The entomopathogenic fungus Metarhizium robertsii communicates with the insect host Galleria mellonella during infection

References

• Vilcinskas A, Götz P. Parasitic Fungi and their Interactions with the Insect Immune System. In: Stothard JR, Baker RM, Rollinson D, editors. Advances in Parasitology USA: Academic Press. 1999. p. 267–313. doi:10.1016/S0065-308X(08)60244-4
   Google Scholar
• St Leger RJ, Joshi L, Bidochka MJ, et al. Biochemical characterization and ultrastructural localization of two extracellular trypsins produced by Metarhizium anisopliae in infected insect cuticles. Appl Environ Microbiol. 1996;62(4):1257–64
   PubMed Web of Science ®Google Scholar
• St Leger RJ, Charnley AK, Cooper RM. Characterization of cuticle-degrading proteases produced by the entomopathogen Metarhizium anisopliae. Arch Biochem Biophys. 1987;253(1):221–32
   PubMed Web of Science ®Google Scholar
• Freimoser FM, Hu G, St Leger RJ. Variation in gene expression patterns as the insect pathogen Metarhizium anisopliae adapts to different host cuticles or nutrient deprivation in vitro. Microbiology. 2005;151(Pt 2):361–71. doi:10.1099/mic.0.27560-0
   PubMed Web of Science ®Google Scholar
• Gillespie JP, Bailey AM, Cobb B, et al. Fungi as elicitors of insect immune responses. Arch Insect Biochem Physiol. 2000;44(2):49–68. doi:10.1002/15206327(200006)44:2<49::AID-ARCH1>3.0.CO;2-F
   PubMed Web of Science ®Google Scholar
• Vilcinskas A. Coevolution between pathogen-derived proteinases and proteinase inhibitors of host insects. Virulence. 2010;1(3):206–14. doi:10.4161/viru.1.3.12072
   PubMed Web of Science ®Google Scholar
• Staats CC, Junges A, Guedes RL, et al. Comparative genome analysis of entomopathogenic fungi reveals a complex set of secreted proteins. BMC Genomics. 2014;15:822. doi:10.1186/1471-2164-15-822
   PubMed Web of Science ®Google Scholar
• Mukherjee K, Vilcinskas A. Development and immunity-related microRNAs of the lepidopteran model host Galleria mellonella. BMC Genomics. 2014;15:705. doi:10.1186/1471-2164-15-705
   PubMed Web of Science ®Google Scholar
• Mukherjee K, Fischer R, Vilcinskas A. Histone acetylation mediates epigenetic regulation of transcriptional reprogramming in insects during metamorphosis, wounding and infection. Front Zool. 2012;9(1):25. doi:10.1186/1742-9994-9-25
   PubMed Web of Science ®Google Scholar
• Vilcinskas A. The role of epigenetics in host-parasite coevolution: lessons from the model host insects Galleria mellonella and Tribolium castaneum. Zoology (Jena, Germany). 2016;119(4):273–80. doi:10.1016/j.zool.2016.05.004
   PubMed Web of Science ®Google Scholar
• Mukherjee K, Twyman RM, Vilcinskas A. Insects as models to study the epigenetic basis of disease. Prog Biophys Mol Biol. 2015;118(1–2):69–78. doi:10.1016/j.pbiomolbio.2015.02.009
   PubMed Web of Science ®Google Scholar
• Adekoya OA, Sylte I. The thermolysin family (M4) of enzymes: therapeutic and biotechnological potential. Chem Biol Drug Des. 2009;73(1):7–16. doi:10.1111/j.1747-0285.2008.00757.x
   PubMed Web of Science ®Google Scholar
• Qazi SS, Khachatourians GG. Hydrated conidia of Metarhizium anisopliae release a family of metalloproteases. J Invertebr Pathol. 2007;95(1):48–59. doi:10.1016/j.jip.2006.12.002
   PubMed Web of Science ®Google Scholar
• Altincicek B, Linder M, Linder D, et al. Microbial metalloproteinases mediate sensing of invading pathogens and activate innate immune responses in the lepidopteran model host Galleria mellonella. Infect Immun. 2007;75(1):175–83. doi:10.1128/iai.01385-06
   PubMed Web of Science ®Google Scholar
• Griesch J, Wedde M, Vilcinskas A. Recognition and regulation of metalloproteinase activity in the haemolymph of Galleria mellonella: a new pathway mediating induction of humoral immune responses. Insect Biochem Mol Biol. 2000;30(6):461–72
   PubMed Web of Science ®Google Scholar
• Altincicek B, Berisha A, Mukherjee K, et al. Identification of collagen IV derived danger/alarm signals in insect immunity by nanoLC-FTICR MS. Biol Chem. 2009;390(12):1303–11. doi:10.1515/bc.2009.128
   PubMed Web of Science ®Google Scholar
• Berisha A, Mukherjee K, Vilcinskas A, et al. High-resolution mass spectrometry driven discovery of peptidic danger signals in insect immunity. PLoS One. 2013;8(11):e80406. doi:10.1371/journal.pone.0080406
   PubMed Web of Science ®Google Scholar
• Clermont A, Wedde M, Seitz V, et al. Cloning and expression of an inhibitor of microbial metalloproteinases from insects contributing to innate immunity. Biochem J. 2004;382(Pt 1):315–22. doi:10.1042/bj20031923
   PubMed Web of Science ®Google Scholar
• Wedde M, Weise C, Nuck C, et al. The insect metalloproteinase inhibitor gene of the lepidopteran Galleria mellonella encodes two distinct inhibitors. Biol Chem. 2007;388(1):119–27. doi:10.1515/BC.2007.013
   PubMed Web of Science ®Google Scholar
• Joop G, Vilcinskas A. Coevolution of parasitic fungi and insect hosts. Zoology (Jena, Germany). 2016;119(4):350–8. doi:10.1016/j.zool.2016.06.005
   PubMed Web of Science ®Google Scholar
• Vogel H, Altincicek B, Glockner G, et al. A comprehensive transcriptome and immune-gene repertoire of the lepidopteran model host Galleria mellonella. BMC Genomics. 2011;12:308. doi:10.1186/1471-2164-12-308
   PubMed Web of Science ®Google Scholar
• Rahnamaeian M, Langen G, Imani J, et al. Insect peptide metchnikowin confers on barley a selective capacity for resistance to fungal ascomycetes pathogens. J Exp Bot. 2009;60(14):4105–14. doi:10.1093/jxb/erp240
   PubMed Web of Science ®Google Scholar
• Griesch J, Vilcinskas A. Proteases released by entomopathogenic fungi impair phagocytic activity, attachment and spreading of plasmatocytes isolated from haemolymph of the greater wax moth Galleria mellonella. Biocontrol Sci Technol. 1998;8(4):517–31. doi:10.1080/09583159830036
   Web of Science ®Google Scholar
• Vilcinskas A, Wedde M. Inhibition of Beauveria bassiana Proteases and Fungal Development by Inducible Protease Inhibitors in the Haemolymph of Galleria mellonella larvae. Biocontrol Sci Technol. 1997;7(4):591–602. doi:10.1080/09583159730640
   Web of Science ®Google Scholar
• Dubovskiy IM, Whitten MM, Kryukov VY, et al. More than a colour change: insect melanism, disease resistance and fecundity. Proc Biol Sci. 2013;280(1763):20130584. doi:10.1098/rspb.2013.0584
   PubMed Web of Science ®Google Scholar
• Vilcinskas A. Evolutionary plasticity of insect immunity. J Insect Physiol. 2013;59(2):123–9
   PubMed Web of Science ®Google Scholar
• Wang S, Leclerque A, Pava-Ripoll M, et al. Comparative genomics using microarrays reveals divergence and loss of virulence-associated genes in host-specific strains of the insect pathogen Metarhizium anisopliae. Eukaryot Cell. 2009;8(6):888–98. doi:10.1128/ec.00058-09
   PubMedGoogle Scholar
• Wang S, Fang W, Wang C, et al. Insertion of an esterase gene into a specific locust pathogen (Metarhizium acridum) enables it to infect caterpillars. PLoS Pathog. 2011;7(6):e1002097. doi:10.1371/journal.ppat.1002097
   PubMed Web of Science ®Google Scholar
• Arolas JL, Botelho TO, Vilcinskas A, et al. Structural evidence for standard-mechanism inhibition in metallopeptidases from a complex poised to resynthesize a peptide bond. Angew Chem Int Ed Engl. 2011;50(44):10357–60. doi:10.1002/anie.201103262
   PubMed Web of Science ®Google Scholar
• Schrank A, Vainstein MH. Metarhizium anisopliae enzymes and toxins. Toxicon. 2010;56(7):1267–74. doi:10.1016/j.toxicon.2010.03.008
   PubMed Web of Science ®Google Scholar
• Vilcinskas A, Matha V, Götz P. Effects of the entomopathogenic fungus Metarhizium anisopliae and its secondary metabolites on morphology and cytoskeleton of plasmatocytes isolated from the greater wax moth, Galleria mellonella. J Insect Physiol. 1997;43(12):1149–59. http://doi.org/10.1016/S0022-1910(97)00066-8
   PubMed Web of Science ®Google Scholar
• Pal S, St Leger RJ, Wu LP. Fungal peptide Destruxin A plays a specific role in suppressing the innate immune response in Drosophila melanogaster. J Biol Chem. 2007;282(12):8969–77. doi:10.1074/jbc.M605927200
   PubMed Web of Science ®Google Scholar
• Wang C, St Leger RJ. A collagenous protective coat enables Metarhizium anisopliae to evade insect immune responses. Proc Natl Acad Sci USA. 2006;103(17):6647–52. doi:10.1073/pnas.0601951103
   PubMed Web of Science ®Google Scholar
• de Bekker C, Quevillon LE, Smith PB, et al. Species-specific ant brain manipulation by a specialized fungal parasite. BMC Evol Biol. 2014;14:166. doi:10.1186/s12862-014-0166-3
   PubMed Web of Science ®Google Scholar
• Bader MW, Sanowar S, Daley ME, et al. Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell. 2005;122(3):461–72. doi:10.1016/j.cell.2005.05.030
   PubMed Web of Science ®Google Scholar
• Yamauchi Y, Boukari H, Banerjee I, et al. Histone deacetylase 8 is required for centrosome cohesion and influenza A virus entry. PLoS Pathog. 2011;7(10):e1002316. doi:10.1371/journal.ppat.1002316
   PubMed Web of Science ®Google Scholar
• Chaal BK, Gupta AP, Wastuwidyaningtyas BD, et al. Histone deacetylases play a major role in the transcriptional regulation of the Plasmodium falciparum life cycle. PLoS Pathog. 2010;6(1):e1000737. doi:10.1371/journal.ppat.1000737
   PubMed Web of Science ®Google Scholar
• Bougdour A, Maubon D, Baldacci P, et al. Drug inhibition of HDAC3 and epigenetic control of differentiation in Apicomplexa parasites. J Exp Med. 2009;206(4):953–66. doi:10.1084/jem.20082826
   PubMed Web of Science ®Google Scholar
• Lopes da Rosa J, Boyartchuk VL, Zhu LJ, et al. Histone acetyltransferase Rtt109 is required for Candida albicans pathogenesis. Proc Natl Acad Sci USA. 2010;107(4):1594–9. doi:10.1073/pnas.0912427107
   PubMed Web of Science ®Google Scholar
• Wurtele H, Tsao S, Lepine G, et al. Modulation of histone H3 lysine 56 acetylation as an antifungal therapeutic strategy. Nat Med. 2010;16(7):774–80. doi:10.1038/nm.2175
   PubMed Web of Science ®Google Scholar
• Mukherjee K, Grizanova E, Chertkova E, et al. Experimental evolution of resistance against Bacillus thuringiensis in the insect model host Galleria mellonella results in epigenetic modifications. Virulence. 2017:1–13. doi: 10.1080/21505594.2017.1325975. ( in press).
   Web of Science ®Google Scholar
• Bolouri Moghaddam MR, Vilcinskas A, Rahnamaeian M. The insect-derived antimicrobial peptide metchnikowin targets Fusarium graminearum beta(1,3)glucanosyltransferase Gel1, which is required for the maintenance of cell wall integrity. Biol Chem. 2016;398(4):491–8. doi:10.1515/hsz-2016-0295
   Web of Science ®Google Scholar
• Baumler A, Fang FC. Host specificity of bacterial pathogens. Cold Spring Harb Perspect Med. 2013;3(12):a010041. doi:10.1101/cshperspect.a010041
   PubMed Web of Science ®Google Scholar
• Hothorn T, Bretz F, Westfall P. Simultaneous inference in general parametric models. Biom J. 2008;50(3):346–63. doi:10.1002/bimj.200810425
   PubMed Web of Science ®Google Scholar
• Zeileis A. Econometric computing with HC and HAC Covariance matrix estimators. J Statistical Software. 2004;11(10):1–17. doi: 10.18637/jss.v011.i10
   Google Scholar