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Immunity in Lepidopteran Insects

  • Haobo Jiang
  • Andreas Vilcinskas
  • Michael R. KanostEmail author
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 708)

Abstract

Lepidopteran insects provide important model systems for innate immunity of insects, particularly for cell biology of hemocytes and biochemical analyses of plasma proteins. Caterpillars are also among the most serious agricultural pests, and understanding of their immune systems has potential practical significance. An early response to infection in lepidopteran larvae is the activation of hemocyte adhesion, leading to phagocytosis, nodule formation, or encapsulation. Plasmatocytes and granular cells are the hemocyte types involved in these responses. Infectious microorganisms are recognized by binding of hemolymph plasma proteins to microbial surface components. This “pattern recognition” triggers phagocytosis and nodule formation, activation of prophenoloxidase and melanization and the synthesis of antimicrobial proteins that are secreted into the hemolymph. Many hemolymph proteins that function in such innate immune responses of insects were first discovered in lepidopterans. Microbial proteinases and nucleic acids released from lysed host cells may also activate lepidopteran immune responses. Hemolymph antimicrobial peptides and proteins can reach high concentrations and may have activity against a broad spectrum of microorganisms, contributing significantly to clearing of infections. Serine proteinase cascade pathways triggered by microbial components interacting with pattern recognition proteins stimulate activation of the cytokine Spätzle, which initiates the Toll pathway for expression of antimicrobial peptides. A proteinase cascade also results in proteolytic activation of phenoloxidase and production of melanin coatings that trap and kill parasites and pathogens. The proteinases in hemolymph are regulated by specific inhibitors, including members of the serpin superfamily. New developments in lepidopteran functional genomics should lead to much more complete understanding of the immune systems of this insect group.

Keywords

Antimicrobial Peptide Nition Protein Lepidopteran Insect Tobacco Hornworm Galleria Mellonella 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Faye I, Pye A, Rasmuson T et al. Insect immunity II. Simultaneous induction of antibacterial activity and selective synthesis of some hemolymph proteins in diapausing pupae of Hyalophora cecropia and Samia cynthia. Infect Immun 1975; 12:1426–1438.PubMedGoogle Scholar
  2. 2.
    Powning RF, Davidson WJ. Studies on the insect bacteriolytic enzymes-II. Some physical and enzymatic properties of lysozyme from haemolymph of Galleria mellonella. Comp Biochem Physiol 1976; 55:221–228.CrossRefGoogle Scholar
  3. 3.
    Hultmark D, Steiner H, Rasmuson T et al. Insect immunity. Purification and properties of three inducible bactericidal proteins from hemolymph of immunized pupae of Hyalophora cecropia. Eur J Biochem 1980; 106:7–16.PubMedCrossRefGoogle Scholar
  4. 4.
    Steiner H, Hultmark D, Engström A et al. Sequence and specificity of two antibacterial proteins involved in insect immunity. Nature 1981; 292:246–248.PubMedCrossRefGoogle Scholar
  5. 5.
    Hultmark D, Engström A, Andersson K et al. Insect immunity. Attacins, a family of antibacterial proteins from Hyalophora cecropia. EMBO J 1983; 2:571–576.PubMedGoogle Scholar
  6. 6.
    Yoshida H, Ochai M, Ashida M. β-1,3-Glucan receptor and peptidoglycan receptor are present as separate entities within insect prophenoloxidase activating system. Biochem Biophys Res Commun 1986; 114:1177–1183.CrossRefGoogle Scholar
  7. 7.
    Kanost MR, Prasad SV, Wells MA. Primary structure of a member of the serpin superfamily of proteinase inhibitors from an insect, Manduca sexta. J Biol Chem 1989; 264:965–972.PubMedGoogle Scholar
  8. 8.
    Yoshida H, Kinoshita K, Ashida M. Purification of a peptidoglycan recognition protein from hemolymph of the silkworm, Bombyx mori. J Biol Chem 1996; 271:13854–13860.PubMedCrossRefGoogle Scholar
  9. 9.
    Ochiai M, Ashida M. Purification of a β-1,3-glucan recognition protein in the prophenoloxidase system from hemolymph of the silkworm, Bombyx mori. J Biol Chem 1998; 263:12056–12062.Google Scholar
  10. 10.
    Kang D, Liu G, Lundström A et al. A peptidoglycan recognition protein in innate immunity conserved from insects to humans. Proc Natl Acad Sci USA 1998; 95:10078–10082.PubMedCrossRefGoogle Scholar
  11. 11.
    Ashida M, Brey PT. Recent advances on the research of the insect prophenoloxidase cascade. In: Brey PT Hultmark D, eds. Molecular Mechanisms of Immune Responses in Insects. London: Chapman and Hall, 1998:135–172.Google Scholar
  12. 12.
    Lavine MD, Strand MR. Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 2002; 32:1295–1309.PubMedCrossRefGoogle Scholar
  13. 13.
    Tanaka H, Ishibashi J, Fujita K et al. A genome-wide analysis of genes and gene families involved in innate immunity of Bombyx mori. Insect Biochem Mol Biol 2008; 38:1087–1110.PubMedCrossRefGoogle Scholar
  14. 14.
    Stevens JM. Bactericidal activity of the blood of actively immunized wax moth larvae. Canadian J Microbiol 1962; 8:491–499.CrossRefGoogle Scholar
  15. 15.
    Powning RF, Davidson WJ. Studies on the insect bacteriolytic enzymes-II. Some physical and enzymatic properties of lysozyme from haemolymph of Galleria mellonella. Comp Biochem Physiol 1976; 55:221–228.CrossRefGoogle Scholar
  16. 16.
    Kanost MR, Jiang H, Yu XQ. Innate immune responses of a lepidopteran insect, Manduca sexta. Immunol Rev 2004; 198:97–105.PubMedCrossRefGoogle Scholar
  17. 17.
    Jiang H. The biochemical basis of antimicrobial responses in Manduca sexta. Insect Science 2008; 15:53–66.CrossRefGoogle Scholar
  18. 18.
    Kanost MR, Gorman MJ. Phenoloxidases in insect immunity. In: Beckage NE ed. Insect Immunology. San Diego: Elsevier, 2008:69–96.CrossRefGoogle Scholar
  19. 19.
    Ragan EJ, An C, Jiang H et al. Roles of hemolymph proteins in antimicrobial defences of Manduca sexta. In: Insect Infection and Immunity. Reynolds S, Rolff J eds. Oxford University Press, 2009:34–48.Google Scholar
  20. 20.
    Dushay MS. Insect hemolymph clotting. Cell Mol Life Sci 2009; 66:2643–2650.PubMedCrossRefGoogle Scholar
  21. 21.
    Vilcinskas A. Lepidopterans as model mini-hosts for human pathogens and as a source for peptide antibiotics. In: Goldsmith M and Marec F, eds. Molecular Biology and Genetics of the Lepidoptera Boca Raton: CRC Press, 2010:293–305.Google Scholar
  22. 22.
    Kanost MR, Nardi JB. Innate immune responses of Manduca sexta. In: Goldsmith M and Marec F, eds. Molecular Biology and Genetics of the Lepidoptera Boca Raton: CRC Press, 2010:271–291.Google Scholar
  23. 23.
    Mukherjee K, Altincicek B, Hain T et al. Galleria mellonella as a model system for studying Listeria pathogenesis. Appl Environ Microbiol. 2010; 76:310–317.PubMedCrossRefGoogle Scholar
  24. 24.
    Mullett H, Ratcliffe NA, Rowley AF. The generation and characterization of anti-insect blood cell monoclonal antibodies. J. Cell Sci 1992; 105:93–100.Google Scholar
  25. 25.
    Willott E, Trenczek T, Thrower LW et al. Immunochemical identification of insect hemocyte populations: monoclonal antibodies distinguish four major hemocyte types in Manduca sexta. Eur J Cell Biol 1994; 65:417–423.PubMedGoogle Scholar
  26. 26.
    Gardiner EM, Strand MR. Monoclonal antibodies bind distinct classes of hemocytes in the moth Pseudoplusia includens. J Insect Physiol 1999; 45:113–126.PubMedCrossRefGoogle Scholar
  27. 27.
    Nardi JB, Pilas B, Bee CM et al. Neuroglian-positive plasmatocytes of Manduca sexta and the initiation of hemocyte attachment to foreign surfaces. Dev Comp Immunol 2006; 30:447–462.PubMedCrossRefGoogle Scholar
  28. 28.
    Gardiner EM, Strand MR. Hematopoiesis in larval Pseudoplusia includens and Spodoptera frugiperda. Arch Insect Biochem Physiol 2000; 43:147–164.PubMedCrossRefGoogle Scholar
  29. 29.
    Beetz S, Holthusen TK, Koolman J et al. Correlation of hemocyte counts with different developmental parameters during the last larval instar of the tobacco hornworm, Manduca sexta. Arch Insect Biochem Physiol 2008; 67:63–75.PubMedCrossRefGoogle Scholar
  30. 30.
    Nardi JB. Embryonic origins of the two main classes of hemocytes—granular cells and plasmatocytes—in Manduca sexta. Dev Genes Evol 2004; 214:19–28.PubMedCrossRefGoogle Scholar
  31. 31.
    Nardi JB, Pilas B, Ujhelyi E et al. Hematopoietic organs of Manduca sexta and hemocyte lineages. Dev Genes Evol 2003; 213(10):477–491.PubMedCrossRefGoogle Scholar
  32. 32.
    Schmidt O, Söderhäll K, Theopold U et al. Role of adhesion in arthropod immune recognition. Annu Rev Entomol 2010; 55:485–504.PubMedCrossRefGoogle Scholar
  33. 33.
    Dean P, Potter U, Richards EH et al. Hyperphagocytic haemocytes in Manduca sexta. J Insect Physiol 2004; 50:1027–1036.PubMedCrossRefGoogle Scholar
  34. 34.
    Nardi JB, Pilas B, Bee CM et al. Neuroglian-positive plasmatocytes of Manduca sexta and the initiation of hemocyte attachment to foreign surfaces. Dev Comp Immunol 2006; 30:447–462.PubMedCrossRefGoogle Scholar
  35. 35.
    Nakatogawa S, Oda Y, Kamiya M et al. A novel peptide mediates aggregation and migration of hemocytes from an insect. Curr Biol 2009; 19:779–785.PubMedCrossRefGoogle Scholar
  36. 36.
    Clark KD, Pech LL, Strand MR. Isolation and identification of a plasmatocyte-spreading peptide from the hemolymph of the lepidopteran insect Pseudoplusia includens. J Biol Chem 1997; 272:23440–23447.PubMedCrossRefGoogle Scholar
  37. 37.
    Wang Y, Jiang H, Kanost MR. Biological activity of Manduca sexta paralytic and plasmatocyte spreading peptide and primary structure of its hemolymph precursor. Insect Biochem Mol Biol 1999; 29:1075–1086.PubMedCrossRefGoogle Scholar
  38. 38.
    Strand MR, Hayakawa Y, Clark KD. Plasmatocyte spreading peptide (PSP1) and growth blocking peptide (GBP) are multifunctional homologs. J Insect Physiol 2000; 46:817–824.PubMedCrossRefGoogle Scholar
  39. 39.
    Volkman BF, Anderson ME, Clark KD et al. Structure of the insect cytokine peptide plasmatocyte-spreading peptide 1 from Pseudoplusia includens. J Biol Chem 1999; 274:4493–4496.PubMedCrossRefGoogle Scholar
  40. 40.
    Matsumoto Y, Oda Y, Uryu M et al. Insect cytokine growth-blocking peptide triggers a termination system of cellular immunity by inducing its binding protein. J Biol Chem 2003; 278:38579–38585.PubMedCrossRefGoogle Scholar
  41. 41.
    Eleftherianos I, Xu M, Yadi H et al. Plasmatocyte-spreading peptide (PSP) plays a central role in insect cellular immune defenses against bacterial infection. J Exp Biol 2009; 212(Pt 12):1840–1848.PubMedCrossRefGoogle Scholar
  42. 42.
    Stanley D. Prostaglandins and other eicosanoids in insects: biological significance. Annu Rev Entomol 2006; 51:25–44.PubMedCrossRefGoogle Scholar
  43. 43.
    Shrestha S, Kim Y. Various eicosanoids modulate the cellular and humoral immune responses of the beet armyworm, Spodoptera exigua. Biosci Biotechnol Biochem 2009; 73:2077–2084.PubMedCrossRefGoogle Scholar
  44. 44.
    Shrestha S, Kim Y. Eicosanoids mediate prophenoloxidase release from oenocytoids in the beet armyworm Spodoptera exigua. Insect Biochem Mol Biol 2008; 38:99–112.PubMedCrossRefGoogle Scholar
  45. 45.
    Lavine MD, Strand MR. Haemocytes from Pseudoplusia includens express multiple alpha and beta integrin subunits. Insect Mol Biol 2003; 12:441–452.PubMedCrossRefGoogle Scholar
  46. 46.
    Wiegand C, Levin D, Gillespie J et al. Monoclonal antibody MS13 identifies a plasmatocyte membrane protein and inhibits encapsulation and spreading reactions of Manduca sexta hemocytes. Arch Insect Biochem Physiol 2000; 45:95–108.PubMedCrossRefGoogle Scholar
  47. 47.
    Levin DM, Breuer LN, Zhuang S et al. A hemocyte-specific integrin required for hemocytic encapsulation in the tobacco hornworm, Manduca sexta. Insect Biochem Mol Biol 2005; 35:369–380.PubMedCrossRefGoogle Scholar
  48. 48.
    Nardi JB, Zhuang S, Pilas B et al. Clustering of adhesion receptors following exposure of insect blood cells to foreign surfaces. J Insect Physiol 2005; 51:555–564.PubMedCrossRefGoogle Scholar
  49. 49.
    Zhuang S, Kelo L, Nardi JB. An integrin-tetraspanin interaction required for cellular innate immune responses of an insect, Manduca sexta. J Biol Chem 2007; 282:22563–22572.PubMedCrossRefGoogle Scholar
  50. 50.
    Zhuang S, Kelo L, Nardi JB et al. Multiple alpha subunits of integrin are involved in cell-mediated responses of the Manduca immune system. Dev Comp Immunol 2008; 32:365–379.PubMedCrossRefGoogle Scholar
  51. 51.
    Zhuang S, Kelo L, Nardi JB et al. Neuroglian on hemocyte surfaces is involved in homophilic and heterophilic interactions of the innate immune system of Manduca sexta. Dev Comp Immunol 2007; 31:1159–1167.PubMedCrossRefGoogle Scholar
  52. 52.
    Andersson K, Steiner H. Structure and properties of protein P4, the major bacteria-inducible protein in pupae of Hyalophora cecropia. Insect Biochem 1987; 17:133–140.CrossRefGoogle Scholar
  53. 53.
    Sun SC, Lindstöm I, Boman HG et al. Hemolin: an insect immune protein belonging to the immunoglobulin superfamily. Science 1990; 250:1729–1732.PubMedCrossRefGoogle Scholar
  54. 54.
    Ladendorff NE, Kanost MR. Isolation and characterization of bacteria induced protein P4 from hemolymph of Manduca sexta. Arch Insect Biochem Physiol 1990; 15:33–41.PubMedCrossRefGoogle Scholar
  55. 55.
    Ladendorff NE, Kanost MR. Bacteria-induced protein P4 (hemolin) from Manduca sexta: a member of the immunoglobulin superfamily which can inhibit hemocyte aggregation. Arch Insect Biochem Physiol 1991; 18:285–300.PubMedCrossRefGoogle Scholar
  56. 56.
    Shin SW, Park SS, Park DS et al. Isolation and characterization of immune-related genes from the fall webworm, Hyphantria cunea, using PCR-based differential display and subtractive cloning. Insect Biochem Mol Biol 1998; 28:827–837.PubMedCrossRefGoogle Scholar
  57. 57.
    Lee KY, Horodyski FM, Valaitis AP et al. Molecular characterization of the insect immune protein hemolin and its high induction during embryonic diapause in the gypsy moth, Lymantria dispar. Insect Biochem Mol Biol 2002; 32:1457–1467.PubMedCrossRefGoogle Scholar
  58. 58.
    Li W, Terenius O, Hirai M et al. Cloning, expression and phylogenetic analysis of hemolin, from the Chinese oak silk moth, Antheraea pernyi. Dev Comp Immunol 2005; 29:853–864.PubMedCrossRefGoogle Scholar
  59. 59.
    Gandhe AS, Arunkumar KP, John SH et al. Analysis of bacteria-challenged wild silkmoth, Antheraea mylitta (Lepidoptera) transcriptome reveals potential immune genes. BMC Genomics 2006; 7:184.PubMedCrossRefGoogle Scholar
  60. 60.
    Eum JH, Seo YR, Yoe SM et al. Analysis of the immune-inducible genes of Plutella xylostella using expressed sequence tags and cDNA microarray. Dev Comp Immunol 2007; 31:1107–1120PubMedCrossRefGoogle Scholar
  61. 61.
    Bao Y, Yamano Y, Morishima I. Induction of hemolin gene expression by bacterial cell wall components in eri-silkworm, Samia cynthia ricini. Comp Biochem Physiol Part B 2007; 146:147–151.CrossRefGoogle Scholar
  62. 62.
    Faye I, Kanost MR. Function and regulation of hemolin. In: Brey PT, Hultmark D eds. Molecular Mechanisms of Immune Responses in Insects. London: Chapman and Hall, 1998:173–188.Google Scholar
  63. 63.
    Gibson NJ, Tolbert LP. Activation of epidermal growth factor receptor mediates receptor axon sorting and extension in the developing olfactory system of the moth Manduca sexta. J Comp Neurol 2006; 495:554–572.PubMedCrossRefGoogle Scholar
  64. 64.
    Chen CL, Lampe DJ, Robertson HM et al. Neuroglian is expressed on cells destined to form the prothoracic glands of Manduca embryos as they segregate from surrounding cells and rearrange during morphogenesis. Dev Biol 1997; 181:1–13.PubMedCrossRefGoogle Scholar
  65. 65.
    Roxström-Lindquist K, Lindström-Dinnetz I, Olesen J et al. An intron enhancer activates the immunoglobulin-related hemolin gene in Hyalophora cecropia. Insect Mol Biol 2002; 11:505–515.PubMedCrossRefGoogle Scholar
  66. 66.
    Yu XQ, Kanost MR. Developmental expression of Manduca sexta hemolin. Arch Insect Biochem Physiol 1999; 42:198–212.PubMedCrossRefGoogle Scholar
  67. 67.
    Roxström-Lindquist K, Assefaw-Redda Y, Rosinska K et al. 20-hydroxyecdysone indirectly regulates hemolin gene expression in Hyalophora cecropia. Insect Mol Biol 2005; 14:645–652.PubMedCrossRefGoogle Scholar
  68. 68.
    Terenius O. Hemolin-A lepidopteran anti-viral defense factor? Dev Comp Immunol 2008; 32:311–316.PubMedCrossRefGoogle Scholar
  69. 69.
    Hirai M, Terenius O, Li W et al. Baculovirus and dsRNA induce hemolin, but no antibacterial activity in Antheraea pernyi. Insect Mol Biol 2004; 13:399–405.PubMedCrossRefGoogle Scholar
  70. 70.
    Terenius O, Popham HJ, Shelby KS. Bacterial, but not baculoviral infections stimulate hemolin expression in noctuid moths. Dev Comp Immunol 2009; 33:1176–1185.PubMedCrossRefGoogle Scholar
  71. 71.
    Daffre S, Faye I. Lipopolysaccharide interaction with hemolin, an insect member of the Ig-superfamily. FEBS Lett 1997; 408:127–130.PubMedCrossRefGoogle Scholar
  72. 72.
    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 2002; 269:1827–1834.PubMedCrossRefGoogle Scholar
  73. 73.
    Zhao L, Kanost MR. In search of a function for hemolin, a hemolymph protein from the immunoglobulin superfamily. J Insect Physiol 1996; 42:73–79.CrossRefGoogle Scholar
  74. 74.
    Bettencourt R, Lanz-Mendoza H, Lindquist KR et al. Cell adhesion properties of hemolin, an insect immune protein in the Ig superfamily. Eur J Biochem 1997; 250:630–637.PubMedCrossRefGoogle Scholar
  75. 75.
    Su XD, Gastinel LN, Vaughn DE et al. Crystal structure of hemolin: a horseshoe shape with implications for homophilic adhesion. Science 1998; 281:991–995.PubMedCrossRefGoogle Scholar
  76. 76.
    Eleftherianos I, Gokcen F, Felfoldi G et al. The immunoglobulin family protein hemolin mediates cellular immune responses to bacteria in the insect Manduca sexta. Cellular Microbiol 2007; 9:1137–1147.CrossRefGoogle Scholar
  77. 77.
    Dziarski R, Gupta D. The peptidoglycan recognition proteins (PGRPs). Genome Biol 2006; 7:232.PubMedCrossRefGoogle Scholar
  78. 78.
    Ochiai M, Ashida M. A pattern recognition protein for peptidoglycan. Cloning the cDNA and the gene of the silkworm, Bombyx mori. J Biol Chem 1999; 274:11854–11858.PubMedCrossRefGoogle Scholar
  79. 79.
    Yu XQ, Zhu YF, Ma C et al. Pattern recognition proteins in Manduca sexta plasma. Insect Biochem Mol Biol 2002; 32:1287–1293.PubMedCrossRefGoogle Scholar
  80. 80.
    Zhu Y, Johnson T, Kanost MR. Identification of differentially expressed genes in the immune response of the tobacco hornworm, Manduca sexta. Insect Biochem Mol Biol 2003; 33:541–559.PubMedCrossRefGoogle Scholar
  81. 81.
    Zou Z, Najar F, Wang Y et al. Pyrosequence analysis of expressed sequence tags for Manduca sexta hemolymph proteins involved in immune responses. Insect Biochem Mol Biol 2008; 38:677–682.PubMedCrossRefGoogle Scholar
  82. 82.
    Seitz V, Clermont A, Wedde M et al. Identification of immunorelevant genes from greater wax moth (Galleria mellonella) by a subtractive hybridization approach. Dev Comp Immunol 2003; 27:207–215.PubMedCrossRefGoogle Scholar
  83. 83.
    Onoe H, Matsumoto A, Hashimoto K et al. Peptidoglycan recognition protein (PGRP) from eri-silkworm, Samia cynthia ricini; protein purification and induction of the gene expression. Comp Biochem Physiol B 2007; 147:512–519.PubMedCrossRefGoogle Scholar
  84. 84.
    Hashimoto K, Mega K, Matsumoto Y et al. Three peptidoglycan recognition protein (PGRP) genes encoding potential amidase from eri-silkworm, Samia cynthia ricini. Comp Biochem Physiol B Biochem Mol Biol 2007; 148:322–328.PubMedCrossRefGoogle Scholar
  85. 85.
    Coates BS, Sumerford DV, Hellmich RL et al. Mining an Ostrinia nubilalis midgut expressed sequence tag (EST) library for candidate genes and single nucleotide polymorphisms (SNPs). Insect Mol Biol 2008; 17:607–620.PubMedCrossRefGoogle Scholar
  86. 86.
    Mellroth P, Karlsson J, Steiner H. A scavenger function for a Drosophila peptidoglycan recognition protein. J Biol Chem 2003; 278:7059–7064.PubMedCrossRefGoogle Scholar
  87. 87.
    Ragan EJ. Immune-related protein complexes and serpin-1 isoforms in Manduca sexta plasma. PhD Dissertation, Kansas State University. 2008.Google Scholar
  88. 88.
    Sumathipala N. Expression, purification and characterization of peptidoglycan recognition protein 1 from Manduca sexta (L.). MS Thesis, Oklahoma State University. 2009.Google Scholar
  89. 89.
    Eleftherianos I, Marokhazi J, Millichap PJ et al. Prior infection of Manduca sexta with nonpathogenic Escherichia coli elicits immunity to pathogenic Photorhabdus luminescens: roles of immune-related proteins shown by RNA interference. Insect Biochem Mol Biol 2006; 36:517–525.PubMedCrossRefGoogle Scholar
  90. 90.
    Eleftherianos I, Millichap PJ, ffrench-Constant RH et al. RNAi suppression of recognition protein mediated immune responses in the tobacco hornworm Manduca sexta causes increased susceptibility to the insect pathogen Photorhabdus. Dev Comp Immunol 2006; 30:1099–1107.PubMedCrossRefGoogle Scholar
  91. 91.
    Royet J, Dziarski R. Peptidoglycan recognition proteins: pleiotropic sensors and effectors of antimicrobial defences. Nat Rev Microbiol 2007; 5:264–277.PubMedCrossRefGoogle Scholar
  92. 92.
    Charroux B, Rival T, Narbonne-Reveau K et al. Bacterial detection by Drosophila peptidoglycan recognition proteins. Microbes Infect 2009; 11:631–636.PubMedCrossRefGoogle Scholar
  93. 93.
    Ochiai M, Ashida M. Apattern-recognition protein for β-1,3-glucan: the binding domain and the cDNA cloning of β-1,3-glucan recognition protein from the silkworm, Bombyx mori. J Biol Chem 2000; 275:4995–5002.PubMedCrossRefGoogle Scholar
  94. 94.
    Ma C, Kanost MR. A β-1,3-glucan recognition protein from an insect, Manduca sexta, agglutinates microorganisms and activates the phenoloxidase cascade. J Biol Chem 2000; 275:7505–7514.PubMedCrossRefGoogle Scholar
  95. 95.
    Jiang H, Ma C, Lu ZQ et al β-1,3-glucan recognition protein-2 (βGRP-2) from Manduca sexta: an acute-phase protein that binds β-1,3-glucan and lipoteichoic acid to aggregate fungi and bacteria and stimulate prophenoloxidase activation. Insect Biochem Mol Biol 2004; 34:89–100.PubMedCrossRefGoogle Scholar
  96. 96.
    Fabrick JA, Baker JE, Kanost MR. cDNA cloning, purification, properties and function of a beta-1,3-glucan recognition protein from a pyralid moth, Plodia interpunctella. Insect Biochem Mol Biol 2003; 33:579–594.PubMedCrossRefGoogle Scholar
  97. 97.
    Fabrick JA, Baker JE, Kanost MR. Innate immunity in a pyralid moth: functional evaluation of domains from a β-1,3-glucan recognition protein. J Biol Chem 2004; 279:26605–26611.PubMedCrossRefGoogle Scholar
  98. 98.
    Takahasi K, Ochiai M, Horiuchi M et al. Solution structure of the silkworm βGRP/GNBP3 N-terminal domain reveals the mechanism for β-1,3-glucan-specific recognition. Proc Natl Acad Sci USA 2009; 106:11679–11684.PubMedCrossRefGoogle Scholar
  99. 99.
    Wang Y, Jiang H. Interaction of β-1,3-glucan with its recognition protein activates hemolymph proteinase 14, an initiation enzyme of the prophenoloxidase activation system in Manduca sexta. J Biol Chem 2006; 281:9271–9278.PubMedCrossRefGoogle Scholar
  100. 100.
    Wang Y, Jiang H. Bindingproperties of the regulatory domains in Manduca sexta hemolymph proteinase-14, an initiation enzyme of the prophenoloxidase activation system. Dev Comp Immunol 2010; 34:316–322.PubMedCrossRefGoogle Scholar
  101. 101.
    Lee WJ, Lee JD, Kravchenko VV et al. 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.PubMedCrossRefGoogle Scholar
  102. 102.
    Pauchet Y, Freitak D, Heidel-Fischer HM et al. Immunity or digestion: glucanase activity in a glucan-binding protein family from Lepidoptera. J Biol Chem 2009; 284:2214–2224.PubMedCrossRefGoogle Scholar
  103. 103.
    Vasta GR, Quesenberry M, Ahmed H et al. C-type lectins and galectins mediate innate and adaptive immune functions: their roles in the complement activation pathway. Dev Comp Immunol 1999; 23,401–420.PubMedCrossRefGoogle Scholar
  104. 104.
    Koizumi N, Morozumi A, Imamura M et al. Lipopolysaccharide-binding proteins and their involvement in the bacterial clearance from the hemolymph of the silkworm Bombyx mori. Eur J Biochem 1997; 248:217–224.PubMedCrossRefGoogle Scholar
  105. 105.
    Koizumi N, Imai Y, Morozumi A et al. Lipopolysaccharide-binding protein of Bombyx mori participates in a hemocyte-mediated defense reaction against Gram-negative bacteria. J Insect Physiol 1999; 45:853–859.PubMedCrossRefGoogle Scholar
  106. 106.
    Shin SW, Park DS, Kim SC et al. Two carbohydrate recognition domains of Hyphantria cunea lectin bind to bacterial lipopolysaccharides through O-specific chain. FEBS Lett 2000; 467:70–74.PubMedCrossRefGoogle Scholar
  107. 107.
    Yu XQ, Gan H, Kanost MR. Immulectin, an inducible C-type lectin from an insect, Manduca sexta, stimulates activation of plasma prophenol oxidase. Insect Biochem Mol Biol 1999; 29:585–597.PubMedCrossRefGoogle Scholar
  108. 108.
    Yu XQ, Kanost MR. Immulectin-2, a lipopolysaccharide-specific lectin from an insect, Manduca sexta, is induced in response to Gram-negative bacteria. J Biol Chem 2000; 275:37373–37381.PubMedCrossRefGoogle Scholar
  109. 109.
    Yu XQ, Tracy ME, Ling E et al. A novel C-type immulectin-3 from Manduca sexta is translocated from hemolymph into the cytoplasm of hemocytes. Insect Biochem Mol Biol 2005; 35:285–295.PubMedCrossRefGoogle Scholar
  110. 110.
    Yu XQ, Ling E, Tracy ME et al. Immulectin-4 from the tobacco hornworm Manduca sexta binds to lipopolysaccharide and lipoteichoic acid. Insect Mol Biol 2006; 15:119–128.PubMedCrossRefGoogle Scholar
  111. 111.
    Watanabe A, Miyazawa S, Kitami M et al. Characterization of a novel C-type lectin, Bombyx mori multibinding protein, from the B. mori hemolymph. J Immunol 2006; 177:4594–4604.PubMedGoogle Scholar
  112. 112.
    Kim SR, Lee KS, Kim I et al. cDNA sequence of a novel immulectin homologue from the silkworm, Bombyx mori. Int J Indust Entomol 2003; 6:99–102.Google Scholar
  113. 113.
    Takase H, Watanabe A, Yoshizawa Y et al. Identification and comparative analysis of three novel C-type lectins from the silkworm with functional implications in pathogen recognition. Dev Comp Immunol 2009; 33:789–800.PubMedCrossRefGoogle Scholar
  114. 114.
    Chai LQ, Tian YY, Yang DT et al. Molecular cloning and characterization of a C-type lectin from the cotton bollworm, Helicoverpa armigera. Dev Comp Immunol 2008; 32:71–83.PubMedCrossRefGoogle Scholar
  115. 115.
    Zou Z, Evans J, Lu Z et al. Comparative genome analysis of the Tribolium immune system. Genome Biol 2007; 8:R177.PubMedCrossRefGoogle Scholar
  116. 116.
    Yu XQ, Kanost MR. Manduca sexta lipopolysaccharide-specific immulectin-2 protects larvae from bacterial infection. Dev Comp Immunol 2003; 27:189–196.PubMedCrossRefGoogle Scholar
  117. 117.
    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 2004; 28:891–900.PubMedCrossRefGoogle Scholar
  118. 118.
    Ling E, Yu XQ. Cellular encapsulation and melanization are enhanced by immulectins, pattern recognition receptors from the tobacco hornworm Manduca sexta. Dev Comp Immunol 2006; 30:289–299.PubMedCrossRefGoogle Scholar
  119. 119.
    Van der Horst DJ, Roosendaal SD, Rodenburg KW. Circulatory lipid transport: lipoprotein assembly and function from an evolutionary perspective. Mol Cell Biochem. 2009; 326:105–119.PubMedCrossRefGoogle Scholar
  120. 120.
    Li D, Scherfer C, Korayem AM et al. Insect hemolymph clotting: evidence for interaction between the coagulation system and the prophenoloxidase activating cascade. Insect Biochem Mol Biol 2002; 32:919–928.PubMedCrossRefGoogle Scholar
  121. 121.
    Ma G, Hay D, Li D et al. Recognition and inactivation of LPS by lipophorin particles. Dev Comp Immunol 2006; 30:619–626.PubMedCrossRefGoogle Scholar
  122. 122.
    Rahman MM, Ma G, Roberts HL et al. Cell-free immune reactions in insects. J Insect Physiol 2006; 52:754–762.PubMedCrossRefGoogle Scholar
  123. 123.
    Kato Y, Motoi Y, Taniai K et al. Lipopolysaccharide-lipophorin complex formation in insect hemolymph: a common pathway of lipopolysaccharide detoxification both in insects and in mammals. Insect Biochem Mol Biol 1994; 24:547–555.PubMedCrossRefGoogle Scholar
  124. 124.
    Dunphy G, Halwani A. Haemolymph proteins of larvae of Galleria mellonella detoxify endotoxins of the insect pathogenic bacteria Xenhorabdus nematophilus (Enterobacteriaceae). J Insect Physiol 1997; 43:1023–1029.PubMedCrossRefGoogle Scholar
  125. 125.
    Halwani AE, Niven DF, Dunphy GB. Apolipophorin-III and the interactions of lipoteichoic acids with the immediate immune responses of Galleria mellonella. J Invertebr Pathol 2000; 76:233–241.PubMedCrossRefGoogle Scholar
  126. 126.
    Pratt CC, Weers PM. Lipopolysaccharide binding of an exchangeable apolipoprotein, apolipophorin III, from Galleria mellonella. Biol Chem 2004; 385:1113–1119.PubMedCrossRefGoogle Scholar
  127. 127.
    Kim HJ, Je HJ, Park SY et al. Immune activation of apolipophorin-III and its distribution in hemocyte from Hyphantria cunea. Insect Biochem Mol Biol 2004; 34:1011–1023.PubMedCrossRefGoogle Scholar
  128. 128.
    Leon LJ, Idangodage H, Wan CP et al. Apolipophorin III: lipopolysaccharide binding requires helix bundle opening. Biochem Biophys Res Commun 2006; 348:1328–1333.PubMedCrossRefGoogle Scholar
  129. 129.
    Weisner A, Losen S, Kopacek P et al. Isolated apolipophorin III from Galleria mellonella stimulates the immune reaction of this insect. J Insect Physiol 1997; 43:383–391.CrossRefGoogle Scholar
  130. 130.
    Halwani AE, Dunphy GB. Apolipophorin-III in Galleria mellonella potentiates hemolymph lytic activity. Dev Comp Immunol 1999; 23:563–570.PubMedCrossRefGoogle Scholar
  131. 131.
    Iimura Y, Ishikawa H, Yamamoto K et al. Hemagglutinating properties of apolipophorin III from the hemolymph of Galleria mellonella larvae. Arch Insect Biochem Physiol 1998; 38:119–125.PubMedCrossRefGoogle Scholar
  132. 132.
    Halwani AE, Niven DF, Dunphy GB. Apolipophorin-III in the greater wax moth, Galleria mellonella (Lepidoptera: Pyralidae). Arch Insect Biochem Physiol 2001; 48:135–143.PubMedCrossRefGoogle Scholar
  133. 133.
    Whitten MM, Tew IF, Lee BL et al. A novel role for an insect apolipoprotein (apolipophorin III) in gb-1,3-glucan pattern recognition and cellular encapsulation reactions. J Immunol 2004; 172:2177–2185.PubMedGoogle Scholar
  134. 134.
    St. Leger RJ, Bidochka MJ, Roberts DW. Isoforms of the cuticle-degrading Pr1 proteinase and production of a metalloproteinase by Metarhizium anisopliae. Arch Biochem Biophys 1994; 313:1–7.CrossRefGoogle Scholar
  135. 135.
    Fedhila S, Nel P, Lereclus D. The InhA2 metalloprotease of Bacillus thuringiensis strain 407 is required for pathogenicity in insects infected via the oral route. J Bacteriol. 2002; 184:3296–3304.PubMedCrossRefGoogle Scholar
  136. 136.
    Held KG, LaRock CN, D’Argenio DA et al. Ametalloprotease secreted by the insect pathogen Photorhabdus luminescens induces melanization. Appl Environ Microbiol 2007; 73(23):7622–7628.PubMedCrossRefGoogle Scholar
  137. 137.
    Qazi SS, Khachatourians GG. Hydrated conidia of Metarhizium anisopliae release a family of metalloproteases. J Invertebr Pathol 2007; 95:48–59.PubMedCrossRefGoogle Scholar
  138. 138.
    Griesch J, Wedde M, Vilcinskas A. Recognition and regulation of metalloproteinase activity in the haemolymph of Galleria mellonella: a new pathway mediating induction of humoral immune responses. Insect Biochem Mol Biol 2000; 30:461–472.PubMedCrossRefGoogle Scholar
  139. 139.
    Altincicek B, Linder M, Linder D et al. Microbial metalloproteinases mediate sensing of invading pathogens and activate innate immune responses in the lepidopteran model host Galleria mellonella. Infect Immun 2007; 75:175–183.PubMedCrossRefGoogle Scholar
  140. 140.
    Altincicek B, Berisha A, Mukherjee K et al. Identification of collagen IV derived danger/alarm signals in insect immunity by nanoLC-FTICR MS. Biological Chemistry 2009; 390:1303–1311.PubMedCrossRefGoogle Scholar
  141. 141.
    Matzinger P. The danger model: a renewed sense of self. Science 2002; 296:301–305.PubMedCrossRefGoogle Scholar
  142. 142.
    Vilcinskas A, Wedde M. Inhibition of Beauveria bassiana proteases and fungal development by inducible protease inhibitors in the haemolymph of Galleria mellonella larvae. Biocontrol Sci Technol 1997; 7:591–601.CrossRefGoogle Scholar
  143. 143.
    Clermont A, Wedde M, Seitz V et al. Cloning and expression of an inhibitor against microbial metalloproteinases from insects (IMPI) contributing to innate immunity. Biochem J 2004; 382:315–322.PubMedCrossRefGoogle Scholar
  144. 144.
    Wedde M, Weise C, Nuck C et al. The insect metallo-proteinase inhibitor gene of the lepidopteran Galleria mellonella encodes two distinct inhibitors. Biol Chem 2007; 388:119–127.PubMedCrossRefGoogle Scholar
  145. 145.
    Kim I, Kim SH, Lee YS et al. Immune stimulation in the silkworm, Bombyx mori L., by CpG oligodeoxy-nucleotides. Arch Insect Biochem Physiol 2004; 55:43–48.PubMedCrossRefGoogle Scholar
  146. 146.
    Altincicek B, Stötzel S, Wygrecka M et al. Host-derived extracellular nucleic acids enhance innate immune responses, induce coagulation and prolong survival upon infection in insects. J Immunol 2008; 181:2705–2712.PubMedGoogle Scholar
  147. 147.
    Lavine MD, Chen G, Strand MR. Immune challenge differentially affects transcript abundance of three antimicrobial peptides in hemocytes from the moth Pseudoplusia includens. Insect Biochem Mol Biol 2005; 35:1335–1346.PubMedCrossRefGoogle Scholar
  148. 148.
    Dunn PE, Bohnert TJ, Russell V. Regulation of antibacterial protein synthesis following infection and during metamorphosis of Manduca sexta. Ann N Y Acad Sci 1994; 712:117–130.PubMedCrossRefGoogle Scholar
  149. 149.
    Gorman MJ, Kankanala P, Kanost MR. Bacterial challenge stimulates innate immune responses in extra-embryonic tissues of tobacco hornworm eggs. Insect Mol Biol 2004; 13:19–24.PubMedCrossRefGoogle Scholar
  150. 150.
    Mohrig W, Messner B. Immunreaktionen bei Insekten. I. Lysozyme als grundlegender antibakterieller Faktor im humoralen Abwehrgeschehen. Biol Zentralbl 1968; 87:439–447.Google Scholar
  151. 151.
    Jolies J, Schoentgen F, Croizier G et al. Insect lysozymes from three species of Lepidoptera: Their structural relatedness to the C (chicken) type lysozyme. J Mol Evol 1979; 14:267–271.CrossRefGoogle Scholar
  152. 152.
    Yu KH, Kim KN, Lee JH et al. Comparative study on characteristics of lysozymes from the hemolymph of three lepidopteran larvae, Galleria mellonella, Bombyx mori, Agrius convolvuli. Dev Comp Immunol 2002; 26:707–713.PubMedCrossRefGoogle Scholar
  153. 153.
    Chapelle M, Girard PA, Cousserans F et al. Lysozymes and lysozyme-like proteins from the fall armyworm, Spodoptera frugiperda. Mol Immunol 2009; 47:261–269.PubMedCrossRefGoogle Scholar
  154. 154.
    Wang WX, Wang YP, Deng XJ et al. Molecular and functional characterization of a c-type lysozyme from the Asian corn borer, Ostrinia furnacalis. J Insect Sci 2009; 9:17.PubMedCrossRefGoogle Scholar
  155. 155.
    Vilcinskas A, Matha V. Effect of the entomopathogenic fungus Beauveria bassiana on humoral immune response of Galleria mellonella larvae (Lepidoptera: Pyralidae). Eur J Entomol 1997; 94:461–472.Google Scholar
  156. 156.
    Rao XJ, Ling E, Yu XQ. The role of lysozyme in the prophenoloxidase activation system of Manduca sexta: an in vitro approach. Dev Comp Immunol 2010; 34:264–271.PubMedCrossRefGoogle Scholar
  157. 157.
    Hemmi H, Ishibashi J, Hara S et al. Solution structure of moricin, an antibacterial peptide, isolated from the silkworm Bombyx mori. FEBS Lett 2002; 518:33–38.PubMedCrossRefGoogle Scholar
  158. 158.
    Dai H, Rayaprolu S, Gong Y et al. Solution structure, antibacterial activity and expression profile of Manduca sexta moricin. J Pept Sci 2008; 14:855–863.PubMedCrossRefGoogle Scholar
  159. 159.
    Hara S, Yamakawa M. Moricin, a novel antibacterial peptide family isolated from the silkworm, Bombyx mori. Biochem J 1995; 310:651–656.PubMedGoogle Scholar
  160. 160.
    Brown S, Howard A, Kasprzak AB et al. The discovery and analysis of a diverged family of novel antifungal moricin-like peptides in the wax moth Galleria mellonella. Insect Biochem Mol Biol 2008; 38:201–212.PubMedCrossRefGoogle Scholar
  161. 161.
    Kockum K, Faye I, Hofsten PV et al. Insect immunity. Isolation and sequence of two cDNA clones corresponding to acidic and basic attacins from Hyalophora cecropia. EMBO J 1984; 3:2071–2075.PubMedGoogle Scholar
  162. 162.
    Axén A, Carlsson A, Engström A et al. Gloverin, an antibacterial protein from the immune hemolymph of Hyalophora pupae. Eur J Biochem 1997; 247:614–619.PubMedCrossRefGoogle Scholar
  163. 163.
    Mrinal N, Nagaraju J. Intron loss is associated with gain of function in the evolution of the gloverin family of antibacterial genes in Bombyx mori. J Biol Chem 2008; 283:23376–23387.PubMedCrossRefGoogle Scholar
  164. 164.
    Kawaoka S, Katsuma S, Daimon T et al. Functional analysis of four Gloverin-like genes in the silkworm, Bombyx mori. Arch Insect Biochem Physiol 2008; 67:87–96.PubMedCrossRefGoogle Scholar
  165. 165.
    Mackintosh JA, Gooley AA, Karuso PH et al. A gloverin-like antibacterial protein is synthesized in Helicoverpa armigera following bacterial challenge. Dev Comp Immunol 1998; 22:387–399.PubMedCrossRefGoogle Scholar
  166. 166.
    Lundström A, Liu G, Kang D et al. Trichoplusia ni gloverin, an inducible immune gene encoding an antibacterial insect protein. Insect Biochem Mol Biol 2002; 32:795–801.PubMedCrossRefGoogle Scholar
  167. 167.
    Seitz V, Clermont A, Wedde M et al. Identification of immunorelevant genes from greater wax moth (Galleria mellonella) by a subtractive hybridization approach. Dev Comp Immunol 2003; 27:207–215.PubMedCrossRefGoogle Scholar
  168. 168.
    Wang Q, Liu Y, He HJ et al. Immune responses of Helicoverpa armigera to different kinds of pathogens. BMC Immunol 2010; 11:9.PubMedCrossRefGoogle Scholar
  169. 169.
    Hara S, Yamakawa M. A novel antibacterial peptide family isolated from the silkworm, Bombyx mori. Biochem J 1995; 310:651–656.PubMedGoogle Scholar
  170. 170.
    Furukawa S, Taniai K, Ishibashi J et al. A novel member of lebocin gene family from the silkworm, Bombyx mori. Biochem Biophys Res Commun 1997; 238:769–774.PubMedCrossRefGoogle Scholar
  171. 171.
    Liu G, Kang D, Steiner H. Trichoplusia ni lebocin, an inducible immune gene with a downstream insertion element. Biochem Biophys Res Commun 2000; 269:803–807.PubMedCrossRefGoogle Scholar
  172. 172.
    Bao Y, Yamano Y, Morishima I. A novel lebocin-like gene from eri-silkworm, Samia cynthia ricini, that does not encode the antibacterial peptide lebocin. Comp Biochem Physiol B Biochem Mol Biol 2005; 140:127–131PubMedCrossRefGoogle Scholar
  173. 173.
    Rayaprolu S, Wang Y, Kanost MR et al. Functional analysis of four processing products from multiple precursors encoded by a lebocin-related gene from Manduca sexta. Dev Comp Immunol 2010; 34:638–647.PubMedCrossRefGoogle Scholar
  174. 174.
    Bulet P, Stöcklin R, Menin L. Anti-microbial peptides: from invertebrates to vertebrates. Immunol Rev 2004; 198:169–184.PubMedCrossRefGoogle Scholar
  175. 175.
    Lamberty M, Ades S, Uttenweiler-Joseph S et al. Insect immunity. Isolation from the lepidopteran Heliothis virescens of a novel insect defensin with potent antifungal activity. J Biol Chem 1999; 274:9320–9326.PubMedCrossRefGoogle Scholar
  176. 176.
    Lamberty M, Caille A, Landon C et al. Solution structures of the antifungal heliomicin and a selected variant with both antibacterial and antifungal activities. Biochemistry 2001; 40:11995–12003.PubMedCrossRefGoogle Scholar
  177. 177.
    Mandrioli M, Bugli S, Saltini S et al. Molecular characterization of a defensin in the IZD-MB-0503 cell line derived from immunocytes of the insect Mamestra brassicae (Lepidoptera). Biol Cell 2003; 95:53–57.PubMedCrossRefGoogle Scholar
  178. 178.
    Volkoff AN, Rocher J, d’Alençon E et al. Characterization and transcriptional profiles of three Spodoptera frugiperda genes encoding cysteine-rich peptides. A new class of defensin-like genes from lepidopteran insects? Gene 2003; 319:43–53.PubMedCrossRefGoogle Scholar
  179. 179.
    Schuhmann B, Seitz, V, Vilcinskas A et al. Cloning and expression of gallerimycin, an antifungal peptide expressed in immune response by the greater wax moth, Galleria mellonella. Arch Insect Biochem Physiol 2003; 53:125–133.PubMedCrossRefGoogle Scholar
  180. 180.
    Lee YS, Yun EK, Jang WS et al. Purification, cDNA cloning and expression of an insect defensin from the great wax moth, Galleria mellonella. Insect Mol Biol 2004; 13:65–72.PubMedCrossRefGoogle Scholar
  181. 181.
    Seitz V, Clermont A, Wedde M et al. Identification of immunorelevant genes from greater wax moth (Galleria mellonella) by a subtractive hybridization approach. Dev Comp Immunol 2003; 27:207–215.PubMedCrossRefGoogle Scholar
  182. 182.
    Girard P, Boublik Y, Wheat CW et al. X-tox: an atypical defensin derived family of immune-related proteins specific to Lepidoptera. Dev Comp Immunol 2008; 32:575–584.PubMedCrossRefGoogle Scholar
  183. 183.
    Destoumieux-Garzón D, Brehelin M, Bulet P et al. Spodoptera frugiperda X-tox protein, an immune related defensin rosary, has lost the function of ancestral defensins. PLoS One 2009; 4(8):e6795.PubMedCrossRefGoogle Scholar
  184. 184.
    Lemaitre B, Hoffmann J. The host defense of Drosophila melanogaster. Ann Rev Immunol 2007; 25:697–743.CrossRefGoogle Scholar
  185. 185.
    Cheng TC, Zhang YL, Liu C et al. Identification and analysis of Toll-related genes in the domesticated silkworm, Bombyx mori. Dev Comp Immunol 2008; 32:464–475.PubMedCrossRefGoogle Scholar
  186. 186.
    Ao JQ, Ling E, Yu XQ. A Toll receptor from Manduca sexta is in response to Escherichia coli infection. Mol Immunol 2008; 45:543–552.PubMedCrossRefGoogle Scholar
  187. 187.
    Wang Y, Cheng T, Rayaprolu S et al. Proteolytic activation of pro-spätzle is required for the induced transcription of antimicrobial peptide genes in lepidopteran insects. Dev Comp Immunol 2007; 31:1002–1012.PubMedCrossRefGoogle Scholar
  188. 188.
    An C, Jiang H, Kanost MR. Proteolytic activation and function of the cytokine Spätzle in innate immune response of a lepidopteran insect, Manduca sexta. FEBS J 2010; 277:148–162.PubMedCrossRefGoogle Scholar
  189. 189.
    An C, Ishibashi J, Ragan EJ et al. Functions of Manduca sexta hemolymph proteinases HP6 and HP8 in two innate immune pathways. J Biol Chem 2009; 284:19716–19726.PubMedCrossRefGoogle Scholar
  190. 190.
    Tanaka H, Yamamoto M, Moriyama Y et al. A novel Rel protein and shortened isoform that differentially regulate antibacterial peptide genes in the silkworm Bombyx mori. Biochim Biophys Acta 2005; 1730:10–21.PubMedGoogle Scholar
  191. 191.
    Tanaka H, Matsuki H, Furukawa S et al. Identification and functional analysis of Relish homologs in the silkworm, Bombyx mori. Biochim Biophys Acta 2007; 1769:559–568.PubMedGoogle Scholar
  192. 192.
    Tanaka H, Sagisaka A, Nakajima Y et al. Correlation of differential expression of silkworm antimicrobial peptide genes with different amounts of rel family proteins and their gene transcriptional activity. Biosci Biotechnol Biochem 2009; 73:599–606.PubMedCrossRefGoogle Scholar
  193. 193.
    Furukawa S, Tanaka H, Ishibashi J et al. Functional characterization of a cactus homolog from the silkworm Bombyx mori. Biosci Biotechnol Biochem 2009; 73:2665–2670.PubMedCrossRefGoogle Scholar
  194. 194.
    Nappi AJ, Christensen BM. Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochem Mol Biol 2005; 35:443–459.PubMedCrossRefGoogle Scholar
  195. 195.
    Cerenius L, Lee BL, Söderhäll K. The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol 2008; 29:263–271.PubMedCrossRefGoogle Scholar
  196. 196.
    Noguchi H, Tsuzuki S, Tanaka K et al. Isolation and characterization of a dopa decarboxylase cDNA and the induction of its expression by an insect cytokine, growth-blocking peptide in Pseudaletia separata. Insect Biochem Mol Biol 2003; 33:209–217.PubMedCrossRefGoogle Scholar
  197. 197.
    Gorman MJ, An C, Kanost MR. Characterization of tyrosine hydroxylase from Manduca sexta. Insect Biochem Mol Biol 2007; 37:1327–1337.PubMedCrossRefGoogle Scholar
  198. 198.
    Hashimoto K, Yamano Y, Morishima I. Induction of tyrosine hydroxylase gene expression by bacteria in the fat body of eri-silkworm, Samia cynthia ricini. Comp Biochem Physiol B 2008; 149:501–506.PubMedCrossRefGoogle Scholar
  199. 199.
    Zhao P, Li J, Wang Y et al. Broad-spectrum antimicrobial activity of the reactive compounds generated in vitro by Manduca sexta phenoloxidase. Insect Biochem Mol Biol 2007; 37:952–959.PubMedCrossRefGoogle Scholar
  200. 200.
    Yasuhara Y, Koizumi Y, Katagiri C et al. Reexamination of properties of prophenoloxidase isolated from larval hemolymph of the silkworm Bombyx mori. Arch Biochem Biophys 1995; 320:14–23.PubMedCrossRefGoogle Scholar
  201. 201.
    Jiang H, Wang Y, Ma C et al. Subunit composition of pro-phenol oxidase from Manduca sexta: molecular cloning of subunit proPO-p1. Insect Biochem Mol Biol 1997; 27:835–850.PubMedCrossRefGoogle Scholar
  202. 202.
    Burmester T. Origin and evolution of arthropod hemocyanins and related proteins. J Comp Physiol B 2002; 172:95–107.PubMedCrossRefGoogle Scholar
  203. 203.
    Iwama R, Ashida M. Biosynthesis of prophenoloxidase in hemocytes of larval hemolymph of the silkworm, Bombyx mori. Insect Biochem 16:547–555.Google Scholar
  204. 204.
    Li Y, Wang Y, Jiang H et al. Crystal structure of Manduca sexta prophenoloxidase provides insights into the mechanism of type-3 copper enzymes. Proc Natl Acad Sci USA 2009; 106:17001–17005.Google Scholar
  205. 205.
    Krem MM, Di Cera E. Evolution of enzyme cascades from embryonic development to blood coagulation. Trends Biochem Sci 2002; 27:67–74.PubMedCrossRefGoogle Scholar
  206. 206.
    Jiang H, Kanost MR. The clip-domain family of serine proteinases in arthropods. Insect Biochem Mol Biol 2000; 30:95–105.PubMedCrossRefGoogle Scholar
  207. 207.
    Jiang H, Wang Y, Gu Y et al. Molecular identification of a bevy of serine proteinases in Manduca sexta hemolymph. Insect Biochem Mol Biol 2005; 35:931–943.PubMedCrossRefGoogle Scholar
  208. 208.
    Jiang H, Wang Y, Kanost MR. Pro-phenol oxidase activating proteinase from an insect, Manduca sexta: a bacteria-inducible protein similar to Drosophila Easter. Proc Natl Acad Sci USA 1998; 95:12220–12225.PubMedCrossRefGoogle Scholar
  209. 209.
    Jiang H, Wang Y, Yu XQ et al. Prophenoloxidase-activating proteinase-2 from hemolymph of Manduca sexta. A bacteria-inducible serine proteinase containing two clip domains. J Biol Chem 2003; 278:3552–3561.PubMedCrossRefGoogle Scholar
  210. 210.
    Jiang H, Wang Y, Yu XQ et al. Prophenoloxidase-activating proteinase-3 (PAP-3) from Manduca sexta hemolymph: a clip-domain serine proteinase regulated by serpin-1J and serine proteinase homologs. Insect Biochem Mol Biol 2003; 33:1049–1060.PubMedCrossRefGoogle Scholar
  211. 211.
    Gupta S, Wang Y, Jiang H. Purification and characterization of Manduca sexta prophenoloxidase-activating proteinase-1 (PAP-1), an enzyme involved in insect immune responses. Protein Exp Purif 2005a; 39:261–268.CrossRefGoogle Scholar
  212. 212.
    Satoh D, Horii A, Ochiai M et al. Prophenoloxidase-activating enzyme of the silkworm, Bombyx mori: purification, characterization and cDNA cloning. J Biol Chem 1999; 274:7441–7453.PubMedCrossRefGoogle Scholar
  213. 213.
    Huang R, Lu Z, Dai H et al. The solution structure of clip domains from Manduca sexta prophenoloxidase activating proteinase-2. Biochemistry 2007; 46:11431–11439.PubMedCrossRefGoogle Scholar
  214. 214.
    Yu XQ, Jiang H, Wang Y et al. Nonproteolytic serine proteinase homologs involved in phenoloxidase activation in the tobacco hornworm, Manduca sexta. Insect Biochem Mol Biol 2003; 33:197–208.PubMedCrossRefGoogle Scholar
  215. 215.
    Wang Y, Jiang H. Prophenoloxidase (proPO) activation in Manduca sexta: an analysis of molecular interactions among proPO, proPO-activating proteinase-3 and a cofactor. Insect Biochem Mol Biol 2004; 34:731–742.PubMedCrossRefGoogle Scholar
  216. 216.
    Gupta S, Wang Y, Jiang H. Manducasexta prophenoloxidase (proPO) activation requires proPO-activating proteinase (PAP) and serine proteinase homologs (SPHs) simultaneously. Insect Biochem Mol Biol 2005; 35:241–248.PubMedCrossRefGoogle Scholar
  217. 217.
    Ji C, Wang Y, Guo X et al. A pattern recognition serine proteinase triggers the prophenoloxidase activation cascade in the tobacco hornworm, Manduca sexta. J Biol Chem 2004; 279:34101–34106.PubMedCrossRefGoogle Scholar
  218. 218.
    Buchon N, Poidevin M, Kwon HM et al. A single modular serine protease integrates signals from pattern-recognition receptors upstream of the Drosophila Toll pathway. Proc Natl Acad Sci USA 2009; 106:12442–12447.PubMedCrossRefGoogle Scholar
  219. 219.
    Roh KB, Kim CH, Lee H et al. Proteolytic cascade for the activation of the insect toll pathway induced by the fungal cell wall component. J Biol Chem 2009; 284:19474–19481.PubMedCrossRefGoogle Scholar
  220. 220.
    Wang Y, Jiang H. Reconstitution of abranch of the Manduca sexta prophenoloxidase activation cascade in vitro: snake-like hemolymph proteinase 21 (HP21) cleaved by HP14 activates prophenoloxidase-activating proteinase-2 precursor. Insect Biochem Mol Biol 2007; 37:1015–1025.PubMedCrossRefGoogle Scholar
  221. 221.
    Gorman MJ, Wang Y, Jiang H et al. Manduca sexta hemolymph proteinase 21 activates prophenoloxidase-activating proteinase 3 in an insect innate immune response proteinase cascade. J Biol Chem 2007b; 282:11742–11749.PubMedCrossRefGoogle Scholar
  222. 222.
    Wang Y, Jiang H. A positive feedback mechanism in the Manduca sexta prophenoloxidase activation system. Insect Biochem Mol Biol 2008; 38:763–769.PubMedCrossRefGoogle Scholar
  223. 223.
    Kanost MR. Serine proteinase inhibitors in arthropod immunity. Dev Comp Immunol 1999; 23:291–301.PubMedCrossRefGoogle Scholar
  224. 224.
    Gettins PG. Serpin structure, mechanism and function. Chem Rev 2002; 102:4751–4804.PubMedCrossRefGoogle Scholar
  225. 225.
    Sasaki T, Kobayashi K. Isolation of two novel proteinase inhibitors from hemolymph of silkworm larva, Bombyx mori: comparison with human serum proteinase inhibitors. J Biochem 1984; 95:1009–1017.PubMedGoogle Scholar
  226. 226.
    Sasaki T. Patchwork-structure serpins from silkworm (Bombyx mori) larval hemolymph. Eur J Biochem 1991; 202:255–261.PubMedCrossRefGoogle Scholar
  227. 227.
    Jiang H, Kanost MR. Characterization and functional analysis of 12 naturally occurring reactive site variants of serpin-1 from Manduca sexta. J Biol Chem 1997; 272:1082–1087.PubMedCrossRefGoogle Scholar
  228. 228.
    Gan H, Wang Y, Jiang H et al. A bacteria-induced, intracellular serpin in granular hemocytes of Manduca sexta. Insect Biochem Mol Biol 2001; 31:887–898.PubMedCrossRefGoogle Scholar
  229. 229.
    Zhu Y, Wang Y, Gorman MJ et al. Manduca sexta serpin-3 regulates prophenoloxidase activation in response to infection by inhibiting prophenoloxidase-activating proteinases. J Biol Chem 2003b; 278:46556–46564.PubMedCrossRefGoogle Scholar
  230. 230.
    Tong Y, Kanost MR. Manduca sexta serpin-4 and serpin-5 inhibit the prophenol oxidase activation pathway: cDNA cloning, protein expression and characterization. J Biol Chem 2005; 280:14923–14931.PubMedCrossRefGoogle Scholar
  231. 231.
    Tong Y, Jiang H, Kanost MR. Identification of plasma proteases inhibited by Manduca sexta serpin-4 and serpin-5 and their association with components of the prophenol oxidase activation pathway. J Biol Chem 2005; 280:14932–14942.PubMedCrossRefGoogle Scholar
  232. 232.
    Wang Y, Jiang H. Purification and characterization of Manduca sexta serpin-6: a serine proteinase inhibitor that selectively inhibits prophenoloxidase-activating proteinase-3. Insect Biochem Mol Biol 2004; 34, 387–395.PubMedCrossRefGoogle Scholar
  233. 233.
    Cherqui A, Cruz N, Simões N. Purification and characterization of two serine protease inhibitors from the hemolymph of Mythimna unipuncta. Insect Biochem Mol Biol 2001; 31:761–769.PubMedCrossRefGoogle Scholar
  234. 234.
    Chamankhah M, Braun L, Visai-Shah S et al. Mamestra configurata serpin-1 homologs: cloning, localization and developmental regulation. Insect Biochem Mol Biol 2003; 33:355–369.PubMedCrossRefGoogle Scholar
  235. 235.
    Zou Z, Zhao P, Weng H et al. A comparative analysis of serpin genes in the silkworm genome. Genomics 2009; 93:367–375.PubMedCrossRefGoogle Scholar
  236. 236.
    Kanost MR. Serpins in a Lepidopteran insect, Manduca sexta. In: Silverman GA, Lomas DA eds. The Serpinopathies: Molecular and Cellular Aspects of Serpins and their Disorders. Hackensack, NJ: World Scientific Publishing. 2007:229–242.CrossRefGoogle Scholar
  237. 237.
    Jiang H, Wang Y, Kanost MR. Mutually exclusive exon use and reactive center diversity in insect serpins. J Biol Chem 1994; 269:55–58.PubMedGoogle Scholar
  238. 238.
    Jiang H, Wang Y, Huang Y et al. Organization of serpin gene-1 from Manduca sexta: evolution of a family of alternate exons encoding the reactive site loop. J Biol Chem 1996; 271:28017–28023.PubMedCrossRefGoogle Scholar
  239. 239.
    Hegedus DD, Erlandson M, Baldwin D et al. Differential expansion and evolution of the exon family encoding the Serpin-1 reactive centre loop has resulted in divergent serpin repertoires among the Lepidoptera. Gene 2008; 418:15–21.PubMedCrossRefGoogle Scholar
  240. 240.
    Zheng YP, He WY, Béliveau C et al. Cloning, expression and characterization of four serpin-1 cDNA variants from the spruce budworm, Choristoneura fumiferana. Comp Biochem Physiol B Biochem Mol Biol 2009; 154:165–173.PubMedCrossRefGoogle Scholar
  241. 241.
    Krüger O, Ladewig J, Köster K et al. Widespread occurrence of serpin genes with multiple reactive centre-containing exon cassettes in insects and nematodes. Gene 2002; 29:97–105.CrossRefGoogle Scholar
  242. 242.
    Zou Z, Jiang H. Manduca sextaserpin-6 regulates immune serine proteinases PAP-3 and HP8. cDNA cloning, protein expression, inhibition kinetics and function elucidation. J Biol Chem 2005; 280:14341–14348.PubMedCrossRefGoogle Scholar
  243. 243.
    Freitak D, Wheat CW, Heckel DG et al. Immune system responses and fitness costs associated with consumption of bacteria in larvae of Trichoplusia ni. BMC Biol 2007; 5:56.PubMedCrossRefGoogle Scholar
  244. 244.
    Freitak D, Heckel DG, Vogel H. Bacterial feeding induces changes in immune-related gene expression and has trans-generational impacts in the cabbage looper (Trichoplusia ni). Front Zool 2009a; 6:7.PubMedCrossRefGoogle Scholar
  245. 245.
    Strand MR. Insect hemocytes and their role in immunity. In: Beckage, NE, ed. Insect Immunology. San Diego, CA: Academic Press. 2008:25–47.CrossRefGoogle Scholar
  246. 246.
    St. Leger RJ, Charnley AK, Cooper RM. Cuticle-degrading enzymes of entomopathogenic fungi: synthesis in culture on cuticle. J Invertebr Pathol 1986; 48:85–95.CrossRefGoogle Scholar
  247. 247.
    Vilcinskas A, Matha V, Götz P. Effects of the entomopathogenic fungus Metarhizium anisopliae and its secondary metabolites on morphology and cytoskeleton of plasmatocytes isolated from Galleria mellonella. J Insect Physiol 1997; 43:1149–1159.PubMedCrossRefGoogle Scholar
  248. 248.
    Vilcinskas A, Götz P. Parasitic fungi and their interactions with the insect immune system. Adv Parasitai 1999; 43:267–213.CrossRefGoogle Scholar
  249. 249.
    Fiolka MJ. Immunosuppressive effect of cyclosporin A on insect humoral immune response. J Invertebr Pathol 2008; 98:287–292.PubMedCrossRefGoogle Scholar
  250. 250.
    Gillespie J, Bailey A, Cobb B et al. Fungal elicitors of insect immune responses. Arch Insect Biochem Physiol 2000; 44:49–68.PubMedCrossRefGoogle Scholar
  251. 251.
    Lord JC, Anderson S, Stanley DW. Eicosanoids mediate Manduca sexta cellular response to the fungal pathogen Beauveria bassiana: a role for the lipoxygenase pathway. Arch Insect Biochem Physiol 2002; 51:46–54.PubMedCrossRefGoogle Scholar
  252. 252.
    Bergin D, Reeves E, Renwick J et al. Superoxide production in Galleria mellonella hemocytes: Identification of proteins homologous to the NADPH oxidase complex of human neutrophils. Infect Immun 2005; 73:4161–4170.PubMedCrossRefGoogle Scholar
  253. 253.
    Ekengren S, Hultmark D. Drosophila cecropin as an antifungal agent. Insect Biochem Mol Biol 1999; 29(11):965–972.PubMedCrossRefGoogle Scholar
  254. 254.
    Langen G, Imani J, Altincicek B et al. Transgenic expression of gallerimycin, a novel antifungal insect defensin from the greater wax moth Galleria mellonella, confers resistance against pathogenic fungi in tobacco. Biol Chem 2006; 387:549–557.PubMedCrossRefGoogle Scholar
  255. 255.
    Wojda I, Kowalski P, Jakubowicz T. Humoral immune response of Galleria mellonella larvae after infection by Beauveria bassiana under optimal and heat-shock conditions. J Insect Physiol 2009; 55:525–531.PubMedCrossRefGoogle Scholar
  256. 256.
    Schmidt O. Insect immune recognition and suppression. In: Beckage, NE, ed. Insect Immunology. San Diego, CA: Academic Press. 2008; 271–294.CrossRefGoogle Scholar
  257. 257.
    Clarke DJ. Photorhabdus: a model for the analysis of pathogenicity and mutualism. Cell Microbiol 2008; 10:2159–2167.PubMedCrossRefGoogle Scholar
  258. 258.
    Beckage NE. Parasitoid polydnaviruses and insect immunity. In: Beckage, NE, ed. Insect Immunology. San Diego, CA: Academic Press. 2008; 243–270.CrossRefGoogle Scholar
  259. 259.
    Suderman RJ, Pruijssers AJ, Strand MR. Protein tyrosine phosphatase-H2 from a polydnavirus induces apoptosis of insect cells. J Gen Virol 2008; 89:1411–1420.PubMedCrossRefGoogle Scholar
  260. 260.
    Thoetkiattikul H, Beck MH, Strand MR. Inhibitor kappaB-like proteins from a polydnavirus inhibit NF-kappaB activation and suppress the insect immune response. Proc Natl Acad Sci USA 2005; 102:11426–11431.PubMedCrossRefGoogle Scholar
  261. 261.
    Lu Z, Beck MH, Wang Y et al. The viral protein Egf1.0 is a dual activity inhibitor of prophenoloxidase-activating proteinases 1 and 3 from Manduca sexta. J Biol Chem 2008; 283:21325–21333.PubMedCrossRefGoogle Scholar
  262. 262.
    Sparks WO, Bartholomay LC, Bonning BC. Insect immunity to viruses. Beckage, NE Parasitoid polydnaviruses and insect immunity. In: Beckage, NE, ed. Insect Immunology. San Diego, CA: Academic Press. 2008; 209242–209270.Google Scholar
  263. 263.
    Clem RJ. Baculoviruses and apoptosis: a diversity of genes and responses. Curr Drug Targets 2007; 8:1069–1074.PubMedCrossRefGoogle Scholar
  264. 264.
    Shelby KS, Popham HJ. Plasma phenoloxidase of the larval tobacco budworm, Heliothis virescens, is virucidal. J Insect Sci 2006; 6:1–12.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Haobo Jiang
    • 1
  • Andreas Vilcinskas
    • 2
  • Michael R. Kanost
    • 3
    Email author
  1. 1.Department of Entomology and Plant PathologyOklahoma State UniversityStillwaterUSA
  2. 2.Institut für Phytopathologie und Angewandte ZoologieJustus-Liebig-Universität GieβenGieβenGermany
  3. 3.Department of BiochemistryKansas State UniversityManhattanUSA

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