A blast from the past: clearance of apoptotic cells regulates immune responses (original) (raw)
Kerr, J. F. R., Wyllie, A. H. & Currie, A. R. Apoptosis: a basic biological phenomenon with widespread implications in tissue kinetics. Br. J. Cancer26, 239–257 (1972). The seminal description of apoptosis. CASPubMedPubMed Central Google Scholar
Krammer, P. H. CD95's deadly mission in the immune system. Nature407, 789–795 (2000). CASPubMed Google Scholar
Savill, J. & Fadok, V. Corpse clearance defines the meaning of cell death. Nature407, 784–788 (2000). CASPubMed Google Scholar
Taylor, P. R. et al. A hierarchical role for classical pathway complement proteins in the clearance of apoptotic cells. J. Exp. Med.192, 359–366 (2000). A crucial demonstration of the links between defective clearance of apoptotic cells and autoimmunity (see also reference 103). CASPubMedPubMed Central Google Scholar
Albert, M. L., Sauter, B. & Bhardwaj, N. Dendritic cells acquire antigen from apoptotic cells and induce class-I-restricted CTLs. Nature392, 86–89 (1998). The first report of mechanisms by which antigens that are expressed by apoptotic cells can be presented to T cells, thereby accounting for cross-presentation. CASPubMed Google Scholar
Savill, J. S., Dransfield, I., Hogg, N. & Haslett, C. Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature343, 170–173 (1990). A description of the first phagocyte receptor for apoptotic cells to be identified, as shown by antibody- and peptide-mediated blockade and the selection of vitronectin-receptor-bearing macrophages. CASPubMed Google Scholar
Fadok, V. A., Bratton, D. L., Henson, P. M. Phagocyte receptors for apoptotic cells: recognition, uptake and consequences. J. Clin. Invest.108, 957–962 (2001). CASPubMedPubMed Central Google Scholar
Hu, B., Sonstein, J., Christensen, P. J., Punturieri, A. & Curtis, J. L. Deficient in vitro and in vivo phagocytosis of apoptotic T cells by resident murine alveolar macrophages. J. Immunol.165, 2124–2133 (2000). CASPubMed Google Scholar
Schagat, T. L., Wofford, J. A. & Wright, J. R. Surfactant protein A enhances alveolar macrophage phagocytosis of apoptotic neutrophils. J. Immunol.166, 2727–2733 (2001). CASPubMed Google Scholar
Mevorach, D., Mascarenhas, J. O., Gershov, D. & Elkon, K. B. Complement-dependent clearance of apoptotic cells by human macrophages. J. Exp. Med.188, 2313–2320 (1998). CASPubMedPubMed Central Google Scholar
Gaipl, U. S. et al. Complement binding is an early feature of necrotic and a rather late event during apoptotic cell death. Cell Death Differ.8, 327–334 (2001). CASPubMed Google Scholar
Savill, J. S., Henson, P. M. & Haslett, C. Phagocytosis of aged human neutrophils by macrophages is mediated by a novel 'charge-sensitive' recognition mechanism. J. Clin. Invest.84, 1518–1527 (1989). CASPubMedPubMed Central Google Scholar
Ren, Y. et al. Non-phlogistic clearance of late apoptotic neutrophils by macrophages: efficient phagocytosis independent of β2-integrins. J. Immunol.166, 4743–4750 (2001). CASPubMed Google Scholar
Scott, R. S. et al. Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature411, 207–211 (2001). The first data to indicate a role in the phagocytosis of apoptotic cells for receptor tyrosine kinases that normally keep immune responses in check (see also reference 104). CASPubMed Google Scholar
Hamon, Y. et al. ABC1 promotes engulfment of apoptotic cells and transbilayer redistribution of phosphatidylserine. Nature Cell Biol.2, 399–406 (2000). An important demonstration of a role for the CED7 homologue ABC1 in altering plasma-membrane lipid distribution in dying cells and phagocytes to promote the clearance of apoptotic cellsin vitroandin vivo(see also reference 37). CASPubMed Google Scholar
Pickering, M. C. et al. Ultraviolet radiation-induced keratinocyte apoptosis in C1q-deficient mice. J. Invest. Dermatol.117, 52–58 (2001). CASPubMed Google Scholar
Ogden, C. A. et al. C1q and mannose-binding lectin engagement of cell-surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J. Exp. Med.194, 781–795 (2001). CASPubMedPubMed Central Google Scholar
Devitt, A. et al. Human CD14 mediates recognition and phagocytosis of apoptotic cells. Nature392, 505–509 (1998). A pioneering report implicating recognition mechanisms of innate immunity in the clearance of dying cells. CASPubMed Google Scholar
Savill, J. Apoptosis: phagocytic docking without shocking. Nature392, 442–443 (1998). CASPubMed Google Scholar
Gershov, D., Kim, S., Brot, N. & Elkon, K. B. C-reactive protein binds to apoptotic cells, protects the cells from assembly of the terminal complement components and sustains an anti-inflammatory innate immune response: implications for systemic autoimmunity. J. Exp. Med.192, 1353–1364 (2001). Google Scholar
Savill, J. S., Hogg, N., Ren, Y. & Haslett, C. Thrombospondin co-operates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J. Clin. Invest.90, 1513–1522 (1992). CASPubMedPubMed Central Google Scholar
Ren, Y., Silverstein, R. L., Allen, J. & Savill, J. CD36 gene transfer confers capacity for phagocytosis of cells undergoing apoptosis. J. Exp. Med.181, 1857–1862 (1995). This study was the first to show the principle of 'gain of phagocytic function'. CASPubMed Google Scholar
Sambrano, G. R. & Steinberg, D. Recognition of oxidatively damaged and apoptotic cells by an oxidized low-density lipoprotein receptor on mouse peritoneal macrophages: role of membrane phosphatidylserine. Proc. Natl Acad. Sci. USA92, 1396–1400 (1995). CASPubMedPubMed Central Google Scholar
Chang, M. -K. et al. Monoclonal antibodies against oxidized low-density lipoprotein bind to apoptotic cells and inhibit their phagocytosis by elicited macrophages: evidence that oxidation-specific epitopes mediate macrophage recognition. Proc. Natl Acad. Sci. USA96, 6353–6358 (1999). CASPubMedPubMed Central Google Scholar
Kagan, V. E. et al. A role for oxidative stress in apoptosis: oxidation and externalisation of phosphatidylserine is required for macrophage clearance of cells undergoing Fas-mediated apoptosis. J. Immunol.169, 487–499 (2002). CASPubMed Google Scholar
Shaw, P. X. et al. Natural antibodies with the T15 idiotype may act in atherosclerosis, apoptotic clearance and protective immunity. J. Clin. Invest.105, 1731–1740 (2000). CASPubMedPubMed Central Google Scholar
Oka, K. et al. Lectin-like oxidized low-density lipoprotein receptor 1 mediates phagocytosis of aged/apoptotic cells in endothelial cells. Proc. Natl Acad. Sci. USA95, 9535–9540 (1998). CASPubMedPubMed Central Google Scholar
Platt, N., Suzuki, H., Kurihara, Y., Kodama, T. & Gordon, S. Role for the class A macrophage scavenger receptor in the phagocytosis of apoptotic thymocytes in vitro. Proc. Natl Acad. Sci. USA93, 12456–12460 (1996). CASPubMedPubMed Central Google Scholar
Platt, N., Suzuki, H., Kodama, T. & Gordon, S. Apoptotic thymocyte clearance in scavenger receptor class A-deficient mice is apparently normal. J. Immunol.164, 4861–4867 (2000). CASPubMed Google Scholar
Dini, L., Autori, F., Lentini, A., Olivierio, S. & Piacentini, M. The clearance of apoptotic cells in the liver is mediated by the asialoglycoprotein receptor. FEBS Lett.296, 174–178 (1992). CASPubMed Google Scholar
Duvall, E., Wyllie, A. H. & Morris, R. G. Macrophage recognition of cells undergoing programmed cell death. Immunology56, 351–358 (1985). CASPubMedPubMed Central Google Scholar
Fadok, V. A., Bratton, D. L., Frasch, S. C., Warner, M. L. & Henson, P. M. The role of phosphatidylserine in recognition of apoptotic cells by phagocytes. Cell Death Differ.5, 557–563 (1998). Google Scholar
Fadok, V. A. et al. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal of macrophages. J. Immunol.148, 2207–2216 (1992). CASPubMed Google Scholar
Fadok, V. A. et al. A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature405, 85–90 (2000). References 33 and 34 describe the discovery of the first 'eat-me' flag on dying cells. CASPubMed Google Scholar
Verhoven, B., Schlegel, R. A. & Williamson, P. Mechanisms of phosphatidylserine exposure, a phagocyte recognition signal, on apoptotic T lymphocytes. J. Exp. Med.182, 1597–1601 (1995). CASPubMed Google Scholar
Frasch, S. C. et al. Regulation of phospholipid scramblase activity during apoptosis and cell activation by protein kinase Cδ. J. Biol. Chem.275, 23065–23073 (2000). CASPubMed Google Scholar
Marguet, D., Luciani, M. F., Moynault, A., Williamson, P. & Chimini, G. Engulfment of apoptotic cells involves the redistribution of membrane phosphatidlyserine on phagocyte and prey. Nature Cell Biol.1, 454–456 (1999). CASPubMed Google Scholar
Balasubramanian, K., Chandra, J. & Schroit, A. J. Immune clearance of phosphatidylserine-expressing cells by phagocytes. The role of β2-glycoprotein I in macrophage recognition. J. Biol. Chem.272, 31113–31117 (1997). CASPubMed Google Scholar
Cocca, B. A. et al. Structural basis for autoantibody recognition of phosphatidylserine-β2 glycoprotein 1 and apoptotic cells. Proc. Natl Acad. Sci.98, 13826–13831 (2001). CASPubMedPubMed Central Google Scholar
Moffatt, O. D., Devitt, A., Bell, E. D., Simmons, D. L. & Gregory, C. D. Macrophage recognition of ICAM-3 on apoptotic leukocytes. J. Immunol.162, 6800–6810 (1999). CASPubMed Google Scholar
Hughes, J., Liu, Y., Ren, Y. & Savill, J. Human glomerular mesangial cell phagocytosis of apoptotic cells is mediated by a CD36-independent vitronectin receptor/thrombospondin recognition mechanism. J. Immunol.158, 4389–4397 (1997). CASPubMed Google Scholar
Parnaik, R., Raff, M. C. & Scholes, J. Differences between the clearance of apoptotic cells by professional and non-professional phagocytes. Curr. Biol.10, 857–860 (2000). CASPubMed Google Scholar
Brown, S. et al. Apoptosis disables CD31-mediated cell detachment from phagocytes promoting binding and engulfment. Nature (in the press). A new insight into discrimination between living and dying cells — apoptosis switches the function of an immunoglobulin-superfamily molecule so that detachment is disabled, which converts a repulsive interaction to an adhesive one.
Knepper-Nicolai, B., Brown, S. B. & Savill, J. Constitutive apoptosis in human neutrophils requires synergy between calpains and the proteasome downstream of caspases. J. Biol. Chem.273, 30530–30536 (1998). CASPubMed Google Scholar
Chimini, G. Apoptosis: repulsive encounters. Nature418, 139–142 (2002). CASPubMed Google Scholar
Reddien, P. W., Cameron, S. & Horvitz, H. R. Phagocytosis promotes programmed cell death in C. elegans. Nature412, 198–202 (2001). CASPubMed Google Scholar
Hoeppner, D. J., Hentgartner, M. O. & Schnabel, R. Engulfment genes cooperate with ced-3 to promote cell death in Caenorhabditis elegans. Nature412, 202–206 (2001). CASPubMed Google Scholar
Brown, S. B. & Savill, J. Phagocytosis triggers macrophage release of Fas-ligand and induces apoptosis of bystander leucocytes. J. Immunol.162, 480–485 (1999). CASPubMed Google Scholar
Hanayama, R. et al. Identification of a factor that links apoptotic cells to phagocytes. Nature417, 182–187 (2002). CASPubMed Google Scholar
Hoffmann, P. R. et al. Phosphatidylserine (PS) induces PS receptor-mediated macropinocytosis and promotes clearance of apoptotic cells. J. Cell Biol.155, 649–660 (2001). A key study indicating that the phosphatidylserine receptor promotes ingestion of tethered apoptotic cells and fluid through macropinocytosis. CASPubMedPubMed Central Google Scholar
Meagher, L. C., Savill, J. S., Baker, A. & Haslett, C. Phagocytosis of apoptotic neutrophils does not induce macrophage release of thromboxane B2 . J. Leukocyte Biol.52, 269–273 (1992). The original demonstration of neutral clearance of apoptotic cells without activating macrophages. CASPubMed Google Scholar
Stern, M., Savill, J. & Haslett, C. Human monocyte-derived macrophage phagocytosis of senescent eosinophils undergoing apoptosis: mediation by αvβ3/CD36/thrombospondin recognition mechanism and lack of phlogistic response. Am. J. Pathol.149, 911–921 (1996). CASPubMedPubMed Central Google Scholar
Wright, S. D. & Silverstein, S. C. Receptors for C3b and C3bi promote phagocytosis but not the release of toxic oxygen from human phagocytes. J. Exp. Med.158, 2016–2023 (1983). CASPubMed Google Scholar
Marth, T. & Kelsall, B. L. Regulation of interleukin-12 by complement receptor 3 signalling. J. Exp. Med.185, 1987–1995 (1997). CASPubMedPubMed Central Google Scholar
Voll, R. E., Herrmann, M., Roth, E. A., Stach, C. & Kalden, J. R. Immunosuppressive effects of apoptotic cells. Nature390, 350–351 (1997). The title of this paper highlights a key discovery in the field of apoptosis. CASPubMed Google Scholar
Newman, S. L., Henson, J. E. & Henson, P. M. Phagocytosis of senescent neutrophils by human monocyte-derived macrophages and rabbit inflammatory macrophages. J. Exp. Med.156, 430–442 (1982). CASPubMed Google Scholar
Byrne, A. & Reen, D. J. Lipopolysaccharide induces rapid production of IL-10 by monocytes in the presence of apoptotic neutrophils. J. Immunol.168, 1968–1997 (2002). CASPubMed Google Scholar
Fadok, V. A. et al. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-β, PGE2 and PAF. J. Clin. Invest.101, 890–898 (1998). A classical paper defining a role for TGF-β1 in the anti-inflammatory clearance of dying cells. CASPubMedPubMed Central Google Scholar
McDonald, P. P., Fadok, V. A., Bratton, D. & Henson, P. M. Transcriptional and translational regulation of inflammatory mediator production by endogenous TGF-β in macrophages that have ingested apoptotic cells. J. Immunol.163, 6164–6172 (1999). CASPubMed Google Scholar
Cocco, R. E. & Ucker, D. S. Distinct modes of macrophage recognition for apoptotic and necrotic cells are not specified exclusively by phosphatidylserine exposure. Mol. Biol. Cell12, 919–930 (2001). CASPubMedPubMed Central Google Scholar
Huynh, M. -L. N., Fadok, V. A. & Henson, P. M. Phosphatidylserine-dependent ingestion of apoptotic cells promoted TGF-β1 secretion and the resolution of inflammation. J. Clin. Invest.109, 41–50 (2002). The firstin vivodemonstration that the clearance of apoptotic cells can suppress inflammatory responses. CASPubMedPubMed Central Google Scholar
Duffield, J. A. et al. Activated macrophages direct apoptosis and suppress mitosis of mesangial cells. J. Immunol.164, 2110–2119 (2000). CASPubMed Google Scholar
Reiter, I., Krammer, B. & Schwamberger, G. Differential effect of apoptotic versus necrotic tumor cells on macrophage antitumor activities. J. Immunol.163, 1730–1732 (1999). CASPubMed Google Scholar
Duffield, J. S., Ware, C. F., Ryffel, B. & Savill, J. Suppression by apoptotic cells defines tumour necrosis factor-mediated induction of glomerular mesangial cell apoptosis by activated macrophages. Am. J. Pathol.159, 1397–1404 (2001). CASPubMedPubMed Central Google Scholar
Freire-de-Lima, C. G. et al. Uptake of apoptotic cells drives the growth of a pathogenic trypanosome in macrophages. Nature403, 199–203 (2000). CASPubMed Google Scholar
Gao, Y., Herndon, J. M., Zhang, H., Griffith, T. S. & Ferguson, T. A. Anti-inflammatory effects of CD95 ligand (FasL)-induced apoptosis. J. Exp. Med.188, 887–896 (1998). CASPubMedPubMed Central Google Scholar
Chen, W. -J., Frank, M. E., Jin, W. & Wahl, S. M. TGF-β released by apoptotic T cells contributes to an immunosuppressive milieu. Immunity14, 715–725 (2001). CASPubMed Google Scholar
Lorimore, S. A., Coates, P. J., Scobie, G. E., Milne, G. & Wright, E. G. Inflammatory-type responses after exposure to ionizing radiation in vivo: a mechanism for radiation-induced bystander effects? Oncogene20, 7085–7095 (2001). CASPubMed Google Scholar
Kurosaka, K., Watanabe, N. & Kobayashi, Y. Production of proinflammatory cytokines by phorbol myristate acetate-treated THP-1 cells and monocyte-derived macrophages after phagocytosis of apoptotic CTLL-2 cells. J. Immunol.161, 6245–6249 (1998). CASPubMed Google Scholar
Basu, S., Binder, R. J., Ramalingam, T. & Srivastava, P. K. CD91 is a common receptor for heat-shock proteins pg96, hsp70 and calreticulin. Immunity14, 303–313 (2001). CASPubMed Google Scholar
Miwa, K. et al. Caspase-1-independent IL-1β release and inflammation induced by the apoptosis inducer Fas ligand. Nature Med.4, 1287–1292 (1998). CASPubMed Google Scholar
Sansonetti, P. J. et al. Caspase-1 activation of IL-1β and IL-8 are essential for _Shigella flexneri_-induced inflammation. Immunity12, 581–590 (2000). CASPubMed Google Scholar
Restifo, N. P. Building better vaccines: how apoptotic cell death can induce inflammation and activate innate and adaptive immunity. Curr. Opin. Immunol.12, 597–603 (2000). CASPubMedPubMed Central Google Scholar
Horino, K. et al. A monocyte chemotactic factor S19 ribosomal protein dimer in phagocytic clearance of apoptotic cells. Lab. Invest.78, 603–617 (1998). CASPubMed Google Scholar
Rubartelli, A., Foggi, A. & Zocchi, M. K. The selective engulfment of apoptotic bodies by dendritic cells is mediated by the αvβ3 integrin and requires intracellular and extracellular calcium. Eur. J. Immunol.27, 1893–1900 (1997). The first report of phagocytosis of apoptotic cells by dendritic cells. CASPubMed Google Scholar
Albert, M. L. et al. Immature dendritic cells phagocytose apoptotic cells via αvβ5 and CD36, and cross-present antigens to cytotoxic T lymphocytes. J. Exp. Med.188, 1359–1368 (1998). CASPubMedPubMed Central Google Scholar
Urban, B. C., Willcox, N. & Roberts, D. J. A role for CD36 in the regulation of dendritic-cell function. Proc. Natl Acad. Sci. USA98, 8750–8755 (2001). CASPubMedPubMed Central Google Scholar
Stuart, L. M. et al. Inhibitory effects of apoptotic-cell ingestion upon endotoxin-driven myeloid dendritic-cell maturation. J. Immunol.168, 1627–1635 (2002). References 77 and 78 show the suppressive effects of apoptotic-cell ingestion on immature dendritic cells, which might contribute to cross-tolerization (see also reference 94). CASPubMed Google Scholar
Urban, B. C. et al. _Plasmodium falciparum_-infected erythrocytes modulate the maturation of dendritic cells. Nature400, 73–77 (1999). CASPubMed Google Scholar
Bellone, M. et al. Processing of engulfed apoptotic bodies yields T-cell epitopes. J. Immunol.159, 5391–5399 (1997). The first demonstration that the phagocytosis of apoptotic cells might promote the presentation of antigen to primed T cells. CASPubMed Google Scholar
Rodriguez, A., Regnault, A., Kleijmeer, M., Ricciardi-Castagnoli, P. & Amigorena, S. Selective transport of internalized antigens to the cytosol for MHC class I presentation in dendritic cells. Nature Cell Biol.1, 362–368 (1999). CASPubMed Google Scholar
Schulz, O., Pennington, D. J., Hodivala-Dilke, K., Febbraio, M. & Reis e Sousa, C. CD36 or αvβ3 and αvβ5 integrins are not essential for MHC class I cross-presentation of cell-associated antigen by CD8α+ murine dendritic cells. J. Immunol.168, 6057–6065 (2002). CASPubMed Google Scholar
Belz, G. T. et al. CD36 is differentially expressed by CD8+ splenic dendritic cells but is not required for cross-presentation in vivo. J. Immunol.168, 6066–6070 (2002). CASPubMed Google Scholar
Inaba, K. et al. Efficient presentation of phagocytosed cellular fragments on the major histocompatibility complex class II products of dendritic cells. J. Exp. Med.188, 2163–2169 (1998). CASPubMedPubMed Central Google Scholar
Casciola-Rosen, L. A., Annhalt, G. J. & Rosen, A. DNA-dependent protein kinase is one of a subset of autoantigens specifically cleaved early during apoptosis. J. Exp. Med.182, 1625–1634 (1995). CASPubMed Google Scholar
Gallucci, S., Lolkema, M. & Matzinger, P. Natural adjuvants: endogenous activators of dendritic cells. Nature Med.5, 1249–1255 (1999). CASPubMed Google Scholar
Sauter, B. B. et al. Consequences of cell death: exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J. Exp. Med.191, 423–433 (2000). CASPubMedPubMed Central Google Scholar
Basu, S., Binder, R. J., Suto, R., Anderson, K. M. & Srivastava, P. K. Necrotic but not apoptotic cell death releases heat-shock proteins which deliver a partial maturation signal to dendritic cells and activate the NF-κB pathway. Int. Immunol.12, 1539–1546 (2000). CASPubMed Google Scholar
Fadok, V. A., Bratton, D. L., Guthrie, L. & Henson, P. M. Differential effects of apoptotic versus lysed cells on macrophage production of cytokines: role of proteases. J. Immunol.166, 6847–6854 (2001). CASPubMed Google Scholar
Rovere, P. et al. Bystander apoptosis triggers dendritic-cell maturation and antigen-presenting function. J. Immunol.161, 4467–4471 (1998). CASPubMed Google Scholar
Steinman, R. M., Turley, S., Mellman, I. & Inaba, K. The induction of tolerance by dendritic cells that have captured apoptotic cells. J. Exp. Med.191, 411–416 (2000). A fundamental position statement in the field. CASPubMedPubMed Central Google Scholar
Huang, F. -P. et al. A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T-cell areas of mesenteric lymph nodes. J. Exp. Med.191, 435–443 (2000). CASPubMedPubMed Central Google Scholar
Nakamura, K. et al. Unresponsiveness of peripheral T cells induced by apoptotic bodies derived from autologous T cells. Cell. Immunol.193, 147–154 (1999). CASPubMed Google Scholar
Albert, M. L., Jegathesan, M. & Darnell, R. B. Dendritic cells acquire antigen from apoptotic cells and cross-tolerize antigen-specific CD8+ T cells. Nature Immunol.2, 1010–1017 (2001). A crucial piece in the puzzle of how dendritic-cell handling of apoptotic cells might regulate immune responses. CAS Google Scholar
Ronchetti, A. et al. Immunogenicity of apoptotic cells in vivo: role of antigen load, antigen-presenting cells and cytokines. J. Immunol.163, 130–136 (1999). CASPubMed Google Scholar
Magnus, T., Chan, A., Grauer, O., Toyka, T. V. & Gold, R. Microglial phagocytosis of apoptotic inflammatory T cells leads to down-regulation of microglial immune activation. J. Immunol.167, 5004–5010 (2001). CASPubMed Google Scholar
Mevorach, D., Zhou, J. L., Song, X. & Elkon, K. B. Systemic exposure to irradiated apoptotic cells induces autoantibody production. J. Exp. Med.188, 387–392 (1998). CASPubMedPubMed Central Google Scholar
Licht, R., Jacobs, C. W. M., Tax, W. J. M. & Berden, J. H. M. No constitutive defect in phagocytosis of apoptotic cells by resident peritoneal macrophages from pre-morbid lupus mice. Lupus10, 102–107 (2001). CASPubMed Google Scholar
Herrmann, M. et al. Impaired phagocytosis of apoptotic-cell material by monocyte-derived macrophages from patients with systemic lupus erythematosus. Arthritis Rheum.41, 1241–1250 (1998). CASPubMed Google Scholar
Napirei, M. et al. Features of systemic lupus erythematosus in DNase1-deficient mice. Nature Genet.25, 177–181 (2000). CASPubMed Google Scholar
Bickerstaff, M. C. et al. Serum amyloid P component controls chromatin degradation and prevents antinuclear autoimmunity. Nature Med.5, 694–697 (1999). CASPubMed Google Scholar
Familian, A. et al. Chromatin-independent binding of serum amyloid P component to apoptotic cells. J. Immunol.167, 647–654 (2001). CASPubMed Google Scholar
Botto, M. et al. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nature Genet.19, 56–59 (1998). CASPubMed Google Scholar
Lu, Q. & Lemke, G. Homeostatic regulation of the immune system by receptor tyrosine kinases of the Tyro-3 family. Science293, 306–311 (2001). CASPubMed Google Scholar
Wilkinson, R. et al. Platelet endothelial-cell adhesion molecule-1 (PECAM-1/CD31) acts as a regulator of B-cell development, B-cell antigen receptor (BCR)-mediated activation and autoimmune disease. Blood100, 184–193 (2002). CASPubMed Google Scholar
Price, B. E. et al. Anti-phospholipid autoantibodies bind to apoptotic, but not viable, thymocytes in a β2-glycoprotein I-independent manner. J. Immunol.157, 2201–2208 (1996). CASPubMed Google Scholar
Manfredi, A. A. et al. Apoptotic-cell clearance in systemic lupus erythematosus. I. Opsonization by antiphospholipid antibodies. Arthritis Rheum.41, 205–214 ( 1998). CASPubMed Google Scholar
Miranda-Carus, M. -E. et al. Anti-SSA/Ro and anti-SSB/La autoantibodies bind the surface of apoptotic fetal cardiocytes and promote secretion of TNF-α by macrophages. J. Immunol.165, 5345–5351 (2000). CASPubMed Google Scholar
Cocca, B. A., Cline, A. M. & Radic, M. Z. Blebs and apoptotic bodies are B-cell autoantigens. J. Immunol.169, 159–166 (2002). CASPubMed Google Scholar
Rovere, P. et al. Dendritic-cell presentation of antigens from apoptotic cells in a proinflammatory context: role of opsonizing anti-β2-glycoprotein I antibodies. Arthritis Rheum.42, 1412–1420 (1999). CASPubMed Google Scholar
Harper, L., Ren, Y., Savill, J., Adu, D. & Savage, C. Antineutrophil cytoplasmic antibodies induce reactive oxygen-dependent dysregulation of primed neutrophil apoptosis and clearance by macrophages. Am. J. Pathol.157, 211–220 (2000). CASPubMedPubMed Central Google Scholar
Reddien, P. W. & Horvitz, H. R. CED-2/Crkll and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans. Nature Cell Biol.2, 131–135 (2000). CASPubMed Google Scholar
Wu, Y. C. & Horvitz, H. R. C. elegans phagocytosis and cell-migration protein CED-5 is similar to human DOCK180. Nature392, 501–504 (1998). CASPubMed Google Scholar
Albert, M. L., Kim, J. -I. & Birge, R. B. The αvβ5 integrin recruits the CrkII/Dock180/Rac1 molecular complex for phagocytosis of apoptotic cells. Nature Cell Biol.2, 899–905 (2000). CASPubMed Google Scholar
Leverrier, Y. & Ridley, A. J. Requirement for Rho GTPases and PI3-kinases during apoptotic-cell phagocytosis by macrophages. Curr. Biol.11, 195–199 (2000). Google Scholar
Tosello-Trampont, A. -C., Brugnera, E. & Ravichandran, K. S. Evidence for a conserved role for CrkII and Rac in engulfment of apoptotic cells. J. Biol. Chem.276, 13797–13802 (2000). Google Scholar
Leverrier, Y. et al. Cutting edge: the Wiskott-Aldrich syndrome protein is required for efficient phagocytosis of apoptotic cells. J. Immunol.166, 4831–4834 (2001). CASPubMed Google Scholar
Caron, E. & Hall, A. Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science282, 1717–1721 (1998). CASPubMed Google Scholar
Hart, S. P., Dougherty, G. J., Haslett, C. & Dransfield, I. CD44 regulates phagocytosis of apoptotic neutrophil granulocytes, but not apoptotic lymphocytes, by human macrophages. J. Immunol.159, 919–925 (1997). CASPubMed Google Scholar
Meagher, L. C., Cousin, J. M., Seckl, J. R. & Haslett, C. Opposing effects of glucocorticoids on the rate of apoptosis in neutrophilic and eosinophilic granulocytes. J. Immunol.156, 4422–4428 (1996). CASPubMed Google Scholar
Liu, Y. et al. Glucocorticoids promote non-phlogistic phagocytosis of apoptotic leukocytes. J. Immunol.162, 3639–3646 (1999). CASPubMed Google Scholar
Giles, K. M. et al. 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. J. Immunol.167, 976–986 (2001). CASPubMed Google Scholar
Godson, C. et al. Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages. J. Immunol.164, 1663–1667 (2000). CASPubMed Google Scholar
McMahon, B., Mitchell, S., Brady, H. R. & Godson, C. Lipoxins: revelations on resolution. Trends Pharmacol. Sci.22, 391–395 (2001). CASPubMed Google Scholar
Mitchell, S. et al. Lipoxins stimulate macrophage phagocytosis of apoptotic neutrophils in acute inflammation in vivo. J. Am. Soc. Nephrol. (in the press).