Studies on the role of protein kinase A in humoral immune response of Galleria mellonella larvae

Journal of Insect Physiology

Volumn 52, Issue 7, 2006, Pages 744-753

  Cytryńska, Małgorzata ^a   Zdybicka Barabas, Agnieszka ^a   Jakubowicz, Teresa ^a  

^a MARIA CURIE SK ODOWSKA UNIVERSITY   (Poland)

Author keywords

Antibacterial activity; Galleria mellonella; H89; Lysozyme; Protein kinase A; Rp 8 Br cAMPS

Indexed keywords

ANTIINFECTIVE AGENT; CYCLIC AMP DEPENDENT PROTEIN KINASE; LYSOZYME;

ANTIBODY; ENZYME ACTIVITY; FAT RESERVE; IMMUNE RESPONSE; INSECT; LARVA; MEMBRANE; METHODOLOGY; PROTEIN;

ANIMAL; ARTICLE; DRUG ANTAGONISM; ENZYMOLOGY; FAT BODY; HEMOLYMPH; IMMUNOLOGY; LARVA; METABOLISM; MOTH;

ANIMALS; ANTI-BACTERIAL AGENTS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; FAT BODY; HEMOLYMPH; LARVA; MOTHS; MURAMIDASE;

GALLERIA MELLONELLA;

EID: 33745228788     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2006.04.002     Document Type: Article

References (62)

1. Beenakkers A.M.T., Van der Horst D.J., and Van Marewijk W.J.A. Regulation of release and metabolic function of the adipokinetic hormone in insects. In: Gaillard P.J., and Boer H.H. (Eds). Comparative Endocrinology (1978), Elsevier/North-Holland Biomedical Press, Amsterdam 445-448
2. Berwick D.C., and Tavaré J.M. Identifying protein kinase substrates: hunting for the organ-grinder's monkeys. Trends in Biochemical Sciences 29 (2004) 227-232
3. Boman H.G., Nilsson-Faye I., Paul K., and Rasmuson Jr. T. Insect immunity. 1. Characteristics of an inducible cell-free antibacterial reaction in hemolymph of Samia cynthia pupae. Infection and Immunity 10 (1974) 136-145
4. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72 (1976) 248-254
5. 312) enhances Dorsal nuclear import through facilitating nuclear localization sequence/importin interaction. The Journal of Biological Chemistry 273 (1998) 22745-22752
6. 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
7. Cao A., Martinez J.I.R., and Barcia R. Implication of PKA and PKC in the activation of the haemocytes of Mytilus galloprovincialis Lmk. by LPS and IL-2. Molecular Immunology 41 (2004) 45-52
8. Chalk R., and Suliaman W.Y. Antimicrobial peptides from small insects: methods for insect culture and for the detection, visualization, isolation and sequencing of active hemolymph peptides. In: Wiesner A., Dunphy G.B., Marmaras V.J., Morishima I., Sugumaran M., and Yamakawa M. (Eds). Techniques in Insect Immunology (1998), SOS Publications, USA 109-124
9. Charalambidis N.D., Zervas C.G., Lambropoulou M., Katsoris P.G., and Marmaras V.J. Lipopolysaccharide-stimulated exocytosis of nonself recognition protein from insect hemocytes depends on protein tyrosine phosphorylation. European Journal of Cell Biology 67 (1995) 32-41
10. Chen C.C., Chiu K.T., Sun Y.T., and Chen W.C. Role of the cyclic AMP-protein kinase A pathway in lipopolysaccharide-induced nitric oxide synthase expression in RAW 264.7 macrophages. Involvement of cyclooxygenase-2. The Journal of Biological Chemistry 274 (1999) 31559-31564
11. Chijiwa T., Mishima A., Hagiwara M., Sano M., Hayashi K., Inoue T., Naito K., Toshioka T., and Hidaka H. Inhibition of forskolin-induced neurite outgrowth and protein phosphorylation by a newly synthesized selective inhibitor of cyclic AMP-dependent protein kinase, N-[2-(p-bromocinnamylamino)ethyl]-5-isoquinolinesulfonamide (H89), of PC12D pheochromocytoma cells. The Journal of Biological Chemistry 265 (1990) 5267-5272
12. Christ B. Partial purification of a cyclic nucleotide-dependent protein kinase from antennal glands of the crayfish, Orconectes limosus. International Journal of Biochemistry 17 (1985) 631-635
13. Cytryńska M., Wojda I., Frajnt M., and Jakubowicz T. PKA from Saccharomyces cerevisiae can be activated by cyclic AMP and cyclic GMP. Canadian Journal of Microbiology 45 (1999) 31-37
14. Cytryńska M., Zdybicka-Barabas A., Jabłoński P., and Jakubowicz T. Detection of antibacterial polypeptide activity in situ after sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Analytical Biochemistry 299 (2001) 274-276
15. Dong C., Davis R.J., and Flavell R.A. MAP kinases in the immune response. Annual Review in Immunology 20 (2002) 55-72
16. Engström Y. Insect immune gene regulation. In: Brey P.T., and Hultmark D. (Eds). Molecular Mechanisms of Immune Responses in Insects (1998), Chapman & Hall, London 209-244
17. Frajnt M., Cytryńska M., and Jakubowicz T. The effect of cAMP and cGMP on the activity and substrate specificity of protein kinase A from methylotrophic yeast Pichia pastoris. Acta Biochimica Polonica 50 (2003) 1111-1118
18. Fujihara M., Muroi M., Muroi Y., Ito N., and Suzuki T. Mechanism of lipopolysaccharide-triggered junB activation in a mouse macrophage-like cell line (J774). The Journal of Biological Chemistry 268 (1993) 14898-14905
19. Ghosh S., and Karin M. Missing pieces in the NF-κB puzzle. Cell 109 (2002) S81-S96
20. Gjertsen B.T., Mellgren G., Otten A., Maronde E., Genieser H.-G., Jastorff B., Vintermyr O.K., McKnight G.S., and Døskeland S.O. Novel (Rp)-cAMPS analogs as tools for inhibition of cAMP-kinase in cell culture. The Journal of Biological Chemistry 270 (1995) 20599-20607
21. Grønborg M., Kristiansen T.Z., Stensballe A., Andersen J.S., Ohara O., Mann M., Jensen O.N., and Pandey A. A mass spectrometry-based proteomic approach for identification of serine/threonine-phosphorylated proteins by enrichment with phospho-specific antibodies. Molecular and Cellular Proteomics 1 (2002) 517-527
22. Han Z.S., Enslen H., Hu X., Meng X., Wu I.H., Barrett T., Davis R.J., and Ip Y.T. A conserved p38-mitogen activated protein kinase pathway regulates Drosophila immunity gene expression. Molecular and Cellular Biology 18 (1998) 3527-3539
23. Hetru C., Troxler L., and Hoffmann J.A. Drosophila melanogaster antimicrobial defense. The Journal of Infectious Diseases 187 Suppl. 2 (2003) S327-S334
24. Hoffmann D., Hultmark D., and Boman H.G. Insect immunity: Galleria mellonella and other Lepidoptera have cecropia-P9-like factors active against gram negative bacteria. Insect Biochemistry 11 (1981) 537-548
25. Hofmann F., Dostmann W., Keilbach A., Landgraf W., and Ruth P. Structure and physiological role of cGMP-dependent protein kinase. Biochimica et Biophysica Acta 1135 (1992) 51-60
26. Hou S., Guan H., and Ricciardi R.P. Phosphorylation of serine 337 of NF-κB p50 is critical for DNA binding. The Journal of Biological Chemistry 278 (2003) 45994-45998
27. Hultmark D. Insect lysozymes. In: Jollés P. (Ed). Lysozymes: Model Enzymes in Biochemistry and Biology (1996), Birkhäuser Verlag, Basel/Switzerland 87-102
28. Hultmark D. Drosophila immunity: paths and patterns. Current Opinion in Immunology 15 (2003) 12-19
29. Hultmark D., Engström A., Bennich H., Kapur R., and Boman H.G. Insect immunity: isolation and structure of cecropin D and four minor antibacterial components from Cecropia pupae. European Journal of Biochemistry 127 (1982) 207-217
30. Imler J.L., and Hoffmann J.A. Signaling mechanisms in the antimicrobial host defense of Drosophila. Current Opinion in Microbiology 3 (2000) 16-22
31. Iwanaga S., and Lee B.L. Recent advances in the innate immunity of invertebrate animals. Journal of Biochemistry and Molecular Biology 38 (2005) 128-150
32. Johansson M.W., and Söderhäll K. Intracellular signaling in arthropod blood cells: involvement of protein kinase C and protein tyrosine phosphorylation in the response to the 76-kDa protein or the β-1,3-glucan-binding protein in crayfish. Developmental and Comparative Immunology 17 (1993) 495-500
33. Karin M. How NF-κB is activated: the role of the IκB kinase (IKK) complex. Oncogene 18 (1999) 6867-6874
34. Khush R.S., Leulier F., and Lemaitre B. Drosophila immunity: two paths to NF-κB. Trends in Immunology 22 (2001) 260-264
35. Lacoste A., Malham S.K., Cueff A., and Poulet S.A. Noradrenaline modulates oyster hemocyte phagocytosis via a β-adrenergic receptor-cAMP signaling pathway. General and Comparative Endocrinology 122 (2001) 252-259
36. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 277 (1970) 680-685
37. Lanz-Mendoza H., Bettencourt R., Fabbri M., and Faye I. Regulation of the insect immune response: the effect of hemolin on cellular immune mechanisms. Cellular Immunology 169 (1996) 47-54
38. Leclerc V., and Reichhart J.-M. The immune response of Drosophila melanogaster. Immunological Reviews 198 (2004) 59-71
39. Malagoli D., Conte A., and Ottaviani E. Protein kinases mediate nitric oxide-induced apoptosis in the insect cell line IPLB-LdFB. Cellular and Molecular Life Sciences 59 (2002) 894-901
40. Mane S.D., Darville R.G., Sauer J.R., and Essenberg R.C. Cyclic AMP-dependent protein kinase from the salivary glands of the tick, Amblyomma americanum. Insect Biochemistry 15 (1985) 777-787
41. Marin D., Dunphy G.B., and Mandato C.A. Cyclic AMP affects the haemocyte responses of larval Galleria mellonella to selected antigens. Journal of Insect Physiology 51 (2005) 575-586
42. Muroi M., and Suzuki T. Role of protein kinase A in LPS-induced activation of NF-kappaB proteins of a mouse macrophage-like cell line, J774. Cellular Signalling 5 (1993) 289-298
43. Norris J.L., and Manley J.L. Selective nuclear transport of the Drosophila morphogen dorsal can be established by a signaling pathway involving the transmembrane protein Toll and protein kinase A. Genes and Development 6 (1992) 1654-1667
44. Øgreid D., Ekanger R., Suva R.H., Miller J.P., Sturm P., Corbin J.D., and Døskeland S.O. Activation of protein kinase isozymes by cyclic nucleotide analogs used singly or in combination. Principles for optimizing the isozyme specificity of analog combinations. European Journal of Biochemistry 150 (1985) 219-227
45. 2+ in LPS-activated expression of the chicken lysozyme gene. Journal of Leukocyte Biology 69 (2001) 651-658
46. Schwede F., Maronde E., Genieser H.-G., and Jastorff B. Cyclic nucleotide analogs as biochemical tools and prospective drugs. Pharmacology and Therapeutics 87 (2000) 199-226
47. Shimabukuro M., Xu J., Sugiyama M., Taniai K., Kadono-Okuda K., Kato Y., Yamamoto M., Chowdhury S., Choi S.K., Choi H.K., Miyanoshita A., Debnath N.C., and Yamakawa M. Signal transduction for cecropin B gene expression in adherent hemocytes of the silkworm, Bombyx mori (Lepidoptera: Bombycidae). Applied Entomology and Zoology 31 (1996) 135-143
48. Silverman N., and Maniatis T. NF-κB signaling pathways in mammalian and insect innate immunity. Genes and Development 15 (2001) 2321-2342
49. Sluss H.K., Han Z., Barrett T., Davis R.J., and Ip Y.T. A JNK signal transduction pathway that mediates morphogenesis and an immune response in Drosophila. Genes and Development 10 (1996) 2745-2758
50. Takahashi S.Y., and Hanaoka K. Multiple protein kinases in the American cockroach Periplaneta americana. Insect Biochemistry 7 (1977) 133-139
51. Taniai K., Furukawa S., Shono T., and Yamakawa M. Elicitors triggering the simultaneous gene expression of antibacterial proteins of the silkworm, Bombyx mori. Biochemical and Biophysical Research Communications 226 (1996) 783-790
52. Torgersen K.M., Vang T., Abrahamsen H., Yaqub S., and Taskén K. Molecular mechanisms for protein kinase A-mediated modulation of immune function. Cellular Signalling 14 (2002) 1-9
53. Tsuzuki J., and Newburgh R.W. Cyclic nucleotide binding and protein kinase in the central nervous system of Galleria mellonella (L.). Biochimica et Biophysica Acta 354 (1974) 101-106
54. Vardanis A. Insect (cAMP-cGMP)-dependent protein kinase. Methods in Enzymology 99 (1983) 71-76
55. Vilcinskas A., and Matha V. Effect of the entomopathogenic fungus Beauveria bassiana on the humoral immune response of Galleria mellonella larvae (Lepidoptera: Pyralidae). European Journal of Entomology 94 (1997) 461-472
56. Weber I.T., Shabb J.B., and Corbin J.D. Predicted structures of the cGMP binding domains of the cGMP-dependent protein kinase: a key alanine/threonine difference in evolutionary divergence of cAMP and cGMP binding sites. Biochemistry 28 (1989) 6122-6127
57. Weinstein S.L., June C.H., and DeFranco A.L. Lipopolysaccharide-induced protein tyrosine phosphorylation in human macrophages is mediated by CD14. The Journal of Immunology 151 (1993) 3829-3838
58. 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
59. Yagura T.S., Kazimierczuk Z., Shugar D., and Miller J.P. Activation of cyclic AMP-dependent protein kinases I and II by cyclic 3′:5′-phosphates of 9-β-D-ribofuranosylpurine and 1-β-D-ribofuranosylbenzimidazole. Biochemical and Biophysical Research Communications 28 (1980) 737-743
60. Zakarian R.J., Dunphy G.B., Rau M.E., and Albert P.J. Kinases, intracellular calcium, and apolipophorin-III influence the adhesion of larval hemocytes of the lepidopterous insect, Galleria mellonella. Archives of Insect Biochemistry and Physiology 53 (2003) 158-171
61. Zervas C.G., Katsoris P.G., and Marmaras V.J. Analysis of tyrosine-phosphorylated proteins in hemocytes. In: Wiesner A., Dunphy G.B., Marmaras V.J., Morishima I., Sugumaran M., and Yamakawa M. (Eds). Techniques in Insect Immunology (1998), SOS Publications, USA 87-90
62. Zhong H., Voll R.E., and Ghosh S. Phosphorylation of NF-κB p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Molecular Cell 1 (1998) 661-671