Immune priming is defined as enhanced protection upon secondary exposure to a pathogen. Such enhanced resistance after prior exposure has been demonstrated for a number of insect species including the red flour beetle, Tribolium castaneum. In testing this phenomenon, the majority of studies have focused on introducing the pathogen into the insect's hemocoel via septic wounding through the cuticle. Although such septic injury can occur in nature, many pathogens enter their hosts via the oral route, i.e. by ingestion. Bacillus thuringiensis bacteria are well-known insect pathogens that infect their host orally. We found that T. castaneum larvae showed increased survival after oral exposure to B. thuringiensis, when they had been orally primed with filter-sterilized media in which spores of B. thuringiensis had been raised. Such priming was achieved only with a naturally pathogenic strain of B. thuringiensis and a strain that was made pathogenic by transfer of plasmids. Moreover, primed larvae were smaller in size 24 h after priming and had a longer developmental time, indicating that investment in such a response comes at a cost. However, the increased survival in primed larvae was not caused by larval size differences upon challenge.

1.
Chambers MC, Schneider DS: Pioneering immunology: insect style. Curr Opin Immunol 2011;24:1-5.
2.
Kurtz J, Franz K: Evidence for memory in invertebrate immunity. Nature 2003;425:37-38.
3.
Kurtz J: Specific memory within innate immune systems. Trends Immunol 2005;26:186-192.
4.
Little TJ, Kraaijeveld AR: Ecological and evolutionary implications of immunological priming in invertebrates. Trends Ecol Evol 2004;19:58-60.
5.
Schmid-Hempel P: Evolutionary ecology of insect immune defenses. Annu Rev Entomol 2005;50:529-551.
6.
Little TJ, Hultmark D, Read AF: Invertebrate immunity and the limits of mechanistic immunology. Nat Immunol 2005;6:651-654.
7.
Flajnik MF, Du Pasquier L: Evolution of innate and adaptive immunity: can we draw a line? Trends Immunol 2004;25:640-644.
8.
Netea MG, Quintin J, van der Meer JWM: Trained immunity: a memory for innate host defense. Cell Host Microbe 2011;9:355-361.
9.
Criscitiello MF, de Figueiredo P: Fifty shades of immune defense. Plos Pathog 2013;9:e1003110.
10.
Moret Y, Siva-Jothy MT: Adaptive innate immunity? Responsive-mode prophylaxis in the mealworm beetle, Tenebrio molitor. P Roy Soc Biol Sci 2003;270:2475-2480.
11.
Sadd BM, Schmid-Hempel P: Insect immunity shows specificity in protection upon secondary pathogen exposure. Curr Biol 2006;16:1206-1210.
12.
Pham LN, Dionne MS, Shirasu-Hiza M, Schneider DS: A specific primed immune response in Drosophila is dependent on phagocytes. Plos Pathog 2007;3:e26.
13.
Roth O, Sadd BM, Schmid-Hempel P, Kurtz J: Strain-specific priming of resistance in the red flour beetle, Tribolium castaneum. P Roy Soc Biol Sci 2009;276:145-151.
14.
Altincicek B, Gross J, Vilcinskas A: Wounding-mediated gene expression and accelerated viviparous reproduction of the pea aphid Acyrthosiphon pisum. Insect Mol Biol 2008;17:711-716.
15.
Freitak D, Knorr E, Vogel H, Vilcinskas A: Gender- and stressor-specific microRNA expression in Tribolium castaneum. Biol Letters 2012;8:860-863.
16.
Rodrigues J, Brayner FA, Alves LC, Dixit R, Barillas-Mury C: Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 2010;329:1353-1355.
17.
Little TJ, O'Connor B, Colegrave N, Watt K, Read AF: Maternal transfer of strain-specific immunity in an invertebrate. Curr Biol 2003;13:489-492.
18.
Soltanian S, François J-M, Dhont J, Arnouts S, Sorgeloos P, Bossier P: Enhanced disease resistance in Artemia by application of commercial beta-glucans sources and chitin in a gnotobiotic Artemia challenge test. Fish Shellfish Immunol 2007;23:1304-1314.
19.
Rowley AF, Pope EC: Vaccines and crustacean aquaculture - a mechanistic exploration. Aquaculture 2012;334-337:1-11.
20.
Freitak D, Wheat CW, Heckel DG, Vogel H: Immune system responses and fitness costs associated with consumption of bacteria in larvae of Trichoplusia ni. BMC Biol 2007;5:56.
21.
Tidbury HJ, Pedersen AB, Boots M: Within and transgenerational immune priming in an insect to a DNA virus. P Roy Soc Biol Sci 2011;278:871-876.
22.
Frankenhuyzen KV: Insecticidal activity of Bacillus thuringiensis crystal proteins. J Inv Path 2009;101:1-16.
23.
Raymond B, Johnston PR, Nielsen-LeRoux C, Lereclus D, Crickmore N: Bacillus thuringiensis: an impotent pathogen? Trends Microbiol 2010;18:189-194.
24.
Milutinović B, Stolpe C, Peuβ R, Armitage SAO, Kurtz J: The red flour beetle as a model for bacterial oral infections. PloS ONE 2013;8:e64638.
25.
Sokoloff A: The Biology of Tribolium, vol 2. Oxford, Clarendon Press, 1974, p 131 (cannibalism), pp 57-59 (hatching rate), p 48 (decrease in size).
26.
Sadd BM, Schmid-Hempel P: A distinct infection cost associated with trans-generational priming of antibacterial immunity in bumble-bees. Biol Lett 2009;5:798-801.
27.
Zanchi C, Troussard JP, Moreau J, Moret Y: Relationship between maternal transfer of immunity and mother fecundity in an insect. P Roy Soc Biol Sci 2012;279:3223-3230.
28.
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;79:403-413.
29.
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.
30.
Daou N, Buisson C, Gohar M, Vidic J, Bierne H, Kallassy M, Lereclus D, Nielsen-LeRoux C: IlsA, a unique surface protein of Bacillus cereus required for iron acquisition from heme, hemoglobin and ferritin. Plos Pathog 2009;5:e1000675.
31.
Huang Y, Lam SL, Ho SH: Bioactivities of essential oil from Elletaria cardamomum (L.) Maton to Sitophilus zeamais Motschulsky and Tribolium castaneum (Herbst). J Stored Prod Res 2000;36:107-117.
32.
Matzinger P: The danger model: a renewed sense of self. Science 2002;296:301-305.
33.
Lehane MJ: Peritrophic matrix structure and function. Annu Rev Entomol 1997;42:525-550.
34.
Soberon M, Gill SS: Signaling versus punching hole: how do Bacillus thuringiensis toxins kill insect midgut cells? Cell Mol Life Sci 2009;66:1337-1349.
35.
Oppert B, Morgan TD, Kramer KJ: Efficacy of Bacillus thuringiensis Cry3Aa protoxin and protease inhibitors against coleopteran storage pests. Pest Manag Sci 2011;67:568-573.
36.
Lee KA, Kim SH, Kim EK, Ha EM, You H, Kim B, Kim MJ, Kwon Y, Ryu JH, Lee WJ: Bacterial-derived uracil as a modulator of mucosal immunity and gut-microbe homeostasis in Drosophila. Cell 2013;153:797-811.
37.
Sheldon BC, Simon V: Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 1996;11:317-321.
38.
Moret Y: Survival for immunity: The price of immune system activation for bumblebee workers. Science 2000;290:1166-1168.
39.
Roth O, Kurtz J: The stimulation of immune defence accelerates development in the red flour beetle (Tribolium castaneum). J Evol Biol 2008;21:1703-1710.
40.
Blaser M, Schmid-Hempel P: Determinants of virulence for the parasite Nosema whitei in its host Tribolium castaneum. J Inv Path 2005;89:251-257.
41.
Millert SC, Bottema CDK, Stathis PA, Tokes LG, Feldman D: Unexpected presence of estrogens in culture medium supplements: subsequent metabolism by the yeast. Endocrinology 1986;119:1362-1369.
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.