Corpse Engulfment Generates a Molecular Memory that Primes the Macrophage Inflammatory Response

Cell

Volumn 165, Issue 7, 2016, Pages 1658-1671

  Weavers, Helen ^a   Evans, Iwan R ^b   Martin, Paul ^a,c,d   Wood, Will ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c CARDIFF UNIVERSITY   (United Kingdom)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; JANUS KINASE; DRAPER PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; MEMBRANE PROTEIN;

APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CELL MOTILITY; CELL PLASTICITY; CONTROLLED STUDY; CORPSE ENGULFMENT; DROSOPHILA; ENZYME ACTIVITY; EXTRACELLULAR SPACE; IMMUNOLOGICAL MEMORY; INFLAMMATION; MACROPHAGE; MACROPHAGE MIGRATION; NONHUMAN; NUCLEAR REPROGRAMMING; PHAGOCYTOSIS; PHENOTYPIC PLASTICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TISSUE INJURY; UPREGULATION; ANIMAL; CYTOLOGY; ESCHERICHIA COLI; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM;

ANIMALS; APOPTOSIS; DROSOPHILA; DROSOPHILA PROTEINS; ESCHERICHIA COLI; IMMUNITY, INNATE; IMMUNOLOGIC MEMORY; MACROPHAGES; MAP KINASE SIGNALING SYSTEM; MEMBRANE PROTEINS; PHAGOCYTOSIS;

EID: 84962855747     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.04.049     Document Type: Article

References (66)

1. T. Adachi-Yamada, M. Nakamura, K. Irie, Y. Tomoyasu, Y. Sano, E. Mori, S. Goto, N. Ueno, Y. Nishida, and K. Matsumoto p38 mitogen-activated protein kinase can be involved in transforming growth factor beta superfamily signal transduction in Drosophila wing morphogenesis Mol. Cell. Biol. 19 1999 2322 2329
2. P.-L. Bardet, G. Kolahgar, A. Mynett, I. Miguel-Aliaga, J. Briscoe, P. Meier, and J.-P. Vincent A fluorescent reporter of caspase activity for live imaging Proc. Natl. Acad. Sci. USA 105 2008 13901 13905
3. F. Bistoni, A. Vecchiarelli, E. Cenci, P. Puccetti, P. Marconi, and A. Cassone Evidence for macrophage-mediated protection against lethal Candida albicans infection Infect. Immun. 51 1986 668 674
4. F. Bistoni, G. Verducci, S. Perito, A. Vecchiarelli, P. Puccetti, P. Marconi, and A. Cassone Immunomodulation by a low-virulence, agerminative variant of Candida albicans. Further evidence for macrophage activation as one of the effector mechanisms of nonspecific anti-infectious protection J. Med. Vet. Mycol. 26 1988 285 299
5. B.A. Blok, R.J.W. Arts, R. van Crevel, C.S. Benn, and M.G. Netea Trained innate immunity as underlying mechanism for the long-term, nonspecific effects of vaccines J. Leukoc. Biol. 98 2015 347 356
6. D.M.E. Bowdish, M.S. Loffredo, S. Mukhopadhyay, A. Mantovani, and S. Gordon Macrophage receptors implicated in the "adaptive" form of innate immunity Microbes Infect. 9 2007 1680 1687
7. N.J. Bump, M. Hackett, M. Hugunin, S. Seshagiri, K. Brady, P. Chen, C. Ferenz, S. Franklin, T. Ghayur, P. Li, and et al. Inhibition of ICE family proteases by baculovirus antiapoptotic protein p35 Science 269 1995 1885 1888
8. N. Chatterjee, and D. Bohmann A versatile ΦC31 based reporter system for measuring AP-1 and Nrf2 signaling in Drosophila and in tissue culture PLoS ONE 7 2012 e34063
9. P. Chen, W. Nordstrom, B. Gish, and J.M. Abrams grim, a novel cell death gene in Drosophila Genes Dev. 10 1996 1773 1782
10. N.K. Cho, L. Keyes, E. Johnson, J. Heller, L. Ryner, F. Karim, and M.A. Krasnow Developmental control of blood cell migration by the Drosophila VEGF pathway Cell 108 2002 865 876
11. L. Cuttell, A. Vaughan, E. Silva, C.J. Escaron, M. Lavine, E. Van Goethem, J.P. Eid, M. Quirin, and N.C. Franc Undertaker, a Drosophila Junctophilin, links Draper-mediated phagocytosis and calcium homeostasis Cell 135 2008 524 534
12. J.R. Davis, C.-Y. Huang, J. Zanet, S. Harrison, E. Rosten, S. Cox, D.Y. Soong, G.A. Dunn, and B.M. Stramer Emergence of embryonic pattern through contact inhibition of locomotion Development 139 2012 4555 4560
13. W.E. Durrant, and X. Dong Systemic acquired resistance Annu. Rev. Phytopathol. 42 2004 185 209
14. I.R. Evans, N. Hu, H. Skaer, and W. Wood Interdependence of macrophage migration and ventral nerve cord development in Drosophila embryos Development 137 2010 1625 1633
15. I.R. Evans, F.S.L.M. Rodrigues, E.L. Armitage, and W. Wood Draper/CED-1 mediates an ancient damage response to control inflammatory blood cell migration in vivo Curr. Biol. 25 2015 1606 1612
16. Y. Feng, and P. Martin Imaging innate immune responses at tumour initiation: new insights from fish and flies Nat. Rev. Cancer 15 2015 556 562
17. N.C. Franc, P. Heitzler, R. Ezekowitz, and K. White Requirement for croquemort in phagocytosis of apoptotic cells in Drosophila Science 284 1999 1991 1994
18. Z.Q. Fu, and X. Dong Systemic acquired resistance: turning local infection into global defense Annu. Rev. Plant Biol. 64 2013 839 863
19. K. Gao, C.R. Wang, F. Jiang, A.Y.K. Wong, N. Su, J.H. Jiang, R.C. Chai, G. Vatcher, J. Teng, J. Chen, and et al. Traumatic scratch injury in astrocytes triggers calcium influx to activate the JNK/c-Jun/AP-1 pathway and switch on GFAP expression Glia 61 2013 2063 2077
20. E.R. Geisbrecht, and D.J. Montell A role for Drosophila IAP1-mediated caspase inhibition in Rac-dependent cell migration Cell 118 2004 111 125
21. R. Greenspan Fly Pushing: The Theory and Practice of Drosophila Genetics 1997 Cold Spring Harbor Press
22. M.E. Grether, J.M. Abrams, J. Agapite, K. White, and H. Steller The head involution defective gene of Drosophila melanogaster functions in programmed cell death Genes Dev. 9 1995 1694 1708
23. M.A. Gronski, J.M. Kinchen, I.J. Juncadella, N.C. Franc, and K.S. Ravichandran An essential role for calcium flux in phagocytes for apoptotic cell engulfment and the anti-inflammatory response Cell Death Differ. 16 2009 1323 1331
24. M.C. Harrisingh, Y. Wu, G.A. Lnenicka, and M.N. Nitabach Intracellular Ca2+ regulates free-running circadian clock oscillation in vivo J. Neurosci. 27 2007 12489 12499
25. Y. Hashimoto, Y. Tabuchi, K. Sakurai, M. Kutsuna, K. Kurokawa, T. Awasaki, K. Sekimizu, Y. Nakanishi, and A. Shiratsuchi Identification of lipoteichoic acid as a ligand for draper in the phagocytosis of Staphylococcus aureus by Drosophila hemocytes J. Immunol. 183 2009 7451 7460
26. B.A. Hay, T. Wolff, and G.M. Rubin Expression of baculovirus P35 prevents cell death in Drosophila Development 120 1994 2121 2129
27. M.D. Jacobson, M. Weil, and M.C. Raff Programmed cell death in animal development Cell 88 1997 347 354
28. J.F. Kerr, A.H. Wyllie, and A.R. Currie Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics Br. J. Cancer 26 1972 239 257
29. J. Kleinnijenhuis, J. Quintin, F. Preijers, L.A. Joosten, D.C. Ifrim, S. Saeed, C. Jacobs, J. van Loenhout, D. de Jong, H.G. Stunnenberg, and et al. Bacille Calmette-Guerin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes Proc. Natl. Acad. Sci. USA 109 2012 17537 17542
30. E. Luna, T. Bruce, M. Roberts, V. Flors, and J. Ton Next-generation systemic acquired resistance Plant Physiol. 158 2012 844 853
31. J.M. Macdonald, J. Doherty, R. Hackett, and M.R. Freeman The c-Jun kinase signaling cascade promotes glial engulfment activity through activation of draper and phagocytic function Cell Death Differ. 20 2013 1140 1148
32. 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. 279 2004 48466 48476
33. P. Martin, and S.J. Leibovich Inflammatory cells during wound repair: the good, the bad and the ugly Trends Cell Biol. 15 2005 599 607
34. F.O. Martinez, and S. Gordon The M1 and M2 paradigm of macrophage activation: time for reassessment F1000Prime Rep. 6 2014 13
35. L.C. Meagher, J.S. Savill, A. Baker, R.W. Fuller, and C. Haslett Phagocytosis of apoptotic neutrophils does not induce macrophage release of thromboxane B2 J. Leukoc. Biol. 52 1992 269 273
36. S. Moreira, B. Stramer, I. Evans, W. Wood, and P. Martin Prioritization of competing damage and developmental signals by migrating macrophages in the Drosophila embryo Curr. Biol. 20 2010 464 470
37. N.T. Mortimer, J. Goecks, B.Z. Kacsoh, J.A. Mobley, G.J. Bowersock, J. Taylor, and T.A. Schlenke Parasitoid wasp venom SERCA regulates Drosophila calcium levels and inhibits cellular immunity Proc. Natl. Acad. Sci. USA 110 2013 9427 9432
38. D.M. Mosser, and J.P. Edwards Exploring the full spectrum of macrophage activation Nat. Rev. Immunol. 8 2008 958 969
39. P.J. Murray, and T.A. Wynn Protective and pathogenic functions of macrophage subsets Nat. Rev. Immunol. 11 2011 723 737
40. H. Nagaso, T. Murata, N. Day, and K.K. Yokoyama Simultaneous detection of RNA and protein by in situ hybridization and immunological staining J. Histochem. Cytochem. 49 2001 1177 1182
41. M.G. Netea, J. Quintin, and J.W.M. van der Meer Trained immunity: a memory for innate host defense Cell Host Microbe 9 2011 355 361
42. P. Niethammer, C. Grabher, A.T. Look, and T.J. Mitchison A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish Nature 459 2009 996 999
43. R. Noy, and J.W. Pollard Tumor-associated macrophages: from mechanisms to therapy Immunity 41 2014 49 61
44. L.N. Pham, M.S. Dionne, M. Shirasu-Hiza, and D.S. Schneider A specific primed immune response in Drosophila is dependent on phagocytes PLoS Pathog. 3 2007 e26
45. J. Quintin, S. Saeed, J.H. Martens, E.J. Giamarellos-Bourboulis, D.C. Ifrim, C. Logie, L. Jacobs, T. Jansen, B.J. Kullberg, C. Wijmenga, and et al. Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes Cell Host Microbe 12 2012 223 232
46. J. Quintin, S.C. Cheng, J.W. van der Meer, and M.G. Netea Innate immune memory: towards a better understanding of host defense mechanisms Curr. Opin. Immunol. 29 2014 1 7
47. W. Razzell, I.R. Evans, P. Martin, and W. Wood Calcium flashes orchestrate the wound inflammatory response through DUOX activation and hydrogen peroxide release Curr. Biol. 23 2013 424 429
48. J. Rodrigues, F.A. Brayner, and L.C. Alves Hemocyte Differentiation Mediates Innate Immune Memory in Anopheles gambiae Mosquitoes Science 329 2010 1353 1356
49. I.M. Roitt, P. Delves, S. Martin, and D. Burton Roitt's essential immunology 2006 Wiley-Blackwell
50. A. Rubartelli, A. Poggi, and M.R. Zocchi The selective engulfment of apoptotic bodies by dendritic cells is mediated by the alpha(v)beta3 integrin and requires intracellular and extracellular calcium Eur. J. Immunol. 27 1997 1893 1900
51. J. Savill, I. Dransfield, C. Gregory, and C. Haslett A blast from the past: clearance of apoptotic cells regulates immune responses Nat. Rev. Immunol. 2 2002 965 975
52. A. Slaughter, X. Daniel, V. Flors, E. Luna, B. Hohn, and B. Mauch-Mani Descendants of primed Arabidopsis plants exhibit resistance to biotic stress Plant Physiol. 158 2012 835 843
53. M. Stern, J. Savill, and C. Haslett Human monocyte-derived macrophage phagocytosis of senescent eosinophils undergoing apoptosis. Mediation by alpha v beta 3/CD36/thrombospondin recognition mechanism and lack of phlogistic response Am. J. Pathol. 149 1996 911 921
54. M. Suzanne, and H. Steller Shaping organisms with apoptosis Cell Death Differ. 20 2013 669 675
55. K.L. Tan, I. Vlisidou, and W. Wood Ecdysone mediates the development of immunity in the Drosophila embryo Curr. Biol. 24 2014 1145 1152
56. D. Tautz, and C. Pfeifle A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback Chromosoma 98 1989 81 85
57. P.R. Taylor, A. Carugati, V.A. Fadok, H.T. Cook, M. Andrews, M.C. Carroll, J.S. Savill, P.M. Henson, M. Botto, and M.J. Walport A hierarchical role for classical pathway complement proteins in the clearance of apoptotic cells in vivo J. Exp. Med. 192 2000 359 366
58. U. Tepass, L.I. Fessler, A. Aziz, and V. Hartenstein Embryonic origin of hemocytes and their relationship to cell death in Drosophila Development 120 1994 1829 1837
59. L. Tian, S.A. Hires, T. Mao, D. Huber, M.E. Chiappe, S.H. Chalasani, L. Petreanu, J. Akerboom, S.A. McKinney, E.R. Schreiter, and et al. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators Nat. Methods 6 2009 875 881
60. A. Vecchiarelli, E. Cenci, M. Puliti, E. Blasi, P. Puccetti, A. Cassone, and F. Bistoni Protective immunity induced by low-virulence Candida albicans: cytokine production in the development of the anti-infectious state Cell. Immunol. 124 1989 334 344
61. I. Vlisidou, A.J. Dowling, I.R. Evans, N. Waterfield, R.H. ffrench-Constant, and W. Wood Drosophila embryos as model systems for monitoring bacterial infection in real time PLoS Pathog. 5 2009 e1000518
62. K. White, M.E. Grether, J.M. Abrams, L. Young, K. Farrell, and H. Steller Genetic control of programmed cell death in Drosophila Science 264 1994 677 683
63. K. White, E. Tahaoglu, and H. Steller Cell killing by the Drosophila gene reaper Science 271 1996 805 807
64. W. Wood, and A. Jacinto Drosophila melanogaster embryonic haemocytes: masters of multitasking Nat. Rev. Mol. Cell Biol. 8 2007 542 551
65. W. Wood, M. Turmaine, R. Weber, V. Camp, R.A. Maki, S.R. McKercher, and P. Martin Mesenchymal cells engulf and clear apoptotic footplate cells in macrophageless PU.1 null mouse embryos Development 127 2000 5245 5252
66. W. Wood, C. Faria, and A. Jacinto Distinct mechanisms regulate hemocyte chemotaxis during development and wound healing in Drosophila melanogaster J. Cell Biol. 173 2006 405 416