Insect immunity and its signalling: An overview

Invertebrate Survival Journal

Volumn 7, Issue 2, 2010, Pages 228-238

  Tsakas, S ^a   Marmaras, Vassilis J ^a  

^a UNIVERSITY OF PATRAS   (Greece)

Author keywords

Innate immunity; Insects; Signalling pathways

Indexed keywords

EID: 79957993822     PISSN: None     EISSN: 1824307X     Source Type: Journal    
DOI: None     Document Type: Review

References (81)

1. Aderem A, Underhill DM. Mechanisms of phagocytosis in macrophages. Annu. Rev. Immunol. 17: 593-623, 1999.
2. Agaisse H, Petersen UM, Boutros M, Mathey-Prevot B, Perrimon N. Signaling role of hemocytes in Drosophila JAK/STAT-dependent response to septic injury. Dev. Cell. 5: 441-450, 2003.
3. Aggrawal K, Silverman N. Peptidoglycan recognition in Drosophila. Biochem. Soc. Trans. 35: 1496-1500, 2007.
4. Aggarwal K, Silverman N. Positive and negative regulation of the Drosophila immune response. BMB Rep. 41: 267-277, 2008.
5. Bettencourt R, Asha H, Dearolf C, Ip YT. Hemolymph-dependent and -independent responses in Drosophila immune tissue. J. Cell. Biochem. 92: 849-863, 2004.
6. Bettencourt R, Lanz-Mendoza H, Lindquist KR, Faye I. Cell adhesion properties of hemolin, an insect immune protein in the Ig superfamily. Eur. J. Biochem. 250: 630-637, 1997.
7. Bettencourt R, Lanz-Mendoza H, Lindquist KR, Faye I. Cell adhesion properties of hemolin, an insect immune protein in the Ig superfamily. Eur. J. Biochem. 250: 630-637, 1997.
8. Bogdan C, Rollinghoff M, Diefenbach A. Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr. Opin. Immunol. 12: 64-76, 2000.
9. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128: 1089-1103, 2007.
10. Bulet P, Hetru C, Diamrco JL, Hoffmann D. Antimicrobial peptides in insect; structure and function. Dev. Comp. Immunol. 23: 329-344, 1999.
11. Bulet, P, Stocklin, R, Menin, L. Anti-microbial peptides: from invertebrates to vertebrates. Immunol. Rev. 198: 169-184. 2004.
12. Cerenius L, Söderhall K. The prophenoloxidase-activating system in invertebrates. Immunol. Rev. 198: 116-126, 2004.
13. Charalambidis ND, Zervas CG, Lambropoulou M, Katsoris PG, Marmaras VJ. Lipopolysaccharide-stimulated exocytosis of nonself recognition protein from insect hemocytes depend on protein tyrosine phosphorylation. Eur. J. Cell. Biol. 67: 32-41, 1995.
14. Daffre S, Faye I. Lipopolysaccharide interaction with hemolin, an insect member of the Ig-superfamily. FEBS Lett. 408: 127-130, 1997.
15. Ding SW, Voinnet O. Antiviral immunity directed by small RNAs. Cell 130: 413-426, 2007.
16. Eleftherianos I, Gökçen F, Felföldi G, Millichap PJ, Trenczek TE, ffrench-Constant RH, et al. The immunoglobulin family protein Hemolin mediates cellular immune responses to bacteria in the insect Manduca sexta. Cell. Microbiol. 9: 1137-1147, 2007.
17. Engström, YI. Insect immune gene regulation. In: Brey P, Hultmark D (ed), Molecular mechanisms of immune responses in insects, Chapman & Hall, London, UK, pp 211-244, 1998.
18. Fearon DT. Seeking wisdom in innate immunity. Nature 388: 323-324, 1997.
19. Feldhaar H, Gross R. Immune reactions of insects on bacterial pathogens and mutualists. Microbes Infect. 10: 1082-1088, 2008.
20. Garcia-Lara J, Needham AJ, Foster SJ. Invertebrates as animal models for Staphylococcus aureus pathogenesis: a window into host-pathogen interaction. FEMS Immunol. Med. Microbiol. 43: 311-23, 2005.
21. Gillespie JP, Kanost MR, Trenczek T. Biological mediators of insect immunity. Annu. Rev. Entomol. 42:611-643, 1997.
22. Hernandez-Martinez S, Lanz H, Rodriguez MH, Gonzalez-Ceron L, Tsutsumi V. Cellular-mediated reactions to foreign organisms inoculated into the hemocoel of Anopheles albimanus (Diptera: Culicidae). J. Med. Entomol. 39: 61-69, 2002.
23. Hillyer JF, Schmidt SL, Christensen BM. Hemocyte-mediated phagocytosis and melanization in the mosquito Armigeres subalbatus following immune challenge by bacteria. Cell Tissue Res. 313: 117-127, 2003a.
24. Hillyer JF, Schmidt SL, Christensen BM. Rapid phagocytosis and melanization of bacteria and Plasmodium sporozoites by hemocytes of the mosquito Aedes aegypti. J. Parasitol. 89: 62-69, 2003b.
25. Hoffmann JA. The immune response of Drosophila. Nature 426: 33-38, 2003.
26. Hoffmann, JA. Innate immunity of insects. Curr. Opin. Immunol. 7: 4-10, 1995.
27. Hughes AL. Evolution of the integrin alpha and beta protein families. J. Mol. Evol. 52: 63-72, 2001.
28. Hultmark D, Steiner H, Rasmuson T, Boman HG. Insect immunity. Purification and properties of three inducible bactericidal proteins from hemolymph of immunized pupae of Hyalophora cecropia. Eur. J. Biochem. 106: 7-16, 1980.
29. Humphries MJ, Travis MA, Clark K, Mould AP. Mechanisms of integration of cells and extracellular matrices by integrins. Biochem. Soc. Trans. 32: 822-825, 2004.
30. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell 110: 673-687, 2002.
31. Johansson MW, Söderhall K. The prophenoloxidase activating system and associated proteins in invertebrates. Prog. Mol. Subcell. Biol. 15: 46-66, 1996.
32. Kaneko T, Silverman N. Bacterial recognition and signalling by the Drosophila IMD pathway. Cell. Microbiol. 7: 461-469, 2005.
33. Keeley LL. Physiology and biochemistry of the fat body. In: Kerkut GA, Gilbert LI (eds), Comprehensive insect physiology, biochemistry and pharmacology. Pergamon Press, Oxford, UK, pp 211-248, 1985.
34. Kemp C, Imler J-L. Antiviral immunity in drosophila. Curr. Opin. Immunol. 21: 3-9, 2009.
35. Kim YS, Ryu JH, Han SJ, Choi KH, Nam KB, Jang IH, 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. 275: 32721-32727, 2000.
36. Lamprou I, Mamali I, Dallas K, Fertakis V, Lampropoulou M, Marmaras VJ. Distinct signalling pathways promote phagocytosis of bacteria, latex beads and lipopolysaccharide in medfly haemocytes. Immunology 121: 314-327, 2007.
37. Lamprou I, Tsakas S, Theodorou GL, Karakantza M, Lampropoulou M, Marmaras VJ. Uptake of LPS/E. coli/latex beads via distinct signalling pathways in medfly hemocytes: the role of MAP kinases activation and protein secretion. Biochim. Biophys. Acta 1744: 1-10, 2005.
38. Lavine MD, Strand MR. Insect hemocytes and their role in immunity. Insect Biochem. Mol. Biol. 32: 1295-1309, 2002.
39. Lavine MD, Strand MR. Surface characteristics of foreign targets that elicit an encapsulation response by the moth Pseudoplusia includens. J. Insect Physiol. 2001 47: 965-974, 2001.
40. Lavine MD, Strand MR. Haemocytes from Pseudoplusia includens express multiple alpha and beta integrin subunits. Insect Mol. Biol. 12: 441-452, 2003.
41. Lemaitre B, Hoffmann J. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25: 697-743, 2007.
42. Levashina EA, Moita LF, Blandin S, Vriend G, Lagueux M, Kafatos FC. Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 104: 709-718, 2001.
43. Ling E, Yu XQ. Prophenoloxidase binds to the surface of hemocytes and is involved in hemocyte melanization in Manduca sexta. Insect Biochem. Mol. Biol. 35: 1356-1366, 2005.
44. Little TJ, Cobbe N The evolution of immune-related genes from disease carrying mosquitoes: diversity in a peptidoglycan- and a thioester-recognizing protein. Insect Mol. Biol. 14: 599-605, 2005.
45. Mamali I, Lamprou I, Karagiannis F, Karakantza M, Lampropoulou M, Marmaras VJ. A beta integrin subunit regulates bacterial phagocytosis in medfly haemocytes. Dev. Comp. Immunol. 33: 858-866, 2009.
46. Marmaras VJ, Lampropoulou M. Regulators and signalling in insect haemocyte immunity. Cell Signal. 21: 186-95, 2009.
47. Mavrouli MD, Tsakas S, Theodorou GL, Lampropoulou M, Marmaras VJ. MAP kinases mediate phagocytosis and melanization via prophenoloxidase activation in medfly hemocytes. Biochim. Biophys. Acta 1744: 145-156, 2005.
48. Medzhitov R, Janeway CA Jr. Innate immunity: impact on the adaptive immune response. Curr. Opin. Immunol. 9: 4-9, 1997.
49. Meister M, Lagueux M. Drosophila blood cells. Cell. Microbiol. 5: 573-580, 2003.
50. Mellroth P, Karlsson J, Steiner H. A scavenger function for a Drosophila peptidoglycan recognition protein. J. Biol. Chem. 278: 7059-7064, 2003.
51. Michel T, Reichhart JM, Hoffmann JA, Royet J. Drosophila Toll is activated by Gram-positive bacteria through a circulating peptidoglycan recognition protein. Nature 414: 756-759, 2001.
52. Miller JS, Howard RW, Rana RL, Tunaz H, Stanley DW. Eicosanoids mediate nodulation reactions to bacterial infections in adults of the cricket, Gryllus assimilis. J. Insect Physiol. 45: 75-83, 1999.
53. Moita LF, Vriend G, Mahairaki V, Louis C, Kafatos FC. Integrins of Anopheles gambiae and a putative role of a new beta integrin, BINT2, in phagocytosis of E. coli. Insect Biochem. Mol. Biol. 36: 282-290, 2006.
54. Nakatogawa S, Oda Y, Kamiya M, Kamijima T, Aizawa T, Clark KD, et al. A novel peptide mediates aggregation and migration of hemocytes from an insect. Curr. Biol. 19: 779-785, 2009.
55. Nappi AJ, Kohler L, Mastore M. Signaling pathways implicated in the cellular innate immune responses of Drosophila. Inv. Surv. J. 1: 5-33, 2004.
56. Nappi AJ, Ottaviani E. Cytotoxicity and cytotoxic molecules in invertebrates. BioEssays 22: 469-480, 2000.
57. Nappi AJ, Vass E. Cytotoxic reactions associated with insect immunity. Adv. Exp. Med. Biol. 484: 329-348, 2001.
58. Nappi AJ, Vass E, Frey F, Carton Y. Nitric oxide involvement in Drosophila immunity. Nitric Oxide 4: 423-430, 2000.
59. Nappi AJ, Vass E, Frey F, Carton Y. Superoxide anion generation in Drosophila during melanotic encapsulation of parasites. Eur. J. Cell Biol. 68: 450-456, 1995.
60. Ribeiro C, Brehelin M. Insect haemocytes: what type of cell is that? J. Insect Physiol. 52: 417-429, 2006.
61. Roma GC, Bueno OC, Camargo-Mathias MI. Morpho-physiological analysis of the insect fat body: A review. Micron 41: 395-401, 2010.
62. Sabin LR, Hanna SL, Cherry S. Innate antiviral immunity in Drosophila. Curr. Opin. Immunol. 22: 4-9, 2010.
63. Schmidt O, Theopold, U, Strand M. Innate immunity and its evasion and suppression by hymenopteran endoparasitoids. BioEssays 23: 344-351, 2001.
64. Shia AK, Glittenberg M, Thompson G, Weber AN, Reichhart JM, Ligoxygakis P. Toll-dependent antimicrobial responses in Drosophila larval fat body require Spätzle secreted by haemocytes. J. Cell Sci. 122: 4505-4515, 2009.
65. Sideri M, Tsakas S, Markoutsa E, Lampropoulou M, Marmaras VJ. Innate immunity in insects: surface-associated dopa decarboxylase-dependent pathways regulate phagocytosis, nodulation and melanization in medfly haemocytes. Immunology 123: 528-537, 2008.
66. Silverman N, Maniatis T. NF-kappaB signaling pathways in mammalian and insect innate immunity. Genes Dev. 15: 2321-2342, 2001.
67. Silverman N, Zhou R, Erlich RL, Hunter M, Bernstein E, Schneider D, et al. Immune activation of NF-kappaB and JNK requires Drosophila TAK1. J. Biol. Chem. 278: 48928-48934, 2003.
68. Steiner H, Hultmark D, Engström A, Bennich H, Boman HG. Sequence and specificity of two antibacterial proteins involved in insect immunity. Nature 292: 246-248, 1981.
69. Theopold U, Rissler M, Fabbri M, Schmidt O, Natori S. Insect glycobiology: a lectin multigene family in Drosophila melanogaster. Biochem. Biophys. Res. Commun. 261: 923-927, 1999.
70. Vilmos P, Kurucz E. Insect immunity: evolutionary roots of the mammalian innate immune system. Immunol. Lett. 62: 59-66, 1998.
71. Wang Y, Jiang H. Binding properties of the regulatory domains in Manduca sexta hemolymph proteinase-14, an initiation enzyme of the prophenoloxidase activation system. Dev. Comp. Immunol. 34: 316-322, 2010.
72. Yount NY, Yeaman MR. Multidimensional signatures in antimicrobial peptides. Proc. Natl. Acad. Sci. USA 101: 7363-7368, 2004.
73. Yu XQ, Kanost MR. Manduca sexta lipopolysaccharide-specific immulectin-2 protects larvae from bacterial infection. Dev. Comp. Immunol. 27: 189-196, 2003.
74. Yu XQ, Kanost MR. Immulectin-2, a pattern recognition receptor that stimulates hemocyte encapsulation and melanization in the tobacco hornworm, Manduca sexta. Dev. Comp. Immunol. 28: 891-900, 2004.
75. Yu XQ, Kanost MR. Binding of hemolin to bacterial lipopolysaccharide and lipoteichoic acid. An immunoglobulin superfamily member from insects as a pattern-recognition receptor. Eur. J. Biochem. 269: 1827-1834, 2002.
76. Yu XQ, Zhu YF, Ma C, Fabrick JA, Kanost MR. Pattern recognition proteins in Manduca sexta plasma. Insect Biochem. Mol. Biol. 32: 1287-1293, 2002.
77. Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 415: 389-395, 2002.
78. Zelensky AN, Gready JE. The C-type lectin-like domain superfamily. FEBS J. 272: 6179-6217, 2005.
79. Zhao P, Li J, Wang Y, Jiang H. Broad-spectrum antimicrobial activity of the reactive compounds generated in vitro by Manduca sexta phenoloxidase. Insect Biochem. Mol. Biol. 37: 952-959, 2007.
80. Zhu Y, Johnson TJ, Myers AA, Kanost MR. Identification by subtractive suppression hybridization of bacteria-induced genes expressed in Manduca sexta fat body. Insect Biochem. Mol. Biol. 33: 541-559, 2003.
81. Zhuang S, Kelo L, Nardi JB, Kanost MR. Multiple alpha subunits of integrin are involved in cell-mediated responses of the Manduca immune system. Dev. Comp. Immunol. 32: 365-379, 2008.