The effect of cold shock on the immune response of the greater wax moth Galleria mellonella after infection with entomopathogenic bacteria Bacillus thuringiensis

Iwona Wojda, Paulina Taszłow, Teresa Jakubowicz

Abstract


Insect immune system consists of only innate mechanisms relied on cellular and humoral branches. Many defence proteins and peptides exist or appear in response to infection in insect’s hemolymph. The interaction between the infected host and the entomopathogen occurs in the conditions of external environment. In this work the greater wax moth larvae of Galleria mellonella were subjected to a temperature of 120C for a short period of time, directly before infection with entomopathogenic bacteria Bacillus thuringiensis. It appeared that the induction of the immune response was higher in cold-shocked animals than in larvae permanently reared at the optimal temperature of 28 0C. This enhanced immune response was manifested as higher antibacterial and lysozyme-type activity detected in full hemolymph, and as a higher level of peptides of molecular weight below 10 kDa having antibacterial activity. Moreover, other changes in the contents of proteins in the hemolymph were observed. These changes concerned inter alia apolipophorin III, the multifunctional protein of immune significance. Its level was higher in the hemolymph of animals pre-exposed to cold shock than in nonshocked, infected ones. Altogether our results indicate that the interdependence mechanisms occur between cold shock and the immune response.

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References


Agaisse H., Gominet M., Økstad O. A., Kolstø A. B., and Lereclus D. 1999. PlcR is a pleiotropic regulator of extracellular virulence factor gene expression in Bacillus thuringiensis. Mol. Microbiol. 32: 1043–1053.

Bravo A., Likitvivatanavong S., Gill S.S., Soberón M. 2011. Bacillus thuringiensis: A story of a successful bioinsecticide. Insect. Biochem. Mol. Biol. 41: 423–431.

Brown S.E., Howard A., Kasprzak A.B., Gordon K.B., East P.D. 2009. A peptidomics study reveals the impressive antimicrobial peptide arsenal of the wax moth Galleria mellonella. Insect Bioch. Mol. Biol. 39: 792–800.

Cymborowski B. 2000. Temperature-dependent regulatory mechanism of larval development of the wax moth (Galleria mellonella). Acta Biochim. Polon. 47: 215–221.

Cytrynska M., Mak P., Zdybicka-Barabas A., Suder P., Jakubowicz, T. 2007. Purification and characterization of eight peptides from Galleria mellonella immune hemolymph. Peptides 28: 533–546.

During K., Porsch P., Mahn A., Brinkmann O., Gieffers, W. 1999. The non-enzymatic microbicidal activity of lysozymes. FEBS Letters 449: 93–100.

Entwistle P.F., Cory J.S., Bailey M.J., Higgs S. (eds) 1993. Bacillus thuringiensis, An Environmental Biopesticide: Theory and Practice. Wiley & Sons.

Fallon J., Kelly J., Kavanagh K. 2012. Galleria mellonella as a model for fungal pathogenicity testing. Meth. Mol. Biol. 845: 469–485.

Halwani A.E., Dunphy G.B. 1999. Apolipophorin- III in Galleria mellonella potentiates hemolymph lytic activity. Dev. Comp. Immunol. 23: 563–570.

Harding C.R., Schroeder G.N., Reynolds S., Kosta A., Collins J.W., Mousnier A., Frankel G. 2012. Legionella pneumophila pathogenesis in the Galleria mellonella infection model. Infect. Immun. 80: 2780–2790.

Hemani Y., Soller M. 2012. Mechanisms of Drosophila Dscam mutually exclusive splicing regulation. Biochem. Soc. Trans. 40: 804–809.

Hetru C., Hoffmann J.A. 2009. NF-kappa B in the immune response of Drosophila. Cold Spring Harb Perspect Biol. 1: a000232.

Hultmark D. 1996. Insect lysozymes. EXS. 75: 87–102.

Hultmark D. 1998. Quantification of antimicrobial activity using the inhibition- zone assay. In: Wiesner A., Dunphy G.B., Marmaras V.J., Morishima I., Sugumaran M., Yamakawa M., editors. Techniques in Insect Immunology. Fair Heaven: SOS Publications.

Imler J.L. 2014. Overview of Drosophila immunity: a historical perspective. Dev. Comp. Immunol. 42: 3–15.

Irving P., Troxler L., Hetru C. 2004. Is innate enough? The innate immune response in Drosophila. Comp. Trend. Biol. 327: 557–570.

Junqueira J.C. 2012. Galleria mellonella as a model host for human pathogens: recent studies and new perspectives. Virulence 3: 474–476.

Kłudkiewicz B., Godlewski J., Grzelak K., Cymborowski B., Lassota Z. 1996. Influence of low temperature on the synthesis of some Galleria mellonella proteins. Acta Biochim. Polon. 43: 639–644.

Laemmli U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685.

Lereclus D., Arantes O., Chaufaux J., Lecadet M. M. 1989. Transformation and expression of a cloned delta-endotoxin gene in Bacillus thuringiensis. FEMS Microbiol. Lett. 60: 211–218.

Mak P., Zdybicka-Barabas A., Cytryńska M. 2010. A different repertoire of Galleria mellonella antimicrobial peptides in larvae challenged with bacteria and fungi. Dev. Comp. Immunol. 34 1129–1136.

Marmaras V.J., Lampropoulou M. 2009. Regulators and signalling in insect haemocyte immunity. Cell Signal 21: 186–195.

Mattson M.P., Calabrese E.J. (eds) 2010. Hormesis: a revolution in biology, toxicology and medicine. Springer, Dordrecht.

Mesa-Arango A.C., Forastiero A., Bernal-Martínez L., Cuenca-Estrella M., Mellado E., Zaragoza O. 2012. The non-mammalian host Galleria mellonella can be used to study the virulence of the fungal pathogen Candida tropicalis and the efficiency of antifungal drugs during infection by this pathogenic yeast. Med. Mycol. 51: 461–472.

Mikołajczyk P., Cymborowski B. 1993. Lower temperature influences developmental rhythms of the wax moth Galleria mellonella: Putative role of ecdysteroids. Comp. Biochem. Physiol. 105A: 57–66.

Mohrig W., Messner B. 1968. Immunoreaktionen bei Insekten. I. Lysozym als grundlegender antibakterieller Faktor im humoralen Abwehrmechanismus der Insekten. Biologische Zentralblatt 87: 439–470.

Park S.Y., Kim C.H., Jeong W.H., Lee J.H., Seo S.J., Han Y.S., Lee I.H., 2005. Effects of two hemolymph proteins on humoral defense reactions in the wax moth, Galleria mellonella. Dev. Comp. Immun. 29: 43–51.

Pham L.N., Dionne M.S., Shirasu-Hiza M., Schneider DS. 2007. A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog. 3: e26.

Ramarao N., Nielsen-Leroux C., Lereclus D. 2012. The insect Galleria mellonella as a powerful infection model to investigate bacterial pathogenesis. Journal of Visualized Experiments. doi: 10.3791/4392.

Schagger H, von Jagow G. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166: 368–379.

Schünemann R., Knaak N., Fiuza L.M. 2014. Mode of action and specificity of Bacillus thuringiensis toxins in the control of caterpillars and stink bugs in soybean culture. ISRN Microbiol. 2014:135–675.

Seitz V., Clermont A., Wedde M., Hummel M., Vilcinskas A., Schlatterer K., Podsiadlowski L. 2003. Identification of immunorelevant genes from greater wax moth (Galleria mellonella) by substractive hybridization approach. Dev. Comp. Immunol. 27: 207–215.

Sinclair B.J., Vernon P., Klok C.J., Chown S.L. 2003. Insects at low temperatures: an ecological perspective. Trends Ecol. Evol. 18: 257–262.

Tammariello S.P., Rinehart J.P. Denlinger D.L. 1999. Desiccation elicits heat shock protein transcription in the Xesh Xy Sarcophaga crassipalpis, but does not enhance tolerance to high or low temperatures. J. Insect Physiol. 45: 933–938.

Taszłow P., Wojda I. 2014. Changes in the hemolymph protein profiles in Galleria mellonella infected with Bacillus thuringiensis involve apolipophorin III. The effect of heat-shock. Arch. Insect Biochem. Physiol. – in press.

Thomaz L., Garcia-Rodas R., Guimaraes A.J., Taborka C.P., Zaragoa,O., Nosanchuk J.D. 2013. Galleria mellonella as a model host to study Paracoccidioides lutzii and Histoplasma capsulatum Virulence 4: 139–146.

Ulvila J., Vanha-Aho L.M., Rämet M. 2011. APMIS. 119: 651-662.

Vachon V., Laprade R., Schwartz J.L. 2012. Current models of the mode of action of Bacillus thuringiensis insecticidal crystal proteins: a critical review. J. Invert. Pathol. 111: 1–12.

Vilcinskas A., Matha V. 1997. Antimycotic activity of lysozyme and its contribution to antifungal humoral defence reactions in Galleria mellonella. Animal Biol. 6: 19–29.

Vogel H., Altincicek B., Glöckner G., Vilcinskas A. 2011. A comprehensive transcriptome and immune-gene repertoire of the lepidopteran model host Galleria mellonella. BMC Genomics. 12: 308.

Wojda I., Kowalski P., Jakubowicz T. 2004. JNK MAP kinase is involved in the humoral immune response of the greater wax moth larvae Galleria mellonella. Arch. Insect Biochem. Physiol. 56: 143–154.

Wojda I., Jakubowicz T. 2007. Humoral immune response upon mild heat-shock conditions in Galleria mellonella larvae. J. Insect Physiol. 53: 1134–1144.

Wojda I., Kowalski P., Jakubowicz T. 2009. Humoral immune response of Galleria mellonella larvae after infection by Beauveria bassiana under optimal and heat-shock conditions. J. Insect Physiol. 55: 525–531.

Wojda I., Taszłow P. 2013. Heat shock affects host-pathogen interaction in Galleria mellonella infected with Bacillus thuringiensis. J. Insect Physiol. 59: 894–905.

Zdybicka-Barabas A., Cytryńska M. 2011. Involvement of apolipophorin III in antibacterial defense of Galleria mellonella larvae. Comp. Biochem. Physiol. B 158: 90–98.

Zdybicka-Barabas A., Cytryńska M. 2013. Apolipophorins and insect immune response. ISJ 10: 58–68.




DOI: http://dx.doi.org/10.17951/c.2014.69.2.7
Date of publication: 2015-05-23 17:52:02
Date of submission: 2015-05-09 17:10:47


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