Within and transgenerational immune priming in an insect to a DNA virus

Proceedings of the Royal Society B: Biological Sciences

Volumn 278, Issue 1707, 2011, Pages 871-876

  Tidbury, Hannah J ^a   Pedersen, Amy B ^b   Boots, Mike ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Immune priming; Invertebrate immunity; PiGV; Plodia interpunctella; Virus

Indexed keywords

BACTERIUM; DNA; GENERATION TIME; GENETIC ANALYSIS; HOST-PARASITE INTERACTION; IMMUNE RESPONSE; INSECT; INVERTEBRATE; VIRUS;

DNA VIRUSES; GRANULOVIRUS; HEXAPODA; INVERTEBRATA; LEPIDOPTERA; PLODIA; PLODIA INTERPUNCTELLA;

EID: 79952330064     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2010.1517     Document Type: Conference Paper

References (40)

1. Anderson, R. M. & May, R. M. 1981 The populationdynamics of micro-parasites and their invertebrate hosts. Phil. Trans. R. Soc. Lond. B 291, 451-524. (doi:10.1098/rstb.1981.0005)
2. Boots, M. & Begon, M. 1993 Trade-offs with resistance to a granulosis-virus in the Indian meal moth, examined by a laboratory evolution experiment. Funct. Ecol. 7, 528-534. (doi:10.2307/2390128)
3. Hudson, P. J., Dobson, A. P. & Newborn, D. 1998 Prevention of population cycles by parasite removal. Science 282, 2256-2258. (doi:10.1126/science.282.5397.2256) (Pubitemid 29004073)
4. Pedersen, A. B. & Greives, T. J. 2008 The interaction of parasites and resources cause crashes in a wild mouse population. J. Anim. Ecol. 77, 370-377. (doi:10.1111/j. 1365-2656.2007.01321.x) (Pubitemid 351191040)
5. Hatcher, M. J., Dick, J. T. A. & Dunn, A. M. 2006 How parasites affect interactions between competitors and predators. Ecol. Lett. 9, 1253-1271. (doi:10.1111/j. 1461-0248.2006.00964.x) (Pubitemid 44571667)
6. Lafferty, K. D., Dobson, A. P. & Kuris, A. M. 2006 Parasites dominate food web links. Proc. Natl Acad. Sci. USA 103, 11 211-11 216. (doi:10.1073/pnas.0604755103) (Pubitemid 44156498)
7. Wood, C. L., Byers, J. E., Cottingham, K. L., Altman, I., Donahue, M. J. & Blakeslee, A. M. H. 2007 Parasites alter community structure. Proc. Natl Acad. Sci. USA 104, 9335-9339. (doi:10.1073/pnas.0700062104) (Pubitemid 47185780)
8. Hoang, A. 2001 Immune response to parasitism reduces resistance of Drosophila melanogaster to desiccation and starvation. Evolution 55, 2353-2358. (Pubitemid 34045564)
9. Kraaijeveld, A. R. & Godfray, H. C. J. 1997 Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389, 278-280. (doi:10.1038/38483) (Pubitemid 27406639)
10. Murphy, K. M., Travers, P. & Walport, M. 2007 Janeway's immunobiology, 7th edn. New York, NY: Garland Science.
11. Little, T. J., O'Connor, B., Colegrave, N., Watt, K. & Read, A. F. 2003 Maternal transfer of strain-specific immunity in an invertebrate. Curr. Biol. 13, 489-492. (doi:10.1016/S0960-9822 (03) 00163-5) (Pubitemid 36345723)
12. Moret, Y. & Siva-Jothy, M. T. 2003 Adaptive innate immunity? Responsive-mode prophylaxis in the mealworm beetle, Tenebrio molitor. Proc. R. Soc. Lond. B 270, 2475-2480. (doi:10.1098/rspb.2003.2511) (Pubitemid 37500241)
13. Pham, L. N., Dionne, M. S., Shirasu-Hiza, M. & Schneider, D. S. 2007 A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog. 3, e26. (doi:10.1371/journal.0030026)
14. Roth, O., Sadd, B. M., Schmid-Hempel, P. & Kurtz, J. 2009 Strain-specific priming of resistance in the red flour beetle, Tribolium castaneum. Proc. R. Soc. B 276, 145-151. (doi:10.1098/rspb.2008.1157)
15. Sadd, B. M. & Schmid-Hempel, P. 2006 Insect immunity shows specificity in protection upon secondary pathogen exposure. Curr. Biol. 16, 1206-1210. (doi:10.1016/j.cub. 2006.04.047) (Pubitemid 43867309)
16. Freitak, D., Heckel, D. G. & Vogel, H. 2009 Dietarydependent trans-generational immune priming in an insect herbivore. Proc. R. Soc. B 276, 2617-2624. (doi:10.1098/rspb.2009.0323)
17. Roth, O., Joop, G., Eggert, H., Hilbert, J., Daniel, J., Schmid-Hempel, P. & Kurtz, J. 2010 Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum. J. Anim. Ecol. 79, 403-413. (doi:10.1111/j.1365-2656.2009.01617.x)
18. Imler, J. & Elftherianos, I. 2009 Drosophila as a model for studying antiviral defences. In Insect infection and immunity (eds J. Rolff & S. E. Reyolds), pp. 49-68. Oxford, UK: Oxford University Press.
19. Strand, M. R. 2008 The insect cellular immune response. Insect Sci. 15, 1-14.
20. Wang, X. H., Aliyari, R., Li, W. X., Li, H. W., Kim, K., Carthew, R., Atkinson, P. & Ding, S. W. 2006 RNA interference directs innate immunity against viruses in adult Drosophila. Science 312, 452-454. (doi:10.1126/science. 1125694)
21. Clarke, T. E. & Clem, R. J. 2003 Insect defenses against virus infection: the role of apoptosis. Int. Rev. Immunol. 22, 401-424. (doi:10.1080/08830180305215) (Pubitemid 37247660)
22. Xi, Z. Y., Ramirez, J. L. & Dimopoulos, G. 2008 The Aedes aegypti Toll pathway controls dengue virus infection. PLoS Pathog. 4, e1000098. (doi:10.1371/journal.ppat.1000098)
23. Zambon, R. A., Nandakumar, M., Vakharia, V. N. & Wu, L. P. 2005 The Toll pathway is important for an antiviral response in Drosophila. Proc. Natl Acad. Sci. USA 102, 7257-7262. (doi:10.1073/pnas.0409181102) (Pubitemid 40696366)
24. Dostert, C., Jouanguy, E., Irving, P., Troxler, L., Galiana-Arnoux, D., Hetru, C., Hoffmann, J. A. & Imler, J. L. 2005 The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of Drosophila. Nat. Immunol. 6, 946-953. (doi:10.1038/ni1237) (Pubitemid 43090450)
25. Sabatier, L., Jouanguy, E., Dostert, C., Zachary, D., Dimarcq, J. L., Bulet, P. & Imler, J. L. 2003 Pherokine-2 and-3: two Drosophila molecules related to pheromone/odor-binding proteins induced by viral and bacterial infections. Eur. J. Biochem. 270, 3398-3407. (doi:10. 1046/j.1432-1033.2003. 03725.x) (Pubitemid 37011632)
26. Costa, A., Jan, E., Sarnow, P. & Schneider, D. 2009 The Imd pathway is involved in antiviral immune responses in Drosophila. PLoS ONE 4, 37436. (doi:10. 1371/journal.pone.0007436)
27. Witteveldt, J., Vlak, J. M. & Van Hulten, M. C. W. 2004 Protection of Penaeus monodon against white spot syndrome virus using a WSSV subunit vaccine. Fish Shellfish Immunol. 16, 571-579. (doi:10.1016/j.fsi.2003. 09.006) (Pubitemid 38630447)
28. Wu, J. L., Nishioka, T., Mori, K., Nishizawa, T. & Muroga, K. 2002 A time-course study on the resistance of Penaeus japonicus induced by artificial infection with white spot syndrome virus. Fish Shellfish Immunol. 13, 391-403. (doi:10.1006/fsim.2002.0414) (Pubitemid 35326373)
29. Sanchez-Vargas, I., Scott, J. C., Poole-Smith, B. K., Franz, A. W. E., Barbosa-Solomieu, V., Wilusz, J., Olson, K. E. & Blair, C. D. 2009 Dengue virus type 2 infections of Aedes aegypti are modulated by the mosquito's RNA interference pathway. PLoS Pathog. 5, e1000299. (doi:10.1371/journal.ppat. 1000299)
30. Tinsley, T. W. 1977 Viruses and biological-control of insect pests. Bioscience 27, 659-661. (doi:10.2307/1297549)
31. Smith, I. R. L. & Crook, N. E. 1988 In vivo isolation of Baculovirus genotypes. Virology 166, 240-244. (doi:10.1016/0042-6822 (88) 90165-1)
32. Boots, M. & Begon, M. 1994 Resource limitation and the lethal and sub-lethal effects of a viral pathogen in the Indian meal moth. Ecol. Entomol. 19, 319-326. (doi:10.1111/j.1365-2311.1994.tb00248.x) (Pubitemid 2157952)
33. Moret, Y. 2006 'Trans-generational immune priming': specific enhancement of the antimicrobial immune response in the mealworm beetle, Tenebrio molitor. Proc. R. Soc. B 273, 1399-1405. (doi:10.1098/rspb. 2006.3465) (Pubitemid 47308761)
34. Sadd, B. M., Kleinlogel, Y., Schmid-Hempel, R. & Schmid-Hempel, P. 2005 Trans-generational immune priming in a social insect. Biol. Lett. 1, 386-388. (doi:10.1098/rsbl.2005.0369) (Pubitemid 41796575)
35. Roth, O. & Kurtz, J. 2009 Phagocytosis mediates specificity in the immune defence of an invertebrate, the woodlouse Porcellio scaber (Crustacea: Isopoda). Dev. Comp. Immunol. 33, 1151-1155. (doi:10.1016/j. dci.2009.04.005)
36. Sadd, B. M. & Schmid-Hempel, P. 2007 Facultative but persistent transgenerational immunity via the mother's eggs in bumblebees. Curr. Biol. 17, R1046-R1047. (doi:10.1016/j.cub.2007.11.007) (Pubitemid 350236860)
37. Voordouw, M. J., Lambrechts, L. & Koella, J. 2008 No maternal effects after stimulation of the melanization response in the yellow fever mosquito Aedes aegypti. Oikos 117, 1269-1279. (doi:10.1111/j.0030-1299.2008. 16741.x)
38. Little, T. J. & Kraaijeveld, A. R. 2004 Ecological and evolutionary implications of immunological priming in invertebrates. Trends Ecol. Evol. 19, 58-60. (doi:10. 1016/j.tree.2003.11.011) (Pubitemid 38105887)
39. Kurtz, J. 2004 Memory in the innate and adaptive immune systems. Microb. Infect. 6, 1410-1417. (doi:10. 1016/j.micinf.2004.10.002) (Pubitemid 41110585)
40. Sadd, B. M. & Schmid-Hempel, P. 2009 A distinct infection cost associated with trans-generational priming of antibacterial immunity in bumble-bees. Biol. Lett. 5, 798-801. (doi:10.1098/rsbl.2009.0458)