Chapter 33 : Phagocytosis in Immune Response

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Analysis of phagocytosis in has been greatly facilitated by the characterization of the phagocytic properties of S2 cells, an embryonic hemocyte-derived cell line that is readily amenable to RNA-mediated interference (RNAi), opening the field to systematic studies. Identification of new genes involved in phagocytosis relies either on genome-wide RNAi screens in S2 cell culture, proteomic analysis of the plasmatocyte phagosome, or in silico homology screening. An eater loss-of-function mutation has been generated, showing that Eater is required for phagocytosis of several types of bacteria in vivo. The second important conclusion from this brief overview of phagocytic receptors concerns the high redundancy in the receptors. Phagocytosis contributes to the natural defenses of insects against all microorganisms, including bacteria, yeast, and parasites, but has mainly been studied in the case of bacteria. The finding that many bacteria proliferate in the circulatory cavity of mutant flies lacking hemocytes demonstrated the role of phagocytosis. This chapter illustrates that in phagocytosis plays a major role in the removal of microorganisms following any type of infections. Understanding the resistance of intracellular bacteria to phagocytosis and identification of the receptors for their uptake will be of special interest. The major challenge is to decipher the relationships between cellular and humoral responses and the relative contribution of phagocytosis and AMP bacterial killing in various infection models.

Citation: Leclerc V, Caldelari I, Veresceaghina N, Reichhart J. 2009. Phagocytosis in Immune Response, p 513-521. In Russell D, Gordon S (ed), Phagocyte-Pathogen Interactions. ASM Press, Washington, DC. doi: 10.1128/9781555816650.ch33
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Model for the interactions between hemocytes and fat body. This model fits with most available data, but is still controversial on some aspects (see text for details). Two complementary signals would be required to activate AMP synthesis in the fat body. The first signal consists of the activation of the Toll and IMD pathways through direct recognition of microorganisms. After a septic injury, the second signal would be produced by the injury itself. The existence and the nature of this signal have not been demonstrated, but observations suggest that a clean injury results in a weak response by the fat body. After natural infections, the second signal would be generated by the hemocytes, activated by phagocytosis of microorganisms (or latex beads in experimental conditions). The nature of this signal is also unknown, but Upd3 or Spaetzle could be candidates.

Citation: Leclerc V, Caldelari I, Veresceaghina N, Reichhart J. 2009. Phagocytosis in Immune Response, p 513-521. In Russell D, Gordon S (ed), Phagocyte-Pathogen Interactions. ASM Press, Washington, DC. doi: 10.1128/9781555816650.ch33
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1. Agaisse, H.,, L. S. Burrack,, J. A. Philips,, E. J. Rubin,, N. Perrimon, and, D. E. Higgins. 2005. Genome-wide RNAi screen for host factors required for intracellular bacterial infection. Science 309: 12481251.
2. Agaisse, H.,, U. M. Petersen,, M. Boutros,, B. Mathey-Prevot, and, N. Perrimon. 2003. Signaling role of hemocytes in Drosophila JAK/STAT-dependent response to septic injury. Dev. Cell 5: 441450.
3. Armstrong, P. B. 2006. Proteases and protease inhibitors: a balance of activities in host-pathogen interaction. Immunobiology 211: 263281.
4. Avet-Rochex, A.,, E. Bergeret,, I. Attree,, M. Meister, and, M. O. Fauvarque. 2005. Suppression of Drosophila cellular immunity by directed expression of the ExoS toxin GAP domain of Pseudomonas aeruginosa. Cell. Microbiol. 7: 799810.
5. Basset, A.,, R. S. Khush,, A. Braun,, L. Gardan,, F. Boccard,, J. A. Hoffmann, and, B. Lemaitre. 2000. The phytopathogenic bacteria Erwinia carotovora infects Drosophila and activates an immune response. Proc. Natl. Acad. Sci. USA 97: 33763381.
6. Braun, A.,, J. A. Hoffmann, and, M. Meister. 1998. Analysis of the Drosophila host defense in domino mutant larvae, which are devoid of hemocytes. Proc. Natl. Acad. Sci. USA 95: 1433714342.
7. Brennan, C. A.,, J. R. Delaney,, D. S. Schneider, and, K. V. Anderson. 2007. Psidin is required in Drosophila blood cells for both phagocytic degradation and immune activation of the fat body. Curr. Biol. 17: 6772.
8. Cherry, S.,, and N. Silverman. 2006. Host-pathogen interactions in drosophila: new tricks from an old friend. Nat. Immunol. 7: 911917.
9. Crozatier, M.,, and M. Meister. 2007. Drosophila haematopoiesis. Cell. Microbiol. 9: 11171126.
10. Desjardins, M.,, and G. Griffiths. 2003. Phagocytosis: latex leads the way. Curr. Opin. Cell. Biol. 15: 498- 503.
11. Dionne, M. S.,, N. Ghori, and, D. S. Schneider. 2003. Drosophila melanogaster is a genetically tractable model host for Mycobacterium marinum. Infect. Immun. 71: 35403550.
12. Dodds, A. W.,, and S. K. Law. 1998. The phylogeny and evolution of the thioester bond-containing proteins C3, C4 and alpha 2-macroglobulin. Immunol. Rev. 166: 1526.
13. Elrod-Erickson, M.,, S. Mishra, and, D. Schneider. 2000. Interactions between the cellular and humoral immune responses in Drosophila. Curr. Biol. 10: 781784.
14. Franc, N. C.,, P. Heitzler,, R. A. Ezekowitz, and, K. White. 1999. Requirement for croquemort in phagocytosis of apoptotic cells in Drosophila. Science 284: 19911994.
15. Garin, J.,, R. Diez,, S. Kieffer,, J. F. Dermine,, S. Duclos,, E. Gagnon,, R. Sadoul,, C. Rondeau, and, M. Desjardins. 2001. The phagosome proteome: insight into phagosome functions. J. Cell Biol. 152: 165180.
16. Garver, L. S.,, J. Wu, and, L. P. Wu. 2006. The peptidoglycan recognition protein PGRP-SC1a is essential for Toll signaling and phagocytosis of Staphylococcus aureus in Drosophila. Proc. Natl. Acad. Sci. USA 103: 660665.
17. Irving, P.,, J. M. Ubeda,, D. Doucet,, L. Troxler,, M. Lagueux,, D. Zachary,, J. A. Hoffmann,, C. Hetru, and, M. Meister. 2005. New insights into Drosophila larval haemocyte functions through genome-wide analysis. Cell. Microbiol. 7: 335350.
18. Jiggins, F. M.,, and K. W. Kim. 2006. Contrasting evolutionary patterns in Drosophila immune receptors. J. Mol. Evol. 63: 769780.
19. Kocks, C.,, J. H. Cho,, N. Nehme,, J. Ulvila,, A. M. Pearson,, M. Meister,, C. Strom,, S. L. Conto,, C. Hetru,, L. M. Stuart,, T. Stehle,, J. A. Hoffmann,, J. M. Reichhart,, D. Ferrandon,, M. Ramet, and, R. A. Ezekowitz. 2005. Eater, a transmembrane protein mediating phagocytosis of bacterial pathogens in Drosophila. Cell 123: 335346.
20. Kurucz, E.,, R. Markus,, J. Zsamboki,, K. Folkl-Medzihradszky,, Z. Darula,, P. Vilmos,, A. Udvardy,, I. Krausz,, T. Lukacsovich,, E. Gateff,, C. J. Zettervall,, D. Hultmark, and, I. Ando. 2007. Nimrod, a putative phagocytosis receptor with EGF repeats in Drosophila plasmatocytes. Curr. Biol. 17: 649654.
21. Lagueux, M.,, E. Perrodou,, E. A. Levashina,, M. Capovilla, and, J. A. Hoffmann. 2000. Constitutive expression of a complement-like protein in toll and JAK gain-of-function mutants of Drosophila. Proc. Natl. Acad. Sci. USA 97: 1142711432.
22. Law, S. K.,, and K. B. M. Reid. 1995. Complement, 2nd ed. IRL Press, Oxford, United Kingdom.
23. Leclerc, V.,, N. Pelte,, L. El Chamy,, C. Martinelli,, P. Ligoxygakis,, J. A. Hoffmann, and, J. M. Reichhart. 2006. Prophenoloxidase activation is not required for survival to microbial infections in Drosophila. EMBO Rep. 7: 231235.
24. Lemaitre, B.,, and J. Hoffmann. 2007. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25: 697743.
25. Levashina, E. A.,, L. F. Moita,, S. Blandin,, G. Vriend,, M. Lagueux, and, F. C. Kafatos. 2001. Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 104: 709718.
26. Little, T. J.,, J. K. Colbourne, and, T. J. Crease. 2004. Molecular evolution of daphnia immunity genes: polymorphism in a gram-negative binding protein gene and an alpha-2-macroglobulin gene. J. Mol. Evol. 59: 498506.
27. Manaka, J.,, T. Kuraishi,, A. Shiratsuchi,, Y. Nakai,, H. Higashida,, P. Henson, and, Y. Nakanishi. 2004. Draper-mediated and phosphatidylserine-independent phagocytosis of apoptotic cells by Drosophila hemocytes/macrophages. J. Biol. Chem. 279: 4846648476.
28. Mansfield, B. E.,, M. S. Dionne,, D. S. Schneider, and, N. E. Freitag. 2003. Exploration of host-pathogen interactions using Listeria monocytogenes and Drosophila melanogaster. Cell. Microbiol. 5: 901911.
29. Matova, N.,, and K. V. Anderson. 2006. Rel/NF-kappaB double mutants reveal that cellular immunity is central to Drosophila host defense. Proc. Natl. Acad. Sci. USA 103: 1642416429.
30. Meister, M. 2004. Blood cells of Drosophila: cell lineages and role in host defence. Curr. Opin. Immunol. 16: 1015.
31. Mukhopadhyay, S.,, and S. Gordon. 2004. The role of scavenger receptors in pathogen recognition and innate immunity. Immunobiology 209: 3949.
32. Nehme, N.,, S. Liégeois,, B. Kele,, P. Giammarinaro,, E. Pradel,, J. A. Hoffmann,, J. J. Ewbank, and, D. Ferrandon. 2007. A model of bacterial intestinal infections in Drosophila melanogaster. PLOS Pathog. 3: e173.
33. Pearson, A. M.,, K. Baksa,, M. Ramet,, M. Protas,, M. McKee,, D. Brown, and, R. A. Ezekowitz. 2003. Identification of cytoskeletal regulatory proteins required for efficient phagocytosis in Drosophila. Microbes Infect. 5: 815824.
34. Philips, J. A.,, E. J. Rubin, and, N. Perrimon. 2005. Drosophila RNAi screen reveals CD36 family member required for mycobacterial infection. Science 309: 12511253.
35. Ramet, M.,, P. Manfruelli,, A. Pearson,, B. Mathey-Prevot, and, R. A. Ezekowitz. 2002. Functional genomic analysis of phagocytosis and identification of a Drosophila receptor for E. coli. Nature 416: 644648.
36. Ramet, M.,, A. Pearson,, P. Manfruelli,, X. Li,, H. Koziel,, V. Gobel,, E. Chung,, M. Krieger, and, R. A. Ezekowitz. 2001. Drosophila scavenger receptor CI is a pattern recognition receptor for bacteria. Immunity 15: 10271038.
37. Royet, J.,, and R. Dziarski. 2007. Peptidoglycan recognition proteins: pleiotropic sensors and effectors of antimicrobial defences. Nat. Rev. Microbiol. 5: 264277.
38. Schmucker, D.,, J. C. Clemens,, H. Shu,, C. A. Worby,, J. Xiao,, M. Muda,, J. E. Dixon, and, S. L. Zipursky. 2000. Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101: 671684.
39. Stroschein-Stevenson, S. L.,, E. Foley,, P. H. O’Farrell, and, A. D. Johnson. 2006. Identification of Drosophila gene products required for phagocytosis of Candida albicans. PLoS Biol. 4: e4.
40. Stuart, L. M.,, J. Boulais,, G. M. Charriere,, E. J. Hennessy,, S. Brunet,, I. Jutras,, G. Goyette,, C. Rondeau,, S. Letarte,, H. Huang,, P. Ye,, F. Morales,, C. Kocks,, J. S. Bader,, M. Desjardins, and, R. A. Ezekowitz. 2007. A systems biology analysis of the Drosophila phagosome. Nature 445: 95101.
41. Stuart, L. M.,, J. Deng,, J. M. Silver,, K. Takahashi,, A. A. Tseng,, E. J. Hennessy,, R. A. Ezekowitz, and, K. J. Moore. 2005. Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain. J. Cell Biol. 170: 477485.
42. Wang, L.,, and P. Ligoxygakis. 2006. Pathogen recognition and signalling in the Drosophila innate immune response. Immunobiology 211: 251261.
43. Watson, F. L.,, R. Puttmann-Holgado,, F. Thomas,, D. L. Lamar,, M. Hughes,, M. Kondo,, V. I. Rebel, and, D. Schmucker. 2005. Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 309: 18741878.
44. Williams, M. J. 2007. Drosophila hemopoiesis and cellular immunity. J. Immunol. 178: 47114716.
45. Wood, W.,, and A. Jacinto. 2007. Drosophila melanogaster embryonic haemocytes: masters of multitasking. Nat. Rev. Mol. Cell Biol. 8: 542551.


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Phagocytic receptors and opsonizing molecules

Citation: Leclerc V, Caldelari I, Veresceaghina N, Reichhart J. 2009. Phagocytosis in Immune Response, p 513-521. In Russell D, Gordon S (ed), Phagocyte-Pathogen Interactions. ASM Press, Washington, DC. doi: 10.1128/9781555816650.ch33

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