From regulation of dying cell engulfment to development of anti-cancer therapy

Cell Death and Differentiation

Volumn 15, Issue 1, 2008, Pages 29-38

  Krysko, D V ^a,b   Vandenabeele, P ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRACYCLINE DERIVATIVE; ANTINEOPLASTIC AGENT; CALRETICULIN; CYTOKINE; DACTINOMYCIN; ETOPOSIDE; FAS ANTIBODY; FAS LIGAND; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HYDROCORTISONE; INTERLEUKIN 2; LACTADHERIN; LIPOCORTIN 5; STAUROSPORINE; TUMOR NECROSIS FACTOR;

ADJUVANT THERAPY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; AUTOCRINE EFFECT; B LYMPHOCYTE ACTIVATION; CANCER CELL; CANCER IMMUNOTHERAPY; CELL DIFFERENTIATION; CELL STRESS; CELL SURFACE; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; DRUG SAFETY; DRUG SYNTHESIS; GAMMA IRRADIATION; HUMAN; HUMORAL IMMUNITY; IMMUNOGENICITY; IMMUNOMODULATION; MACROPHAGE FUNCTION; MACROPHAGE MIGRATION; MELANOMA; NEOPLASM; NONHUMAN; OXIDATION REDUCTION REACTION; PARACRINE SIGNALING; PHAGOCYTE; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TUMOR IMMUNITY;

ANIMALS; APOPTOSIS; AUTOPHAGY; CELL DEATH; CYTOKINES; HUMANS; IMMUNITY, NATURAL; IMMUNOTHERAPY; INFLAMMATION; INFLAMMATION MEDIATORS; LIGANDS; MACROPHAGES; NECROSIS; NEOPLASMS; PHAGOCYTES; PHAGOCYTOSIS; RECEPTORS, CELL SURFACE;

EID: 37349110382     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/sj.cdd.4402271     Document Type: Review

References (90)

1. Mangahas PM, Zhou Z. Clearance of apoptotic cells in Caenorhabditis elegans. Semin Cell Dev Biol 2005; 16: 295-306.
2. Yu X, Odera S, Chuang CH, Lu N, Zhou Z. C. elegans dynamin mediates the signaling of phagocytic receptor CED-1 for the engulfment and degradation of apoptotic cells. Dev Cell 2006; 10: 743-757.
3. Bondanza A, Zimmermann VS, Rovere-Querini P, Tumay J, Dumitriu IE, Stach CM et al. Inhibition of phosphatidylserine recognition heightens the immunogenicity of irradiated lymphoma cells in vivo. J Exp Med 2004; 200: 1157-1165.
4. Obeid M, Tesniere A, Ghiringhelli F, Fimia GM, Apetoh L, Perfettini JL et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 2007; 13: 54-61.
5. Fadok VA, Voelker DR, Campbell PA, Cohen JJ, Bratton DL, Henson PM. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol 1992; 148: 2207-2216.
6. Williamson P, Schlegel RA. Transbilayer phospholipid movement and the clearance of apoptotic cells. Biochim Biophys Acta 2002; 1585 53-63.
7. Zullig S, Neukomm LJ, Jovanovic M, Charette SJ, Lyssenko NN, Halleck MS et al. Aminophospholipid translocase TAT-1 promotes phosphatidylserine exposure during C. elegans apoptosis. Curr Biol 2007; 17: 994-999.
8. Krysko DV, D'Herde K, Vandenabeele P. Clearance of apoptotic and necrotic cells and its immunological consequences. Apoptosis 2006; 11: 1709-1726.
9. 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: 943-945.
10. Greenberg ME, Sun M, Zhang R, Febbraio M, Silverstein R, Hazen SL. Oxidized phosphatidylserine-CD36 interactions play an essential role in macrophage-dependent phagocytosis of apoptotic cells. J Exp Med 2006; 203: 2613-2625.
11. Kiss RS, Elliott MR, Ma Z, Marcel YL, Ravichandran KS. Apoptotic cells induce a phosphatidylserine-dependent homeostatic response from phagocytes. Curr Biol 2006; 16: 2252-2258.
12. Morimoto K, Janssen WJ, Fessler MB, Xiao YQ, McPhillips KA, Borges VM et al. Statins enhance clearance of apoptotic cells through modulation of Rho-GTPases. Proc Am Thorac Soc 2006; 3: 516-517.
13. Gardai SJ, McPhillips KA, Frasch SC, Janssen WJ, Starefeldt A, Murphy-Ullrich JE et al. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through transactivation of LRP on the phagocyte. Cell 2005; 123: 321-334.
14. Arur S, Uche UE, Rezaul K, Fong M, Scranton V, Cowan AE et al. Annexin I is an endogenous ligand that mediates apoptotic cell engulfment. Dev Cell 2003; 4: 587-598.
15. Johnson S, Michalak M, Opas M, Eggleton P. The ins and outs of calreticulin: From the ER lumen to the extracellular space. Trends Cell Biol 2001; 11: 122-129.
16. Arosa FA, de Jesus O, Porto G, Carmo AM, de Sousa M. Calreticulin is expressed on the cell surface of activated human peripheral blood T lymphocytes in association with major histocompatibility complex class I molecules. J Biol Chem 1999; 274: 16917-16922.
17. Taylor RC, Brumatti G, Ito S, Hengartner MO, Deny WB, Martin SJ. Establishing a blueprint for CED-3-dependent killing through identification of multiple substrates for this protease. J Biol Chem 2007; 282: 15011-15021.
18. Franz S, Herrmann K, Fuhmrohr B, Sheriff A, Frey B, Gaipl US et al. After shrinkage apoptotic cells expose internal membrane-derived epitopes on their plasma membranes. Cell Death Differ 2007; 14 733-742.
19. Gagnon E, Duclos S, Rendeau C, Chevet E, Cameron PH, Steele-Mortimer O et al. Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 2002; 110: 119-131.
20. Muller-Taubenberger A, Lupas AN, Li H, Ecke M, Simmeth E, Gerisch G. Calreticulin and calnexin in the endoplasmic reticulum are important for phagocytosis. EMBO J 2001; 20: 6772-6782.
21. Kuraishi T, Manaka J, Kona M, Ishii H, Yamamoto N, Koizumi K et al. Identification of calreticulin as a marker for phagocytosis of apoptotic cells in Drosophila. Exp Cell Res 2007; 313: 500-510.
22. Ogden CA, deCathelineau A, Hoffmann PR, Bratton D, Ghebrehlwet B, Fadok VA et al. C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic; calls. J Exp Med 2001; 194: 781-795.
23. Gardai SJ, Bratton DL, Ogden CA, Henson PM. Recognition ligands on apoptotic cells: A perspective. J Leukoc Biol 2006; 79: 896-903.
24. Basu S, Binder RJ, Ramalingam T, Srivastava PK. CD91 is a common receptor for heat shock proteins gp96, hsp90, hsp70, and calreticulin. Immunity 2001; 14: 303-313.
25. Gardai SJ, Xiao-YQ, Dickinson M, Nick JA, Voelker DR, Greene KE et al. By binding SIRPalpha or calreticulin/CD91, lung collectins act as duet function surveillance molecules, to suppress or enhance inflammation. Cell 2003; 115: 13-23.
26. Takemura Y, Ouchi N, Shibata R, Aprahamian T, Kirber MT, Summer RS et al. Adiponectin modulates inflammatory reaction via calreticulin receptor-dependent clearance of early apoptotic bodies. J Clin Invest 2007; 117: 375-386.
27. Fan X, Krahling S, Smith D, Wlliamson P, Schlegel RA. Macrophage surface expression of annexins I and 11 in the phagocytosis of apoptotic lymphocytes. Mol Biol Cell 2004; 15: 2863-2872.
28. Dini L, Carla EC. Hepatic sinusoidal endothelium heterogeneity with respect to the recognition of apoptotic cells. Exp Call Res 1998; 240: 388-393.
29. Bilyy R, Stoika R. Search for novel, cell surface markers of apoptotic cells. Autoimmunity 2007; 40: 249-253.
30. Franz S, Frey B, Sheriff A, Galpi US, Beer A, Voll RE et al. Lectins defect changes of the glycosylation status of plasma membrane constituents during late apoptosis. Cytomefry A 2006; 69: 230-239.
31. Krysko DV, Brouckaert G, Katei M, Vandenabeele P, D'Herde K. Mechanisms of internalization of apoptotic and necrotic L929 cells by a macrophage cell line studied by electron microscopy. J Morphol 2003; 258 336-345.
32. Krysko DV, Denecker G, Festjens N, Gabriels S, Parthoens E, D'Harde K et al. Macrophages use different internalization mechanisms to clear acoptotic and necrotic cells. Cell Death Differ 2006; 13: 2011-2022.
33. Krysko O, De Ridder L, Comelissen M. Phosphatidylserine exposure during early primary necrosi s (oncosis) in JB6 cells as evidenced by immunogold labeling technique. Apoptosis 2004; 9: 495-500.
34. Brouckaert G, Kalai M, Krysko DV, Seelens X, Vercammen D, Ndlovu M et al. Phagocytosis of necrotic cells by macrophages is phosphatidylserine dependent and does not induce inflammatory cytokine production. Mol Biol Cell 2004; 15: 1089-1100.
35. Petrovski G, Zahuczky G, Katona K, Vereb G, Martinel W, Names Z et al. Clearance of dying autophagic cells of different origin by professional and non-professional phagocytes. Cell Death Differ 2007; 14: 1117-1128.
36. Bottcher A, Galpi US, Fumrohr BG, Herrmann M, Girkontalte I, Kalden JR et al. Involvement of phosphatidylserine, alphavbeta3, CD14, CD36, and complement C1q in the phagocytosis of primary necrotic lymphocytes by macrophages. Arthritis Rheum 2006; 54: 927-938.
37. Brown S, Heinisch I, Ross E, Shaw K Buckley CD, Savill J. Apoptosis disables CD31-mediated cell detachment-from phagocytes promoting binding and engultment. Nature 2002; 418: 200-203.
38. Erwig LP, Gordon S; Walsh GM, Raw AJ. Previous uptake of spoptotic neurtrophils or ligation at integrin receptors downmodulates the ability of macrophages to ingest apoptoatic neutrophils. Blood 1999; 93 1406-1412.
39. Lugini L Matarrese P, Tinani A, Lozupone F, Federid C, Iessi E et al. Cannibalism of live lymphocytes by human metastatic but not primary melanoma cells. Cancer Res 2006; 66: 3629-3638.
40. Babior OM. Phagocytes end oxidative stress. Am J Med 2000; 109 33-44.
41. McPhillips K; Janssen WJ, Ghosh M, Byrne A, Gardai S, Remigio L et al. TNF-(alpha) inhibits macropbage clearance of apoptotic cells via cytosollic phospholipase A2 and oxidant-dependent mechanisms. J Immunol 2067; 178: 8117-8126.
42. Nakaya M, Tanaka M, Okabe Y, Hanayama R, Nagata S. Opposite effects of rho family GTPases on engulfment of apoptotic cells by macrophages. J Biol Chem 2006; 281: 8836-8842.
43. Kagan VE, Gleiss B, Tyurina YY, Tyurin VA, Elenstrom-Magnusson C, Liu SX et al. A role for oxidative strew in apoptosis: Oxidation and externalization of phosphatidylserine is required for macrophage clearance of cells undergoing Fas-mediated apoptosis. J Immunol 2002; 169: 487-490.
44. Sather S, Kenyon KD, Lefkowitz JB, Liang X, Vamum-BC, Henson PM et al. A soluble form of the Mer receptor tyrosine kinase inhibits macrophage clearance of apoptotic cells and platelet aggregation. Blood 2007; 109: 1026-1033.
45. Distler JH, Huber LC, Gay S, Distler O, Pisetsky DS. Microparticles as mediators of cellular cross-talk in inflammatory disease. Autoimmunity 2006; 39: 683-690.
46. Lauber K, Bohn E, Krober SM, Xiao YJ, Blumenthal SG, Lindemann RK et al. Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell 2003; 113: 717-730.
47. Pletjushkina OY, Fetisova EK, Lyamzaev KG, Ivanova OY, Domnina LV, Vyssokikh MY et al. Long-distance apoptotic killing of cells is mediated by hydrogen peroxide in a mitochondrial ROS-dependent fashion. Cell Death Differ 2005; 12: 1442-1444.
48. Krispin A, Bledi Y, Atallah M, Trahtemberg U, Verbovetski I, Nahad E et al. Apoptotic cell thrombospondin-1 and heparin-binding domain lead to dendritic-cell phagocytic and tolerizing states. Blood 2006; 108: 3580-3589.
49. Scannell M, Flanagan MB, deStefani A, Wynne KJ, Cagney G, Godson C et al. Annexin-1 and peptide derivatives are released by apoptotic cells and stimulate phagocytosis of apoptotic neutrophils by macrophages. J Immunol 2007; 178: 4595-4605.
50. Yamamoto T. Roles of the ribosomal protein S19 dimer and the C5a receptor in pathophysiological functions of phagocytic leukocytes. Pathol Int 2007; 57: 1-11.
51. Beau S, Binder RJ, Suto R, Anderson KM, Srivastava PK. Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendrictic cells and activate the NF-kappa B pathway. Int Immunol 2000; 12: 1539-1546.
52. Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002; 418: 191-195.
53. Shi Y, Evans JE, Rock KL. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 2003; 425 516-521.
54. Kariko K, Ni H, Capodici J, Lamphier M, Weissman D. mRNA is an endogenous ligand for Toll-like receptor 3. J Biol Chem 2004; 279: 12542-12550.
55. Vanden Berghe T, Kalai M, Denecker G, Meeus A, Saelens X, Vandenabeele P. Necrosis is associated with IL-6 production but apoptosis is not. Cell Signal 2006; 18: 328-335.
56. Qu X, Zou Z, Sun Q, Luby-Phelps K, Cheng P, Hogan RN et al. Autophagy gene-dependent clearance of apoptotic cells during embryonic development. Cell 2007; 128: 931-946.
57. Shalak V, Kaminska M, Mitnacht-Kraus R, Vandenabeele P, Clause M, Mirande M. The EMAPII cytoldne is released from the mammalian multisynthetase complex after cleavage of its p43/proEMAPII component. J Biol Chem 2001; 276: 23769-23776.
58. Kageyama S, Isono T, Iwaki H, Wakabayashi Y, Okada Y, Kontani K et al. Identification by proteomic analysis of calreticulin as a marker for bladder cancer and evaluation of the diagnostic accuracy of its detection in urine. Clin Chem 2004; 50: 857-866.
59. Saelens X, Festjens N, Parthoens E, Vanoverberghe I, Kalai M, van Kuppeveld F et al. Protein synthesis persists during necrotic cell death. J Cell Biol 2005; 168: 545-551.
60. Fadok VA, Bratton DL, Konowal A, Freed PW, Westcott JY, Henson PM. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J Clin Invest 1998; 101: 890-898.
61. Li M, Carpio DF, Zheng Y, Bruzzo P, Singh V, Ouaaz F et al 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 2001; 166: 7128-7135.
62. Kawagishi C, Kurosaka K, Watanabe N, Kobayashi Y. Cytokine production by macrophages in association with phagocytosis of etoposide-treated P388 cells in vitro and in vivo. Biochim Biophys Acta 2001; 1541: 221-230.
63. Reddy SM, Hsiao KH, Abernethy VE, Fan H, Longacre A, Lieberthal W et al. Phagocytosis of apoptotic cells by macrophages induces novel signaling events leading to cytolkine-independent survival and inhibition of proliferation: Activation of Akt and inhibition of extracellular signal-regulated kinases 1 and 2. J Immunol 2002; 169: 702-713.
64. Byme A, Reen DJ. Lipopolysaccharide induces rapid production of IL-10 by monocytes in the presence of apoptotic neutrophils. J Immunol 2002; 168: 1968-1977.
65. Kurosaka K, Takahashi M, Watanabe N, Kobayashi Y. Silent cleanup of very early apoptotic cells by macrophages. J Immunol 2003; 1711: 4672-4679.
66. Canbay A, Feldstein AE, Higuchi H, Werneburg N, Grambihler A, Bronk SF et al. Kupffer cell engulfment of apoptotic bodies stimulates death ligand and cytokine expression. Hepatology 2003; 38: 1188-1198.
67. Cvetanovic M, Ucker DS. Innate immune discrimination of apoptotic calls: repression of proinflammatory macrophage transcription is coupled directly to specific recognition. J Immunol 2004; 172: 880-889.
68. Lucas M, Stuart LM, Zhang A, Hodivala-Dilke K, Febbraio M, Silverstein R et al. Requirements for apoptotic cell contact in regulation of macrophage responses. J Immunol 2006; 177: 4047-4054.
69. Freire-de-Lima CG, Xiao YQ, Gardai SJ, Bratton DL, Schiemann WP, Henson PM. Apoptotic cells, through transforming growth factor-beta, coordinately induce anti-inflammatory and suppress pro-inflammatory eicosanoid and NO synthesis in murine macrophages. J Biol Chem 2006; 281: 38376-38384.
70. Shibata T, Nagata K, Kobayashi Y. A suppressive role of nitric oxide in MIP-2 production by macrophages upon coculturing with apoptotic cells. J Leukoc Biol 2006; 80: 744-752.
71. Patel VA, Longacre A, Hsiao K, Fan H, Meng F, Mitchell JE et al. Apoptotic cells, at all stages of the death process, trigger characteristic signaling events that are divergent from and dominant over those triggered by necrotic cells: Implications for the delayed clearance model of autoimmunity. J Biol Chem 2006; 281: 4663-4670.
72. Tassiulas I, Park-Min KH, Hu Y, Kellerman L, Mevorach D, Ivashkiv, LB. Apoptotic cells inhibit LPS-induced cytokine and chemokine production and IFN responses in macrophages. Hum Immunol 2007; 68: 156-164.
73. Xiao YQ, Malcolm K, Worthen GS, Gardal S, Schiemann WP, Fadok VA et al. Cross-talk between ERK and p38 MAPK mediates selective suppression of pro-inflammatory cytokines by transforming growth factor-beta. J Biol Chem 2002; 277; 14884-14893.
74. Kim S, Elkon KB, Ma X. Transcriptional suppression of interleukin-12 gene expression following phagocytosis of apoptotic cells. Immunity 2004; 21: 643-653.
75. Zheng L, He M, Long M, Blomgran R, Stendahl O. Pathogen-induced apoptotic neutrophils express heat shock proteins and elicit activation of human macrophages. J Immunol 2004; 173: 6319-6326.
76. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol 2005; 5: 953-964.
77. Gratchev A, Schledzewsld K, Guillot P, Goerdt S. Alternatively activated antigen-presenting cells: Molecular repertoire, immune regulation, and healing. Skin Pharmacol Appl Skin Physiol 2001; 14: 272-279.
78. Xu W, Roos A, Schlagwein N, Woltman AM, Daha MR, van Kooten C. IL-10-producing macrophages preferentially dear early apoptotic cells. Blood 2006; 107: 4930-4937.
79. Lorimore SA, Coates PJ, Scobie GE, Milne G, Wright EG. Inflammatory-type responses after exposure to ionizing radiation in vivo. a mechanism for radiation-induced bystander effects? Oncogene 2001; 20: 7085-7095.
80. Blander JM, Medzhitov R. Toll-dependent selection of microbial antigens for presentation by dendritic cells. Nature 2006; 440: 808-812.
81. Johansson U, Walther-Jallow L, Smed-Sorensen A, Spetz AL Triggering of dendritic cell responses after exposure to activated, but not resting, apoptotic PBMCs. J Immunol 2007; 179: 1711-1720.
82. Fadok VA, Bratton DL, Guthrie L, Henson PM. Differential effects of apoptotic versus lysed cells on macrophage production of cytokines: Role of proteases. J Immunol 2001; 166: 6847-6854.
83. Skobeme M, Somersan S, Almodovar W, Truong T, Petrova K, Henson PM et al. The apoptotic cell receptor CR3, but not (alpha)v(beta)5, is a regulator of human dendritic cell immunostimulatory function. Blood 2006; 108: 947-955.
84. Ran S, He J, Huang X, Soares M, Scothom D, Thorpe PE. Antitumor effects of a monoclonal antibody that binds anionic phospholipids on the surface of tumor blood vessels in mice. Clin-Cancer Res 2005; 11: 1551-1562.
85. Caron E, Hall A. Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science 1998; 282: 1717-1721.
86. Kenis H, van Genderen H, Deckers NM, Lux PA, Hofstra L, Narula J et al. Annexin A5 inhibits engulfment through internalization of PS-expressing call membrane patches. Exp Cell Res 2006; 312: 719-726.
87. Jinushi M, Nakazaki Y, Dougan M, Carrasco DR, Mihm M, Dranoff G. MFG-E8-mediated uptake of apoptotic cells by APCs links the pro and antinflammatory activities of GM-CSF J Clin Invest 2007; 117 1902-1913.
88. Asano K, Miwa M; Miwa K, Hanayama R, Nagase H, Nagata S et al. Masking of phosphatidylserine inhibits apoptotic call engulfment and induces autoantibody production in mice. J Exp Med 2004; 200 459-467.
89. Zeng G, Aldridge ME, Tian X, Seiler D, Zhang X, Jin Y et al. Dendritic cell surface calreticulin is a receptor for NY-ESO-1: Direct interactions between tumor-associated antigen and the innate immune system. J Immunol 2006; 177: 3582-3589.
90. Storkus WJ, Falo Jr LD. A 'good death' for tumor immunology. Nat Med 2007; 13: 28-30.