Advertisement

Cytotoxic Reactions Associated with Insect Immunity

  • A. J. Nappi
  • E. Vass
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 484)

Abstract

Insects and other invertebrates lack the immunoglobulins and adaptive responses that characterize vertebrates yet possess efficient innate immune systems comprised of both cellular and humoral elements (Gillespie et al., 1997; Vilmos and Kurucz, 1998). The evolutionary origins and molecular basis for the various recognitive mechanisms remain among the most intriguing of immunological puzzles at all levels of biological organization (Ratcliffe, 1993; Ottaviani and Franceschi, 1998). Frequently, the first line of defense against potentially invasive organisms are integumental or midgut defenses, which may involve various cytotoxic proteins and antimicrobial peptides synthesized by epidermal cells and transported to the sites of wounding (Brey et al., 1993; Furukawa et al., 1999). Foreign organisms that breach integumental barriers or instead pass through the gut wall to invade the host’s hemocoel encounter reactive blood cells, and an array of both non-specific and specific inducible cytotoxic molecules.

Keywords

Nitric Oxide Phenol Oxidase Quinone Methides Insect Defensin Insect Immunity 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aroca P, Solano F, Garcia-Borron JC, Lozano JA. Specificity of dopachrome tautomerase and inhibition by carboxylated indoles. Considerations on the enzyme active site. Biochemical Journal 1991; 277(Pt 2):393–397.PubMedGoogle Scholar
  2. Ashida M, Brey PT. Role of the integument in insect defense - pro-phenol oxidase cascade in the cuticular matrix. Proc.Natl. Acad.Sci. USA 1995; 92(23):10698–10702.PubMedCrossRefGoogle Scholar
  3. Beck G, Cardinale S, Wang L, Reiner M, Sugumaran M. Characterization of a defense complex consisting of interleukin 1 and phenol oxidase from the hemolymph of the tobacco homworm, Manduca sexta. Journal of Biological Chemistry 1996; 271(19):11035–11038.PubMedCrossRefGoogle Scholar
  4. Beck G, Habicht GS. ,Primitive cytokines: Harbingers of vertebrate defense. Immunology Today 1991; 12:180–183.PubMedCrossRefGoogle Scholar
  5. Beck G, RF OB, Habicht GS. Invertebrate cytokines: the phylogenetic emergence of interleukin-1. Bioessays 1989; 11(2–3):62–7.PubMedCrossRefGoogle Scholar
  6. Bettencourt R, Lanz-Mendoza H, Lindquist KR, Faye I. Cell adhesion properties of hemolin, an insect immune protein in the Ig superfamily. European Journal of Biochemistry 1997; 250(3):630–7.PubMedCrossRefGoogle Scholar
  7. Boman HG. Gene-encoded peptide antibiotics and the concept of innate immunity: an update review. Scandinavian Journal of Immunology 1998; 48(1):15–25.PubMedCrossRefGoogle Scholar
  8. Bosetto M, Arfaioli P, Ristori GG, Fusi P. Formation of melanin-yype compounds from L-tryptophan on Ca-saturated and Al-saturated clays. Fresenius Environmental Bulletin 1995; 4(6):369–374.Google Scholar
  9. Braun A, Hoffmann JA, Meister M. Analysis of the Drosophila host defense in domino mutant larvae, which are devoid ofhemocytes. Proceedings of the National Academy of Sciences of the United States of America 1998; 95(24):14337–14342.PubMedCrossRefGoogle Scholar
  10. Brehelin M. Hemolymph coagulation in Locusta migratoria. Ann Parasitol Hum Comp 1977; 52(1):98–99.PubMedGoogle Scholar
  11. Brey PT, Lee WJ, Yamakawa M, Koizumi Y, Perrot S, Francois M, Ashida M. Role of the integument in insect immunity: Epicuticular abrasion and induction of cecropin synthesis in cuticular epithelial cells. Proceedings of the National Academy of Sciences of the United States of America 1993; 90(13):6275–6279.Google Scholar
  12. Carlsson A, Nystrom T, de Cock H, Bennich H. Attacin—an insect immune protein—binds LPS and triggers the specific inhibition of bacterial outer-membrane protein synthesis. Microbiology 1998; 144(Pt 8):2179–2188.Google Scholar
  13. Carton Y, Nappi AJ. Drosophila cellular immunity against parasitoids. Parasitology Today 1997; 13(6):218–227.Google Scholar
  14. Chakraborty AK, Chakraborty DP. The effect of tryptophan on dopa-oxidation by melanosomal tyrosinase. International Journal of Biochemistry 1993; 25(9):1277–1280.PubMedCrossRefGoogle Scholar
  15. Chakraborty AK, Platt JT, Kim KK, Kwon BS, Bennett DC, Pawelek JM. Polymerization of 5,6dihydroxyindole-2-carboxylic acid to melanin by the pmel 17/silver locus protein. European Journal of Biochemistry 1996; 236(1):180–188.PubMedCrossRefGoogle Scholar
  16. Chakraborty DP, Roy S, Chakraborty AK. Vitiligo, psoralen, and melanogenesis: some observations and understanding. Pigment Cell Research 1996; 9(3):107–116.PubMedCrossRefGoogle Scholar
  17. Christensen B, Fink J, Merrifield RB, Mauzerall D. Channel-forming properties of cecropins and related model compounds incorporated into planar lipid membranes. Proceedings of the National Academy of Sciences of the United States of America 1988; 85(14):5072–5076.PubMedCrossRefGoogle Scholar
  18. Cociancich S, Bulet C, Hetru C, Hoffmann JA. The inducible antibacterial peptides in insects. Parasitology Today 1994; 10:131–139.CrossRefGoogle Scholar
  19. Cociancich S, Ghazi A, Hetru C, Hoffmann JA, Letellier L. Insect defensin, an inducible antibacterial peptide, forms voltage-dependent channels in Micrococcus luteus. Journal of Biological Chemistry 1993; 268(26):19239–19245.PubMedGoogle Scholar
  20. Cooper EL. Overview of immunoevolution. Boll. Zool. 1992; 59:119–129.CrossRefGoogle Scholar
  21. D’Acquisto F, Carnuccio R, d’Ischia M, Misuraca G. 5,6-Dihydroxyindole-2-carboxylic acid, a diffusible melanin precursor, is a potent stimulator of lipopolysaccharide-induced production of nitric oxide by J774 macrophages. Life Sci 1995; 57(26):PL401–6.PubMedCrossRefGoogle Scholar
  22. Daffre S, Faye I. Lipopolysaccharide interaction with hemolin, an insect member of the Ig-superfamily. FEBS Lett 1997; 408(2):127–30.PubMedCrossRefGoogle Scholar
  23. Dimarcq JL, Bulet P, Hetru C, Hoffmann J. Cysteine-rich antimicrobial peptides in invertebrates. Biopolymers 1999; 47:465–477.CrossRefGoogle Scholar
  24. d’Ischia M, Napolitano A, Prota G. Peroxidase as an alternative to tyrosinase in the oxidative polymerization of 5,6-dihydroxyindoles to melanin(s). Biochim Biophys Acta 1991; 1073(2):423–30.PubMedCrossRefGoogle Scholar
  25. Duvic B, Brehelin M. Two major proteins from locust plasma are involved in coagulation and are specifically precipitated by laminarin, a beta-1,3-glucan. Insect Biochemistry & Molecular Biology 1998; 28(12):959–967.Google Scholar
  26. Faye I, Kanost M, editors. Function and regulation of hemolin. London: Chapman & Hall; 1997. pp. 173–188.Google Scholar
  27. Fehlbaum P, Bulet P, Chernysh S, Briand JP, Roussel JP, Letellier L, Hetru C, Hoffmann JA. Structure-activity analysis of thanatin, a 21-residue inducible insect defense peptide with sequence homology to frog skin antimicrobial peptides. Proc Natl Acad Sci USA 1996; 93(3):1221–5.PubMedCrossRefGoogle Scholar
  28. Foppoli C, Coccia R, Cini C, Rosei MA. Catecholamines oxidation by xanthine oxidase. Biochim Biophys Acta 1997; 1334(2–3):200–6.PubMedCrossRefGoogle Scholar
  29. Franc NC, Dimarcq JL, Lagueux M, Hoffmann J, Ezekowitz RA. Croquemort, a novel Drosophila hemocyte/ macrophage receptor that recognizes apoptotic cells. Immunity 1996; 4(5):431–43.PubMedCrossRefGoogle Scholar
  30. Furukawa S, Taniai K, Yang J, Shono T, Yamakawa M. Induction of gene expression of antibacterial proteins by chitin oligomers in the silkworm, Bombyx mori. Insect Molecular Biology 1999; 8(1):145–148.Google Scholar
  31. Gillespie JP, Kanost MR, Trenczek T. Biological mediators of insect immunity. Annual Review of Entomology 1997; 42:611–643.PubMedCrossRefGoogle Scholar
  32. Hall M, Scott T, Sugumaran M, Soderhall K, Law JH. Proenzyme of Manduca sexta phenol oxidase: purification, activation, substrate specificity of the active enzyme, and molecular cloning. Proceedings of the National Academy of Sciences of the United States of America 1995; 92(17):7764–7768.PubMedCrossRefGoogle Scholar
  33. Hanusova R, Bilej M, Brys L, De-Baestselier P, Beschin A. Identification of a coelomic mitogenic factor in Eisenia foetida earthworm. Immunological Letters 1999; 65:203–211.CrossRefGoogle Scholar
  34. Hearing VJ, Tsukamoto K. Enzymatic control of pigmentation in mammals. EASESJ 1991; 5(14):2902–9.Google Scholar
  35. Hegedus ZL, Frank HA, Altschule MD, Nayak U. Human plasma lipofuscin melanins formed from tryptophan metabolites. Archives of International Physiology & Biochemistry 1986; 94(5):339–48.CrossRefGoogle Scholar
  36. Hoffmann JA, Kafatos FC, Janeway CA, Ezekowitz RAB. Phylogenetic perspectives in innate immunity. Science 1999; 284:1313–1318.PubMedCrossRefGoogle Scholar
  37. Hoffmann JA, Reichhart JM, Hetru C. Innate immunity in higher insects. Current Opinion in Immunology 1996; 8(1):8–13.PubMedCrossRefGoogle Scholar
  38. Hopkins TL, Morgan TD, Kramer KJ. Catecholamines in haemolymph and cuticle during larval, pupal and adult development of Manduca sexta. Insect Biochemistry 1984; 14:533–540.CrossRefGoogle Scholar
  39. Hughes AL. Protein phylogenies provide evidence of a radical discontinuity between arthropod and vertebrate immune systems. Immunogenetics 1998; 47(4):283–96.PubMedCrossRefGoogle Scholar
  40. Hughes AL. Evolution of the arthropod prophenoloxidase/hexamerin protein family. Immunogenetics 1999; 49(2):106–14.PubMedCrossRefGoogle Scholar
  41. Iimura Y, Ishikawa H, Yamamoto K, Sehnal F. Hemagglutinating properties of apolipophorin III from the hemolymph of Galleria mellonella larvae. Archives of Insect Biochemistry & Physiology 1998; 38(3):119–25.CrossRefGoogle Scholar
  42. Ito S. Reexamination of the structure of eumelanin. Biochimies et Biophysica Acta 1986; 883(1):155–161.CrossRefGoogle Scholar
  43. Ito S, Wakamatsu K. Melanin chemistry and melanin precursors in melanoma. Journal of Investigative Dermatology 1989; 92(5 Suppl):261S–265S.Google Scholar
  44. Ito S, Wakamatsu K, Ozeki H. Spectrophotometric assay of eumelanin in tissue samples. Anal Biochem 1993; 215(2):273–7.PubMedCrossRefGoogle Scholar
  45. Jimenez-Cervantes C, Solano F, Lozano JA, Garcia-Borron JC. The DHICA oxidase activity of the melanosomal tyrosinases LEMT and HEMT. Pigment Cell Research 1994; 7(5):298–304.PubMedCrossRefGoogle Scholar
  46. Johansson MW, Soderhall K. The prophenoloxidase activating system and associated proteins in invertebrates. Progress in Molecular Subcellular Biology 1996; 15:46–66.CrossRefGoogle Scholar
  47. Kanost MR, Zepp MK, Ladendorff NE, Andersson LA. Isolation and characterization of a hemocyte aggregation inhibitor from hemolymph of Manduca sexta larvae. Arch Insect Biochem Physiol 1994; 27(2):123–36.PubMedCrossRefGoogle Scholar
  48. Kato Y, Motoi Y, Taniai K, Kadono-Okuda K, Yamamoto M, Higashino Y, Shimabukuro M, Chowdhury S, Xu J, Sugiyama M and others. 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(6):547–55.PubMedCrossRefGoogle Scholar
  49. Kotani E, Yamakawa M, Iwamoto S, Tashiro M, Mori H, Sumida M, Matsubara F, Taniai K, Kadono-Okuda K, Kato Y and others. Cloning and expression of the gene of hemocytin, an insect humoral lectin which is homologous with the mammalian von Willebrand factor. Biochim Biophys Acta 1995; 1260(3):24558.Google Scholar
  50. Kylsten P, Kimbrell DA, Daffre S, Samakovlis C, Hultmark D. The lysozyme locus in Drosophila melanogaster: different genes are expressed in midgut and salivary glands. Mol Gen Genet 1992; 232(3):335–43.PubMedCrossRefGoogle Scholar
  51. Kyriakides TR, McKillip JL, Spence KD. Biochemical characterization, developmental expression, and induction of the immune protein scolexin from Manduca sexta. Arch Insect Biochem Physiol 1995; 29(3):269–80.PubMedCrossRefGoogle Scholar
  52. Lackie AM, Vasta GR. The role of galactosyl-binding lectin in the cellular immune response of the cockroach Periplaneta americana (Dictyoptera). Immunology 1988; 64(2):353–7.PubMedGoogle Scholar
  53. 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(4):285–300.PubMedCrossRefGoogle Scholar
  54. Lamberty M, Ades S, Uttenweiler-Joseph S, Brookhart G, Bushey D, Hoffmann JA, Bulet P. Insect immunity. Isolation from the lepidopteran Heliothis virescens of a novel insect defensin with potent antifungal activity. Journal of Biological Chemistry 1999; 274(14):9320–6.PubMedCrossRefGoogle Scholar
  55. Lanz-Mendoza H, Bettencourt R, Fabbri M, Faye I. Regulation of the insect immune response: the effect of hemolin on cellular immune mechanisms. Cell Immunol 1996; 169(1):47–54.PubMedCrossRefGoogle Scholar
  56. Levashina EA, Ohresser S, Bulet P, Reichhart JM, Hetru C, Hoffmann JA. Metchnikowin, a novel immune-inducible proline-rich peptide from Drosophila with antibacterial and antifungal properties. Eur J Biochem 1995; 233(2):694–700.PubMedCrossRefGoogle Scholar
  57. Levashina EA, Ohresser S, Lemaitre B, Imler JL. Two distinct pathways can control expression of the gene encoding the Drosophila antimicrobial peptide metchnikowin. Journal of Molecular Biology 1998; 278(3):515–27.PubMedCrossRefGoogle Scholar
  58. Lockey TD, Ourth DD. Formation of pores in Escherichia coli cell membranes by a cecropin isolated from hemolymph of Heliothis virescens larvae. European Journal of Biochemistry 1996; 236(1):263–71.PubMedCrossRefGoogle Scholar
  59. MacMicking J, Xie Q, Nathan C. Nitric oxide and macrophage function. Annu. Rev. Immunol. 1997; 15(323–350.).PubMedCrossRefGoogle Scholar
  60. Mandato CA, Diehljones WL, Downer RGH. Insect hemocyte adhesion in vitro: Inhibition by apoliphorin I and an artificial substrate. Journal of Insect Physiology 1996; 42(2):143–148.CrossRefGoogle Scholar
  61. Marchalonis JJ, Schluter SF. Immunoproteins in evolution. Dev Comp Immunol 1989; 13(4):285–301.PubMedCrossRefGoogle Scholar
  62. Marchalonis JJ, Schluter SF. On the relevance of invertebrate recognition and defence mechanisms to the emergence of the immune response of vertebrates. Scand J Immunol 1990; 32(l):13–20.PubMedCrossRefGoogle Scholar
  63. Marmaras VJ, Charalambidis ND, Zervas CG. Immune response in insects: the role of phenoloxidase in defense reactions in relation to melanization and sclerotization. Arch Insect Biochem Physiol 1996; 31(2):119–33.PubMedCrossRefGoogle Scholar
  64. Marmaras VJ, Charalambidis ND, Zervas CG. Immune response in insects: The role of phenoloxidase in defense reactions in relation to melanization and sclerotization. Arch Insect Biochem. Physiol. 1996; 31:119–133.Google Scholar
  65. Medzhitov R, Preston-Hurlburt P, Janeway CA, Jr. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 1997; 388(6640):394–7.PubMedCrossRefGoogle Scholar
  66. Meister M, Lemaitre B, Hoffmann JA. Antimicrobial peptide defense in Drosophila. BioEssays 1997; 19(11):1019–26.PubMedCrossRefGoogle Scholar
  67. Minnick MF, Rupp RA, Spence KD. A bacterial-induced lectin which triggers hemocyte coagulation in Manduca sexta. Biochem Biophys Res Commun 1986; 137(2):729–35.PubMedCrossRefGoogle Scholar
  68. Morishima I, Horiba T, Iketani M, Nishioka E, Yamano Y. Parallel induction if cecropin and lysozyme in larvae of the silkworm, Bombyx mori. Developmental & Comparative Immunology 1995; 19(5):357–363.Google Scholar
  69. Morishima I, Yamano Y, Inoue K, Matsuo N. Eicosanoids mediate induction of immune genes in the fat body of the silkworm, Bombyx mori. FEBS Letters 1997; 419(1):83–6.PubMedCrossRefGoogle Scholar
  70. Mosca L, Blarzino C, Coccia R, Foppoli C, Rosei MA. Melanins from tetrahydroisoquinolines: spectroscopic characteristics, scavenging activity and redox transfer properties. Free Radical Biology & Medicine 1998; 24(1):161–7.CrossRefGoogle Scholar
  71. Mosca L, Foppoli C, Coccia R, Rosei MA. Pheomelanin production by the lipoxygenase-catalyzed oxidation of 5-S-cysteinyldopa and 5-S-cysteinyldopamine. Pigment Cell Research 1996; 9(3):117–25.PubMedCrossRefGoogle Scholar
  72. Muta T, Iwanaga S. The role of hemolymph coagulation in innate immunity. Current Opinion in Immunology 1996; 8(1):41–7.PubMedCrossRefGoogle Scholar
  73. Muta T, Oda T, Iwanaga S. Horseshoe crab coagulation factor B. A unique serine protease zymogen activated by cleavage of an Ile-Ile bond. J Biol Chem 1993; 268(28):21384–8.PubMedGoogle Scholar
  74. Nappi AJ. Hemocyte reactions and early cellular changes during melanotic tumor formation in Drosophila melanogaster. J. Invertebr. Pathol 1984; 43:395–406.CrossRefGoogle Scholar
  75. Nappi AJ, Carton Y. Cellular immune responses and their genetic aspects in Drosophila. In: Brehelin M, editor. Immunity in Invertebrates. Berlin: Springer-Verlag; 1986. p 171–187.CrossRefGoogle Scholar
  76. Nappi AJ, Carton Y, Frey F. Parasite-induced enhancement of hemolymph tyrosinase activity in a selected immune reactive strain of Drosophila melanogaster. Arch Insect Biochem Physiol 1991; 18(3):159–68.PubMedCrossRefGoogle Scholar
  77. Nappi AJ, Carton Y, Li J, Vass E. Reduced cellular immune competence of a temperature-sensitive dopa decarboxylase mutant strain of Drosophila melanogaster against the parasite Leptopilina boulardi Comp. Biochem. Physiol. 1992; 101B:453–460.Google Scholar
  78. Nappi AJ, Vass E. Melanogenesis and the generation of cytotoxic molecules during insect cellular immune reactions. Pigment Cell Res 1993; 6(3):117–26.PubMedCrossRefGoogle Scholar
  79. Nappi AJ, Vass E. Hydrogen peroxide production in immune-reactive Drosophila melanogaster. Journal of Parasitology 1998; 84(6):1150–7.PubMedCrossRefGoogle Scholar
  80. Nappi AJ, Vass E. Hydroxyl radical formation resulting from the interaction of nitric oxide and hydrogen peroxide. Biochimica et Biophysica Acta 1998; 1380:55–63.PubMedCrossRefGoogle Scholar
  81. Nappi AJ, Vass E, Carton Y, Frey F. Identification of 3,4-dihydroxyphenylalanine, 5,6-dihydroxyindole and N-acetylarterenone during eumelanin formation in immune reactive larvae ofDrosphila melanogaster. Arch. Insect Biochem Physiol 1992; 20: 181–191.CrossRefGoogle Scholar
  82. Nappi AJ, Vass E, Frey F, Carton Y. Superoxide anion generation in Drosophila during melanotic encapsulation of parasites. Eur J Cell Biol 1995; 68(4):450–6.PubMedGoogle Scholar
  83. Nayar JK, Mikarts LL, Chikilian ML, Knight JW, Bradley TJ. Lectin binding to extracellularly mclanized microfilariae of Brugia malayi from the hemocoel of Anopheles quadrimaculatus. J Invertebr Pathol 1995; 66(3):277–86.PubMedCrossRefGoogle Scholar
  84. Nelson RE, Fessler LI, Takagi Y, Blumberg B, Keene DR, Olson PF, Parker CG, Fessier JH. Peroxidasin: a novel enzyme-matrix protein of Drosophila development. Embo J 1994; 13(15):3438–47.PubMedGoogle Scholar
  85. Ochiai M, Ashida M. A pattern recognition protein for peptidoglycan. Cloning the cDNA and the gene of the silkworm, Bombyx mori. Journal of Biological Chemistry 1999; 274(17):11854–8.CrossRefGoogle Scholar
  86. Ottaviani E, Capriglione T, Franceschi C. Invertebrate and vertebrate immune cells express pro-opiomelanocortin (POMC) mRNA. Brain Behav Immun 1995; 9(1):1–8.PubMedCrossRefGoogle Scholar
  87. Ottaviani E, Caselgrandi E, Franceschi C. Cytokines and evolution: in vitro effects of IL-1 alpha, IL-1 beta, TNF-alpha and IMF-beta on an ancestral type of stress response. Biochem Biophys Res Commun 1995; 207(1):288–92.PubMedCrossRefGoogle Scholar
  88. Ottaviani E, Franceschi C. A new theory on the common evolutionary origin of natural immunity, inflammation and stress response: the invertebrate phagocytic immunocyte as an eye-witness. Domestic Animal Endocrinology 1998; 15(5):291–6.PubMedCrossRefGoogle Scholar
  89. Ottaviani E, Franchini A, Cassanelli S, Genedani S. Cytokines and invertebrate immune responses. Biology of the Cell 1995; 85(1):87–91.PubMedGoogle Scholar
  90. Parrinello N. Humoral and cellular lectins of ascidians. J. Mar. Biotechnol. 1995; 3:29–34.Google Scholar
  91. Pentz ES, Black BC, Wright TRF. Mutation affecting phenol oxidase activity in Drosophila: quicksilver and tyrosinase-i. Biochem. Genetics 1990; 28:151–171.Google Scholar
  92. Pentz ES, Wright TR. Drosophila melanogaster diphenol oxidase A2: gene structure and homology with the mouse mast-cell tum-transplantation antigen, P91A. Gene 1991; I 03(2):239–42.CrossRefGoogle Scholar
  93. Prota G. The role of peroxidase in melanogenesis revisited. Pigment Cell Res 1992; Suppl(2):25–31.Google Scholar
  94. Prota G, Lamoreux ML, Muller J, Kobayashi T, Napolitano A, Vincensi MR, Sakai C, Hearing VJ. Comparative analysis of melanins and melanosomes produced by various coat color mutants. Pigment Cell Research 1995; 8(3):153–163.PubMedCrossRefGoogle Scholar
  95. Raftos DA, Cooper EL. Proliferation of lymphocyte-like cells from the solitary tunicate, Styela clava, in response to allogeneic stimuli. J Exp Zool 1991; 260(3):391–400.PubMedCrossRefGoogle Scholar
  96. Raftos DA, Cooper EL, Habicht GS, Beck G. Invertebrate cytokines: tunicate cell proliferation stimulated by an interleukin 1-like molecule. Proc Natl Acad Sci U S A 1991; 88(21):9518–22.PubMedCrossRefGoogle Scholar
  97. Ratios DA, Cooper EL, Stillman DL, Habicht GS, Beck G. Invertebrate cytokines II: release of interleukin1-like molecules from tunicate hemocytes stimulated with zymosan. Lymphokine Cytokine Res 1992; I1(4):235–40.Google Scholar
  98. Ratcliffe NA. The prophenoloxidase system and its role in arthropod immunity. In: Wan GW, Cohen N, editors. Phylogenesis of Immune Functions. Boca Raton, FL: CRC Press; 1991. p 45–71.Google Scholar
  99. Ratcliffe NA. Cellular defense responses of insects: unresolved problems. In: Beckage NE, Thompson SN, Federici BA, editors. Parasites and Pathogens of Insects. San Diego: Academic Press; 1993. p 267–304.CrossRefGoogle Scholar
  100. Ratcliffe NA, Brookman JL, Rowley AF. Activation of the prophenoloxidase cascade and initiation of nodule formation in locusts by bacterial lipopolysaccharides. Dev Comp Immunol 1991; 15(1–2):33–9.PubMedCrossRefGoogle Scholar
  101. Riley PA. Melanin. International Journal of Biochemistry & Cell Biology 1997; 29(11):1235–9.Google Scholar
  102. Rizki TM, Rizki RM. The cellular defense system of Drosophila melanogaster. In: King RC, H. Akai H, editors. Insect ultrastructure. Volume 2. New York: Plenum Press; 1984. p 579–604.CrossRefGoogle Scholar
  103. Rizki TM, Rizki RM. Encapsulation of parasitoid eggs in phenoloxidase-deficient mutants of Drosophila melanogaster. J. Insect Physiol. 1990; 36:523–529.CrossRefGoogle Scholar
  104. Rosei MA. Melanins from opioid peptides. Pigment Cell Res 1996; 9(6):273–80.PubMedCrossRefGoogle Scholar
  105. Rosei MA, Blarzino C, Coccia R, Foppoli C, Mosca L, Cini C. Production of melanin pigments by cytochromec/H2O2 system. International Journal of Biochemistry & Cell Biology 1998; 30(4):457–63.CrossRefGoogle Scholar
  106. Rosei MA, Blarzino C, Foppoli C, Mosca L, Coccia R. Lipoxygenase-catalyzed oxidation of catecholamines. Biochem Biophys Res Commun 1994; 200(1):344–50.PubMedCrossRefGoogle Scholar
  107. Rosei MA, Mosca L. Production of melanin pigments by chemical and enzymatic oxidation of tetrahydroisoquinolines. Biochemistry & Molecular Biology International 1995; 35(6):1253–9.Google Scholar
  108. Rosei MA, Mosca L, Coccia R, Blarzino C, Musci G, De Marco C. Some biochemical properties of melanins from opioid peptides. Biochim Biophys Acta 1994; 1199(2):123–9.PubMedCrossRefGoogle Scholar
  109. Rosei MA, Mosca L, De Marco C. Spectroscopic features of native and bleached opio-melanins. Biochim BiophysActa 1995; 1243(1):71–7.CrossRefGoogle Scholar
  110. Rosetto M, Manetti AG, Giordano PC, Marri L, Amons R, Baldari CT, Marchini D, Dallai R. Molecular characterization of ceratotoxin C, a novel antibacterial female-specific peptide of the ceratotoxin family from the medfly Ceratitis capitata. European Journal of Biochemistry 1996; 241(2):330–7.PubMedCrossRefGoogle Scholar
  111. Rowley AF. The role of the haemocytes of Clitumnus extradentatus in haemolymph coagulation. Cell Tissue Res 1977; 182(4):513–24.PubMedCrossRefGoogle Scholar
  112. Rozanowska M, Sama T, Land EJ, Truscott TG. Free radical scavenging properties of melanin interaction of eu-and pheo-melanin models with reducing and oxidising radicals. Free Rad. Biol. Med. 1999; 26:518–525.Google Scholar
  113. Russell V, Dunn PE. Antibacterial proteins in the midgut of Manduca sexta during metamorphosis. Journal of Insect Physiology 1996; 42(1):65–71.CrossRefGoogle Scholar
  114. 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(Pt 1):135–42.PubMedCrossRefGoogle Scholar
  115. Samakovlis C, Kylsten P, Kimbrell DA, Engstrom A, Hultmark D. The andropin gene and its product, a male-specific antibacterial peptide in Drosophila melanogaster. Embo J 1991; 10(1):163–9.PubMedGoogle Scholar
  116. Sato T, Endo Y, Matsushita M, Fujita T. Molecular characterization of a novel serine protease involved in activation of the complement system by mannose-binding protein. International Immunology 1994; 6(4):665–669.PubMedCrossRefGoogle Scholar
  117. Schallreuter K, Slominski A, Pawelek JM, Jimbow K, Gilchrest BA. What controls melanogenesis? Experimental Dermatology 1998; 7(4):143–50.PubMedCrossRefGoogle Scholar
  118. Schmidt O, Faye I, Lindstrom-Dinnetz I, Sun SC. Specific immune recognition of insect hemolin. Dev Comp Immunol 1993; 17(3):195–200.PubMedCrossRefGoogle Scholar
  119. Shalev A, Segal S, Eli MB. Evolutionary conservation of brain Thy-1 glycoprotein in vertebrates and invertebrates. Dev Comp Immunol 1985; 9(3):497–509.PubMedCrossRefGoogle Scholar
  120. Shin SW, Park SS, Park DS, Kim MG, Kim SC, Brey PT, Park HY. Isolation and characterization of immune-related genes from the fall webworm, Hyphantria cunea, using PCR-based differential display and subtractive cloning. Insect Biochemistry & Molecular Biology 1998; 28(11):827–37.CrossRefGoogle Scholar
  121. Slominski A, Paus R, Mihm MC. Inhibition of melanogenesis as an adjuvant strategy in the treatment of melanotic melanomas: selective review and hypothesis. Anticancer Research 1998; 18(5B):3709–15.PubMedGoogle Scholar
  122. Soderhall K, AspanA. Prophenoloxidase activating system and its role in cellular communication. In: Pathak JPN, editor. Insect immunity. New Delhi: Oxford & IBH Publishing Co. Pvt. Ltd.; 1993. p 113–129.Google Scholar
  123. Soderhall K, Cerenius L, Johansson MW. The prophenoloxidase activating system and its role in invertebrate defence. Ann N Y Acad Sci 1994; 712:155–61.PubMedCrossRefGoogle Scholar
  124. Stanley DW. Eicosanoids mediate insect cellular immune reactions to bacterial infections. Advances in Experimental Medicine & Biology 1997; 433:359–62.Google Scholar
  125. Stanley-Samuelson DW, Jensen E, Nickerson KW, Tiebel K, Ogg CL, Howard RW. Insect immune response to bacterial infection is mediated 15y eicosanoids. Proc Natl Acad Sci U S A 1991; 88(3):1064–8.PubMedCrossRefGoogle Scholar
  126. Stokes AH, Hastings TG, Vrana KE. Cytotoxic and genotoxic potential of dopamine. J, Neurosci. Res.1999; 55:659–665.CrossRefGoogle Scholar
  127. Su XD, Gastinel LN, Vaughn DE, Faye I, Poon P, Bjorkman PJ. Crystal structure of hemolin: a horseshoe shape with implications for homophilic adhesion. Science 1998; 281(5379):991–5.PubMedCrossRefGoogle Scholar
  128. Sun SC, Lindstrom 1, Boman HG, Faye I, Schmidt O. Hemolin: an insect-immune protein belonging to the immunoglobulin superfamily. Science 1990; 250(4988):1729–32.PubMedCrossRefGoogle Scholar
  129. Theopold U, Samakovlis C, Erdjument-Bromage H, Dillon N, Axelsson B, Schmidt O, Tempst P, Hultmark D. Helix pomatia lectin, an inducer of Drosophila immune response, binds to hemomucin, a novel surface mucin. J Biol Chem 1996; 271(22):12708–15.PubMedCrossRefGoogle Scholar
  130. Thiel S, Vorupjensen T, Stover CM, Schwaeble W, Laursen SB, Poulsen K, Willis AC, Eggleton P, Hansen S, Holmskov U and others. A second serine protease associated with mannan-binding lectin that activates complement. Nature 1997; 386(6624):506–510.PubMedCrossRefGoogle Scholar
  131. Trenczek T. Endogenous defense mechanisms of insects. Zoology 1998; 101:298–315.Google Scholar
  132. Uscian JM, Stanley-Samuelson DW. Phospholipase A2 activity in the fat body of the tobacco hornworm Manduca sexta. Arch Insect Biochem Physiol 1993; 24(4):187–201.PubMedCrossRefGoogle Scholar
  133. Vass E, Nappi AJ, Carton Y. Alterations in the activities of tyrosinase, N-acetyltransferase, and tyrosine aminotransferase in immune reactive larvae of Drosophila melanogaster. Dev Comp Immunol 1993; 17(2):109–18.CrossRefGoogle Scholar
  134. Vasta GR, Ahmed H. Animal lectins as cell surface receptors: current status for invertebrate species. Progress in Molecular & Subcellular Biology 1996; 17:158–182.CrossRefGoogle Scholar
  135. Vasta GR, Ahmed H, E. FN, T. EM, G. MA, Snowden A, Odom EW. Animal lectins as self/non-self recognition molecules: Biochemical and genetic approaches to understanding their biological roles and evolution. Annals of the New York Academy of Sciences 1994; 712:55–73.PubMedCrossRefGoogle Scholar
  136. Vilmos P, Kurucz E. Insect immunity: evolutionary roots of the mammalian innate immune system. Immunology Letters 1998; 62(2):59–66.PubMedCrossRefGoogle Scholar
  137. Winder A, Kobayashi T, Tsukamoto K, Urabe K, Aroca P, Kameyama K, Hearing VJ. The tyrosinase gene family—interactions of melanogenic proteins to regulate melanogenesis. Cell Mol Biol Res 1994; 40(78):613–26.PubMedGoogle Scholar
  138. Wright TRF. The genetic of biogenic amine metabolism, sclerotization and melanization in Drosophila melanogaster. Adv Genet 1987; 24:127–222.PubMedCrossRefGoogle Scholar
  139. Zhao L, Kanost MR. In search of a function for hemolin, a hemolymph protein from the immunoglobulin superfamily. Journal of Insect Physiology 1996; 42(1):73–79.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2001

Authors and Affiliations

  • A. J. Nappi
    • 1
  • E. Vass
    • 1
  1. 1.Department of BiologyLoyola University Chicago Chicago

Personalised recommendations