Inducible Humoral Immune Defense Responses in Insects

  • R. D. Karp
Part of the Progress in Molecular and Subcellular Biology book series (PMSB, volume 15)

Abstract

There is a revolution taking place in the field of immunobiology that is challenging the widely held dogmatic belief that invertebrates are incapable of mounting true adaptive immune responses when exposed to foreign substances. If the definition of adaptive immunity is predicated on the possession of a thymus or lymph nodes, then invertebrates will never satisfy these requirements. However, a growing body of evidence from representatives of various invertebratephyla, clearly indicate that the two basic criteria of an adaptive immune response, specificity and immunologic memory, have evolved in some of these animals. The data from these studies will hopefully force us to rethink, and redefine, what we mean by immunity. This will require that we no longer use anatomical complexity to gauge what is physiologically possible, but rather measure an animal’s potential by the degree of molecular complexity that is engendered in its genome. This will surely open up our minds and lead to a better perspective concerning an understanding of how the sophisticated mechanisms of adaptive immunity evolved.

Keywords

Permeability Agar Aldehyde Electrophoresis Syringe 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anderson RS, Cook ML (1979) Induction of lysozymelike activity in the hemolymph and hemocytes of an insect, Spodoptera eridania. J Invertebr Pathol 33: 197–203CrossRefGoogle Scholar
  2. Ando K, Okada M, Natori S (1987) Purification of sareotoxin II, antibacterial proteins of Sarcophaga peregrina (flesh fly) larvae. Biochemistry 26: 226–230PubMedCrossRefGoogle Scholar
  3. Baba K, Okada M, Kawano M, Kormano T, Natori S (1987) Purification of sareotoxin III, a new antibacterial protein of Sarcophaga peregrina. J Biochem (Tokyo) 102: 69–74Google Scholar
  4. Belisle EH, Strausser HR (1981) Sex-related immunocompetence of Balb/c mice. II. Study of immunologic responsiveness of young, adult and aged mice. Dev Comp Immunol 5: 661–670PubMedGoogle Scholar
  5. Bettini S (1965) Acquired immune response of the housefly Musca domestica (Linnaeus), to injected venom of the spider Lactrodectus mactans tredecimagluttatus (Rossi). J Invertebr Pathol 7: 378–383PubMedCrossRefGoogle Scholar
  6. Boman HG, Nilsson-Faye I, Paul K, Rasmuson T (1974) Insect immunity. I. Characterstics of an inducible cell-free antibacterial reaction in hemolymph of Samia cythia pupae. Inf Immunol 10: 136–145Google Scholar
  7. Bulet P, Cociancich S, Dimarcq J-L, Lambert J, Reichhart J-M, Hoffmann D, Hetru C, Hoffmann JA (1991) Isolation from a coleopteran insect of a novel inducible antibacterial peptide and of new members of the insect defensin family. J Biol Chem 266: 24520–24525PubMedGoogle Scholar
  8. Casteels P, Anipe C, Jacobs F, Vaeck M, Tempst P (1989) Apidaecins - antibacterial peptides from honeybees. EMBO J 8: 2387–2391PubMedGoogle Scholar
  9. Casteels P, Ampe C, Riviere L, Van Damme J, Elicone C, Fleming M, Jacobs F, Tempst P (1990) Isolation and characterization of abaecin, a major antibacterial response peptide in the honeybee (Apis mellifera). Eur J Biochem 187: 381–386PubMedCrossRefGoogle Scholar
  10. Carlsson A, Engstrom P, Palva ET, Bennich H (1991) Attacin, an antibacterial protein from Hyalophora cecropia, inhibits synthesis of outer membrane proteins in Escherichia coli by interfering with OMP gene transcription. Inf Immunol 59: 3040–3045Google Scholar
  11. Castro VM, Boman HG, Hammarstrom S (1987) Isolation and characterization of a group of isolectins with galactose/N-aeetygalactoseamine specificity from hemolymph of the giant silk moth Hyalophora cecropia. Insect Biochem 17: 513–523CrossRefGoogle Scholar
  12. Chadwick JS (1970) Relation of lysozyme concentration to acquired immunity against Pseudomonas aeruginosa in Galleria mellonella. J Invertebr Pathol 15: 455–456CrossRefGoogle Scholar
  13. Chen C, Rateliffe NA, Rowley AF (1993) Detection, isolation and characterization of multiple lectins from the haemolymph of the cockroachBlaberus discoidalis. Biochem J 294: 181–190PubMedGoogle Scholar
  14. Christensen B, Fink J, Merrifield RB, Mauzerall D (1988) Channel-forming properties of cecropins and related model compounds incorporated into planar lipid membranes. Proc Natl Acad Sci USA 85: 5072–5076PubMedCrossRefGoogle Scholar
  15. Dickinson L, Russell V, Dunn PE (1988) A family of bacteria-regulated, cecropin D-like peptides from Manduca sexta. J Biol Chem 263: 19424–19429PubMedGoogle Scholar
  16. Dimarcq JL, Keppi E, Dunbar B, Lambert J, Reichhart JM, Hoffmann D, Rankine S, Fothergill JE, Hoffmann J A (1988) Insect immunity. Purification and characterization of a family of novel inducible antibacterial proteins from immunized larvae of the dipteran Phormia terranovae and complete amino-acid sequence of the predominant member, diptericin A. Eur J Biochem 171: 17–29PubMedCrossRefGoogle Scholar
  17. Dimarcq JL, Zachary D, Hoffmann J A, Hoffmann D, Reichhart JM (1990) Insect immunity - Expression of the two major inducible antibacterial peptides, defensin and diptericin, in Phormia terranovae. EMBO J 9: 2507–2515PubMedGoogle Scholar
  18. Drif L, Brehelin M (1989) Agglutinin mediated immune recognition in Locusta migratoria (Insecta). J Insect Physiol 35: 729–736CrossRefGoogle Scholar
  19. Dunn PE (1986) Biochemical aspects of insect immunology. Annu Rev Entomol 31: 321–339CrossRefGoogle Scholar
  20. Dunn PE, Dai W, Kanost MR, Geng D (1985) Soluble peptidoglycan fragments stimulate, antibacterial protein synthesis by fat body from larvae of Manduca sexta. Dev Comp Immunol 9: 559–568PubMedCrossRefGoogle Scholar
  21. Duwel-Eby LE, Faulhaber LM, Karp RD (1991) The inducible humoral response in the cockroach. In: Gupta AP (ed) Immunology of insects and other arthropods. Academic Press, New York, pp 385–402Google Scholar
  22. Faulhaber LM, Karp RD (1992) A diphasic immune response against bacteria in the American cockroach. Immunology 75: 378–381PubMedGoogle Scholar
  23. Faulhaber LM, Karp RD (1995) An inducible antibacterial protein in the American cockroach that demonstrates killing activity in vitro. J Insect Physiol (submitted)Google Scholar
  24. Faye I, Hultmark D (1993) The insect immune proteins and the regulation of their genes. In: Beckage NE, Thompson SN, Federici BA (eds) Parasites and pathogens of insects. Volume 2: Pathogens. Academic Press, New York, pp 25–53Google Scholar
  25. Faye I Pye A, Rasmuson T, Boman HG, Boman IA (1975) Insect immunity. II. Simultaneous induction of antibacterial activity and selective synthesis of some hemolymph proteins in diapausing pupae of Hyalophora cecropia andSamia cynthia. Inf Immunol 12: 1426–1438Google Scholar
  26. Fujiwara S, Imai J, Fujiwara M, Yaeshima T, Kawashima T, Kobayashi K (1990) A potent antibacterial protein in royal jelly - purification and determination of the primary structure of royalisin. J Biol Chem 265: 11333–11337PubMedGoogle Scholar
  27. George JF, Howcroft TK, Karp RD (1987a) Primary integumentary allograft reactivity in the American cockroach Periplaneta americana. Transplantation 43: 514–519PubMedCrossRefGoogle Scholar
  28. George JF, Karp RD, Rellahan BL, Lessard JL (1987b) Alteration of the protein composition in the hemolymph of American cockroaches immunized with soluble proteins. Immunology 62: 505–509PubMedGoogle Scholar
  29. Gilliam M, Jeter WS (1970) Synthesis of agglutinating substances in adult honeybees against Bacillus larva. J Invertebr Pathol 16: 69–70PubMedCrossRefGoogle Scholar
  30. Gudmundsson GG, Lidholm D-A, Asling B, Gan R, Boman HG (1991) The cecropin locus: cloning and expression of a gene cluster encoding three antibacterial peptides in Hyalophora cecropia. J Biol Chem 266: 11510–11517PubMedGoogle Scholar
  31. Hapner KD, Jermyn MA (1981) Haemagglutinin activity in the haemolymph of Teleogryllus commodus (Walker). Insect Biochem 11: 287–295CrossRefGoogle Scholar
  32. Harrelson AL, Goodman CS (1988) Growth cone guidance in insects: fascilin II is a member of the immunoglobulin superfamily. Science 242: 700–708PubMedCrossRefGoogle Scholar
  33. Hartman RS, Karp RD (1989) Short-term immunologic memory in the allograft response of the American cockroach. Transplantation 47: 920–922PubMedCrossRefGoogle Scholar
  34. Hoffmann D (1980) Induction of antibacterial activity in the blood of the migratory locust Locus ta migratoria L. J Insect Physiol 26: 539–549CrossRefGoogle Scholar
  35. Hoffmann D, Hultmark D, Boman HG (1981) Insect immunity: Galleria mellonella and other Lepidoptera have eecropia-P9-like factors active against gram negative bacteria. Insect Bochem 11: 537–548CrossRefGoogle Scholar
  36. Hultmark D, Steiner H, Rasmuson T, Boman HG (1980) Insect immunity. Purification and properties of three inducible bactericidal proteins from hemolymph of immunized pupae ofHyalophora cecropia. Eur J Biochem 106: 7–16PubMedCrossRefGoogle Scholar
  37. Hultmark D, Engstrom A, Bennich H, Kapur R, Boman HG (1982) Insect immunity: Isolation and structure of cecropin D and four minor antibacterial components from cecropia pupae. Eur J Biochem 127: 207–217PubMedCrossRefGoogle Scholar
  38. Hultmark D, Engstrom A, Andersson K, Steiner H, Bennich H, Boman HG (1983) Insect immunity. Attacins, a family of antibacterial proteins from Hyalophora cecropia. EMBO J 2: 571–576PubMedGoogle Scholar
  39. Hurlbert RE, Karlinsey JE, Spence KD (1985) Differential synthesis of bacteria-induced proteins of Manduca sexta pupae and larvae. J Insect Physiol 31: 205–215CrossRefGoogle Scholar
  40. Huws Davies D, Siva-Jothy T (1991) Encapsulation in insects: polydnaviruses and encapsulation-promoting factors. In: Gupta AP (ed) Immunology of Insects and other arthropods. CRC Press, Boca Raton, pp 119–132Google Scholar
  41. Ibrahim EAR, Ingram GA, Molyneux DH (1984) Haemagglutinins and parasite agglutinins in haemolymph and gut of Glossina. Tropenmed Parasitol 35: 151–156PubMedGoogle Scholar
  42. Ishikawa M, Kubo T, Natori S (1992) Purification and characterization of diptericin homologue from Sarcophaga peregrina (flesh fly) Biochem J 287: 573–578PubMedGoogle Scholar
  43. Jollès J, Sehoentgen F, Croizier G, Croizier L, Jolles P (1979) Insect lysozymes from three species of lepidoptera: Their structural relatedness to the C (chicken) type lysozyme: J Mol Evol 14: 267–271PubMedCrossRefGoogle Scholar
  44. Jomori T, Natori S (1991) Molecular cloning of cDN A of lipopolysaccharide-binding protein from the hemolymph of the American cockroach, Periplaneta americana - Similarity of the protein with animal lectins and its acute phase expression. J Biol Chem 266: 13318–13323PubMedGoogle Scholar
  45. Jomori T, Kubo T, Natori S (1990) Purification and characterization of lipopolysaccharide-binding protein from the hemolymph of the American cockroach. Eur J Biochem 190: 201–206PubMedCrossRefGoogle Scholar
  46. Jurenka R, Manfredi K, Hapner KD (1982) Haemagglutinin activity in Acrididae (grasshopper) haemolymph. J Insect Physiol 28: 177–181CrossRefGoogle Scholar
  47. Kaaya GP, Flyg C, Boman HG (1987) Induction of cecropin and attacin-like antibacterial factors in the haemolymph of Glossina morsitans morsitans. Insect Biochem 17: 309–315CrossRefGoogle Scholar
  48. Kamon E, Shulov A (1965) Immune response of locusts to venom of the scorpion. J Invertebr Pathol 7: 192–198PubMedCrossRefGoogle Scholar
  49. Kanai A, Natori S (1989) Cloning of gene cluster for sarcotoxin I, antibacterial proteins of Sarcophaga peregrina. FEBS Lett 258: 199–202PubMedCrossRefGoogle Scholar
  50. Kanai A, Natori S (1990) Analysis of a gene cluster for sarcotoxin II, a group of antibacterial proteins ofSarcophaga peregrina. Mol Cell Biol 10: 6114–6122PubMedGoogle Scholar
  51. Kanost MR, Dai W, Dunn PE (1988) Petidoglycan fragments elicit antibacterial protein synthesis in larvae of Manduca sexta. Arch Insect Biochem Physiol 8: 147–164CrossRefGoogle Scholar
  52. Karp RD, Rheins LA (1980) Induction of specific humoral immunity to soluble proteins in the American cockroach(Periplaneta americand). II. Nature of the secondary response. Dev Comp Immunol 4: 629–639PubMedCrossRefGoogle Scholar
  53. Komano H, Natori S (1985) Participation of Sarcophaga peregrina humoral lectin in the lysis of sheep red blood cells injected into the abdominal cavity of larvae. Dev Comp Immunol 9: 31–40PubMedCrossRefGoogle Scholar
  54. Komano H, Mizuno D, Natori S (1980) Purification of lectin induced in the hemolymph of Sarcophaga peregrina larvae on injury. J Biol Chem 255: 2919–2924PubMedGoogle Scholar
  55. Kubo T, Natori S (1987) Purification and some properties of a lectin from the hemolymph of Periplaneta americana (American cockroach). Eur J Biochem 168: 75–82PubMedCrossRefGoogle Scholar
  56. Kubo T, Komano H, Okada M, Natori S (1984) Identification of hemagglutinating protein and bactericidal activity in the hemolymph of adultSarcophaga peregrina on injury of the body wall. Dev Comp Immunol 8: 283–291PubMedCrossRefGoogle Scholar
  57. Kubo T, Kawasaki K, Natori S (1990) Sucrose-binding lectin in regenerating cockroach (Periplaneta americana) legs: Purification from adult hemolymph. Insect Biochem 20: 585–591CrossRefGoogle Scholar
  58. Kylsten P, Kimbrell DA, Daffre S, Samakovlis C, Hultmark D (1992) The lysozyme locus in Drosophila melanogaster. Different genes are expressed in midgut and salivary glands. Mol Gen Genet 232: 335–343PubMedCrossRefGoogle Scholar
  59. Ladendorff NE, Kanost MR (1990) Isolation and characterization of bacteria-induced protein-P4 from hemolymph ofManduca sexta, Arch Insect Biochem Physiol 15: 33–41PubMedCrossRefGoogle Scholar
  60. Ladendorff NE, Kanost MR (1991) Becteria-induced protein P4 (hemolin) from Manduca sexta: A member of the immunoglobulin superfamily which can inhibit hemocyte aggregation. Arch Insect Biochem Physiol 18: 285–300PubMedCrossRefGoogle Scholar
  61. Lahita RG (1982) In: Stites DP, Stobo JD, Fudenberg H, Wells JV (eds) Basic and clinical immunology, 4th edn. Lange, Los Altos, CAGoogle Scholar
  62. Lambert J, Keppi E, Dimarcq JL, Wicker C, Reichhart JM, Dunbar B, Lepage P, Van Dorsselaer A, Hoffmann J, Fothergill J, Hoffmann D (1989) Insect immunity: isolation from immune blood of the dipteran Phormia terranovae of two insect antibacterial peptides with sequence homology to rabbit lung macrophage bactericidal peptides. Proc Natl Acad Sci USA 86: 262–266PubMedCrossRefGoogle Scholar
  63. Lee J-Y, Edlund T, Ny T, Faye I, Boman HG (1983) Insect immunity. Isolation of cDNA clones corresponding to attacins and immune protein P4 from Hyalophora cecropia. EMBO J 2: 577–581PubMedGoogle Scholar
  64. Lee J-Y, Boman A, Chuanxin S, Andersson M, Jornvall H, Mutt V, Boman HG (1989) Antibacterial peptides from pig intestine: Isolation of a mammalian cecropin. Proc Natl Acad Sci USA 86: 9159–9162PubMedCrossRefGoogle Scholar
  65. Lehrer RI, Ganz T, Selsted ME (1991) Defensins - endogenous antibiotic peptides of animal cells. Cell 64: 229–230PubMedCrossRefGoogle Scholar
  66. Ludwig D, Tracey KM, Burns ML (1957) Ratio of ions required to maintain the heartbeat of the American cockroach, Periplaneta americana Linnaeus. Ann Entomol Soc Am 50: 244–246Google Scholar
  67. Matsuyama K, Natori S (1988a) Purification of three antibacterial proteins from the culture medium of NIH-Sape-4, an embryonic cell line of Sarcophaga peregrina. J Biol Chem 263: 17112–17116PubMedGoogle Scholar
  68. Matsuyama K, Natori S (1988b) Molecular cloning of cDNA for sapecin and unique expression of the sapecin gene during the development of Sarcophaga peregrina. J Biol Chem 263: 17117–17121PubMedGoogle Scholar
  69. Matsuyama K, Natori S (1990) Mode of action of sapecin, a novel antibacterial protein of Sarcophaga peregrina (flesh fly) J Biochem (Tokyo) 108: 128–132Google Scholar
  70. Minnick MF, Rupp RA, Spence KD (1986) A bacterial-induced lectin which triggers hemocyte coagulation in Manduca sexta. Biochem Biophys Res Commun 137: 729–735PubMedCrossRefGoogle Scholar
  71. Morishima I, Suginaka S, Ueno T, Hirano H (1990) Isolation and structure of cecropins, inducible antibacterial peptides from the silkworm, Bomhyx mori. Comp Biochem Physiol B 95: 551–554PubMedCrossRefGoogle Scholar
  72. Mulnix AB, Dunn PE (1994) Structure and induction of a lysozyme gene from the Tobacco Hornworm, Manduca sexta. Insect Biochem Mol Biol 24: 271–281PubMedCrossRefGoogle Scholar
  73. Okada M, Natori S (1983) Puriification and characterization of an antibacterial protein from haemolymph of Sarcophaga peregrina (flesh fly) larvae. Biochem J 211: 727–734PubMedGoogle Scholar
  74. Okada M, Natori S (1984) Mode of action of a bactericidal protein induced in the haemolymph of Sarcophaga peregrina (flesh-fly) larvae. Biochem J 222: 119–124PubMedGoogle Scholar
  75. Okada M, Natori S (1985) lonophore activity of sarcotoxin I, a bactericidal protein ofSarcophaga peregrina. Biochem J 229: 453–458PubMedGoogle Scholar
  76. Pendland JC, Boucias DG (1985) Hemagglutinin activity in the hemolymph ofAnticarsia gemmatalis larvae infected with the fungus Nomuraea rileyi. Dev Comp Immunol 9: 21–30PubMedCrossRefGoogle Scholar
  77. Pendland JC, Heath MA, Boucias DG (1988) Function of a galactose-binding lectin from Spodopetera exigua larval haemolymph: opsonization of blastospores from entomopathogenous hypomycetes. J Insect Physiol 34: 533–540CrossRefGoogle Scholar
  78. Postlethwait JH, Saul SH, Postlethwait JA (1988) The antibacterial immune response of the medfly Ceratitis capitata. J Insect Physiol 34: 91–96CrossRefGoogle Scholar
  79. Powning RF, Irzykiewicz H (1967) Lysozyme-like action of enzymes from the cockroach Periplaneta americana and from some other sources. J Insect Physiol 13: 1293–1299PubMedCrossRefGoogle Scholar
  80. Powning RF, Davidson WJ (1973) Studies on insect bacteriolytic enzymes. I. lysozyme in the haemolymph of Galleria mellonella and Bomhyx mori. Comp Biochem Physiol B 45B: 669–681CrossRefGoogle Scholar
  81. Rheins LA, Karp RD (1982) Cockroach inducible humoral factor: Precipitin activity that is sensitive to a proteolytic enzyme. J Invertebr Pathol 40: 190–196CrossRefGoogle Scholar
  82. Rheins LA, Karp RD (1985a) Effect of gender on the inducible humoral immune response to Honeybee venom in the American cockroach (Periplaneta americana). Dev Comp Immunol 9: 41–49PubMedCrossRefGoogle Scholar
  83. Rheins LA, Karp RD (1985b) Ontogeny of the invertebrate humoral immune response: Studies on various developmental stages of the American cockroach. Dev Comp Immunol 9: 395–406PubMedCrossRefGoogle Scholar
  84. Rheins LA, Karp RD, Butz A (1980) Induction of specific humoral immunity to soluble proteins in the American cockroach(Periplaneta americana). I. Nature of the primary response. Dev Comp Immunol 4: 447–458PubMedCrossRefGoogle Scholar
  85. Robertson M, Postlethwait JH (1986) The humoral antibacterial response of Drosophila adults. Dev Comp Immunol 10: 167–179PubMedCrossRefGoogle Scholar
  86. Ryan NA, Karp RD (1993) Stimulation of hemocyte proliferation in the American cockroach (.Periplaneta americana) by injection of Enterobacter cloacae. J Insect Physiol 39: 601–608CrossRefGoogle Scholar
  87. Samakovlis C, Kimbrell DA, Kylsten P, Engström A, Hultmark D (1990) The immune response in Drosophila: pattern of cecropin expression and biological activity. EMBO J 9: 2969–2976PubMedGoogle Scholar
  88. Samakovlis C, Kylsten P, Kimbrell DA, Engström A, Hultmark D (1991) The Andropin gene and its product, a male-specific antibacterial peptide in Drosophila melanogaster. EMBO J 10: 163–169PubMedGoogle Scholar
  89. Seeger MA, Haffley L, Kaufman TC (1988) Characterization of amalgam: a member of the immunoglobulin superfamily fromDrosophila. Cell 55: 589–600PubMedCrossRefGoogle Scholar
  90. Steiner H, Hultmark D, Engström A, Bennich H, Boman HG (1981) Sequence and specificity of two antibacterial proteins involved in insect immunity. Nature 292: 246–248PubMedCrossRefGoogle Scholar
  91. Steiner H, Andreu D, Merrifield RB (1988) Binding and action of cecropin and cecropin analogues: antibacterial peptides from insects. Biochim Biophys Acta 939: 260–266PubMedCrossRefGoogle Scholar
  92. Sugumaran M, Kanost MR (1993) Regulation of insect hemolymph phenoloxidases. In: Beckage NE, Thompson SN, Federici BA (eds) Parasites and pathogens of insects, vol 2. Parasites. Academic Press, New York, pp 317–342Google Scholar
  93. Sun SC, Lindstrom I, Boman HG, Faye I, Schmidt O (1990) Hemolin - an insect immune protein belonging to the immunoglobulin superfamily. Science 250: 1729–1732PubMedCrossRefGoogle Scholar
  94. Sun S-C, Asling B, Faye I (1991a) Organization and expression of the immunoresponsive lysozyme, gene in the giant silk moth, Hyalophora cecropia. J Biol Chem 266: 6644–6649PubMedGoogle Scholar
  95. Sun S-C, Lindstrom I, Faye I (1991b) Structure and expression of the attacin genes in Hyalophora cecropia. Eur J Biochem 196: 247–254PubMedCrossRefGoogle Scholar
  96. Suzuki T, Natori S (1983) Identificiation of a protein having hemagglutinating activity in the hemo-lymph of the silkworm, Bombyx mori. J Biochem 93: 583–590PubMedCrossRefGoogle Scholar
  97. Takahashi H, Komano H, Kawaguchi N, Kitamura N, Nakanishi S, Natori S (1985) Cloning and sequencing of cDNA of Sarcophaga peregrina humoral lectin induced on injury of the body wall. J Biol Chem 260: 12228–12233PubMedGoogle Scholar
  98. Takahashi H, Komano H, Natori S (1986) Expression of the lectin gene in Sarcophaga peregrina during normal development and under conditions where the defence mechanism is activated. J Insect Physiol 32: 771–779CrossRefGoogle Scholar
  99. Wago H (1991) Phagocytic recognition in Bombyx mori. In: Gupta AP (ed) Immunology of insects and other arthropods. CRC Press, Boca Raton, pp 215–235Google Scholar
  100. Wang Y, Willott E, Kanost MR (1995) Organization and expression of the hemolin gene, a member of the immunoglobulin superfamily in an insect, Manduca sexta. Insect Mol Biol 4: 113–123PubMedCrossRefGoogle Scholar
  101. Zachary D, Hoffmann D (1984) Lysozyme is stored in the granules of certain haemocyte types in Locusta. J Insect Physiol 30: 405–411CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1996

Authors and Affiliations

  • R. D. Karp
    • 1
  1. 1.Department of Biological SciencesUniversity of CincinnatiCincinnatiUSA

Personalised recommendations