Contributions of cellular and humoral immunity of Galleria mellonella larvae in defence against oral infection by bacillus thuringiensis

Journal of Invertebrate Pathology

Volumn 119, Issue , 2014, Pages 40-46

  Grizanova, E V ^a   Dubovskiy, I M ^a   Whitten, M M A ^b   Glupov, V V ^a  

^a INSTITUTE OF SYSTEMATICS AND ECOLOGY OF ANIMALS   (Russian Federation)

^b SWANSEA UNIVERSITY   (United Kingdom)

Author keywords

Bt; Encapsulation; Insects immunity; Phagocytosis; PO; Resistance

Indexed keywords

ANIMAL; BACILLUS THURINGIENSIS; BIOLOGICAL PEST CONTROL; CELLULAR IMMUNITY; HUMORAL IMMUNITY; IMMUNOLOGY; INSECTICIDE RESISTANCE; LARVA; MICROBIOLOGY; MOTH;

ANIMALS; BACILLUS THURINGIENSIS; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; INSECTICIDE RESISTANCE; LARVA; MOTHS; PEST CONTROL, BIOLOGICAL;

EID: 84901507282     PISSN: 00222011     EISSN: 10960805     Source Type: Journal    
DOI: 10.1016/j.jip.2014.04.003     Document Type: Article

References (55)

1. Abd El-Aziz N.M., Awad H.H. Changes in the haemocytes of Agrotis ipsilon larvae (Lepidoptera: Noctuidae) in relation to dimilin and Bacillus thuringiensis infections. Micron 2010, 41:203-209.
2. Altincicek B., Linder M., Linder D., Preissner K.T., Vilcinskas A. Microbial metalloproteinases mediate sensing of invading pathogens and activate innate immune responses in the lepidopteran model host Galleria mellonella. Infect. Immun. 2007, 75:175-183.
3. Altincicek B., Stotzel S., Wygrecka M., Preissner K.T., Vilcinskas A. Host-derived extracellular nucleic acids enhance innate immune responses, induce coagulation, and prolong survival upon infection in insects. J. Immunol. 2008, 181:2705-2712.
4. Aptosoglou S.G., Sivropoulou A., Koliais S.I. Distribution and characterization of Bacillus thuringiensis in the environment of the olive in Greece. Microbiologica 1997, 20:69-76.
5. Ashida M., Soderhall K. The prophenoloxidase activating system in crayfish. Comp. Biochem. Phys. B 1984, 77:21-26.
6. Ayres J.S., Schneider D.S. A signaling protease required for melanization in Drosophila affects resistance and tolerance of infections. PLoS Biol. 2008, 6:2764-2773.
7. Basset A., Khush R.S., Braun A., Gardan L., Boccard F., Hoffmann J.A., Lemaitre B. The phytopathogenic bacteria Erwinia carotovora infects Drosophila and activates an immune response. Proc. Natl. Acad. Sci. USA 2000, 97:3376-3381.
8. Baton L.A., Ranford-Cartwright L.C. Morphological evidence for proliferative regeneration of the Anopheles stephensi midgut epithelium following Plasmodium falciparum ookinete invasion. J. Invertebr. Pathol. 2007, 96:244-254.
9. Bravo A., Gill S.S., Soberon M. Bacillus thuringiensis: mechanisms and use. Comprehensive Molecular Insect Science 2005, 175-205. Elsevier, Amsterdam. L.I. Gilbert, I. Kostas, S.S. Gill (Eds.).
10. Broderick N.A., Raffa K.F., Handelsman J. Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proc. Natl. Acad. Sci. USA 2006, 103:15196-15199.
11. Broderick N.A., Welchman D.P., Lemaitre B. Recognition and response to microbial infection in Drosophila. Insect Infection and Immunity: Evolution, Ecology, and Mechanisms 2009, 13-34. Oxford University Press. J. Rolff, S.E. Reynolds (Eds.).
12. Broderick N.A., Raffa K.F., Handelsman J. Chemical modulators of the innate immune response alter gypsy moth larval susceptibility to Bacillus thuringiensis. BMC Microbiol. 2010, 10.
13. Buchon N., Broderick N.A., Kuraishi T., Lemaitre B. Drosophila EGFR pathway coordinates stem cell proliferation and gut remodeling following infection. BMC Biol. 2010, 8.
14. Castagnola A., Eda S., Jurat-Fuentes J.L. Monitoring stem cell proliferation and differentiation in primary midgut cell cultures from Heliothis virescens larvae using flow cytometry. Differentiation 2011, 81:192-198.
15. Cerenius L., Lee B.L., Soderhall K. The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol. 2008, 29:263-271.
16. Chak K.F., Chao D.C., Tseng M.Y., Kao S.S., Tuan S.J., Feng T.Y. Determination and distribution of Cry-type genes of Bacillus thuringiensis isolates from Taiwan. Appl. Environ. Microbiol. 1994, 60:2415-2420.
17. Chilcott C.N., Wigley P.J. Isolation and toxicity of Bacillus thuringiensis from soil and insect habitats in New Zealand. J. Invertebr. Pathol. 1993, 61:244-247.
18. Darboux I., Pauchet Y., Castella C., Silva-Filha M.H., Nielsen-LeRoux C., Charles J.F., Pauron D. Loss of the membrane anchor of the target receptor is a mechanism of bioinsecticide resistance. Proc. Natl. Acad. Sci. USA 2002, 99:5830-5835.
19. de Maagd R.A., Bravo A., Berry C., Crickmore N., Schnepf H.E. Structure, diversity, and evolution of protein toxins from spore-forming entomopathogenic bacteria. Annu. Rev. Genet. 2003, 37:409-433.
20. Dubovskiy I.M., Krukova N.A., Glupov V.V. Phagocytic activity and encapsulation rate of Galleria mellonella larval haemocytes during bacterial infection by Bacillus thuringiensis. J. Invertebr. Pathol. 2008, 98:360-362.
21. Dubovskiy I.M., Whitten M.A., Kryukov V.Y., Yaroslavtseva O.N., Grizanova E.V., Greig C., Mukherjee K., Vilcinskas A., Mitkovets P.V., Glupov V.V., Butt T.M. More than a colour change: insect melanism, disease resistance and fecundity. Proc. Roy. Soc. B - Biol. Sci. 2013, 280.
22. Dushay M.S. Insect hemolymph clotting. Cell. Mol. Life Sci. 2009, 66:2643-2650.
23. Eleftherianos I., Revenis C. Role and importance of phenoloxidase in insect hemostasis. J. Innate. Immun. 2011, 3:28-33.
24. Ericsson J.D., Janmaat A.F., Lowenberger C., Myers J.H. Is decreased generalized immunity a cost of Bt resistance in cabbage loopers Trichoplusia ni?. J. Invertebr. Pathol. 2009, 100:61-67.
25. Gahan L.J., Gould F., Heckel D.G. Identification of a gene associated with Bt resistance in Heliothis virescens. Science 2001, 293:857-860.
26. Garbutt J., Bonsall M.B., Wright D.J., Raymond B. Antagonistic competition moderates virulence in Bacillus thuringiensis. Ecol. Lett. 2011, 14:765-772.
27. Griffitts J.S., Aroian R.V. Many roads to resistance: how invertebrates adapt to Bt toxins. BioEssays 2005, 27:614-624.
28. Haine E.R., Rolff J., Siva-Jothy M.T. Functional consequences of blood clotting in insects. Dev. Comp. Immunol. 2007, 31:456-464.
29. Hernandez-Martinez P., Navarro-Cerrillo G., Caccia S., de Maagd R.A., Moar W.J., Ferre J., Escriche B., Herrero S. Constitutive activation of the midgut response to Bacillus thuringiensis in Bt-resistant Spodoptera exigua. PLoS ONE 2010, 5.
30. Higuchi M., Haginoya K., Yamazaki T., Miyamoto K., Katagiri T., Tomimoto K., Shitomi Y., Hayakawa T., Sato R., Hori H. Binding of Bacillus thuringiensis Cry1A toxins to brush border membrane vesicles of midgut from Cry1Ac susceptible and resistant Plutella xylostella. Comp. Biochem. Phys. B 2007, 147:716-724.
31. Kryukova N.A., Dubovskiy I.M., Chertkova E.A., Vorontsova Y.L., Slepneva I.A., Glupov V.V. The effect of Habrobracon hebetor venom on the activity of the prophenoloxidase system, the generation of reactive oxygen species and encapsulation in the haemolymph of Galleria mellonella larvae. J. Insect Physiol. 2011, 57:796-800.
32. Kwon S., Kim Y. Immunosuppressive action of pyriproxyfen, a juvenile hormone analog, enhances pathogenicity of Bacillus thuringiensis subsp kurstaki against diamondback moth, Plutella xylostella (Lepidoptera: Yponoineutidae). Biol. Control 2007, 42:72-76.
33. Li D., Scherfer C., Korayem A.M., Zhao Z., Schmidt O., Theopold U. Insect hemolymph clotting: evidence for interaction between the coagulation system and the prophenoloxidase activating cascade. Insect Biochem. Mol. Biol. 2002, 32:919-928.
34. Ma G., Sarjan M., Preston C., Asgari S., Schmidt O. Mechanisms of inducible resistance against Bacillus thuringiensis endotoxins in invertebrates. Insect Sci. 2005, 12:319-330.
35. Ma G., Rahman M.M., Grant W., Schmidt O., Asgari S. Insect tolerance to the crystal toxins Cry1Ac and Cry2Ab is mediated by the binding of monomeric toxin to lipophorin glycolipids causing oligomerization and sequestration reactions. Dev. Comp. Immunol. 2012, 37:184-192.
36. Manachini B., Arizza V., Parrinello D., Parrinello N. Hemocytes of Rhynchophorus ferrugineus (Olivier) (Coleoptera: Curculionidae) and their response to Saccharomyces cerevisiae and Bacillus thuringiensis. J. Invertebr. Pathol. 2011, 106:360-365.
37. Martinez-Ramirez A.C., Gould F., Ferre J. Histopathological effects and growth reduction in a susceptible and a resistant strain of Heliothis virescens (Lepidoptera: Noctuidae) caused by sublethal doses of pure Cry1A crystal proteins from Bacillus thuringiensis. Biocontrol Sci. Technol. 1999, 9:239-246.
38. Mohrig W., Messner B. Immunoreaktionen bei Insekten. I. Lysozym alsgrundlegender antibakterieller Faktor im humoralen Abwehrmechanismus der Insekten. Biol. Zbl. 1968, 87:439-470.
39. Nielsen-LeRoux C., Gaudriault S., Ramarao N., Lereclus D., Givaudan A. How the insect pathogen bacteria Bacillus thuringiensis and Xenorhabdus/Photorhabdus occupy their hosts. Curr. Opin. Microbiol. 2012, 15:220-231.
40. Oppert B., Kramer K.J., Johnson D.E., Macintosh S.C., Mcgaughey W.H. Altered protoxin activation by midgut enzymes from a Bacillus thuringiensis resistant strain of Plodia interpunctella. Biochem. Biophys. Res. Commun. 1994, 198:940-947.
41. Pigott C.R., Ellar D.J. Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol. Mol. Biol. Rev. 2007, 71:255-281.
42. Rahman M.M., Roberts H.L.S., Sarjan M., Asgari S., Schmidt O. Induction and transmission of Bacillus thuringiensis tolerance in the flour moth Ephestia kuehniella. Proc. Natl. Acad. Sci. USA 2004, 101:2696-2699.
43. Rantala M.J., Roff D.A. Analysis of the importance of genotypic variation, metabolic rate, morphology, sex and development time on immune function in the cricket, Gryllus firmus. J. Evol. Biol. 2006, 19:834-843.
44. Raymond B., Johnston P.R., Nielsen-LeRoux C., Lereclus D., Crickmore N. Bacillus thuringiensis: an impotent pathogen?. Trends Microbiol. 2010, 18:189-194.
45. Richards E.H., Dani M.P. A recombinant immunosuppressive protein from Pimpla hypochondriaca (rVPr1) increases the susceptibility of Lacanobia oleracea and Mamestra brassicae larvae to Bacillus thuringiensis. J. Invertebr. Pathol. 2010, 104:51-57.
46. Rohloff L.H., Wiesner A., Gotz P. A fluorescence assay demonstrating stimulation of phagocytosis by hemolymph molecules of Galleria mellonella. J. Insect Physiol. 1994, 40:1045-1049.
47. Rowley A.F., Ratcliffe N.A. A histological study of wound healing and hemocyte function in the wax-moth Galleria mellonella. J. Morphol. 1978, 157:181-199.
48. Shrestha S., Hong Y.P., Kim Y. Two chemical derivatives of bacterial metabolites suppress cellular immune responses and enhance pathogenicity of Bacillus thuringiensis against the diamondback moth, Plutella xylostella. J. Asia-Pac. Entomol. 2010, 13:55-60.
49. Siva-Jothy M.T., Thompson J.J.W. Short-term nutrient deprivation affects immune function. Physiol. Entomol. 2002, 27:206-212.
50. Smith R.A., Couche G.A. The phylloplane as a source of Bacillus thuringiensis variants. Appl. Environ. Microbiol. 1991, 57:311-315.
51. Vallet-Gely I., Lemaitre B., Boccard F. Bacterial strategies to overcome insect defences. Nat. Rev. Microbiol. 2008, 6:302-313.
52. van Frankenhuyzen K., Liu Y.H., Tonon A. Interactions between Bacillus thuringiensis subsp kurstaki HD-1 and midgut bacteria in larvae of gypsy moth and spruce budworm. J. Invertebr. Pathol. 2010, 103:124-131.
53. Wang Q., Liu Y., He H.J., Zhao X.F., Wang J.X. Immune responses of Helicoverpa armigera to different kinds of pathogens. BMC Immunol. 2010, 11.
54. Wojda I., Kowalski P., Jakubowicz T. JNK MAP kinase is involved in the humoral immune response of the greater wax moth larvae Galleria mellonella. Arch. Insect Biochem. 2004, 56:143-154.
55. Zhang X.B., Candas M., Griko N.B., Taussig R., Bulla L.A. A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis. Proc. Natl. Acad. Sci. USA 2006, 103:9897-9902.