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Humoral and Cellular Responses in Drosophila Innate Immunity

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Innate Immunity

Part of the book series: Infectious Disease ((ID))

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Abstract

The immune system of invertebrates has been the object of intense scrutiny ever since Elie Metchnikoff first discovered phagocytosis in starfish embryos in 1884 (1). Not surprisingly, the cellular arm of the insect innate immune response was the first to be investigated at the turn of the 20th century. Glaser and Paillot, followed later on by Metalnikow, uncovered the existence of a humoral arm of the insect host defense (2–5). However, the nature of the antimicrobial activity found in the hemolymph of immunized insects was not determined until the early 1980s, when Hans Boman’s pioneering work led to the purification in the moth Hyalophora cecropia of small cationic peptides that were called cecropins (6). Hundreds of peptides with antimicrobial activities were subsequently identified and characterized from insects of most orders (reviewed in ref. 7). Understanding the mechanisms responsible for their production is a major goal of recent research in innate immunity. For the last 10 years, Drosophila has been one major model system successfully used to dissect the molecular cascades controlling innate immunity in invertebrates. We describe here the current knowledge of the humoral and cellular arms of Drosophila immunity and highlight the similarities and disparities with the mammalian immune system.

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References

  1. Metchnikoff E. Untersuchung über die intracellular Verdauung bei Wirbellosen Tieren. Arbeiten aus dem zoologischen Institut der universität zu Wien 1884;2:241.

    Google Scholar 

  2. Glaser RW. On the existence of immunity principles in insects. Psyche 1918;25:39–46.

    Article  Google Scholar 

  3. Paillot A. Immunité naturelle chez les insectes. CR Acad Sci Paris 1919;169:202–204.

    Google Scholar 

  4. Paillot A. Contribution à l’étude de l’immunité humorale chez les insectes. CR Acad Sci Paris 1921;172:546–548.

    CAS  Google Scholar 

  5. Metalnikov S. Infection Microbienne et L’immunité chez la Mite des Abeilles Galleria mellonella. Paris: Masson, 1927.

    Google Scholar 

  6. Steiner H, Hultmark D, Engström A, Bennich H, Boman HG. Sequence and specificity of two antibacterial proteins involved in insect immunity. Nature 1981;292:246–248.

    Article  PubMed  CAS  Google Scholar 

  7. Bulet P, Hetru C, Dimarcq JL, Hoffmann D. Antimicrobial peptides in insects; structure and function. Dev Comp Immunol 1999;23:329–344.

    Article  PubMed  CAS  Google Scholar 

  8. Lemaitre B, Reichhart JM, Hoffmann JA. Drosophila host defense: differential display of antimicrobial peptide genes after infection by various classes of microorganisms. Proc Natl Acad Sci USA 1997;94:14614–14619.

    Article  PubMed  CAS  Google Scholar 

  9. Engström Y. Induction and regulation of antimicrobial peptides in Drosophila. Dev Comp Immunol 1999;23:345–358.

    Article  PubMed  Google Scholar 

  10. Engström Y, Kadalayil L, Sun S-C, et al. KappaB-like motifs regulate the induction of immune genes in Drosophila. J Mol Biol 1993;232:327–333.

    Article  PubMed  Google Scholar 

  11. Kappler C, Meister M, Lagueux M, et al. Insect immunity. Two 17-bp repeats nesting a kappaB-related sequence confer inducibility to the diptericin gene and bind a polypeptide in bacteriachallenged Drosophila. EMBO J 1993;12:1561–1568.

    PubMed  CAS  Google Scholar 

  12. Meister M, Braun A, Kappler C, Reichhart J-M, Hoffmann JA. Insect immunity. A transgenic analysis in Drosophila defines several functional domains in the diptericin promoter. EMBO J 1994;13:5958–5966.

    PubMed  CAS  Google Scholar 

  13. Karin M, Ben-Neriah Y. Phosphorylation meets ubiquitination: the control of NF-kappaB activity. Annu Rev Immunol 2000;18:621–663.

    Article  PubMed  CAS  Google Scholar 

  14. Pahl H. Activators and target genes of Rel/NF-ĸB transcription factors. Oncogene 1999;18:6853–6866.

    Article  PubMed  CAS  Google Scholar 

  15. Silverman N, Maniatis T. NF-kappaB signaling pathways in mammalian and insect innate immunity. Genes Dev 2001;15:2321–2342.

    Article  PubMed  CAS  Google Scholar 

  16. Nusslein-Volhard C, Lohs-Schardin M, Sander K, Cremer C. A dorso-ventral shift of embryonic primordia in a new maternal-effect mutant of Drosophila. Nature 1980;283:474–476.

    Article  PubMed  CAS  Google Scholar 

  17. St Johnston D, Nüsslein-Volhard C. The origin of pattern and polarity in the Drosophila embryo. Cell 1992;68:201–219.

    Article  Google Scholar 

  18. Belvin MP, Anderson KV. A conserved signaling pathway: the Drosophila Toll-dorsal pathway. Annu Rev Cell Dev Biol 1996;12:393–416.

    Article  PubMed  CAS  Google Scholar 

  19. Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA. The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 1996;86:973–983.

    Article  PubMed  CAS  Google Scholar 

  20. Michel T, Reichhart J, Hoffmann JA, Royet J. Drosophila Toll is activated by Gram-positive bacteria through a circulating peptidoglycan recognition protein. Nature 2001;414:756–759.

    Article  PubMed  CAS  Google Scholar 

  21. Rutschmann S, Jung AC, Hetru C, et al. The Rel protein DIF mediates the antifungal, but not the antibacterial, response in Drosophila. Immunity 2000;12:569–580.

    Article  PubMed  CAS  Google Scholar 

  22. Rutschmann S, Kilinc A, Ferrandon D. The Toll pathway is required for resistance to Gram-positive bacterial infections in Drosophila. J Immunol 2002;168:1542–1546.

    PubMed  CAS  Google Scholar 

  23. Lemaitre B, Meister M, Govind S, et al. Functional analysis and regulation of nuclear import of dorsal during the immune response in Drosophila. EMBO J 1995;14:536–545.

    PubMed  CAS  Google Scholar 

  24. Ip YT, Reach M, Engstrom Y, et al. Dif, a dorsal-related gene that mediates an immune-response in Drosophila. Cell 1993;75:753–763.

    Article  PubMed  CAS  Google Scholar 

  25. Dushay MS, Asling B, Hultmark D. Origins of immunity: Relish, a compound Rel-like gene in the antibacterial defense of Drosophila. Proc Natl Acad Sci USA 1996;93:10343–10347.

    Article  PubMed  CAS  Google Scholar 

  26. Meng X, Khanuja BS, Ip YT. Toll receptor-mediated Drosophila immune response requires Dif, an NF-kappaB factor. Genes Dev 1999;13:792–797.

    Article  PubMed  CAS  Google Scholar 

  27. Manfruelli P, Reichhart JM, Steward R, Hoffmann JA, Lemaitre B. A mosaic analysis in Drosophila fat body cells of the control of antimicrobial peptide genes by the Rel proteins Dorsal and DIF. EMBO J 1999;18:3380–3391.

    Article  PubMed  CAS  Google Scholar 

  28. Hedengren M, Asling B, Dushay MS, et al. Relish, a central factor in the control of humoral but not cellular immunity in Drosophila. Mol Cell 1999;4:1–20.

    Article  Google Scholar 

  29. Lemaitre B, Kromer-Metzger E, Michaut L, et al. A recessive mutation, immune deficiency (imd), defines two distinct control pathways in the Drosophila host defence. Proc Natl Acad Sci USA 1995;92:9465–9469.

    Article  PubMed  CAS  Google Scholar 

  30. Stöven S, Ando I, Kadalayil L, Engström Y, Hultmark D. Activation of the Drosophila NF-kappaB factor Relish by rapid endoproteolytic cleavage. EMBO Rep 2000;1:347–352.

    Article  PubMed  Google Scholar 

  31. Leulier F, Rodriguez A, Khush RS, Abrams JM, Lemaitre B. The Drosophila caspase Dredd is required to resist Gram-negative bacterial infections. EMBO Rep 2000;1:353–358.

    Article  PubMed  CAS  Google Scholar 

  32. Elrod-Erickson M, Mishra S, Schneider D. Interactions between the cellular and humoral immune responses in Drosophila. Curr Biol 2000;10:781–784.

    Article  PubMed  CAS  Google Scholar 

  33. Georgel P, Naitza S, Kappler C, et al. Drosophila immune deficiency (IMD) is a death domain protein that activates antibacterial defense and can promote apoptosis. Dev Cell 2001;1:503–514.

    Article  PubMed  CAS  Google Scholar 

  34. Senftleben U, Cao Y, Xiao G, et al. Activation by IKKalpha of a second, evolutionary conserved, NF-kappa B signaling pathway. Science 2001;293:1495–1499.

    Article  PubMed  CAS  Google Scholar 

  35. Silverman N, Zhou R, Stoven S, et al. A Drosophila IkappaB kinase complex required for Relish cleavage and antibacterial immunity. Genes Dev 2000;14:2461–2471.

    Article  PubMed  CAS  Google Scholar 

  36. Rutschmann S, Jung AC, Rui Z, et al. Role of Drosophila IKKy in a Toll-independent antibacterial immune response. Nat Immunol 2000;1:342–347.

    Article  PubMed  CAS  Google Scholar 

  37. Lu Y, Wu LP, Anderson KV. The antibacterial arm of the Drosophila innate immune response requires an IkappaB kinase. Genes Dev 2001;15:104–110.

    Article  PubMed  CAS  Google Scholar 

  38. Huguet C, Crepieux P, Laudet V. Rel/NF-kappa B transcription factors and I kappa B inhibitors: evolution from a unique common ancestor. Oncogene 1997;15:2965–2974.

    Article  PubMed  CAS  Google Scholar 

  39. Fernandez NQ, Grosshans J, Goltz JS, Stein D. Separable and redundant regulatory determinants in Cactus mediate its dorsal group dependent degradation. Development 2001;128:2963–2974.

    PubMed  CAS  Google Scholar 

  40. Kim YS, Han SJ, Ryu JH, et al. Lipopolysaccharide-activated kinase, an essential component for the induction of the antimicrobial peptide genes in Drosophila melanogaster cells. J Biol Chem 2000;275:2071–2079.

    Article  PubMed  CAS  Google Scholar 

  41. Wang C, Deng L, Hong M, et al. TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 2001;412:346–351.

    Article  PubMed  CAS  Google Scholar 

  42. Deng L, Wang C, Spencer E, et al. Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 2000;103:351–361.

    Article  PubMed  CAS  Google Scholar 

  43. Vidal S, Khush RS, Leulier F, et al. Mutations in the Drosophila dTAK1 gene reveal a conserved function for MAPKKKs in the control of rel/NF-ĸB dependent innate immune responses. Genes Dev 2001;15:1900–1912.

    Article  PubMed  CAS  Google Scholar 

  44. Kelliher MA, Grimm S, Ishida Y, et al. The death domain kinase RIP mediates the TNF-induced NF-kappaB signal. Immunity 1998;8:297–303.

    Article  PubMed  CAS  Google Scholar 

  45. Zhang SQ, Kovalenko A, Cantarella G, Wallach D. Recruitment of the IKK signalosome to the p55 TNF receptor: RIP and A20 bind to NEMO (IKKgamma) upon receptor stimulation. Immunity 2000;12:301–311.

    Article  PubMed  CAS  Google Scholar 

  46. Xiao T, Towb P, Wasserman SA, Sprang SR. Three-dimensional structure of a complex between the death domains of Pelle and Tube. Cell 1999;99:545–555.

    Article  PubMed  CAS  Google Scholar 

  47. Galindo RL, Edwards DN, Gillespie SK, Wasserman SA. Interaction of the pelle kinase with the membrane-associated protein tube is required for transduction of the dorsoventral signal in Drosophila embryos. Development 1995;121:2209–2218.

    PubMed  CAS  Google Scholar 

  48. Grosshans, J, Bergmann A, Haffter P, Nüsslein-Volhard C. Activation of the kinase Pelle by Tube in the dorsoventral signal transduction pathway of Drosophila embryo. Nature 1994;372:563–566.

    Article  PubMed  CAS  Google Scholar 

  49. Towb P, Galindo RL, Wasserman SA. Recruitment of Tube and Pelle to signaling sites at the surface of the Drosophila embryo. Development 1998;125:2443–2450.

    PubMed  CAS  Google Scholar 

  50. Horng T, Medzhitov R. Drosophila MyD88 is an adapter in the Toll signaling pathway. Proc Natl Acad Sci USA 2001;98:12654–12658.

    Article  PubMed  CAS  Google Scholar 

  51. Tauszig-Delamasure S, Bilak H, Capovilla M, Hoffmann JA, Imler JL. Drosophila MyD88 is required for the response to fungal and Gram-positive bacterial infections. Nat Immunol 2002;3:91–97.

    Article  PubMed  CAS  Google Scholar 

  52. LeMosy EK, Tan YQ, Hashimoto C. Activation of a protease cascade involved in patterning the Drosophila embryo. Proc Natl Acad Sci USA 2001;98:5055–5060.

    Article  PubMed  CAS  Google Scholar 

  53. Dissing M, Giordano H, DeLotto R. Autoproteolysis and feedback in a protease cascade directing Drosophila dorsal-ventral cell fate. EMBO J 2001;20:2387–2393.

    Article  PubMed  CAS  Google Scholar 

  54. Levashina EA, Langley E, Green C, et al. Constiutive activation of Toll-mediated antifungal defense in serpin-deficient Drosophila. Science 1999;285:1917–1919.

    Article  PubMed  CAS  Google Scholar 

  55. Imler J, Hoffmann JA. Toll receptors in innate immunity. Trends Cell Biol 2001;11:304–311.

    Article  PubMed  CAS  Google Scholar 

  56. Poltorak A, He X, Smirnova I, et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in T1r4 gene. Science 1998;282:2085–2088.

    Article  PubMed  CAS  Google Scholar 

  57. Takeuchi O, Hoshino K, Kawai T, et al. Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 1999;11:443–451.

    Article  PubMed  CAS  Google Scholar 

  58. Hayashi F, Smith KD, Ozinsky A, et al. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 2001;410:1099–1103.

    Article  PubMed  CAS  Google Scholar 

  59. Hemmi H, Takeuchi O, Kawai T, et al. A Toll-like receptor recognizes bacterial DNA. Nature 2000;408:740–745.

    Article  PubMed  CAS  Google Scholar 

  60. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001;413:732–738.

    Article  PubMed  CAS  Google Scholar 

  61. da Silva Correia J, Soldau K, Christen U, Tobias PS, Ulevitch RJ. Lipopolysaccharide is in close proximity to each of the proteins in its membrane receptor complex: transfer from CD 14 to TLR4 and MD-2. J Biol Chem 2001;276:21129–21135.

    Article  Google Scholar 

  62. Lien E, Means TK, Heine H, et al. Toll-like receptor 4 imparts ligand-specific recognition of bacterial lipopolysaccharide. J Clin Invest 2000;105:497–504.

    Article  PubMed  CAS  Google Scholar 

  63. Poltorak A, Ricciardi-Castagnoli P, Citterio S, Beutler B. Physical contact between lipoplysaccharide and Toll-like receptor 4 revealed by genetic complementation. Proc Natl Acad Sci USA 2000;97:2163–2167.

    Article  PubMed  CAS  Google Scholar 

  64. Viriyakosol S, Tobias PS, Kitchens RL, Kirkland TN. MD-2 binds to bacterial lipopolysaccharide. J Biol Chem 2001;276:38044–38051.

    PubMed  CAS  Google Scholar 

  65. Janeway CA. Approaching the asymptote: evolution and revolution in immunology. Cold Spring Harbor Symp Quant Biol 1989;54:1–13.

    Article  PubMed  CAS  Google Scholar 

  66. Schnare M, Barton GM, Holt AC, et al. Toll-like receptors control activation of adaptive immune responses. Nat Immunol 2001;2:947–950.

    Article  PubMed  CAS  Google Scholar 

  67. Rubin GM, Yandell MD, Wortman JR, et al. Comparative genomics of the eukaryotes. Science 2000;287:2204–2215.

    Article  PubMed  CAS  Google Scholar 

  68. Werner T, Liu G, Kang D, et al. A family of peptidoglycan recognition proteins in the fruit fly Drosophila melanogaster. Proc Natl Acad Sci USA 2000;97:13772–7.

    Article  PubMed  CAS  Google Scholar 

  69. Williams M, Rodriguez A, Kimbrell D, Eldon E. The 18-wheeler mutation reveals complex antibacterial gene regulation in Drosophila host defense. EMBO J 1997;15:6120–6130.

    Article  Google Scholar 

  70. Ligoxygakis P, Bulet P, Reichhart JM. Critical evaluation of the role of the Toll-like receptor 18-Wheeler in the host defense of Drosophila. EMBO Rep 2002;3:666–673.

    Article  PubMed  CAS  Google Scholar 

  71. Tauszig S, Jouanguy E, Hoffmann JA, Imler JL. Toll-related receptors and the control of antimicrobial peptide expression in Drosophila. Proc Natl Acad Sci USA 2000;97:10520–10525.

    Article  PubMed  CAS  Google Scholar 

  72. Lee WJ, Lee JD, Kravchenko VV, Ulevitch RJ, Brey PT. Purification and molecular cloning of an inducible gram-negative bacteria-binding protein from the silkworm, Bombyx mori. Proc Natl Acad Sci USA 1996;93:7888–7893.

    Article  PubMed  CAS  Google Scholar 

  73. Kim YS, Ryu JH, Han SJ, et al. Gram-negative bacteria-binding protein, a pattern recognition receptor for lipopolysaccharide and beta-1,3-glucan that mediates the signaling for the induction of innate immune genes in Drosophila melanogaster cells. J Biol Chem 2000;275:32721–32727.

    Article  PubMed  CAS  Google Scholar 

  74. Pimentel-Muinos FX, Seed B. Regulated commitment of TNF receptor signaling: a molecular switch for death or activation. Immunity 1999;11:783–793.

    Article  PubMed  CAS  Google Scholar 

  75. Chen P, Rodriguez A, Erskine R, Thach T, Abrams JM. Dredd, a novel effector of the apoptosis activators reaper, grim, and hid in Drosophila. Dev Biol 1998;201:202–216.

    Article  PubMed  CAS  Google Scholar 

  76. Hu S, Yang X. dFADD, a novel death domain-containing adapter protein for the Drosophila caspase DREDD. J Biol Chem 2000;275:30761–30764.

    Article  PubMed  CAS  Google Scholar 

  77. Zachary D, Hoffmann JA. The haemocytes of Calliphora erythrocephala (Meig.) (Diptera). Z Zellforsch Mikrosk Anat 1973;141:55–73.

    Article  PubMed  CAS  Google Scholar 

  78. Akai H, Sato S. Surface and internal ultrastructure of hemocytes of some insects. In: Gupta AP (ed.). Insect Hemocytes: Development, Forms, Functions and Techniques. Cambridge: Cambridge University Press, 1979, pp. 129–154.

    Chapter  Google Scholar 

  79. Iwanaga S, Kawabata S. Evolution and phylogeny of defense molecules associated with innate immunity in horseshoe crab. Front Biosci 1998;3:D973–D984.

    PubMed  CAS  Google Scholar 

  80. Rizki TM, Rizki RM. The cellular defense system of Drosophila melanogaster. In: King RC, Akai H (eds.). Insect Ultrastructure, vol 2. New York: Plenum, 1984, pp. 579–604.

    Chapter  Google Scholar 

  81. Shrestha R, Gateff E. Ultrastructure and cytochemistry of the cell types in the larval hematopoietic organs and hemolymph of Drosophila melanogaster. Dev Growth Differ 1982;24:65–82.

    Article  Google Scholar 

  82. Braun A, Hoffmann JA, Meister M. Analysis of the Drosophila host defense in domino mutant larvae, which are devoid of hemocytes. Proc Natl Acad Sci USA 1998;95:14337–14342.

    Article  PubMed  CAS  Google Scholar 

  83. Rizki TM, Rizki RM, Grell EH. A mutant affecting the crystal cells in Drosophila melanogaster. Wilhelm Rouxs Arch 1980;188:91–99.

    Article  Google Scholar 

  84. Lagueux M, Perrodou E, Levashina EA, Capovilla M, Hoffmann JA. Constitutive expression of a complement-like protein in toll and JAK gain-of-function mutants of Drosophila. Proc Natl Acad Sci USA 2000;97:11427–11432.

    Article  PubMed  CAS  Google Scholar 

  85. Levashina EA, Moita LF, Blandin S, et al. Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 2001;104:709–718.

    Article  PubMed  CAS  Google Scholar 

  86. Carton Y, Nappi AJ. The Drosophila immune reaction and the parasitoid capacity to evade it: genetic and coevolutionary aspects. Acta Oecol 1991;12:89–104.

    Google Scholar 

  87. Sparrow JC. Melanotic tumours. In: Ashburner M, Wright TRF (eds.). The Genetics and Biology of Drosophila, vol 2B. New-York: Academic, 1978, pp. 277–313.

    Google Scholar 

  88. Russo J, Dupas S, Frey F, Carton Y, Brehelin M. Insect immunity: early events in the encapsulation process of parasitoid (Leptopilina boulardi) eggs in resistant and susceptible strains of Drosophila. Parasitology 1996;112:135–142.

    Article  PubMed  Google Scholar 

  89. Lanot R, Zachary D, Holder F, Meister M. Postembryonic hematopoiesis in Drosophila. Dev Biol 2001;230:243–257.

    Article  PubMed  CAS  Google Scholar 

  90. Nappi AJ, Ottaviani E. Cytotoxicity and cytotoxic molecules in invertebrates. Bioessays 2000;22:469–480.

    Article  PubMed  CAS  Google Scholar 

  91. Nappi AJ, Vass E. Melanogenesis and the generation of cytotoxic molecules during insect cellular immune reactions. Pigment Cell Res 1993;6:117–126.

    Article  PubMed  CAS  Google Scholar 

  92. Watson KL, Johnson TK, Denell RE. Lethal(1) aberrant immune response mutations leading to melanotic tumor formation in Drosophila melanogaster. Dev Genet 1991;12:173–187.

    Article  PubMed  CAS  Google Scholar 

  93. Ashida M, Brey P. Recent advances in research on the insect prophenoloxidase cascade. In: Brey PT, Hultmark D (eds.). Molecular Mechanisms of Immune Response in Insects. London: Chapman & Hall, 1997:135–172.

    Google Scholar 

  94. Soderhall K, Cerenius L. Role of the prophenoloxidase-activating system in invertebrate immunity. Curr Opin Immunol 1998;10:23–28.

    Article  PubMed  CAS  Google Scholar 

  95. Lai-Fook J. The repair of wounds in the integument of insects. J. Insect Physiol 1966;12:195–226.

    Article  Google Scholar 

  96. Rizki TM, Rizki RM, Bellotti RA. Genetics of a Drosophila phenoloxidase. Mol Gen Genet 1985;201:7–13.

    Article  PubMed  CAS  Google Scholar 

  97. Ramet M, Lanot R, Zachary D, Manfruelli P. JNK signaling pathway is required for efficient wound healing in Drosophila. Dev Biol 2001;241:145–156.

    Article  Google Scholar 

  98. Basset A, Khush RS, Braun A, et al. The phytopathogenic bacteria Erwinia carotovora infects Drosophila and activates an immune response. Proc Natl Acad Sci USA 2000;97:3376–3381.

    PubMed  CAS  Google Scholar 

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Royet, J., Meister, M., Ferrandon, D. (2003). Humoral and Cellular Responses in Drosophila Innate Immunity. In: Ezekowitz, R.A.B., Hoffmann, J.A. (eds) Innate Immunity. Infectious Disease. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-59259-320-0_8

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