Phagoptosis - Cell death by phagocytosis - Plays central roles in physiology, host defense and pathology

Current Molecular Medicine

Volumn 15, Issue 9, 2015, Pages

  Brown, G C ^a   Vilalta, A ^a   Fricker, M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Apoptosis; Cell death; Clearance; Inflammation; Phagocytosis; Turnover

Indexed keywords

ARTICLE; CELL DEATH; DENDRITIC CELL; HOST RESISTANCE; HUMAN; IMMUNITY; NONHUMAN; PATHOLOGY; PHAGOCYTOSIS; SENESCENCE; SIGNAL TRANSDUCTION; ANIMAL; APOPTOSIS; HOST PATHOGEN INTERACTION; METABOLISM; PHYSIOLOGY;

OPSONIN;

ANIMALS; APOPTOSIS; CELL DEATH; HOST-PATHOGEN INTERACTIONS; HUMANS; OPSONIN PROTEINS; PHAGOCYTOSIS; SIGNAL TRANSDUCTION;

EID: 84980584691     PISSN: 15665240     EISSN: 18755666     Source Type: Journal    
DOI: 10.2174/156652401509151105130628     Document Type: Article

References (95)

1. Brown GC, Neher JJ. Eaten alive! Cell death by primary phagocytosis: ‘phagoptosis’. Trends Biochem Sci 2012; 37: 325-32.
2. Brown GC, Neher JJ. Microglial phagocytosis of live neurons. Nat Rev Neurosci 2014; 15: 209-16.
3. Hoeppner DJ, Hengartner MO, Schnabel R. Engulfment genes cooperate with ced-3 to promote cell death in Caenorhabditis elegans. Nature 2001; 412: 202-6.
4. Reddien P, Cameron S, Horvitz HR. Phagocytosis promotes programmed cell death in C. elegans. Nature 2001; 412: 198-202.
5. Galvin BD, Kim S, Horvitz HR. Caenorhabditis elegans genes required for the engulfment of apoptotic corpses function in the cytotoxic cell deaths induced by mutations in lin-24 and lin-33. Genetics 2008; 179: 403-17.
6. Neukomm LJ, Frei AP, Cabello J, et al. Loss of the RhoGAP SRGP-1 promotes the clearance of dead and injured cells in Caenorhabditis elegans. Nat Cell Biol 2011; 13: 79-86.
7. Kao AW, Eisenhut RJ, Martens LH, et al. A neurodegenerative disease mutation that accelerates the clearance of apoptotic cells. Proc Natl Acad Sci U S A 2011; 108: 4441-6.
8. Metchnikoff E. The struggle for existence between parts of the animal organism. In: The Evolutionary Biology Papers of Elie Metchnikoff; Gourko H, et al., Eds., Dordrecht: Springer Science 2000.
9. Fadok VA, de Cathelineau A, Daleke DL, Henson PM, Bratton DL. Loss of phospholipid asymmetry and surface exposure of phosphatidylserine is required for phagocytosis of apoptotic cells by macrophages and fibroblasts. J Biol Chem 2001; 276: 1071-7.
10. Ravichandran KS. Beginnings of a good apoptotic meal: the find-me and eat-me signaling pathways. Immunity 2011; 35: 445-55.
11. Levano K, Punia V, Raghunath M, et al. Atp8a1 deficiency is associated with phosphatidylserine externalization in hippocampus and delayed hippocampus-dependent learning. J Neurochem 2012; 120, 302-13.
12. Segawa K, Kurata S, Yanagihashi Y, Brummelkamp TR, Matsuda F, Nagata S. Caspase-mediated cleavage of phospholipid flippase for apoptotic phosphatidylserine exposure. Science 2014; 344: 1164-8.
13. Tyurina YY, Basova LV, Konduru NV, et al. Nitrosative stress inhibits the aminophospholipid translocase resulting in phosphatidylserine externalization and macrophage engulfment: implications for the resolution of inflammation. J Biol Chem 2007; 282: 8498-509.
14. Suzuki J, Fujii T, Imao T, Ishihara K, Kuba H, Nagata S. Calcium-dependent phospholipid scramblase activity of TMEM16 protein family members. J Biol Chem 2013; 288: 13305-16.
15. Suzuki J, Denning DP, Imanishi E, Horvitz HR, Nagata S. Xk-related protein 8 and CED-8 promote phosphatidylserine exposure in apoptotic cells. Science 2013; 341: 403-6.
16. Callahan MK, Surprenant A, Marelli-Berg FM, et al. Phosphatidylserine expression and phagocytosis of apoptotic thymocytes during differentiation of monocytic cells. J Leukoc Biol 2003; 74: 846-56.
17. Elliott JI, Surprenant A, Marelli-Berg FM, et al. Membrane phosphatidylserine distribution as a nonapoptotic signaling mechanism in lymphocytes. Nat Cell Biol 2005; 7: 808-16.
18. Fischer K, Voelkl S, Berger J, Andreesen R, Pomorski T, Mackensen A. Antigen recognition induces phosphatidylserine exposure on the cell surface of human CD8+ T cells. Blood 2006; 108: 4094-101.
19. Balasubramanian K, Mirnikjoo B, Schroit AJ. Regulated externalization of phosphatidylserine at the cell surface: implications for apoptosis. J Biol Chem 2007; 282: 18357-64.
20. Jitkaew S, Witasp E, Zhang S, Kagan VE, Fadeel B. Induction of caspase- and reactive oxygen species-independent phosphatidylserine externalization in primary human neutrophils: role in macrophage recognition and engulfment. J Leukoc Biol 2009; 85: 427-37.
21. Frasch SC, Berry KZ, Fernandez-Boyanapalli R, et al. NADPH oxidase-dependent generation of lysophosphatidylserine enhances clearance of activated and dying neutrophils via G2A. J Biol Chem 2008; 283: 33736-49.
22. Frasch SC, Fernandez-Boyanapalli RF, Berry KA, et al. Neutrophils regulate tissue Neutrophilia in inflammation via the oxidant-modified lipid lysophosphatidylserine. J Biol Chem 2013; 288: 4583-93.
23. Park D, Tosello-Trampont AC, Elliott MR, et al. BAI1 is an engulfment receptor for apoptotic cells upstream of the ELMO/Dock180/Rac module. Nature 2007; 450: 430-4.
24. Segawa K, Suzuki J, Nagata S. Constitutive exposure of phosphatidylserine on viable cells. Proc Natl Acad Sci U S A 2011; 108: 19246-51.
25. Borisenko GG, Iverson SL, Ahlberg S, Kagan VE, Fadeel B. Milk fat globule epidermal growth factor 8 (MFG-E8) binds to oxidized phosphatidylserine: implications for macrophage clearance of apoptotic cells. Cell Death Differ 2004; 11: 943-5.
26. Dalli J, Jones CP, Cavalcanti DM, Farsky SH, Perretti M, Rankin SM. Annexin A1 regulates neutrophil clearance by macrophages in the mouse bone marrow. FASEB J 2011; 26: 387-96.
27. Albacker LA, Karisola P, Chang YJ, et al. TIM-4, a receptor for phosphatidylserine, controls adaptive immunity by regulating the removal of antigen-specific T cells. J Immunol 2010; 185: 6839-49.
28. Gardai SJ, McPhillips KA, Frasch SC, et al. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 2005; 123: 321-34.
29. Panaretakis T, Kepp O, Brockmeier U, et al. Mechanisms of pre-apoptotic calreticulin exposure in immunogenic cell death. EMBO J 2009; 28: 578-90.
30. Ghiran I, Klickstein LB, Nicholson-Weller A. Calreticulin is at the surface of circulating neutrophils and uses CD59 as an adaptor molecule. J Biol Chem 2003; 278: 21024-31.
31. Gül N, Babes L, Siegmund K, et al. Macrophages eliminate circulating tumor cells after monoclonal antibody therapy. J Clin Invest 2014; 124, 812-23.
32. Païdassi H, Tacnet-Delorme P, Verneret M, et al. Investigations on the C1q-calreticulin-phosphatidylserine interactions yield new insights into apoptotic cell recognition. J Mol Biol 2011; 408: 277-90.
33. Oldenborg PA, Zheleznyak A, Fang YF, Lagenaur CF, Gresham HD, Lindberg FP. Role of CD47 as a marker of self on red blood cells. Science 2000; 288: 2051-4.
34. Olsson M, Oldenborg PA. CD47 on experimentally senescent murine RBCs inhibits phagocytosis following Fcγ receptor-mediated but not scavenger receptor-mediated recognition by macrophages. Blood 2008; 112: 4259-67.
35. Khandelwal S, van Rooijen N, Saxena RK. Reduced expression of CD47 during murine red blood cell (RBC) senescence and its role in RBC clearance from the circulation. Transfusion 2007; 47: 1725-32.
36. Burger P, Hilarius-Stokman P, de Korte D, van den Berg TK, van Bruggen R. CD47 functions as a molecular switch for erythrocyte phagocytosis. Blood 2012; 119: 5512-21.
37. Jaiswal S, Jamieson CH, Pang WW, et al. CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell 2009; 138: 271-85.
38. Jaiswal S, Jamieson CH, Pang WW, et al. CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell 2009; 138: 271-85.
39. Ide K, Wang H, Tahara H, et al. Role for CD47-SIRPalpha signaling in xenograft rejection by macrophages. Proc Natl Acad Sci U S A 2007; 104: 5062-6.
40. Kang TW, Yevsa T, Woller N, et al. Senescence surveillance of pre-malignant hepatocytes limits liver cancer development. Nature 2011; 479: 547-51.
41. Majeti R, Chao MP, Alizadeh AA, et al. CD47 is an adverse prognostic factor and therapeutic antibody target on human acute myeloid leukemia stem cells. Cell 2009; 138: 286-99.
42. Chao MP, Alizadeh AA, Tang C, et al. Therapeutic antibody targeting of CD47 eliminates human acute lymphoblastic leukemia. Cancer Res 2011; 71: 1374-84.
43. Linnartz B, Kopatz J, Tenner AJ, Neumann H. Sialic Acid on the neuronal glycocalyx prevents complement c1 binding and complement receptor-3-mediated removal by microglia. J Neurosci 2012; 32: 946-52.
44. Meesmann HM, Fehr EM, Kierschke S, et al. Decrease of sialic acid residues as an eat-me signal on the surface of apoptotic lymphocytes. J Cell Sci 2010; 123: 3347-56.
45. Wang Y, Neumann H. Alleviation of neurotoxicity by microglial human Siglec-11. J Neurosci 2010; 30: 3482-8.
46. de Back DZ, Kostova EB, van Kraaij M, van den Berg TK, van Bruggen R. Of macrophages and red blood cells; a complex love story. Front Physiol 2014; 30: 5-9.
47. Lutz HU, Bogdanova A. Mechanisms tagging senescent red blood cells for clearance in healthy humans. Front Physiol 2013; 4: 387.
48. Lee SJ, Park SY, Jung MY, Bae SM, Kim IS. Mechanism for phosphatidylserine-dependent erythrophagocytosis in mouse liver. Blood 2011; 117: 5215-23.
49. Casanova-Acebes M, Pitaval C, Weiss LA, et al. Rhythmic Modulation of the Hematopoietic Niche through Neutrophil Clearance. Cell 2013; 153: 1025-35.
50. Lagasse E, Weissman IL. Bcl-2 inhibits apoptosis of neutrophils but not their engulfment by macrophages. J Exp Med 1994; 179: 1047-52.
51. Weinmann P, Scharffetter-Kochanek K, Forlow SB, Peters T, Walzog B. A role for apoptosis in the control of neutrophil homeostasis in the circulation: insights from CD18-deficient mice. Blood 2003; 101: 739-46.
52. Hong C, Kidani Y, A-Gonzalez N, et al. Coordinate regulation of neutrophil homeostasis by liver X receptors in mice. J Clin Invest 2012; 122: 337-47.
53. Park YJ, Liu G, Lorne EF, et al. PAI-1 inhibits neutrophil efferocytosis. Proc Natl Acad Sci U S A 2008; 105: 11784-9.
54. Xie R, Gao C, Li W, et al. Phagocytosis by macrophages and endothelial cells inhibits procoagulant and fibrinolytic activity of acute promyelocytic leukemia cells. Blood 2012; 119: 2325-34.
55. Olsson M, Bruhns P, Frazier WA, Ravetch JV, Oldenborg PA. Platelet homeostasis is regulated by platelet expression of CD47 under normal conditions and in passive immune thrombocytopenia. Blood 2005; 105: 3577-82.
56. Maugeri N, Rovere-Querini P, Evangelista V, et al. Neutrophils phagocytise activated platelets in vivo: a phosphatidylserine, P-selectin, and β2 integrin-dependent cell clearance program. Blood 2009; 113: 5254-65.
57. Stowell SR, Karmakar S, Arthur CM, et al. Galectin-1 induces reversible phosphatidylserine exposure at the plasma membrane. Mol Biol Cell 2009; 20: 1408-18.
58. Neumann J, Sauerzweig S, Rönicke R, et al. Microglia Cells Protect Neurons by Direct Engulfment of Invading Neutrophil Granulocytes: A New Mechanism of CNS Immune Privilege. J Neurosci 2008; 28: 5965-75.
59. Cunningham CL, Martinez-Cerdeno V, Noctor SC. Microglia Regulate the Number of Neural Precursor Cells in the Developing Cerebral Cortex. J Neurosci 2013; 33: 4216-33.
60. Kuriyama T, Takenaka K, Kohno K, et al. Engulfment of hematopoietic stem cells caused by down-regulation of CD47 is critical in the pathogenesis of hemophagocytic lymphohistiocytosis. Blood 2012; 120: 4058-67.
61. Muñoz-Espín D, Cañamero M, Maraver A, et al. Programmed cell senescence during mammalian embryonic development. Cell 2013; 155: 1104-18.
62. Lovewell RR, Patankar YR, Berwin B. Mechanisms of phagocytosis and host clearance of Pseudomonas aeruginosa. Am J Physiol Lung Cell Mol Physiol 2014; 306: L591-603.
63. Mayadas TN, Cullere X, Lowell CA. The multifaceted functions of neutrophils. Annu Rev Pathol 2014; 9: 181-218.
64. Alfaro C, Suarez N, Oñate C, et al. Dendritic cells take up and present antigens from viable and apoptotic polymorphonuclear leukocytes. PLoS One 2011; 6: e29300.
65. Teraoka Y, Ide K, Morimoto H, Tahara H, Ohdan H. Expression of recipient CD47 on rat insulinoma cell xenografts prevents macrophage-mediated rejection through SIRPα inhibitory signaling in mice. PLoS One 2013; 8: e58359.
66. Munn DH, Cheung NK. Antibody-independent phagocytosis of tumor cells by human monocyte-derived macrophages cultured in recombinant macrophage colony-stimulating factor. Cancer Immunol Immunother 1995; 41: 46-52.
67. Woelders H, Matthijs A. Phagocytosis of boar spermatozoa in vitro and in vivo. Reprod Suppl 2001; 58: 113-27.
68. Marey MA, Liu J, Kowsar R, et al. Bovine oviduct epithelial cells downregulate phagocytosis of sperm by neutrophils: prostaglandin E2 as a major physiological regulator. Reproduction 2013; 147: 211-9.
69. Kopatz J, Beutner C, Welle K, et al. Siglec-h on activated microglia for recognition and engulfment of glioma cells. Glia 2013; 61: 1122-33.
70. Chao MP, Jaiswal S, Weissman-Tsukamoto R, et al. Calreticulin is the dominant pro-phagocytic signal on multiple human cancers and is counterbalanced by CD47. Sci Transl Med 2010; 2: 63ra94.
71. Zoller EE, Lykens JE, Terrell CE, et al. Hemophagocytosis causes a consumptive anemia of inflammation. J Exp Med 2011; 208: 1203-14.
72. Neher JJ, Neniskyte U, Zhao ZW, Bal-Price A, Tolkovsky AM, Brown GC. Inhibition of microglial phagocytosis is sufficient to prevent inflammatory neuronal death. J Immunol 2011; 186: 4973-83.
73. Neniskyte U, Neher JJ, Brown GC. Neuronal death induced by nanomolar amyloid beta is mediated by primary phagocytosis of neurons by microglia. J Biol Chem 2011; 286: 39904-13.
74. Fricker M, Oliva-Martin MJ, Brown GC. Primary phagocytosis of viable neurons by microglia activated with LPS or Abeta is dependent on calreticulin/LRP phagocytic signalling. J Neuroinflammation 2012; 9: 196.
75. Fricker M, Neher JJ, Zhao JW, Théry C, Tolkovsky AM, Brown GC. MFG-E8 Mediates Primary Phagocytosis of Viable Neurons during Neuroinflammation. J Neurosci 2012; 32: 2657-66.
76. Emmrich J, Hornik T, Neher J, Brown GC. Rotenone induces neuronal death by microglial phagocytosis of neurons. FEBS J 2013; 280: 5030-8.
77. Neniskyte U, Brown GC. Lactadherin/MFG-E8 is essential for microglia-mediated neuronal loss and phagoptosis induced by amyloid β. J Neurochem 2013; 126: 312-7.
78. Fricker M, Vilalta A, Tolkovsky AM, Brown GC. Caspase inhibitors protect neurons by enabling selective necroptosis of inflamed microglia. J Biol Chem 2013; 288: 9145-52.
79. Neher JJ, Emmrich JV, Fricker M, Mander PK, Thery C, Brown GC. Phagocytosis executes delayed neuronal death after focal brain ischemia. Proc Natl Acad Sci 2013; 110: E4098-107.
80. Neniskyte U, Vilalta A, Brown GC. Tumour necrosis factor alpha-induced neuronal loss is mediated by microglial phagocytosis. FEBS Lett 2014; 588: 2952-6.
81. Neher JJ, Neniskyte U, Hornik T, Brown GC. Inhibition of UDP/P2Y6 purinergic signaling prevents phagocytosis of viable neurons by activated microglia in vitro and in vivo. Glia 2014; 62: 1463-75.
82. Hornik TC, Neniskyte U, Brown GC. Inflammation induces Multinucleation of Microglia via PKC inhibition of Cytokinesis, generating highly phagocytic Multinucleated Giant Cells. J. Neurochem 2014; 128: 650-61.
83. Neher JJ, Neniskyte U, Brown GC. Primary phagocytosis of neurons by inflamed microglia: potential roles in neurodegeneration. Front Pharmacol 2012; 3: 27.
84. Fadeel B, Xue D, Kagan V. Programmed cell clearance: molecular regulation of the elimination of apoptotic cell corpses and its role in the resolution of inflammation. Biochem Biophys Res Commun 2010; 396: 7-10.
85. Chao MP, Majeti R, Weissman IL. Programmed cell removal: a new obstacle in the road to developing cancer. Nat Rev Cancer 2011; 12: 58-67.
86. Zhang B, Hirahashi J, Cullere X, Mayadas TN. Elucidation of molecular events leading to neutrophil apoptosis following phagocytosis: cross-talk between caspase 8, reactive oxygen species, and MAPK/ERK activation. J Biol Chem 2003; 278: 28443-54.
87. Overholtzer M, Mailleux AA, Mouneimne G, et al. A nonapoptotic cell death process, entosis, that occurs by cell-in-cell invasion. Cell 2007; 131: 966-79.
88. Sharma N, Dey P. Cell cannibalism and cancer. Diagn Cytopathol 2011; 39: 229-33.
89. Lugini L, Matarrese P, Tinari A, et al. Cannibalism of live lymphocytes by human metastatic but not primary melanoma cells. Cancer Res 2006; 66: 3629-38.
90. Wang S, Guo Z, Xia P, et al. Internalization of NK cells into tumour cells requires ezrin and leads to a programmed cell-in-cell death. Cell Res 2009; 19: 1350-62.
91. Mormone E, Matarrese P, Tinari A, et al. Genotype-dependent priming to self- and xeno-cannibalism in heterozygous and homozygous lymphoblasts from patients with Huntington's disease. J Neurochem 2006; 98: 1090-9.
92. Sun Q, Cibas ES, Huang H, Hodgson L, Overholtzer M. Induction of entosis by epithelial cadherin expression. Cell Res 2014; 24: 1288-98.
93. Smith LM, May RC. Mechanisms of microbial escape from phagocyte killing. Biochem Soc Trans 2013; 41: 475-90.
94. Erwig LP, McPhilips KA, Wynes MY, Ivetic A, Ridley AJ, Henson PM. Differential regulation of phagosome maturation in macrophages and dendritic cells mediated by Rho GTPases and ezrin-radixin-moesin (ERM) proteins. Proc Natl Acad Sci U S A 2006; 103: 12825-30.
95. Wang S, He MF, Chen YH, et al. Rapid reuptake of granzyme B leads to emperitosis: an apoptotic cell-in-cell death of immune killer cells inside tumor cells. Cell Death Dis 2013; 4: e856.