inflammation
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BackgroundIdentification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases
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Apoptosis and caspases regulate death and inflammation in sepsis
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“To investigate the interactions between MSCs and macrophages we used macrophages derived from peripheral blood monocytes by seven days of culture without added cytokines; these macrophages are equivalent to steady state peripheral blood monocyte derived-macrophages [49-51].”
MethodMicroglia and neurodegeneration: The role of systemic inflammation
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“Microglia in prion disease also show only limited evidence of IL-1b and TNF-a expression, but instead appear to be dominated by TGFb1 and PGE2 (Cunningham et al., 2002; Minghetti et al., 2000; Walsh et al., 2001).”
BackgroundThe role of phosphatidylserine in recognition of apoptotic cells by phagocytes
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BackgroundSelf-citationPattern Recognition Receptors and the Host Cell Death Molecular Machinery
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“In addition, it is well established that recognition of apoptotic cells by macrophages, in particular, results in the production of anti-inflammatory molecules, such as TGF-β and PGE2 (11).”
BackgroundRhythmic Modulation of the Hematopoietic Niche through Neutrophil Clearance
Casanova-Acebes, M., Pitaval, C., Weiss, L. A., Nombela‐Arrieta, C., Chèvre, R., A-González, N., Kunisaki, Y., Zhang, D., van Rooijen, N., Silberstein, L. E., et al. (2013) · Cell · doi:10.1016/j.cell.2013.04.040 · Cited by 752 · see citing works
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Regulation of Muscle Growth and Regeneration by the Immune System
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Resolution of inflammation: an integrated view
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“In addition, resolution-phase macrophages express TIM4 and TGF-b , key molecules in the clearance of inflammatory cells and the return to tissue homeostasis.”
InfluentialTaylor, P. R., Carugati, A., Fadok, V. A., Cook, H. T., Andrews, M., Carroll, M. C., Savill, J., Henson, P. M., Botto, M., & Walport, M. J. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.192.3.359 · Cited by 724 · see citing works
“PBMCs were isolated from C1qdeficient and normal humans and cultured as previously described ( 11 ) on coverslips in 24-well plates.”
MethodSelf-citationPhagocytosis and the actin cytoskeleton
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Macrophage Dysfunction Impairs Resolution of Inflammation in the Wounds of Diabetic Mice
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“Results of this work support that efferocytosis may be one of such cues that drives the switching of macrophages towards an anti-inflammatory state [60].”
BackgroundMacrophages, Foreign Body Giant Cells and Their Response to Implantable Biomaterials
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“Additionally, after phagocytosing apoptotic cells, TGFβ expression can lead to the immune regulatory activities of this cell type [46].”
BackgroundComplement-dependent Clearance of Apoptotic Cells by Human Macrophages
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“In human peripheral blood–derived macrophages, the known receptors show a relatively low uptake of apoptotic cells (average of 40 apoptotic cells per 100 macrophages [12, 13]) and are only partially inhibited by specific blocking agents in vitro (3, 9, 14).”
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“It has been shown that phagocytosis of apoptotic or necrotic cells leads to the synthesis of anti- or proinflammatory cytokines such as TGFb or TNFa , respectively (33, 34).”
BackgroundResultInfluentialCD47-blocking antibodies restore phagocytosis and prevent atherosclerosis
Kojima, Y., Volkmer, J.-P., McKenna, K., Civelek, M., Lusis, A. J., Miller, C. L., Direnzo, D., Nanda, V., Ye, J., Connolly, A. J., et al. (2016) · Nature · doi:10.1038/nature18935 · Cited by 683 · see citing works
“Because impaired efferocytosis is known to incite proinflammatory cytokine elaboration 9 , it is possible that a positive feedback loop underlies the co-localization of TNF-α , CD47, and uncleared pathological cells and apoptotic bodies within the atherosclerotic plaque 22 .”
BackgroundInnate Immunity and the Failing Heart
Mann, D. L. (2015) · Circulation Research · doi:10.1161/circresaha.116.302317 · Cited by 690 · see citing works
Goerdt, S., & Orfanos, C. E. (1999) · Immunity · doi:10.1016/s1074-7613(00)80014-x · Cited by 678 · see citing works
Human CD14 mediates recognition and phagocytosis of apoptotic cells
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“Tolerance is accomplished through several distinct mech- anisms, including suppression of inflammatory cytokine produc- tion and release of anti-inflammatory cytokines such as IL-10 and TGF-b (Fadok et al., 1998b; Li and Flavell, 2008; Voll et al., 1997).”
InfluentialResolution of Lung Inflammation by CD44
Teder, P., Vandivier, R. W., Jiang, D., Liang, J., Cohn, L. E., Puré, E., Henson, P. M., & Noble, P. W. (2002) · Science · doi:10.1126/science.1069659 · Cited by 676 · see citing works
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RetractedPara-Inflammation in the Aging Retina
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“Uptake of apoptotic cells by phagocytes induces anti-inflammatory responses, including the production of transforming growth factor b (TGF-b) and interleukin-10 production (Fadok et al., 1998a,b; Voll et al., 1997).”
BackgroundStuart, L. M., & Ezekowitz, R. A. B. (2005) · Immunity · doi:10.1016/j.immuni.2005.05.002 · Cited by 667 · see citing works
Adiponectin Promotes Macrophage Polarization toward an Anti-inflammatory Phenotype
Ohashi, K., Parker, J. L., Ouchi, N., Higuchi, A., Vita, J. A., Gokce, N., Pedersen, A. A., Kalthoff, C., Tullin, S., Sams, A., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.088708 · Cited by 646 · see citing works
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“of regulatory pathways in phagocytes and release of anti-inflammatory cytokines (1, 2).”
BackgroundFadok, 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
Self-citationThe immune system and cardiac repair
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Resolution of Inflammation: What Controls Its Onset?
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“Early data from Kunkel’s group showed a suppressive effect of PGE2 on macrophage TNF-α and IL-1β production (242, 243), and this has been confirmed by other investigators (238).”
BackgroundResultEngulfment 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
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Role of innate and adaptive immune mechanisms in cardiac injury and repair
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Tissue-specific macrophages: how they develop and choreograph tissue biology
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“Although these mediators can stimulate immunity, apoptotic cells can inhibit inflammatory and immunological responses driven by macrophages and DCs (Fadok et al., 1998).”
BackgroundInfluentialScientific and Medical Aspects of Ozone Therapy. State of the Art
Bocci, V. A. (2006) · Archives of Medical Research · doi:10.1016/j.arcmed.2005.08.006 · Cited by 626 · see citing works
“As might be expected, two biological studies (40,41) have shown the possibility of controlling a chronic oxidative stress (33) and of activating regulatory T cells for downregulating a chronic inflammation.”
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Macrophage activation by endogenous danger signals
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“Thus, two classes of apoptosis-related events in the gut mucosa may contribute to the generation of an immunosuppressive milieu: apoptosis of T cells (61) and clearance of apoptotic cells by macrophages (65) and DCs (64).”
BackgroundJanus-faced microglia: beneficial and detrimental consequences of microglial phagocytosis
Sierra, A., Abiega, O., Shahraz, A., & Neumann, H. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00006 · Cited by 574 · see citing works
“Over the past 20 years, it has been made clear that the phagocytosis of apoptotic cells is largely anti-inflammatory (Stern et al., 1996; Voll et al., 1997; Fadok et al., 1998).”
BackgroundDiverse macrophage populations mediate acute lung inflammation and resolution
Aggarwal, N. R., King, L. S., & D’Alessio, F. R. (2014) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00341.2013 · Cited by 583 · see citing works
“AEC, alveolar epithelial cell; CCL2, chemokine (C-C motif) ligand 2; CCR2, chemokine (C-C motif) receptor 2; GM-CSF, granulocyte macrophage colony-stimulating factor; IFN-␥, interferon-␥; IL, interleukin; IL-1ra, interleukin 1 receptor antagonist; iNOS, inducible nitric oxide synthase; IRF, interferon regulator factor…”
InfluentialInhibition of apoptosis induced by ischemia-reperfusion prevents inflammation
Daemen, M. A. R. C., Veer, C. V. ′., Denecker, G., Heemskerk, V. H., Wolfs, T. G. A. M., Clauss, M. A., Vandenabeele, P., & Buurman, W. A. (1999) · Journal of Clinical Investigation · doi:10.1172/jci6974 · Cited by 565 · see citing works
“which states that apoptosis represents a physiological mode of cell deletion allowing disposal of superfluous cells with minimal tissue reaction, or even with active restraining of inflammation (5).”
BackgroundBeginnings of a Good Apoptotic Meal: The Find-Me and Eat-Me Signaling Pathways
Ravichandran, K. S. (2011) · Immunity · doi:10.1016/j.immuni.2011.09.004 · Cited by 559 · see citing works
- Authors
- Fadok, V. A., Bratton, D. L., Konowal, A., Freed, P. W., Westcott, J. Y., & Henson, P. M.
- Affiliations
- National Jewish Health (US)
- ORCID
- Henson, P M
- Venue
- Journal of Clinical Investigation
- Published
- 1998-02-15
- Volume
- 101
- Issue
- 4
- Pages
- 890-898
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC508637
- OpenAlex
- W2095537212
- Semantic Scholar
- 3e88d8a52759097d481b92ec0d06606afbadafab
- Cited by
- 3,166
- References
- 50
- Citations by year
- 2026: 60 · 2025: 74 · 2024: 91 · 2023: 82 · 2022: 91 · 2021: 129 · 2020: 114 · 2019: 125 · 2018: 106 · 2017: 113 · 2016: 117 · 2015: 109 · 2014: 116 · 2013: 130 · 2012: 133
- FWCI
- 29.16
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Heart, Lung, and Blood Institute (HL34303, P01HL034303)
- National Institute of General Medical Sciences (GM48211, R01GM048211)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Keywords
- phagocytosis of apoptotic cells, macrophages, inflammation resolution, anti-inflammatory macrophages, inflammatory cytokines, TGF-β1, prostaglandin E2, platelet-activating factor, autocrine and paracrine signaling, neutrophil apoptosis, monocyte-derived macrophages, indomethacin, PAF receptor antagonists
- MeSH terms
- Humans, Inflammation, Macrophages, Neutrophils, Phagocytosis, Platelet Activating Factor, Solubility, Thromboxane B2, Dinoprostone, Cytokines, Transforming Growth Factor beta, Apoptosis, Leukotriene C4, Jurkat Cells
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