Kinases, intracellular calcium, and apolipophorin-III influence the adhesion of larval hemocytes of the lepidopterous insect, Galleria mellonella

Archives of Insect Biochemistry and Physiology

Volumn 53, Issue 4, 2003, Pages 158-171

  Zakarian, Robert J ^a   Dunphy, Gary B ^a,c   Rau, Manfred E ^a   Albert, Paul J ^b  

^a MCGILL UNIVERSITY   (Canada)

^b Gina Cody School of Engineering and Computer Science   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Adhesion; Granular cells; Hemocyte; Intracellular calcium; Plasmatocyte; Protein kinase

Indexed keywords

GALLERIA MELLONELLA; INSECTA;

APOLIPOPHORIN III; APOLIPOPROTEIN; CALCIUM; DIACYLGLYCEROL; ENZYME INHIBITOR; ISOENZYME; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHOLIPASE C; PHOSPHOTRANSFERASE;

ANIMAL; ARTICLE; BLOOD CELL; CELL ADHESION; CHEMISTRY; CLASSIFICATION; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; DRUG INTERACTION; ENZYME ACTIVATION; ENZYMOLOGY; INTRACELLULAR FLUID; LARVA; LEPIDOPTERA; METABOLISM; PHYSIOLOGY;

ANIMALS; APOLIPOPROTEINS; CALCIUM; CELL ADHESION; DIGLYCERIDES; DRUG INTERACTIONS; ENZYME ACTIVATION; ENZYME INHIBITORS; HEMOCYTES; INTRACELLULAR FLUID; ISOENZYMES; LARVA; LEPIDOPTERA; PHOSPHOLIPASE C; PHOSPHOTRANSFERASES; TETRADECANOYLPHORBOL ACETATE;

EID: 0043234718     PISSN: 07394462     EISSN: None     Source Type: Journal    
DOI: 10.1002/arch.10097     Document Type: Article

References (69)

1. Anggraeni T, Ratcliffe NA. 1991. Studies on cell-cell co-operation during phagocytosis by purified hemocyte populations of the wax moth, Galleria mellonella. J Insect Physiol 37:453-460.
2. Canesi L, Betti M, Ciacci C, Scarpato A, Citterio B, Pruzzo C, Gallo G. 2002. Signaling pathways involved in the physiological response of mussel hemocytes to bacterial challenge: the role of stress-activated p38 MAP kinases. Dev Comp Immunol 26:325-334.
3. Charalambidis ND, Zervas CG, Lambropoulou M, Katsoris PG, Marmaras VJ. 1995. Lipopolysaccharide-stimulated exocytosis of nonself recognition protein from insect hemocytes depend on protein tyrosine phosphorylation. Eur J Cell Biol 67:32-41.
4. Chen JH, Bayne CJ. 1994. The roles of carbohydrates in aggregation and adhesion of hemocytes from the California mussel (Mytilus californianus). Comp Biochem Physiol 109A:117-125.
5. Cherbas L. 1973. The induction of an injury reaction in cultured haemocytes from saturniid pupae. J Insect Physiol 19:2011-2023
6. Chiu JK, Aston WP, Chadwick JS. 1991. A suggested role for phospholipase C in the immune response of Galleria mellonella. J Invertebr Pathol 57:128-130.
7. Choi HK, Taniai K, Kato Y, Kadono-Okuda K, Yamamoto M, Chowdhury S, Xu J, Sugiyama M, Choi SK, Miyanoshita A, Debnath NC, Asaoka A, Ishii T, Yamakawa M. 1995. Induction of activity of protein kinase C and A by bacterial lipopolysaccharide in isolated hemocytes from silkworm, Bombyx mori. J Ser Sci Jpn 64:450-456.
8. Clapham DE. 1995. Calcium signaling. Cell 80:259-268.
9. Clark KD, Pech LL, Strand MR. 1997. Isolation and identification of a plasmatocyte-spreading peptide from the hemolymph of the lepidopteran insect Pseudoplusia includens. J Biol Chem 272:23440-23447.
10. Coodin S, Caveney S. 1992. Lipophorin inhibits the adhesion of cockroach (Periplaneta americana) haemocytes in vitro. J Insect Physiol 38:853-862.
11. Davies DH, Hayes TK, Vinson SB. 1988. Preliminary characterization and purification of an in vitro encapsulation promoting factor: a peptide that mediates insect haemocyte adhesion. Dev Comp Immunol 12:241-253.
12. Dettloff M, Wiesner A. 1998. Immune stimulation by lipid A-bound apolipophorin III. In: Wiesner A, Dunphy GB, Marmaras VJ, Morishima I, Sugumaran M, Yamakawa M, editors. Techniques in insect immunology. Fairhaven, NJ: SOS Publication. p 243-252.
13. Dettloff M, Kaiser B, Weisner A. 2001. Localization of injected apoLp-III in vivo: new insights into the immune activation process directed by this protein. J Insect Physiol 47:789-797.
14. Diehl-Jones WL, Mandato CA, Whent G, Downer RGH. 1996. Monoaminergic regulation of hemocyte activity. J Insect Physiol 42:13-19.
15. Dunphy GB, Downer RGH. 1994. Octopamine a modulator of the haemocytic nodulation response of non-immune Galleria mellonella larvae. J Insect Physiol 40:267-273.
16. Dunphy GB, Halwani AE. 1997. Haemolymph proteins of larvae of Galleria mellonella detoxify endotoxins of the insect pathogenic bacteria Xenorhabdus nematophilus (Enterobacteriaceae). J Insect Physiol 43:1023-1029.
17. Dunphy GB, Niven DF, Chadwick JS. 2002. Iron contributes to the antibacterial functions of the haemolymph of Galleria mellonella. J Insect Physiol 48:903-914.
18. Dutky SR, Thompson JV, Cantwell GE. 1962. A technique for mass rearing of the greater wax moth (Lepidoptera: Galleridae). Proc Entomol Soc Wash 64:56-58.
19. Ehlers D, Beet S. 1998. Activation of the phenoloxidase system and its relation to the recognition of foreign material. In: Simoes N, Boemare N, Ehlers RU, editors. Entomopathogenic nematodes. Pathogenicity of entomopathogenic nematodes versus insect defence mechanisms. Brussels: Directorate-General for Science, Research and Development, Commission of the European Community, p 123-133.
20. Eichholtz T, de Bont DB, de Widt J, Liskamp RM, Ploegh HL. 1993. A myristoylated pseudosubstrate peptide, a novel protein kinase C inhibitor. J Biol Chem 268:1982-1986.
21. Foukas LC, Katsoulas HL, Paraskevopoulou N, Metheniti A, Lambropoulou M, Marmaras VJ. 1998. Phagocytosis of Escherichia coli by insect hemocytes requires both activation of the ras-mitogen-activated protein kinase signal transduction pathway for attachment and beta 3 integrin for internalization. J Biol Chem 273:14813-14818.
22. Gillespie JP, Kanost MR, Trenczek T. 1997. Biological mediators of insect immunity. Ann Rev Entomol 42:611-643.
23. Gole JWD, Downer RGH, Sohi SS. 1982. Octopamine-sensitive adenylate cyclase in haemocytes of the forest tent caterpillar, Malacosoma disstria (Lepidoptera). Can J Zool 60:825-829.
24. Gschwendt M, Dieterich S, Rennecke J, Kittstein W, Mueller Hans-J, Johannes Franz-J. 1996. Inhibition of protein kinase C mu by various inhibitors. Differentiation from protein kinase C isoenzymes. FEBS Lett 392:77-80.
25. Halwani AE, Dunphy GB. 1999. Apolipophorin-III in Galleria mellonella potentiates hemolymph lytic activity. Dev Comp Immunol 23:563-570.
26. Halwani AE, Niven DF, Dunphy GB. 2000. Apolipophorin-III and the interactions of lipoteichoic acids with the immediate immune responses of Galleria mellonella. J Invertebr Pathol 76:233-241.
27. 2+ entry in Jurkat T cells. J Biol Chem 272: 15426-15433.
28. Hayakawa Y. 1994. Cellular immunosuppressive protein in the plasma of parasitized insect larvae. J Biol Chem 269: 14536-14540.
29. Imler J-L, Hoffman JA. 2000. Signaling mechanisms in the antimicrobial host defense of Drosophila. Curr Opin Microbiol 3:16-22.
30. Kanost MR, Zepp MK, Ladendorff NE, Andersson LA. 1994. Isolation and characterization of a hemocyte aggregation inhibitor from the hemolymph of Manduca sexta larvae. Arch Insect Biochem Physiol 27:123-136.
31. Keely LL, Hesson AS. 1995. Calcium-dependent signal transduction by the hypertrehalosemic hormone in the cockroach fat body. Gen Comp Endocrinol 99:373-381.
32. Koizumi N, Imamura M, Kadotani T, Yaoi K, Iwahana H, Sato R. 1999. The lipopolysaccharide-binding protein participating in hemocyte nodule formation in the silkworm Bombyx mori is a novel member of the C-type lectin superfamily with two different tandem carbohydrate-recognition domains. FEBS Lett 443:139-143.
33. Laenen B, Verhaert P, Schoofs L, Steels P, van Kerkhoue E. 1999. Partial purification of a peptide that stimulates the primary urine production of single isolated Malpighian tubules of the forest ant, Formica polycteria. J Insect Physiol 45:743-753.
34. Lanz-Mendoza H, Bettencourt R, Fabbri M, Faye I. 1996. Regulation of the insect immune response: the effect of hemolin on cellular immune mechanisms. Cell Immunol 169:47-54.
35. Lavine MD, Strand MR. 2002. Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 32:1295-1309.
36. Lee C, Levin A, Branton D. 1987. Copper staining: a five minute protein strain for sodium dodecyl-sulfate polyacrylamide gels. Anal Biochem 166:308-312.
37. Mandato CA, Diehl-Jones WI, Moore SI, and Downer RGH. 1997. The effects of eicosanoid biosynthesis inhibitors on prophenoloxidase activation, phagocytosis and cell spreading in Galleria mellonella. J Insect Physiol 43:1-8.
38. McCarthy TL, Ji C, Casinghino S, Centrella M. 1998. Alternate signaling pathways selectively regulate binding of insulin-like growth factor I and II on fetal rat bone cells. J Cell Biochem 68:446-456.
39. Marmaras VJ, Charalambidis ND, Lambropoulou M. 1994. Cellular defense mechanisms in Ceratitis capitata: recognition and entrapment of Escherichia coli by hemocytes. Arch Insect Biochem Physiol 26:1-14.
40. Mellor H, Parker PJ. 1998. The extended protein kinase C superfamily. Biochem J 332: 281-292.
41. Metheniti A, Paraskevopoulou N, Lambropoulou M, Marmaras VJ. 2001. Involvement of FAK/Src complex in the process of Escherichia coli phagocytosis by insect hemocytes. FEBS Lett 496:55-59.
42. Miller JC, Stanley DW. 2001. Eicosanoids mediate microaggregation reactions to bacterial challenge in isolated hemocyte preparations. J Insect Physiol 47:1409-1417.
43. O'Gara BA, Brown PL, Dlugosch D, Kandiel A, Ku JW, Geier JK, Henggeler NC, Abbasi A, Kounalakis N. 1999. Regulation of pharyngeal motility by FMRFamide and related peptides in the medicinal leech, Hirudo medicinalis. Invertebr Neurosci 4:41-53.
44. Ottaviani E, Sassi D, Kletsas D. 1997. PDGF- and TGF-B-induced changes in cell shape of invertebrate immunocytes: effect of calcium entry blockers. Eur J Cell Biol 74:336-341.
45. Ottaviani E, Barbieri D, Malagoli D, Kletsas D. 2001. Involvement of PI 3-kinase, PKA and PKC in PDGF- and TGF-B-mediated prevention of 2-deoxy-D-ribose-induced apoptosis in the insect cell line IPLB-LdFB. Cell Biol Int 25:171-177.
46. Park Y, Kim Y. 2000. Eicosanoids rescue Spodoptera exigua infected with Xenorhabdus nematophilus, the symbiotic bacteria to the entomopathogenic nematode Steinernema carpocapsae. J Insect Physiol 46:1469-1476.
47. Park Y, Kim Y, Putnam SM, Stanley DW. 2003. The bacterium Xenorhabdus nematophilus depresses nodulation reactions to infection by inhibiting eicosanoid biosynthesis in Tobacco Hornworm Manduca sexta. Arch Insect Biochem Physiol 52:71-80.
48. Price CD, Ratcliffe NA 1974. A reappraisal of insect haemocyte classification by the examination of blood from fifteen insect orders. Z Zellforsch Mikroskop Anat 147:537-549.
49. Ratcliffe NA, Götz P. 1990. Functional studies on insect haemocytes, including non-self recognition. Res Immunol 141:919-923.
50. Samakovlis C, Asling B, Boman HG, Gateff E, Hultmark D. 1992. In vitro induction of cecropin genes - an immune response in a Drosophila blood cell line. Biochem Biophys Res Commun 188:1169-1175.
51. Schnyder B, Meunier PC, Car BD. 1998. Inhibition of kinases impairs neutrophil activation and killing of Staphylococcus aureus. Biochem J 331:489-495.
52. Shimabukuro M, Xu J, Sugiyama M, Taniai K, Kadono-Okuda K, Kato Y, Yamamoto M, Chowdhury S, Choi SK, Choi HK, Miyanoshit A, Debnath NC, Yamakawa M. 1996. Signal transduction of cecropin B gene expression in adherent hemocytes of the silkworm, Bombyx mori (Lepidoptera: Bombycidae). Appl Entomol Zool 31:135-143.
53. Shinomura T, Asaoka Y, Oka M, Yoshida K, Nishizuka Y. 1991. Synergistic action of diacylglycerol and unsaturated fatty acid for protein kinase C activation its possible implications. Proc Natl Acad Sci 88:5149-5153.
54. Skeer MM, Pruitt N, Sattelle DB. 1992. Pharmacologically distinct calcium channels are present in insect nervous system and skeletal muscle. Insect Biochem Mol Biol 22:539-545.
55. Smith WL. 1989. The eicosanoids and their biochemical mechanisms of action. Biochem J 259:315-324.
56. Sokal RR, Rohlf FJ. 1969. Biometry. New York: Freeman Press 523 p.
57. Stanley DW. 2000. Eicosanoids in invertebrate signal transduction systems. Princeton, NJ: Princeton University Press. pp 272.
58. Strand MR, Hayakawa Y, Clark KD. 2000. Plasmatocyte spreading peptide (PSP1) and growth blocking peptide (GBP) are multifunctional homologs. J Insect Physiol 46:817-824.
59. Taniai K, Furukawa S, Shon T, Yamakawa M. 1996. Elicitors triggering the simultaneous gene expression of antibacterial proteins of the silkworm, Bombyx mori. Biochem Biophys Res Commun 226:783-790.
60. Theopold U, Schmidt O. 1997. Helix pomatia lectin and annexin V, two molecular probes for insect microparticles: possible involvement in hemolymph coagulation. J Insect Physiol 43:667-674.
61. Tojo SS, Naganuma F, Arakawa K, Yokoo S. 2000. Involvement of both granular cells and plasmatocytes in phagocytic reactions in the greater wax moth, Galleria mellonella. J Insect Physiol 46:1129-1135.
62. Wago H. 1980. Humoral factors promoting the adhesive properties of the granular cells and plasmatocytes of the silkworm Bombyx mori and their possible role in the initial cellular reactions to being foreign. Cell Immunol 54: 155-169.
63. Wang Y, Jiang H, Kanost MR. 1999. Biological activity of Manduca sexta paralytic and plasmatocyte spreading peptide and primary structure of its hemolymph precursor. Insect Biochem Mol Biol 29:1075-1086.
64. Wiesner A, Losen S, Kopáček P, Weise C, Götz P. 1997. Isolated apolipophorin III from Galleria mellonella stimulates the immune reactions of this insect. J Insect Physiol 43: 383-391.
65. Willott E, Hallberg CA, Tran HQ. 2002. Influence of calcium on Manduca sexta plasmatocyte spreading and network formation. Arch Insect Biochem Physiol 49:187-202.
66. Wittwer D, Weisner A. 1996. Peptide RGDS inhibits the fibronectin-enhanced phagocytosis of yeast cells by Galleria mellonella hemocytes in vitro. J Invertebr Pathol 68:199-200.
67. Yadwad VB, Downer RGH. 1993. Phosphatidylinositol kinase and phosphatidylinositol-4-phosphate kinase activities in Md 66 insect cell line. Arch Int Physiol Biochim Biophys 101:203-205.
68. Yokoo S, Gotz P, Tojo S. 1995. Phagocytic activities of haemocytes separated by two simple methods from larvae of two lepidopteran species, Agrotis segetum and Galleria mellonella. Appl Entomol Zool 30:343-350.
69. Zakarian RJ, Dunphy GB, Albert PJ, Rau ME. 2002. Apolipophorin-III affects the activity of the haemocytes of Galleria mellonella. J Insect Physiol 48:717-725.