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A blast from the past: clearance of apoptotic cells regulates immune responses

Savill, John, Dransfield, Ian, Gregory, Chris, Haslett, Chris·2002·Nature Reviews Immunology

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  1. Kerr, J. F. R., Wyllie, A. H. & Currie, A. R. Apoptosis: a basic biological phenomenon with widespread implications in tissue kinetics. Br. J. Cancer 26, 239–257 (1972). The seminal description of apoptosis. · DOI · Paper page
  2. Krammer, P. H. CD95's deadly mission in the immune system. Nature 407, 789–795 (2000). · DOI · Paper page
  3. Savill, J. & Fadok, V. Corpse clearance defines the meaning of cell death. Nature 407, 784–788 (2000). · DOI · Paper page
  4. 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). · DOI · Paper page
  5. Albert, M. L., Sauter, B. & Bhardwaj, N. Dendritic cells acquire antigen from apoptotic cells and induce class-I-restricted CTLs. Nature 392, 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. · DOI · Paper page
  6. Savill, J. S., Dransfield, I., Hogg, N. & Haslett, C. Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature 343, 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. · DOI · Paper page
  7. 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). · DOI
  8. 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). · DOI
  9. 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). · DOI · Paper page
  10. 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). · DOI · Paper page
  11. 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). · DOI · Paper page
  12. 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). · DOI · Paper page
  13. 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). · DOI
  14. 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 cells in vitro and in vivo (see also reference 37). · DOI · Paper page
  15. Pickering, M. C. et al. Ultraviolet radiation-induced keratinocyte apoptosis in C1q-deficient mice. J. Invest. Dermatol. 117, 52–58 (2001). · DOI
  16. 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). · DOI · Paper page
  17. Devitt, A. et al. Human CD14 mediates recognition and phagocytosis of apoptotic cells. Nature 392, 505–509 (1998). A pioneering report implicating recognition mechanisms of innate immunity in the clearance of dying cells. · DOI · Paper page
  18. Savill, J. Apoptosis: phagocytic docking without shocking. Nature 392, 442–443 (1998). · DOI
  19. 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). · DOI · Paper page
  20. 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). · DOI · Paper page
  21. 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'. · DOI · Paper page
  22. 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. USA 92, 1396–1400 (1995). · DOI · Paper page
  23. 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. USA 96, 6353–6358 (1999). · DOI · Paper page
  24. 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). · DOI · Paper page
  25. 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). · DOI · Paper page
  26. 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. USA 95, 9535–9540 (1998). · DOI · Paper page
  27. 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. USA 93, 12456–12460 (1996). · DOI · Paper page
  28. 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). · DOI
  29. 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). · DOI · Paper page
  30. Duvall, E., Wyllie, A. H. & Morris, R. G. Macrophage recognition of cells undergoing programmed cell death. Immunology 56, 351–358 (1985).
  31. 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). · DOI · Paper page
  32. 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). · DOI · Paper page
  33. Fadok, V. A. et al. A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405, 85–90 (2000). References 33 and 34 describe the discovery of the first 'eat-me' flag on dying cells. · DOI · Paper page
  34. 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). · DOI · Paper page
  35. 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). · DOI · Paper page
  36. 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). · DOI · Paper page
  37. 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). · DOI
  38. 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). · DOI
  39. 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). · DOI
  40. 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). · DOI
  41. 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). · DOI · Paper page
  42. 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). · DOI
  43. Chimini, G. Apoptosis: repulsive encounters. Nature 418, 139–142 (2002). · DOI
  44. Reddien, P. W., Cameron, S. & Horvitz, H. R. Phagocytosis promotes programmed cell death in C. elegans. Nature 412, 198–202 (2001). · DOI · Paper page
  45. Hoeppner, D. J., Hentgartner, M. O. & Schnabel, R. Engulfment genes cooperate with ced-3 to promote cell death in Caenorhabditis elegans. Nature 412, 202–206 (2001). · DOI · Paper page
  46. Brown, S. B. & Savill, J. Phagocytosis triggers macrophage release of Fas-ligand and induces apoptosis of bystander leucocytes. J. Immunol. 162, 480–485 (1999). · DOI · Paper page
  47. 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. · DOI · Paper page
  48. 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. · DOI · Paper page
  49. 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).
  50. 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). · DOI · Paper page
  51. Marth, T. & Kelsall, B. L. Regulation of interleukin-12 by complement receptor 3 signalling. J. Exp. Med. 185, 1987–1995 (1997). · DOI · Paper page
  52. Voll, R. E., Herrmann, M., Roth, E. A., Stach, C. & Kalden, J. R. Immunosuppressive effects of apoptotic cells. Nature 390, 350–351 (1997). The title of this paper highlights a key discovery in the field of apoptosis. · DOI · Paper page
  53. 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). · DOI · Paper page
  54. 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). · DOI
  55. 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). · DOI · Paper page
  56. 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. Cell 12, 919–930 (2001). · DOI · Paper page
  57. 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 first in vivo demonstration that the clearance of apoptotic cells can suppress inflammatory responses. · DOI · Paper page
  58. Duffield, J. A. et al. Activated macrophages direct apoptosis and suppress mitosis of mesangial cells. J. Immunol. 164, 2110–2119 (2000). · DOI
  59. Reiter, I., Krammer, B. & Schwamberger, G. Differential effect of apoptotic versus necrotic tumor cells on macrophage antitumor activities. J. Immunol. 163, 1730–1732 (1999). · DOI
  60. 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). · DOI
  61. Freire-de-Lima, C. G. et al. Uptake of apoptotic cells drives the growth of a pathogenic trypanosome in macrophages. Nature 403, 199–203 (2000). · DOI · Paper page
  62. 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). · DOI · Paper page
  63. Chen, W. -J., Frank, M. E., Jin, W. & Wahl, S. M. TGF-β released by apoptotic T cells contributes to an immunosuppressive milieu. Immunity 14, 715–725 (2001). · DOI · Paper page
  64. 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? Oncogene 20, 7085–7095 (2001). · DOI · Paper page
  65. 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). · DOI
  66. Basu, S., Binder, R. J., Ramalingam, T. & Srivastava, P. K. CD91 is a common receptor for heat-shock proteins pg96, hsp70 and calreticulin. Immunity 14, 303–313 (2001). · DOI · Paper page
  67. 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). · DOI · Paper page
  68. Sansonetti, P. J. et al. Caspase-1 activation of IL-1β and IL-8 are essential for Shigella flexneri-induced inflammation. Immunity 12, 581–590 (2000). · DOI · Paper page
  69. 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). · DOI
  70. Horino, K. et al. A monocyte chemotactic factor S19 ribosomal protein dimer in phagocytic clearance of apoptotic cells. Lab. Invest. 78, 603–617 (1998).
  71. 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. · DOI · Paper page
  72. 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). · DOI · Paper page
  73. Urban, B. C., Willcox, N. & Roberts, D. J. A role for CD36 in the regulation of dendritic-cell function. Proc. Natl Acad. Sci. USA 98, 8750–8755 (2001). · DOI · Paper page
  74. 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). · DOI · Paper page
  75. Urban, B. C. et al. Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature 400, 73–77 (1999). · DOI · Paper page
  76. 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. · DOI · Paper page
  77. 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). · DOI · Paper page
  78. 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). · DOI
  79. 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). · DOI
  80. 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). · DOI · Paper page
  81. 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). · DOI · Paper page
  82. Gallucci, S., Lolkema, M. & Matzinger, P. Natural adjuvants: endogenous activators of dendritic cells. Nature Med. 5, 1249–1255 (1999). · DOI · Paper page
  83. 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). · DOI · Paper page
  84. 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). · DOI · Paper page
  85. 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). · DOI · Paper page
  86. Rovere, P. et al. Bystander apoptosis triggers dendritic-cell maturation and antigen-presenting function. J. Immunol. 161, 4467–4471 (1998). · DOI · Paper page
  87. 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. · DOI · Paper page
  88. 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). · DOI · Paper page
  89. Nakamura, K. et al. Unresponsiveness of peripheral T cells induced by apoptotic bodies derived from autologous T cells. Cell. Immunol. 193, 147–154 (1999). · doi:10.1006/cimm.1999.1459
  90. 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. · DOI · Paper page
  91. 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). · DOI · Paper page
  92. 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). · DOI
  93. 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). · DOI · Paper page
  94. 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. Lupus 10, 102–107 (2001). · doi:10.1191/096120301672276558
  95. 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). · DOI · Paper page
  96. Napirei, M. et al. Features of systemic lupus erythematosus in DNase1-deficient mice. Nature Genet. 25, 177–181 (2000). · DOI · Paper page
  97. Bickerstaff, M. C. et al. Serum amyloid P component controls chromatin degradation and prevents antinuclear autoimmunity. Nature Med. 5, 694–697 (1999). · DOI · Paper page
  98. Familian, A. et al. Chromatin-independent binding of serum amyloid P component to apoptotic cells. J. Immunol. 167, 647–654 (2001). · DOI
  99. Botto, M. et al. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nature Genet. 19, 56–59 (1998). · DOI · Paper page
  100. Lu, Q. & Lemke, G. Homeostatic regulation of the immune system by receptor tyrosine kinases of the Tyro-3 family. Science 293, 306–311 (2001). · DOI · Paper page
  101. 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. Blood 100, 184–193 (2002). · DOI
  102. 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). · DOI · Paper page
  103. Manfredi, A. A. et al. Apoptotic-cell clearance in systemic lupus erythematosus. I. Opsonization by antiphospholipid antibodies. Arthritis Rheum. 41, 205–214 ( 1998). · DOI · Paper page
  104. 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). · DOI · Paper page
  105. Cocca, B. A., Cline, A. M. & Radic, M. Z. Blebs and apoptotic bodies are B-cell autoantigens. J. Immunol. 169, 159–166 (2002). · DOI
  106. 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). · DOI
  107. 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). · DOI
  108. 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). · DOI · Paper page
  109. Wu, Y. C. & Horvitz, H. R. C. elegans phagocytosis and cell-migration protein CED-5 is similar to human DOCK180. Nature 392, 501–504 (1998). · DOI · Paper page
  110. 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). · DOI · Paper page
  111. Leverrier, Y. & Ridley, A. J. Requirement for Rho GTPases and PI3-kinases during apoptotic-cell phagocytosis by macrophages. Curr. Biol. 11, 195–199 (2000). · DOI
  112. 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). · DOI
  113. 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). · DOI
  114. 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). · DOI
  115. 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). · DOI · Paper page
  116. Liu, Y. et al. Glucocorticoids promote non-phlogistic phagocytosis of apoptotic leukocytes. J. Immunol. 162, 3639–3646 (1999). · DOI · Paper page
  117. 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). · DOI · Paper page
  118. Godson, C. et al. Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages. J. Immunol. 164, 1663–1667 (2000). · DOI · Paper page
  119. McMahon, B., Mitchell, S., Brady, H. R. & Godson, C. Lipoxins: revelations on resolution. Trends Pharmacol. Sci. 22, 391–395 (2001). · DOI
  120. Mitchell, S. et al. Lipoxins stimulate macrophage phagocytosis of apoptotic neutrophils in acute inflammation in vivo. J. Am. Soc. Nephrol. (in the press).

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Metadata

Authors
Savill, J., Dransfield, I., Gregory, C., & Haslett, C.
Venue
Nature Reviews Immunology
Published
2002-12
Volume
2
Issue
12
Pages
965-975
ISSN
  • 1474-1733 (ISSN-L)
  • 1474-1741
OpenAlex
W2091493364
Cited by
1,574
References
6
FWCI
3.43
Type
journal article
Language
en
Open access
closed
Licence
www.springer.com/tdm (tdm)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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How to cite

Cite CoChat for the checks on this page, and the paper for its own findings.

This page
CoChat. (2026). Citation check: A blast from the past: clearance of apoptotic cells regulates immune responses. https://app.cochat.ai/papers/10.1038/nri957
The paper
Savill, J., Dransfield, I., Gregory, C., & Haslett, C. (2002). A blast from the past: clearance of apoptotic cells regulates immune responses. Nature Reviews Immunology. https://doi.org/10.1038/nri957

Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.