Humoral immune response upon mild heat-shock conditions in Galleria mellonella larvae

Journal of Insect Physiology

Volumn 53, Issue 11, 2007, Pages 1134-1144

  Wojda, Iwona ^a   Jakubowicz, Teresa ^a  

^a MARIA CURIE SK ODOWSKA UNIVERSITY   (Poland)

Author keywords

Antimicrobial peptides; Galleria mellonella; Heat shock; Insect immunity

Indexed keywords

17 DEMETHOXY 17 (2 DIMETHYLAMINOETHYLAMINO)GELDANAMYCIN; 17-(DIMETHYLAMINOETHYLAMINO)-17-DEMETHOXYGELDANAMYCIN; BENZOQUINONE DERIVATIVE; HEAT SHOCK PROTEIN 90; INSECT PROTEIN; MACROCYCLIC LACTAM; MITOGEN ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; BACTERIUM; ENTOMOPATHOGENIC ORGANISM; FLY; GENE; HEAT SHOCK; IMMUNE RESPONSE; LARVA; SURVIVAL;

ANIMAL; ANTIBODY PRODUCTION; ARTICLE; DRUG EFFECT; FAT BODY; GENE; GENE EXPRESSION REGULATION; GENETICS; HEAT SHOCK RESPONSE; IMMUNOLOGY; LARVA; METABOLISM; MOTH;

ANIMALS; ANTIBODY FORMATION; BENZOQUINONES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FAT BODY; GENE EXPRESSION REGULATION; GENES, INSECT; HEAT-SHOCK RESPONSE; HSP90 HEAT-SHOCK PROTEINS; INSECT PROTEINS; LACTAMS, MACROCYCLIC; LARVA; MOTHS;

ANIMALIA; BACTERIA (MICROORGANISMS); GALLERIA MELLONELLA; HEXAPODA; PSEUDOMONAS AERUGINOSA;

EID: 35548949738     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2007.06.003     Document Type: Article

References (54)

1. Akira S., Uematsu S., and Takeuchi O. Pathogen recognition and innate immunity. Cell 124 (2006) 783-801
2. Bartha B.B., Ajtai K., Toft D.O., and Burghardt T.P. ATP sensitive tryptophans of Hsp90. Biophysical Chemistry 72 (1998) 313-321
3. Boman H.G., Nilsson-Faye I., Paul K., and Rasmuson Jr. T. Insect immunity .I. Characteristics of an inducible cell-free antibacterial reaction in hemolymph of Samia cythia pupae. Infection and Immunity 10 (1974) 136-145
4. Bradford M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilising the principle of protein-dye binding. Analytical Biochemistry 72 (1976) 248
5. Brooks C.L., and Dunphy G.B. Protein kinase A affects Galleria mellonella (Insecta: Lepidoptera) larval haemocyte non-self responses. Immunology and Cell Biology 83 (2005) 150-159
6. Buchner J. Hsp90 & Co.-a holding for folding. Trends in Biochemical Sciences 24 (1999) 136-141
7. Cherry S., and Silverman N. Host-pathogen interactions in Drosophila: new tricks from an old friend. Nature Immunology 7 (2006) 911-917
8. Cytrynska M., Zdybicka-Barabas A., Jablonski P., and Jakubowicz T. Detection of antibacterial polypeptide activity "in situ" after sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Analytical Biochemistry 299 (2001) 274-276
9. Cytrynska M., Zdybicka-Barabas A., and Jakubowicz T. Studies on the role of protein kinase A in humoral immune reponse of Galleria mellonella larvae. Journal of Insect Physiology 52 (2006) 744-753
10. Cytrynska M., Mak P., Zdybicka-Barabas A., Suder P., and Jakubowicz T. Purification and characterization of eight peptides from Galleria mellonella immune hemolymph. Peptides 28 (2007) 533-546
11. Davies A., Kalb S., Liang B., Aldrich C.J., Lemonnier F.A., Jiang H., Cotter R., and Soloski M.J. A peptide from heat-shock protein 60 is the dominant peptide bound to Qa-1 in the absence of the MHC class Ia leader sequence peptide Qdm. Journal of Immunology 170 (2003) 5027-5033
12. De Gregorio E., Spellman P.T., Tzou P., Rubin G.M., and Lemaitre B. The Toll and Imd pathways are the major regulators of the immune response in Drosophila. EMBO Journal 21 (2002) 2568-2579
13. De Nardo D., Masendycz P., Ho S., Cross M., Fleetwood A.J., Reynolds E.C., Hamilton J.A., and Scholz G.M. A central role for the Hsp90 Cdc37 molecular chaperone module in Interleukin-1 receptor-associated-kinase-dependent signalling by Toll-like receptors. The Journal of Biological Chemistry 280 (2005) 9813-9822
14. Fearns C., Pan Q., Mathison J.C., and Chuang T.-S. Triad3A regulates ubiquitination and proteasomal degradation o RIP1 following disruption of Hsp90 binding. The Journal of Biological Chemistry 281 (2006) 34592-34600
15. Cdc31 acting with Hsp90 is required for Raf-1 function. Molecular and Cellular Biology 19 (1999) 1661-1672
16. Grenert J.P., Sullivan W.P., Fadden P., Haystead T.A.J., Clark J., Mimnaugh E., Krutzsch H., Ochel H.J., Schulte T.W., Sausville E., Neckers L.M., and Toft D.O. The amino-terminal domain of heat-shock protein 90 (Hsp90) that binds geldanamycin is an ATP/ADP switch domain that regulates Hsp90 conformation. Journal of Biological Chemistry 272 (1997) 23843-23850
17. Gupta R.S. Phylogenetic analysis of the 90 kDa heat shock family of protein sequences and an examination of the relationship among animals, plants, and fungi species. Molecular Biology and Evolution 12 (1995) 1063-1073
18. Halwani A.E., and Dunphy G.B. Apolipophorin-III in Galleria mellonella potentiates hemolymph lytic activity. Developmental and Comparative Immunology 23 (1999) 563-570
19. Hancock R.E.W., Brown K.L., and Mookherjee N. Host defence peptides from invertebrates-emerging antimicrobial strategies. Immunobiology 211 (2006) 315-322
20. Herberts C.A., van Gaans-van den Brink J., van der Heeft E., van Wijk M., Hoekman J., Jaye A., Poelen M.C., Boog C.J., Roholl P.J., Whittle H., de Jong A.P., and van Els C.A. Autoreactivity against induced or upregulated abundant self-peptides in HLA-A*0201 following measles virus infection. Human Immunology 64 (2003) 44-55
21. Hickman-Miller H.D., and Hildebrand W.H. The immune reponse under stress: the role of HSP-derived peptides. Trends in Immunology 25 (2004) 427-433
22. Hultmark D. Quantification of antimicrobial activity using the inhibition-zone assay. In: Wiesner A., Dunphy G.B., Marmaras V.J., Morishima I., Sugumaran M., and Yamakawa M. (Eds). Techniques in Insect Immunology (1998), SOS Publications, Fair Heaven
23. Janeway C., and Medshitov R. Innate immune recognition. Annual Review of Immunology 20 (2002) 197-216
24. Johnson B.D., Chadli A., Felts S.J., Bouhouche I., Catelli M.G., and Toft D.O. Hsp90 chaperone activity requires the full-length protein and interaction among its multiple domains. Journal of Biological Chemistry 275 (2000) 32499-32507
25. Kambris Z., Brun S., Jang I.H., Nam H.J., Romeo Y., Takahashi K., Lee W.J., Ueda R., and Lemaitre B. Drosophila immunity: a large scale in vivo RNAi screen identifies five serine proteases required for Toll activation. Current Biology 16 (2006) 808-813
26. Kaneko T., Golenbock D., and Silverman N. Peptidoglycan recognition by the Drosophila Imd pathway. Journal of Endotoxin Researh 11 (2005) 383-389
27. Kim C.H., Lee J.H., Kim I., Seo S.J., Son S.M., Lee K.Y., and Lee I.H. Purification and cDNA cloning of a cecropin-like peptide from the Great Wax Moth, Galleria mellonella. Molecular Cell 17 (2004) 262-266
28. Koga F., Xu W., Karpova T., McNally, Baron R., and Neckers L. Hsp90 inhibition transiently activates Src kinase and promotes Src-dependent Akt and ERK activation. Proceedings of the National Academy of Sciences 103 (2006) 11318-11322
29. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
30. Lee Y.S., Yun E.K., Jang W.S., Kim I., Lee J.H., Park S.Y., Ryu K.S., Seo S.J., Kim C.H., and Lee I.H. Purification, cDNA cloning and expression of an insect defensin from the great wax moth, Galleria mellonella. Insect Molecular Biology 13 (2004) 65-72
31. Leulier F., Parquet C., Pili-Floury S., Ryu J.-H., Caroff M., Lee W.-J., Mengin-Lecreulx D., and Lemaitre B. The Drosophila immune system detects both Gram-positive and Gram-negative bacteria through specific peptidoglycan recognition. Nature Immunology 4 (2003) 478-484
32. Lindguist S., and Craig E.A. The heat-shock proteins. Annual Review of Genetics 22 (1988) 631-677
33. Medzhitov R., and Janeway Jr. C.A. Decoding the patterns of self and nonself by the innate immune system. Science 296 (2002) 298-300
34. Michaëlsson J., Teixeira de Matos C., Achour A., Lanier L.L., Kärre K., and Söderström K. A signal peptide derived from Hsp60 binds HLA-E and interferes with CD94/NKG2A recognition. Journal of Experimental Medicine 196 (2002) 1403-1414
35. Murtagh J., Lu H., and Schwartz E.L. Taxotere-induced inhibition of human endothelial cell migration is a result of heat-shock protein 90 degradation. Cancer Research 66 (2006) 8192-8199
36. Panaretou B., Sinclair K., Prodromou C., Johal J., Pearl L., and Piper P.W. The Hsp90 of Candida albicans can confer Hsp90 functions in Saccharomyces cerevisiae: a potential model for the processes that generate immunogenic fragments of this molecular chaperone in C. albicans infections. Microbiology 145 (1999) 3455-3463
37. Park S.Y., Kim C.H., Jeong W.H., Lee J.H., Seo S.J., Han Y.S., and Le I.H. Effects of two hemolymph proteins on humoral defense reactions in the wax moth, Galleria mellonella. Developmental and Comparative Immunology 29 (2005) 43-51
38. Peng X., Guo X., Borkan S.C., Bharti A., Kuramochi Y., Calderwood S., and Sawyer D.B. Heat-shock protein 90 stabilisation of erb2 expression is disrupted by ATP depletion in myocytes. Journal of Biological Chemistry 280 (2005) 13148-13152
39. Pratt W.B. The role of heat-shock proteins in regulation the function, folding, and traffiking of the glucorticoid receptor. Journal of Biological Chemistry 268 (1993) 21455-21458
40. Pratt W.B., and Toft D.O. Regulation of signalling protein function and trafficking by the Hsp90/Hsp70-based chaperone machinery. Experimental Biology and Medicine 22 (2003) 111-133
41. Prodromou C., Roe S.M., O'Brien R., Ladbury J.E., Piper P.W., and Pearl L.H. Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 90 (1997) 65-75
42. Royet J. Infectious non-self recognition in invertebrates: lessons from Drosophila and other insect models. Molecular Immunology 41 (2004) 1063-1075
43. Schagger H., and von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Analytical Biochemistry 166 (1987) 368-379
44. Scheibel T., Neuhofen S., Weikl T., Mayr C., Reinstein J., Vogel P.D., and Buchner J. ATP-binding properties of human Hsp90. Journal of Biological Chemistry 272 (1997) 18608-18613
45. Schmolz E., and Schulz O. Colorimetric investigations on thermoregulation and growth of wax moth larvae Galleria mellonella. Thermochimica Acta 251 (1995) 241-245
46. Schuhmann B., Seitz V., Vilcinskas A., and Podsiadlowski L. Cloning and expression of gallerimycin, an antifungal peptide expressed in immune response of greater wax moth larvae, Galleria melonella. Archives of Insect Biochemistry and Physiology 53 (2003) 125-133
47. Seitz V., Clermont A., Wedde M., Hummel M., Vilcinskas A., Schlatterer K., and Podsiadlowski L. Identification of immunorelevant genes from greater wax moth (Galleria mellonella) by substractive hybridization approach. Developmental and Comparative Immunology 27 (2003) 207-215
48. Stenbak C., Ryu J., Leulier F., Pili-Floury S., Parquet C., Hervé M., Boneca I., Lee W., Lemaitre B., and Mengin-Lecreulx D. Peptidoglycan molecular requirements allowing detection by the Drosophila Imd pathway. Journal of Immunology 173 (2004) 7339-7348
49. Wallin R.P.A., Lundqvist A., More S.H., von-Bonin A., Kiessling R., and Ljunggren H.-G. Heat-shock proteins as activators of the innate immune system. Trends in Immunology 23 (2002) 130-135
50. Wang L., and Ligoxygakis P. Pathogen recognition and signalling in the Drosophila innate immune reponse. Immunobiology 211 (2006) 251-261
51. Wojda I., Kowalski P., and Jakubowicz T. JNK MAP kinase is involved in the humoral immune response of the greater wax moth larvae Galleria mellonella. Archives of Insect Biochemistry and Physiology 56 (2004) 143-154
52. Young J.C., Agashe V.R., Siegers K., and Hartl F.U. Pathways of chaperone-mediated protein folding in the cytosol. Nature Reviews in Molecular and Biology 5 (2004) 781-791
53. Zakarian R.J., Dunphy G.B., and Quiot J.M. Apolipophorin-III affects the activity of the haemocytes of Galleria mellonella larvae. Journal of Insect Physiology 48 (2002) 715-723
54. Zugel U., Schoel B., Yamamoto S., Hengel H., Morein B., and Kaufmann S.H. Crossrecognition by CD8T cell receptor alpha beta cytotoxic T lymphocytes of peptides in the self and the mycobacterial Hsp60 which share intermediate sequence homology. European Journal of Immunology 25 (1995) 451-458