The maternal transfer of bacteria can mediate trans-generational immune priming in insects

Virulence

Volumn 5, Issue 4, 2014, Pages 547-554

  Freitak, Dalial ^a,c   Schmidtberg, Henrike ^a   Dickel, Franziska ^a,c   Lochnit, Günther ^a   Vogel, Heiko ^b   Vilcinskas, Andreas ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Fitness costs; Galleria mellonella; Innate immunity; Maternal inheritance; Parental investment; Trans generational immune priming

Indexed keywords

GLUTATHIONE TRANSFERASE; LIPOPOLYSACCHARIDE BINDING PROTEIN; LYSOZYME; MONOPHENOL MONOOXYGENASE; PEPTIDOGLYCAN RECOGNITION PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSAY; BACTERIAL PHENOMENA AND FUNCTIONS; CONTROLLED STUDY; ESCHERICHIA COLI; FEMALE; GALLERIA MELLONELLA; GENE EXPRESSION; HEMOLYMPH; IMMUNE RESPONSE; INNATE IMMUNITY; INSECT REARING; LARVA; LYTIC ZONE ASSAY; MATERNAL TRANSFER OF BACTERIA; MICROCOCCUS LUTEUS; NONHUMAN; PROTEIN ANALYSIS; PSEUDOMONAS; REAL TIME POLYMERASE CHAIN REACTION; REARING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SERRATIA; TRANS GENERATIONAL IMMUNE PRIMING; TWO DIMENSIONAL GEL ELECTROPHORESIS; ANIMAL; BACTERIAL TRANSLOCATION; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; MALE; MICROBIOLOGY; MOTH; PHYSIOLOGY;

ANIMALS; BACTERIAL TRANSLOCATION; FEMALE; LARVA; MALE; MOTHS; PSEUDOMONAS; SERRATIA;

EID: 84900533744     PISSN: 21505594     EISSN: 21505608     Source Type: Journal    
DOI: 10.4161/viru.28367     Document Type: Article

References (32)

1. Schmid-Hempel P. Natural insect host-parasite systems show immune priming and specificity: puzzles to be solved. Bioessays 2005; 27:1026-34; PMID:16163710; http://dx.doi.org/10.1002/ bies.20282
2. Sadd BM, Schmid-Hempel P. Insect immunity shows specificity in protection upon secondary pathogen exposure. Curr Biol 2006; 16:1206-10; PMID:16782011; http://dx.doi.org/10.1016/j. cub.2006.04.047
3. Zanchi C, Troussard JP, Moreau J, Moret Y. Relationship between maternal transfer of immunity and mother fecundity in an insect. Proc Biol Sci 2012; 279:3223-30; PMID:22535782; http://dx.doi. org/10.1098/rspb.2012.0493
4. Little TJ, O'Connor B, Colegrave N, Watt K, Read AF. Maternal transfer of strain-specific immunity in an invertebrate. Curr Biol 2003; 13:489-92; PMID:12646131; http://dx.doi.org/10.1016/ S0960-9822(03)00163-5
5. Sadd BM, Kleinlogel Y, Schmid-Hempel R, Schmid-Hempel P. Trans-generational immune priming in a social insect. Biol Lett 2005; 1:386-8; PMID:17148213; http://dx.doi.org/10.1098/ rsbl.2005.0369
6. Sadd BM, Schmid-Hempel P. Facultative but persistent trans-generational immunity via the mother's eggs in bumblebees. Curr Biol 2007; 17:R1046-7; PMID:18088585; http://dx.doi.org/10.1016/j. cub.2007.11.007
7. Moret Y. "Trans-generational immune priming": specific enhancement of the antimicrobial immune response in the mealworm beetle, Tenebrio molitor. Proc Biol Sci 2006; 273:1399-405; PMID:16777729; http://dx.doi.org/10.1098/rspb.2006.3465
8. Roth O, Sadd BM, Schmid-Hempel P, Kurtz J. Strainspecific priming of resistance in the red flour beetle, Tribolium castaneum. Proc Biol Sci 2009; 276:145-51; PMID:18796392; http://dx.doi.org/10.1098/ rspb.2008.1157
9. Freitak D, Heckel DG, Vogel H. Dietary-dependent trans-generational immune priming in an insect herbivore. Proc Biol Sci 2009; 276:2617-24; PMID:19369263; http://dx.doi.org/10.1098/ rspb.2009.0323
10. Freitak D, Heckel DG, Vogel H. Bacterial feeding induces changes in immune-related gene expression and has trans-generational impacts in the cabbage looper (Trichoplusia ni). Front Zool 2009; 6:7; PMID:19422678; http://dx.doi. org/10.1186/1742-9994-6-7
11. 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 2010; 79:403-13; PMID:19840170; http://dx.doi. org/10.1111/j.1365-2656.2009.01617.x
12. Seppola M, Johnsen H, Mennen S, Myrnes B, Tveiten H. Maternal transfer and transcriptional onset of immune genes during ontogenesis in Atlantic cod. Dev Comp Immunol 2009; 33:1205-11; PMID:19577592; http://dx.doi.org/10.1016/j. dci.2009.06.013
13. Richards EJ. Inherited epigenetic variation--revisiting soft inheritance. Nat Rev Genet 2006; 7:395-401; PMID:16534512; http://dx.doi.org/10.1038/ nrg1834
14. Mukherjee K, Hain T, Fischer R, Chakraborty T, Vilcinskas A. Brain infection and activation of neuronal repair mechanisms by the human pathogen Listeria monocytogenes in the lepidopteran model host Galleria mellonella. Virulence 2013; 4:324-32; PMID:23348912; http://dx.doi.org/10.4161/ viru.23629
15. Mukherjee K, Raju R, Fischer R, Vilcinskas A. Galleria mellonella as a model host to study gut microbe homeostasis and brain infection by the human pathogen listeria monocytogenes. Adv Biochem Eng Biotechnol 2013; 135:27-39; PMID:23708825; http://dx.doi.org/10.1007/10_2013_203
16. Banville N, Browne N, Kavanagh K. Effect of nutrient deprivation on the susceptibility of Galleria mellonella larvae to infection. Virulence 2012; 3:497-503; PMID:23076277; http://dx.doi.org/10.4161/ viru.21972
17. Vilcinskas A. Anti-infective therapeutics from the Lepidopteran model host Galleria mellonella. Curr Pharm Des 2011; 17:1240-5; PMID:21470117; http://dx.doi.org/10.2174/138161211795703799
18. Vogel H, Altincicek B, Glöckner G, Vilcinskas A. A comprehensive transcriptome and immunegene repertoire of the lepidopteran model host Galleria mellonella. BMC Genomics 2011; 12:308; PMID:21663692; http://dx.doi. org/10.1186/1471-2164-12-308
19. Jiang H, Vilcinskas A, Kanost MR. Immunity in lepidopteran insects. Adv Exp Med Biol 2010; 708:181-204; PMID:21528699; http://dx.doi. org/10.1007/978-1-4419-8059-5_10
20. Gorman MJ, Kankanala P, Kanost MR. Bacterial challenge stimulates innate immune responses in extra-embryonic tissues of tobacco hornworm eggs. Insect Mol Biol 2004; 13:19-24; PMID:14728663; http://dx.doi.org/10.1111/j.1365-2583.2004.00454.x
21. Sowa-Jasiłek A, Zdybicka-Barabas A, Sta{ogonek}czek S, Wydrych J, Mak P, Jakubowicz T, Cytryńska M. Studies on the role of insect hemolymph polypeptides: Galleria mellonella anionic peptide 2 and lysozyme. Peptides 2014; (forthcoming) http:// dx.doi.org /10.1016/ j.pept ide s.2014.01.012; PMID:24472857.
22. Browne N, Heelan M, Kavanagh K. An analysis of the structural and functional similarities of insect hemocytes and mammalian phagocytes. Virulence 2013; 4:597-603; PMID:23921374; http://dx.doi. org/10.4161/viru.25906
23. Moret Y. "Trans-generational immune priming": specific enhancement of the antimicrobial immune response in the mealworm beetle, Tenebrio molitor. Proc Biol Sci 2006; 273:1399-405; PMID:16777729; http://dx.doi.org/10.1098/rspb.2006.3465
24. Balzan S, de Almeida Quadros C, de Cleva R, Zilberstein B, Cecconello I. Bacterial translocation: overview of mechanisms and clinical impact. J Gastroenterol Hepatol 2007; 22:464-71; PMID:17376034; http://dx.doi. org/10.1111/j.1440-1746.2007.04933.x
25. Nehme NT, Liégeois S, Kele B, Giammarinaro P, Pradel E, Hoffmann JA, Ewbank JJ, Ferrandon D. A model of bacterial intestinal infections in Drosophila melanogaster. PLoS Pathog 2007; 3:e173; PMID:18039029; http://dx.doi.org/10.1371/journal. ppat.0030173
26. Telfer WH. Egg formation in lepidoptera. J Insect Sci 2009; 9:1-21; PMID:20050770; http://dx.doi. org/10.1673/031.009.5001
27. Altincicek B, Stötzel S, Wygrecka M, Preissner KT, Vilcinskas A. Host-derived extracellular nucleic acids enhance innate immune responses, induce coagulation, and prolong survival upon infection in insects. J Immunol 2008; 181:2705-12; PMID:18684961
28. Zanchi C, Troussard JP, Martinaud G, Moreau J, Moret Y. Differential expression and costs between maternally and paternally derived immune priming for offspring in an insect. J Anim Ecol 2011; 80:1174-83; PMID:21644979; http://dx.doi. org/10.1111/j.1365-2656.2011.01872.x
29. Freitak D, Knorr E, Vogel H, Vilcinskas A. Gender-and stressor-specific microRNA expression in Tribolium castaneum. Biol Lett 2012; 8:860-3; PMID:22628099; http://dx.doi.org/10.1098/ rsbl.2012.0273
30. Vilcinskas A, Matha V. Effect of the entomopathogenic fungus Beauveria bassiana on humoral immune response of Galleria mellonella larvae (Lepidoptera: Pyralidae). Eur J Entomol 1997; 94:461-72
31. Mukherjee K, Fischer R, Vilcinskas A. Histone acetylation mediates epigenetic regulation of transcriptional reprogramming in insects during metamorphosis, wounding and infection. Front Zool 2012; 9:25; PMID:23035888; http://dx.doi. org/10.1186/1742-9994-9-25
32. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T) Method. Methods 2001; 25:402-8; PMID:11846609; http://dx.doi. org/10.1006/meth.2001.1262