| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
British Medical Bulletin 53:491-508 (1997)
© 1997 The British Council
research-article |
Recognition and phagocytosis of cells undergoing apoptosis
Division of Renal & Inflammatory Disease, Department of Medicine, University Hospital Nottingham, UK
Prof John Savill, Division of Renal & Inflammatory Disease, Department of Medicine, University Hospital, Nottingham NG7 2UH, UK
Abstract
In vivo, the normal fate of cells undergoing apoptosis is recognition, uptake and degradation of the intact dying cell by phagocytes. Cell clearance by this mechanism is fast, efficient and injury-limiting, being mediated by macrophages and semi-professional phagocytes. Apoptotic cells are marked for disposal by mechanisms which remain poorly understood, although in some circumstances surface sugar changes and exposure of phosphatidylserine lead to recognition by uncharacterised phagocyte receptors. Furthermore, there is specific evidence in vitro for involvement of phagocyte receptors including the thrombospondin receptors
ß3 and CD36, scavenger receptors, the 61D3 antigen and the ABC1 transporter. It is conceivable that recognition mechanisms may be ordered in a hierarcht of back ups, each recognising cells at different stages of the death program. Nevertheless, a full understanding of this complexity will require definition of recognition mechanisms which operate in vivo in higher organisms.
![]()
CiteULike
Connotea
Del.icio.us What's this?
This article has been cited by other articles:
![]() |
E. Kim, A. T. Tolhurst, L. Y. Qin, X.-Y. Chen, M. Febbraio, and S. Cho CD36/Fatty Acid Translocase, An Inflammatory Mediator, Is Involved in Hyperlipidemia-Induced Exacerbation in Ischemic Brain Injury J. Neurosci., April 30, 2008; 28(18): 4661 - 4670. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Cui, E. Thorp, Y. Li, N. Wang, L. Yvan-Charvet, A. R. Tall, and I. Tabas Pivotal Advance: Macrophages become resistant to cholesterol-induced death after phagocytosis of apoptotic cells J. Leukoc. Biol., November 1, 2007; 82(5): 1040 - 1050. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. Tacke, F. Ginhoux, C. Jakubzick, N. van Rooijen, M. Merad, and G. J. Randolph Immature monocytes acquire antigens from other cells in the bone marrow and present them to T cells after maturing in the periphery J. Exp. Med., March 20, 2006; 203(3): 583 - 597. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. I. Finkelstein, J. Ruben, C. W. Koot, M. Hristova, and A. van der Vliet Regulation of constitutive neutrophil apoptosis by the {alpha},{beta}-unsaturated aldehydes acrolein and 4-hydroxynonenal Am J Physiol Lung Cell Mol Physiol, December 1, 2005; 289(6): L1019 - L1028. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. A. Kuznetsova, A. J. Day, D. J. Mahoney, M. S. Rugg, D. F. Mosher, and D. D. Roberts The N-terminal Module of Thrombospondin-1 Interacts with the Link Domain of TSG-6 and Enhances Its Covalent Association with the Heavy Chains of Inter-{alpha}-trypsin Inhibitor J. Biol. Chem., September 2, 2005; 280(35): 30899 - 30908. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. K. Rai, K. Tripathi, D. Sharma, and V. K. Shukla Apoptosis: A Basic Physiologic Process in Wound Healing International Journal of Lower Extremity Wounds, September 1, 2005; 4(3): 138 - 144. [Abstract] [PDF] |
||||
![]() |
P. Li, G. E. Garcia, Y. Xia, W. Wu, C. Gersch, P. W. Park, L. Truong, C. B. Wilson, R. Johnson, and L. Feng Blocking of Monocyte Chemoattractant Protein-1 during Tubulointerstitial Nephritis Resulted in Delayed Neutrophil Clearance Am. J. Pathol., September 1, 2005; 167(3): 637 - 649. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. M. Rhodes, P. Kopsombut, M. C. Bondurant, J. O. Price, and M. J. Koury Bcl-xL prevents apoptosis of late-stage erythroblasts but does not mediate the antiapoptotic effect of erythropoietin Blood, September 1, 2005; 106(5): 1857 - 1863. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. M. Schrijvers, G. R.Y. De Meyer, M. M. Kockx, A. G. Herman, and W. Martinet Phagocytosis of Apoptotic Cells by Macrophages Is Impaired in Atherosclerosis Arterioscler. Thromb. Vasc. Biol., June 1, 2005; 25(6): 1256 - 1261. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Wu, S. Singh, M.-M. Georgescu, and R. B. Birge A role for Mer tyrosine kinase in {alpha}v{beta}5 integrin-mediated phagocytosis of apoptotic cells J. Cell Sci., February 1, 2005; 118(3): 539 - 553. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Manaka, T. Kuraishi, A. Shiratsuchi, Y. Nakai, H. Higashida, P. Henson, and Y. Nakanishi Draper-mediated and Phosphatidylserine-independent Phagocytosis of Apoptotic Cells by Drosophila Hemocytes/Macrophages J. Biol. Chem., November 12, 2004; 279(46): 48466 - 48476. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. ALMEIDA, J. FERREIRA, and D. NEVES Macrophages of the Adrenal Cortex: A Morphological Study of the Effects of Aging and Dexamethasone Administration Ann. N.Y. Acad. Sci., June 1, 2004; 1019(1): 135 - 140. [Abstract] [Full Text] [PDF] |
||||
![]() |
Z. Dogusan, E. Montecino-Rodriguez, and K. Dorshkind Macrophages and Stromal Cells Phagocytose Apoptotic Bone Marrow-Derived B Lineage Cells J. Immunol., April 15, 2004; 172(8): 4717 - 4723. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Y. Tyurina, F. B. Serinkan, V. A. Tyurin, V. Kini, J. C. Yalowich, A. J. Schroit, B. Fadeel, and V. E. Kagan Lipid Antioxidant, Etoposide, Inhibits Phosphatidylserine Externalization and Macrophage Clearance of Apoptotic Cells by Preventing Phosphatidylserine Oxidation J. Biol. Chem., February 13, 2004; 279(7): 6056 - 6064. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Cartee, S. C. Maggio, R. Smith, H. M. Sankala, P. Dent, and S. Grant Protein Kinase C-dependent Activation of the Tumor Necrosis Factor Receptor-mediated Extrinsic Cell Death Pathway Underlies Enhanced Apoptosis in Human Myeloid Leukemia Cells Exposed to Bryostatin 1 and Flavopiridol Mol. Cancer Ther., January 1, 2003; 2(1): 83 - 93. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. J. Kaplan, E. E. Lewis, E. A. Shelden, E. Somers, R. Pavlic, W. J. McCune, and B. C. Richardson The Apoptotic Ligands TRAIL, TWEAK, and Fas Ligand Mediate Monocyte Death Induced by Autologous Lupus T Cells J. Immunol., November 15, 2002; 169(10): 6020 - 6029. [Abstract] [Full Text] [PDF] |
||||
![]() |
V. Mateo, E. J. Brown, G. Biron, M. Rubio, A. Fischer, F. L. Deist, and M. Sarfati Mechanisms of CD47-induced caspase-independent cell death in normal and leukemic cells: link between phosphatidylserine exposure and cytoskeleton organization Blood, September 26, 2002; 100(8): 2882 - 2890. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Kawasaki, A. Nakagawa, K. Nagaosa, A. Shiratsuchi, and Y. Nakanishi Phosphatidylserine Binding of Class B Scavenger Receptor Type I, a Phagocytosis Receptor of Testicular Sertoli Cells J. Biol. Chem., July 19, 2002; 277(30): 27559 - 27566. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Denda-Nagai, N. Kubota, M. Tsuiji, M. Kamata, and T. Irimura Macrophage C-type lectin on bone marrow-derived immature dendritic cells is involved in the internalization of glycosylated antigens Glycobiology, July 1, 2002; 12(7): 443 - 450. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Cartee, R. Smith, Y. Dai, M. Rahmani, R. Rosato, J. Almenara, P. Dent, and S. Grant Synergistic Induction of Apoptosis in Human Myeloid Leukemia Cells by Phorbol 12-Myristate 13-Acetate and Flavopiridol Proceeds via Activation of Both the Intrinsic and Tumor Necrosis Factor-Mediated Extrinsic Cell Death Pathways Mol. Pharmacol., June 1, 2002; 61(6): 1313 - 1321. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Watanabe, A. Shiratsuchi, K. Shimizu, T. Takizawa, and Y. Nakanishi Role of Phosphatidylserine Exposure and Sugar Chain Desialylation at the Surface of Influenza Virus-infected Cells in Efficient Phagocytosis by Macrophages J. Biol. Chem., May 10, 2002; 277(20): 18222 - 18228. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Ma, K. A. Reed, and J. M. Gallo Cells Designed to Deliver Anticancer Drugs by Apoptosis Cancer Res., March 1, 2002; 62(5): 1382 - 1387. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Igarashi, C. R. Brown, R. A. Byrum, Y. Nishimura, Y. Endo, R. J. Plishka, C. Buckler, A. Buckler-White, G. Miller, V. M. Hirsch, et al. Rapid and Irreversible CD4+ T-Cell Depletion Induced by the Highly Pathogenic Simian/Human Immunodeficiency Virus SHIVDH12R Is Systemic and Synchronous J. Virol., January 1, 2002; 76(1): 379 - 391. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. A. Ogden, A. deCathelineau, P. R. Hoffmann, D. Bratton, B. Ghebrehiwet, V. A. Fadok, and P. M. Henson C1q and Mannose Binding Lectin Engagement of Cell Surface Calreticulin and CD91 Initiates Macropinocytosis and Uptake of Apoptotic Cells J. Exp. Med., September 17, 2001; 194(6): 781 - 796. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Li, D. F. Carpio, Y. Zheng, P. Bruzzo, V. Singh, F. Ouaaz, R. M. Medzhitov, and A. A. Beg An Essential Role of the NF-{{kappa}}B/Toll-Like Receptor Pathway in Induction of Inflammatory and Tissue-Repair Gene Expression by Necrotic Cells J. Immunol., June 15, 2001; 166(12): 7128 - 7135. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. T. Finegood, M. D. McArthur, D. Kojwang, M. J. Thomas, B. G. Topp, T. Leonard, and R. E. Buckingham {beta}-Cell Mass Dynamics in Zucker Diabetic Fatty Rats: Rosiglitazone Prevents the Rise in Net Cell Death Diabetes, May 1, 2001; 50(5): 1021 - 1029. [Abstract] [Full Text] |
||||
![]() |
L. E. L. Perkins and D. E. Swayne Pathobiology of A/Chicken/Hong Kong/220/97 (H5N1) Avian Influenza Virus in Seven Gallinaceous Species Vet. Pathol., March 1, 2001; 38(2): 149 - 164. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. R. Goth and R. S. Stephens Rapid, Transient Phosphatidylserine Externalization Induced in Host Cells by Infection with Chlamydia spp. Infect. Immun., February 1, 2001; 69(2): 1109 - 1119. [Abstract] [Full Text] [PDF] |
||||
![]() |
R Licht, C W. Jacobs, W J. Tax, and J H. Berden No constitutive defect in phagocytosis of apoptotic cells by resident peritoneal macrophages from pre-morbid lupus mice Lupus, February 1, 2001; 10(2): 102 - 107. [Abstract] [PDF] |
||||
![]() |
H. C McGill Jr, C A. McMahan, E. E Herderick, G. T Malcom, R. E Tracy, and J. P Strong Origin of atherosclerosis in childhood and adolescence Am. J. Clinical Nutrition, November 1, 2000; 72 (5): 1307S - 1315S. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Shiratsuchi, M. Kaido, T. Takizawa, and Y. Nakanishi Phosphatidylserine-Mediated Phagocytosis of Influenza A Virus-Infected Cells by Mouse Peritoneal Macrophages J. Virol., October 1, 2000; 74(19): 9240 - 9244. [Abstract] [Full Text] |
||||
![]() |
A. C. Chin, W. D. Lee, K. A. Murrin, D. W. Morck, J. K. Merrill, P. Dick, and A. G. Buret Tilmicosin Induces Apoptosis in Bovine Peripheral Neutrophils in the Presence or in the Absence of Pasteurella haemolytica and Promotes Neutrophil Phagocytosis by Macrophages Antimicrob. Agents Chemother., September 1, 2000; 44(9): 2465 - 2470. [Abstract] [Full Text] |
||||
![]() |
M. Li and A. A. Beg Induction of Necrotic-Like Cell Death by Tumor Necrosis Factor Alpha and Caspase Inhibitors: Novel Mechanism for Killing Virus-Infected Cells J. Virol., August 15, 2000; 74(16): 7470 - 7477. [Abstract] [Full Text] |
||||
![]() |
V. Terpstra, E. S. van Amersfoort, A. G. van Velzen, J. Kuiper, and T. J. C. van Berkel Hepatic and Extrahepatic Scavenger Receptors : Function in Relation to Disease Arterioscler. Thromb. Vasc. Biol., August 1, 2000; 20(8): 1860 - 1872. [Full Text] [PDF] |
||||
![]() |
P. J. Delves and I. M. Roitt The Immune System- First of Two Parts N. Engl. J. Med., July 6, 2000; 343(1): 37 - 49. [Full Text] [PDF] |
||||
![]() |
E. Shacter, J. A. Williams, R. M. Hinson, S. Senturker, and Y.-j. Lee Oxidative stress interferes with cancer chemotherapy: inhibition of lymphoma cell apoptosis and phagocytosis Blood, July 1, 2000; 96(1): 307 - 313. [Abstract] [Full Text] [PDF] |
||||
![]() |
U. A. Hirt, F. Gantner, and M. Leist Phagocytosis of Nonapoptotic Cells Dying by Caspase- Independent Mechanisms J. Immunol., June 15, 2000; 164(12): 6520 - 6529. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. Shiraishi, L. M. Curtis, L. Truong, K. Poss, G. A. Visner, K. Madsen, H. S. Nick, and A. Agarwal Heme oxygenase-1 gene ablation or expression modulates cisplatin-induced renal tubular apoptosis Am J Physiol Renal Physiol, May 1, 2000; 278(5): F726 - F736. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. Platt, H. Suzuki, T. Kodama, and S. Gordon Apoptotic Thymocyte Clearance in Scavenger Receptor Class A-Deficient Mice Is Apparently Normal J. Immunol., May 1, 2000; 164(9): 4861 - 4867. [Abstract] [Full Text] [PDF] |
||||
![]() |
I. Fujimoto, J. Pan, T. Takizawa, and Y. Nakanishi Virus Clearance through Apoptosis-Dependent Phagocytosis of Influenza A Virus-Infected Cells by Macrophages J. Virol., April 1, 2000; 74(7): 3399 - 3403. [Abstract] [Full Text] |
||||
![]() |
S. Ge, S. A. Rempel, G. Divine, and T. Mikkelsen Carboxyamido-triazole Induces Apoptosis in Bovine Aortic Endothelial and Human Glioma Cells Clin. Cancer Res., April 1, 2000; 6(4): 1248 - 1254. [Abstract] [Full Text] |
||||
![]() |
H. P. Su, E. Brugnera, W. Van Criekinge, E. Smits, M. Hengartner, T. Bogaert, and K. S. Ravichandran Identification and Characterization of a Dimerization Domain in CED-6, an Adapter Protein Involved in Engulfment of Apoptotic Cells J. Biol. Chem., March 24, 2000; 275(13): 9542 - 9549. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. Sauter, M. L. Albert, L. Francisco, M. Larsson, S. Somersan, and N. Bhardwaj 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., February 7, 2000; 191(3): 423 - 434. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. M Kockx and A. G Herman Apoptosis in atherosclerosis: beneficial or detrimental? Cardiovasc Res, February 1, 2000; 45(3): 736 - 746. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. J. McCarthy and M. Bennett The regulation of vascular smooth muscle cell apoptosis Cardiovasc Res, February 1, 2000; 45(3): 747 - 755. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Salmon and C. Gordon The role of apoptosis in systemic lupus erythematosus Rheumatology, December 1, 1999; 38(12): 1177 - 1183. [Full Text] [PDF] |
||||
![]() |
I. Reiter, B. Krammer, and G. Schwamberger Cutting Edge: Differential Effect of Apoptotic Versus Necrotic Tumor Cells on Macrophage Antitumor Activities J. Immunol., August 15, 1999; 163(4): 1730 - 1732. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Brochu, B. Rioux-Masse, J. Roy, D.-C. Roy, and C. Perreault Massive Activation-Induced Cell Death of Alloreactive T Cells With Apoptosis of Bystander Postthymic T Cells Prevents Immune Reconstitution in Mice With Graft-Versus-Host Disease Blood, July 15, 1999; 94(2): 390 - 400. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y.-j. Lee and E. Shacter Oxidative Stress Inhibits Apoptosis in Human Lymphoma Cells J. Biol. Chem., July 9, 1999; 274(28): 19792 - 19798. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. C. Franc, P. Heitzler, R. Alan B. , Ezekowitz, and K. White Requirement for Croquemort in Phagocytosis of Apoptotic Cells in Drosophila Science, June 18, 1999; 284(5422): 1991 - 1994. [Abstract] [Full Text] |
||||
![]() |
M.-K. Chang, C. Bergmark, A. Laurila, S. Horkko, K.-H. Han, P. Friedman, E. A. Dennis, and J. L. Witztum 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 PNAS, May 25, 1999; 96(11): 6353 - 6358. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Shiratsuchi, Y. Kawasaki, M. Ikemoto, H. Arai, and Y. Nakanishi Role of Class B Scavenger Receptor Type I in Phagocytosis of Apoptotic Rat Spermatogenic Cells by Sertoli Cells J. Biol. Chem., February 26, 1999; 274(9): 5901 - 5908. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. L. Albert, S.F. A. Pearce, L. M. Francisco, B. Sauter, P. Roy, R. L. Silverstein, and N. Bhardwaj Immature Dendritic Cells Phagocytose Apoptotic Cells via alpha vbeta 5 and CD36, and Cross-present Antigens to Cytotoxic T Lymphocytes J. Exp. Med., October 5, 1998; 188(7): 1359 - 1368. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. C. Urban, N. Willcox, and D. J. Roberts A role for CD36 in the regulation of dendritic cell function PNAS, July 17, 2001; 98(15): 8750 - 8755. [Abstract] [Full Text] [PDF] |
||||





























