The role of epigenetics in host–parasite coevolution: lessons from the model host insects Galleria mellonella and Tribolium castaneum

Zoology

Volumn 119, Issue 4, 2016, Pages 273-280

  Vilcinskas, Andreas ^a,b  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b FRAUNHOFER INSTITUTE FOR MOLECULAR BIOLOGY AND APPLIED ECOLOGY IME   (Germany)

Author keywords

DNA methylation; Epigenetics; Histone acetylation; Immunity; microRNAs

Indexed keywords

ANIMAL; BACTERIAL PHENOMENA AND FUNCTIONS; BEETLE; EVOLUTION; GENETIC EPIGENESIS; GENETICS; HOST PATHOGEN INTERACTION; MICROBIOLOGY; MOTH;

ANIMALS; BACTERIAL PHYSIOLOGICAL PHENOMENA; BEETLES; BIOLOGICAL EVOLUTION; EPIGENESIS, GENETIC; HOST-PATHOGEN INTERACTIONS; MOTHS;

EID: 84989878673     PISSN: 09442006     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.zool.2016.05.004     Document Type: Review

References (59)

1. Altincicek, B., Gross, J., Vilcinskas, A., Wounding-mediated gene expression and accelerated viviparous reproduction of the pea aphid Acyrthosiphon pisum. Insect Mol. Biol. 17 (2008), 711–716.
2. Anderson, R.M., May, R.M., Coevolution of hosts and parasites. Parasitology 85 (1982), 411–426.
3. Asgari, S., MicroRNA functions in insects. Insect Biochem. Mol. Biol. 43 (2013), 388–397.
4. Bingsohn, L., Knorr, E., Vilcinskas, A., The model beetle Tribolium castaneum can be used as an early warning system for transgenerational epigenetic side effects caused by pharmaceuticals. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 185/186 (2016), 57–64.
5. Brockhurst, M.A., Koskella, B., Experimental coevolution of species interactions. Trends Ecol. Evol. 28 (2013), 367–375.
6. Bushati, N., Cohen, S.M., MicroRNA functions. Annu. Rev. Cell Dev. Biol. 23 (2007), 175–205.
7. Decaestecker, E., Gaba, S., Raeymaekers, J.A.M., Stoks, R., Van Kerckhoven, L., Ebert, D., De Meester, L., Host–parasite Red Queen dynamics archived in pond sediment. Nature 450 (2007), 870–873.
8. Dubovskiy, I.M., Whitten, M.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. R. Soc. B, 280, 2013, 20130584.
9. Dubovskiy, I.M., Whitten, M.M.A., Yaroslavtseva, O.N., Greig, C., Kryukov, V.Y., Grizanova, E.V., Mukherjee, K., Vilcinskas, A., Glupov, V.V., Butt, T.M., Can insects develop resistance to insect pathogenic fungi?. PLoS ONE, 8, 2013, e60248.
10. Eggert, H., Kurtz, J., Diddens-de Buhr, M., Different effects of paternal trans-generational immune priming on survival and immunity in step and genetic offspring. Proc. R. Soc. B, 281, 2014, 20142089.
11. Eggert, H., Diddens-de Buhr, M.F., Kurtz, J., A temperature shock can lead to trans-generational immune priming in the red flour beetle, Tribolium castaneum. Ecol. Evol. 5 (2015), 1318–1326.
12. Feliciello, I., Parazajder, J., Akrap, I., Ugarkovic, D., First evidence of DNA methylation in insect Tribolium castaneum: environmental regulation of DNA methylation within heterochromatin. Epigenetics 8 (2013), 534–541.
13. Fisher, J., Hajek, A., Maternal exposure of a beetle to pathogens protects offspring against fungal diseases. PLoS One, 10, 2015, e0125197.
14. Freitak, D., Heckel, D.G., Vogel, H., Dietary-dependent trans-generational immune priming in an insect herbivore. Proc. R. Soc. B 276 (2009), 2617–2624.
15. Freitak, D., Knorr, E., Vogel, H., Vilcinskas, A., Gender- and stressor-specific microRNA expression in Tribolium castaneum. Biol. Lett. 8 (2012), 860–863.
16. Freitak, D., Schmidtberg, H., Dickel, F., Lochnit, G., Vogel, H., Vilcinskas, A., The maternal transfer of bacteria can mediate trans-generational immune priming in insects. Virulence 5 (2014), 547–554.
17. Futo, M., Armitage, S., Kurtz, J., Microbiota plays a role in oral immune priming in Tribolium castaneum. Front. Microbiol., 6, 2016, 1383.
18. Gerardo, N., Altincicek, B., Anselme, C., Atamian, H., Barribeau, S., de Vos, M., Evans, J., Gabaldón, T., Ghanim, M., Heddi, A., Kaloshian, I., Latorre, A., Monegat, C., Moya, A., Nakabachi, A., Parker, B., Pérez-Brocal, V., Pignatelli, M., Rahbé, Y., Ramsey, J., Tamames, J., Tamarit, D., Tamborindeguy, C., Vilcinskas, A., Immunity and other defenses in pea aphids Acyrthosiphon pisum. Genome Biol., 11, 2010, R21.
19. Gillespie, J.P., Bailey, A.M., Cobb, B., Vilcinskas, A., Fungi as elicitors of insect immune responses. Arch. Insect Biochem. Physiol. 44 (2000), 49–68.
20. Gomez-Diaz, E., Jorda, M., Peindo, M.A., Rivero, A., Epigenetics of host–pathogen interactions: the road ahead and the road behind. PLoS Pathog., 8, 2012, e1003007.
21. Greenwood, J.M., Ezquerra, A.L., Behrens, S., Branca, A., Mallet, L., Current analysis of next-generation sequencing data with a focus on host–parasite interactions. Zoology 119 (2016), 298–306.
22. Haase, D., Rieger, J.K., Witten, A., Stoll, M., Bornberg-Bauer, E., Kalbe, M., Schmidt-Drewello, A., Scharsack, J.P., Reusch, T.B.H., Comparative transcriptomics of stickleback immune gene responses upon infections by two helminth parasites, Diplostomum pseudospathaceum and Schistocephalus solidus. Zoology 119 (2016), 307–313.
23. Harris, J.F., Micheva-Viteva, S., Li, N., Hong-Gellner, E., Small RNA-mediated regulation of host–pathogen interactions. Virulence 4 (2013), 785–795.
24. Hussain, M., Asgari, S., MicroRNAs as mediators of insect–host–pathogen interactions and immunity. J. Insect Physiol. 70 (2014), 151–158.
25. Jaenisch, R., Bird, A., Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genetics 33 (2003), 245–254.
26. Joop, G., Vilcinskas, A., Coevolution of parasitic fungi and insect hosts. Zoology 119 (2016), 350–358.
27. Knorr, E., Schmidtberg, H., Arslan, D., Bingsohn, L., Vilcinskas, A., Translocation of bacteria from the gut to the eggs triggers maternal trans-generational immune priming in Tribolium castaneum. Biol. Lett., 11, 2015, 20150885.
28. Little, T.J., O'Connor, B., Colegrave, N., Watt, K., Read, A.F., Maternal transfer of strain-specific immunity in an invertebrate. Curr. Biol. 13 (2003), 489–492.
29. Little, T.J., Hultmark, D., Read, A., Invertebrate immunity and the limits of mechanistic immunology. Nature Immunol. 6 (2005), 651–654.
30. Meagher, R.B., Müssar, K.J., The influence of DNA sequence on epigenome-induced pathologies. Epigen. Chrom., 5, 2012, 11.
31. Milutinovic, B., Fritzlar, S., Kurtz, J., Increased survival in the red flour beetle after oral priming with bacteria-conditioned media. J. Innate Immunol. 6 (2014), 306–314.
32. Milutinovic, B., Peuß, R., Ferro, K., Kurtz, J., Immune priming in arthropods: an update focusing on the red flour beetle. Zoology 119 (2016), 254–261.
33. Moret, Y., Trans-generational immune priming: specific enhancement of the antimicrobial immune response in the mealworm beetle, Tenebrio molitor. Proc. R. Soc. B 273 (2006), 1399–1405.
34. Mukherjee, K., Vilcinskas, A., Development and immunity-related microRNAs of the lepidopteran model host Galleria mellonella. BMC Genomics, 15, 2014, 705.
35. Mukherjee, K., Fischer, R., Vilcinskas, A., Histone acetylation mediates epigenetic regulation of transcriptional reprogramming in insects during metamorphosis, wounding and infection. Front. Zool., 9, 2012, 25.
36. Mukherjee, K., Hain, T., Fischer, R., Chakraborty, T., Vilcinskas, A., Brain infection and activation of neuronal repair mechanisms caused by the human pathogen Listeria monocytogenes in the lepidopteran model host Galleria mellonella. Virulence 4 (2013), 324–332.
37. Mukherjee, K., Twyman, R.M., Vilcinskas, A., Insects as models to study the epigenetic basis of disease. Prog. Biophys. Mol. Biol. 118 (2015), 69–78.
38. Mylonakis, E., Podsiadlowski, L., Muhammed, M., Vilcinskas, A., Diversity, evolution and medical applications of insect antimicrobial peptides. Phil. Trans. R. Soc. B, 371, 2016, 20150290.
39. Paterson, S., Vogwill, T., Buckling, A., Benmayor, R., Spiers, A.J., Thomson, N.R., Quail, M., Smith, F., Walker, D., Libberton, B., Fenton, A., Hall, N., Brockhurst, M.A., Antagonistic coevolution accelerates molecular evolution. Nature 464 (2009), 275–278.
40. Rafaluk, C., Gildenhar, M., Mitschke, A., Telschow, A., Schulenburg, H., Joop, G., Rapid evolution of virulence leading to host extinction under host–parasite coevolution. BCM Evol. Biol., 15, 2015, 112.
41. Roth, O., Sadd, B.M., Schmid-Hempel, P., Kurtz, J., Strain specific priming of resistance in the red flour beetle, Tribolium castaneum. Proc. Biol. Sci. 276 (2009), 145–151.
42. Roth, O., Joop, G., Eggert, H., Hilbert, J., Daniel, J., Schmid-Hempel, P., Kurtz, J., Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum. J. Anim. Ecol. 79 (2010), 403–413.
43. Sadd, B.M., Kleinlogel, Y., Schmid-Hempel, R., Schmid-Hempel, P., Trans-generational immune priming in a social insect. Biol. Lett. 1 (2005), 386–388.
44. Sackton, T.B., Lazzaro, B.P., Schlenke, T.A., Evans, J.D., Hultmark, D., Clark, A.G., Dynamic evolution of the innate immune system in Drosophila. Nat. Gent. 39 (2007), 1461–1468.
45. Sato, F., Tsuchiya, S., Meltzer, S., Shimizu, K., MicroRNAs and epigenetics. FEBS J. 278 (2011), 1598–1609.
46. Trauer, U., Hilker, M., Parental legacy in insects: variation of transgenerational immune priming during offspring development. PLoS One, 8, 2013, e63392.
47. Trauer-Kizilelma, U., Hilker, M., Insect parents improve the anti-parasitic and anti-bacterial defence of their offspring by priming the expression of immune-relevant genes. Insect Biochem. Mol. Biol. 64 (2015), 91–99.
48. Vilcinskas, A., Insects emerge as valuable model hosts to explore virulence. Virulence 2 (2011), 376–378.
49. Vilcinskas, A., Anti-infective therapeutics from the Lepidopteran model host Galleria mellonella. Curr. Pharm. Des. 17 (2011), 1240–1245.
50. Vilcinskas, A., Evolutionary plasticity of insect immunity. J. Insect Physiol. 59 (2013), 123–129.
51. Vilcinskas, A., Götz, P., Parasitic fungi and their interactions with the insect immune system. Adv. Parasitol. 43 (1999), 267–313.
52. Vilcinskas, A., Matha, V., Effect of the entomopathogenic fungus Beauveria bassiana on humoral immune response of Galleria mellonella larvae (Lepidoptera: Pyralidae). Eur. J. Entomol. 94 (1997), 461–472.
53. Vilcinskas, A., Mukherjee, K., Vogel, H., Expansion of the antimicrobial peptide repertoire in the invasive ladybird Harmonia axyridis. Proc. R. Soc. B, 280, 2013, 20122113.
54. Vogel, H., Altincicek, B., Glöckner, G., Vilcinskas, A., A comprehensive transcriptome and immune-gene repertoire of the lepidopteran model host Galleria mellonella. BMC Genomics, 12, 2011, 308.
55. Waterhouse, R.M., Kriventseva, E.V., Meister, S., Xi, Z., Alvarez, K.S., Bartholomay, L.C., Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 316 (2007), 1738–1743.
56. Woolhouse, M.E.J., Webster, J.P., Domingo, E., Charlesworth, B., Levin, B.R., Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat. Genet. 32 (2002), 569–577.
57. Xiao, C., Rajewsky, K., MicroRNA control in the immune system: basic principles. Cell 136 (2009), 26–36.
58. Yang, W., Dierking, K., Rosenstiel, P.C., Schulenburg, H., GATA transcription factor as a likely key regulator of the Caenorhabditis elegans innate immune response against gut pathogens. Zoology 119 (2016), 244–253.
59. Youngson, N.A., Whitelaw, E., Transgenerational epigenetic effects. Annu. Rev. Genomics Hum. Genet. 9 (2008), 233–257.