The potential of the Galleria mellonella innate immune system is maximized by the co-presentation of diverse antimicrobial peptides

References

Al Souhail, Q., Hiromasa, Y., Rahnamaeian, M., Giraldo, M.C., Takahashi, D., Valent, B., Vilcinskas, A., and Kanost, M.R. (2016). Characterization and regulation of expression of an antifungal peptide from hemolymph of an insect, Manduca sexta, Dev. Comp. Immunol. 61, 258–268.10.1016/j.dci.2016.03.006Search in Google Scholar

Barribeau, S.M., Sadd, B., du Plessis, L., and Schmid-Hempel, P. (2014). Gene expression differences underlying genotype-by-genotype specificity in a host-parasite system. Proc. Natl. Acad. Sci. USA 111, 3496–3501.10.1073/pnas.1318628111Search in Google Scholar

Biasini, M., Bienert, S., Waterhouse, A., Arnold, K., Studer, G., Schmidt, T., Kiefer, F., Cassarino, T.G., Bertoni, M., Bordoli, L., et al. (2014). Swiss-Model: modelling protein tertiary and quaternary structure using evolutionary information. Nuc. Acids Res. 42, 252–258.10.1093/nar/gku340Search in Google Scholar

Bolouri Moghaddam, M.R., Vilcinskas, A., and Rahnamaeian, M. (2015). Cooperative interaction of antimicrobial peptides with the interrelated immune pathways in plants. Mol. Plant Pathol. 17, 464–471.10.1111/mpp.12299Search in Google Scholar

Brogden, K.A. (2005). Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria. Nat. Rev. Microbiol. 3, 238–250.10.1038/nrmicro1098Search in Google Scholar

Brown, S.E., Howard, A., Kasprzak, A.B., Gordon, K.H., and East, P.D. (2009). A peptidomics study reveals the impressive antimicrobial peptide arsenal of the wax moth Galleria mellonella. Insect Biochem. Mol. Biol. 39, 792–800.10.1016/j.ibmb.2009.09.004Search in Google Scholar

Cai, Z., Xu, C.Q., Xu, Y.Q., Lu, W.Y., Chi, C.W., Shi, Y.Y., and Wu, J.H. (2004). Solution structure of BmBKTx1, a new BKCa1 channel blocker from the Chinese scorpion Buthus martensi Karsch. Biochemistry 43, 3764–3771.10.1021/bi035412+Search in Google Scholar

Choi, H. and Lee, D.G. (2012). Synergistic effect of antimicrobial peptide arenicin-1 in combination with antibiotics against pathogenic bacteria. Res. Microbiol. 163, 479–486.10.1016/j.resmic.2012.06.001Search in Google Scholar

Christensen, B., Fink, J., Merrifield, R.B., and Mauzerall, D. (1988). Channel-forming properties of cecropins and related model compounds incorporated into planar lipid-membranes. Proc. Natl. Acad. Sci. USA 85, 5072–5076.10.1073/pnas.85.14.5072Search in Google Scholar

Cociancich, S., Ghazi, A., Hetru, C., Hoffmann, J.A., and Letellier, L. (1993). Insect defensin, an inducible antibacterial peptide, forms voltage-dependent channels in Micrococcus luteus. J. Biol. Chem. 268, 19239–19245.10.1016/S0021-9258(19)36505-6Search in Google Scholar

DeLucca, A.J., Bland, J.M., Jacks, T.J., Grimm, C., Cleveland, T.E., and Walsh, T.J. (1997). Fungicidal activity of cecropin A. Antimicrob. Agents Chemother. 41, 481–483.10.1128/AAC.41.2.481Search in Google Scholar PubMed PubMed Central

Dobson, A.J., Purves, J., Kamysz, W., and Rolff, J. (2013). Comparing Selection on S. aureus between antimicrobial peptides and common antibiotics. PLoS One 8, e76521.10.1371/journal.pone.0076521Search in Google Scholar PubMed PubMed Central

Engstrom, P., Carlsson, A., Engstrom, A., Tao, Z.J., and Bennich, H. (1984). The antibacterial effect of attacins from the silk moth hyalophora-cecropia is directed against the outer-membrane of Escherichia coli. EMBO J. 3, 3347–3351.10.1002/j.1460-2075.1984.tb02302.xSearch in Google Scholar PubMed PubMed Central

Epand, R.M. and Epand, R.F. (2011). Bacterial membrane lipids in the action of antimicrobial agents. J. Pept. Sci. 17, 298–305.10.1002/psc.1319Search in Google Scholar PubMed

Epand, R.F., Pollard, J.E., Wright, J.O., Savage, P.B., and Epand, R.M. (2010). Depolarization, bacterial membrane composition, and the antimicrobial action of ceragenins. Antimicrob. Agents Chemother. 54, 3708–3713.10.1128/AAC.00380-10Search in Google Scholar PubMed PubMed Central

Fieck, A., Hurwitz, I., Kang, A.S., and Durvasula, R. (2010). Trypanosoma cruzi: synergistic cytotoxicity of multiple amphipathic anti-microbial peptides to T. cruzi and potential bacterial hosts. Exp. Parasitol. 125, 342–347.10.1016/j.exppara.2010.02.016Search in Google Scholar PubMed PubMed Central

Gifford, J.L., Hunter, H.N., and Vogel, H.J. (2005). Lactoferricin: a lactoferrin-derived peptide with antimicrobial, antiviral, antitumor and immunological properties. Cell. Mol. Life Sci. 62, 2588–2598.10.1007/s00018-005-5373-zSearch in Google Scholar PubMed

Haine, E.R., Moret, Y., Siva-Jothy, M.T., and Rolff, J. (2008). Antimicrobial defense and persistent infection in insects. Science 322, 1257–1259.10.1126/science.1165265Search in Google Scholar PubMed

Hara, S. and Yamakawa, M. (1995). Moricin, a novel type of antibacterial peptide isolated from the silkworm, Bombyx mori. J. Biol. Chem. 270, 29923–29927.10.1074/jbc.270.50.29923Search in Google Scholar PubMed

Jeu, L.A. and Fung, H.B. (2004). Daptomycin: a cyclic lipopeptide antimicrobial agent. Clin. Ther. 26, 1728–1757.10.1016/j.clinthera.2004.11.014Search in Google Scholar PubMed PubMed Central

Kelley, L.A., Mezulis, S., Yates, C.M., Wass, M.N., and Sternberg, M.J.E. (2015). The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10, 845–858.10.1038/nprot.2015.053Search in Google Scholar PubMed PubMed Central

Langen, G., Imani, J., Altincicek, B., Kieseritzky, G., Kogel, K.H., and Vilcinskas, A. (2006). Transgenic expression of gallerimycin, a novel antifungal insect defensin from the greater wax moth Galleria mellonella, confers resistance to pathogenic fungi in tobacco. Biol. Chem. 387, 549–557.10.1515/BC.2006.071Search in Google Scholar PubMed

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. (2004). Purification, cDNA cloning and expression of an insect defensin from the great wax moth, Galleria mellonella. Insect Mol. Biol. 13, 65–72.10.1111/j.1365-2583.2004.00462.xSearch in Google Scholar PubMed

Levy, O., Ooi, C.E., Weiss, J., Lehrer, R.I., and Elsbach, P. (1994). Individual and synergistic effects of rabbit granulocyte proteins on Escherichia coli. J. Clin. Invest. 94, 672–682.10.1172/JCI117384Search in Google Scholar PubMed PubMed Central

Lockey, T.D. and Ourth, D.D. (1996). Formation of pores in Escherichia coli cell membranes by a cecropin isolated from hemolymph of Heliothis virescens larvae. Eur. J. Biochem. 236, 263–271.10.1111/j.1432-1033.1996.00263.xSearch in Google Scholar PubMed

Matsuzaki, K., Mitani, Y., Akada, K., Murase, O., Yoneyama, S., Zasloff, M., and Miyajima, K. (1998). Mechanism of synergism between antimicrobial peptides magainin 2 and PGLa. Biochemistry 37, 15144–15153.10.1021/bi9811617Search in Google Scholar PubMed

Moore, A.J., Beazley, W.D., Bibby, M.C., and Devine, D.A. (1996). Antimicrobial activity of cecropins. J. Antimicrob. Chemother. 37, 1077–1089.10.1093/jac/37.6.1077Search in Google Scholar PubMed

Nakajima, Y., Ishibashi, J., Yukuhiro, F., Asaoka, A., Taylor, D., and Yamakawa, M. (2003). Antibacterial activity and mechanism of action of tick defensin against Gram-positive bacteria. Biochim. Biophys. Acta Gen. Subj. 1624, 125–130.10.1016/j.bbagen.2003.10.004Search in Google Scholar PubMed

Poeppel, A.K., Vogel, H., Wiesner, J., and Vilcinskas, A. (2015). Antimicrobial peptides expressed in medicinal maggots of the blow fly Lucilia sericata show combinatorial activity against bacteria. Antimicrob. Agents Chemother. 59, 2508–2514.10.1128/AAC.05180-14Search in Google Scholar PubMed PubMed Central

Rahnamaeian, M. (2011). Antimicrobial peptides: modes of mechanism, modulation of defense responses. Plant Signal. Behav. 6, 1325–1332.10.4161/psb.6.9.16319Search in Google Scholar PubMed PubMed Central

Rahnamaeian, M., Cytrynska, M., Zdybicka-Barabas, A., Dobslaff, K., Wiesner, J., Twyman, R.M., Zuchner, T., Sadd, B.M., Regoes, R.R., Schmid-Hempel, P., et al. (2015). Insect antimicrobial peptides show potentiating functional interactions against Gram-negative bacteria. Proc. R. Soc. Lond. B. Biol. Sci. 282:20150293.10.1098/rspb.2015.0293Search in Google Scholar

Rahnamaeian, M., Cytrynska, M., Zdybicka-Barabas, A., and Vilcinskas, A. (2016). The functional interaction between abaecin and pore-forming peptides indicates a general mechanism of antibacterial potentiation. Peptides 78, 17–23.10.1016/j.peptides.2016.01.016Search in Google Scholar

Samakovlis, C., Kimbrell, D.A., Kylsten, P., Engstrom, A., and Hultmark, D. (1990). The immune-response in Drosophila–pattern of cecropin expression and biological activity. EMBO J. 9, 2969–2976.10.1002/j.1460-2075.1990.tb07489.xSearch in Google Scholar

Schuhmann, B., Seitz, V., Vilcinskas, A., and Podsiadlowski, L. (2003). Cloning and expression of gallerimycin, an antifungal peptide expressed in immune response of greater wax moth larvae, Galleria mellonella. Arch. Insect Biochem. Physiol. 53, 125–133.10.1002/arch.10091Search in Google Scholar

Seitz, V., Clermont, A., Wedde, M., Hummel, M., Vilcinskas, A., Schlatterer, K., and Podsiadlowski, L. (2003). Identification of immunorelevant genes from greater wax moth (Galleria mellonella) by a subtractive hybridization approach. Dev. Comp. Immunol. 27, 207–215.10.1016/S0145-305X(02)00097-6Search in Google Scholar

Thevissen, K., Warnecke, D.C., Francois, E.J.A., Leipelt, M., Heinz, E., Ott, C., Zahringer, U., Thomma, B., Ferkel, K.K.A., and Cammue, B.P.A. (2004). Defensins from insects and plants interact with fungal glucosylceramides. J. Biol. Chem. 279, 3900–3905.10.1074/jbc.M311165200Search in Google Scholar PubMed

Tonk, M., Cabezas-Cruz, A., Valdes, J.J., Rego, R.O.M., Grubhoffer, L., Estrada-Pena, A., Vilcinskas, A., Kotsyfakis, M., and Rahnamaeian, M. (2015). Ixodes ricinus defensins attack distantly-related pathogens. Dev. Comp. Immunol. 53, 358–365.10.1016/j.dci.2015.08.001Search in Google Scholar PubMed

Vilcinskas, A., Mukherjee, K., and Vogel, H. (2013). Expansion of the antimicrobial peptide repertoire in the invasive ladybird Harmonia axyridis. Proc. R. Soc. Lond. B. Biol. Sci. 280, 1–9.10.1098/rspb.2012.2113Search in Google Scholar

Vogel, H., Altincicek, B., Gloeckner, G., and Vilcinskas, A. (2011). A comprehensive transcriptome and immune-gene repertoire of the lepidopteran model host Galleria mellonella. BMC Genomics 12, 308.10.1186/1471-2164-12-308Search in Google Scholar PubMed PubMed Central

Westerhoff, H.V., Zasloff, M., Rosner, J.L., Hendler, R.W., Dewaal, A., Gomes, A.V., Jongsma, A.P.M., Riethorst, A., and Juretic, D. (1995). Functional synergism of the magainins PGLa and magainin-2 in Escherichia coli, tumor cells and liposomes. Eur. J. Biochem. 228, 257–264.10.1111/j.1432-1033.1995.00257.xSearch in Google Scholar

Yi, H.-Y., Chowdhury, M., Huang, Y.-D., and Yu, X.-Q. (2014). Insect antimicrobial peptides and their applications. Appl. Microbiol. Biotechnol. 98, 5807–5822.10.1007/s00253-014-5792-6Search in Google Scholar PubMed PubMed Central

Zdybicka-Barabas, A., Mak, P., Klys, A., Skrzypiec, K., Mendyk, E., Fiolka, M.J., and Cytrynska, M. (2012). Synergistic action of Galleria mellonella anionic peptide 2 and lysozyme against Gram-negative bacteria. Biochim. Biophys. Acta Biomembr. 1818, 2623–2635.10.1016/j.bbamem.2012.06.008Search in Google Scholar PubMed

Zdybicka-Barabas, A., Staczek, S., Mak, P., Skrzypiec, K., Mendyk, E., and Cytrynska, M. (2013). Synergistic action of Galleria mellonella apolipophorin III and lysozyme against Gram-negative bacteria. Biochim. Biophys. Acta Biomembr. 1828, 1449–1456.10.1016/j.bbamem.2013.02.004Search in Google Scholar PubMed