Immune priming in arthropods: an update focusing on the red flour beetle

Zoology

Volumn 119, Issue 4, 2016, Pages 254-261

  Milutinović, Barbara ^a,b   Peuß, Robert ^a,c   Ferro, Kevin ^a   Kurtz, Joachim ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b INSTITUTE OF SCIENCE AND TECHNOLOGY AUSTRIA   (Austria)

^c STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

Immune memory; Immune priming; Infection route; Priming specificity; Tribolium castaneum

Indexed keywords

ANIMAL; BEETLE; EVOLUTION; GENE EXPRESSION REGULATION; GENETICS; HOST PARASITE INTERACTION; IMMUNOLOGY; PHYSIOLOGY;

ANIMALS; BEETLES; BIOLOGICAL EVOLUTION; GENE EXPRESSION REGULATION; HOST-PARASITE INTERACTIONS;

EID: 84977636058     PISSN: 09442006     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.zool.2016.03.006     Document Type: Review

References (93)

1. Altincicek, B., Knorr, E., Vilcinskas, A., Beetle immunity: identification of immune-inducible genes from the model insect Tribolium castaneum. Dev. Comp. Immunol. 32 (2008), 585–595.
2. Anderson, R.M., May, R.M., Coevolution of hosts and parasites. Parasitology 85 (1982), 411–426.
3. Armitage, S.A., Peuß, R., Kurtz, J., Dscam and pancrustacean immune memory − a review of the evidence. Dev. Comp. Immunol. 48 (2014), 315–323.
4. Armitage, S.A., Sun, W., You, X., Kurtz, J., Schmucker, D., Chen, W., Quantitative profiling of Drosophila melanogaster Dscam1 isoforms reveals no changes in splicing after bacterial exposure. PLoS One, 9, 2014, e108660.
5. Beemelmanns, A., Roth, O., Biparental immune priming in the pipefish Syngnathus typhle. Zoology 119 (2016), 262–272.
6. Behrens, S., Peuß, R., Milutinović, B., Eggert, H., Esser, D., Rosenstiel, P., Schulenburg, H., Bornberg-Bauer, E., Kurtz, J., Infection routes matter in population-specific responses of the red flour beetle to the entomopathogen Bacillus thuringiensis. BMC Genom., 15, 2014, 445.
7. Blaser, M., Schmid-Hempel, P., Determinants of virulence for the parasite Nosema whitei in its host Tribolium castaneum. J. Invertebr. Pathol. 89 (2005), 251–257.
8. Boehm, T., Two in one: dual function of an invertebrate antigen receptor. Nat. Immunol. 8 (2007), 1031–1033.
9. Browne, N., Surlis, C., Kavanagh, K., Thermal and physical stresses induce a short-term immune priming effect in Galleria mellonella larvae. J. Insect Physiol. 63 (2014), 21–26.
10. Bulet, P., Stöcklin, R., Insect antimicrobial peptides: structures, properties and gene regulation. Protein Pept. Lett. 12 (2005), 3–11.
11. Cerenius, L., Lee, B.L., Söderhäll, K., The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol. 29 (2008), 263–271.
12. Chambers, M.C., Schneider, D.S., Pioneering immunology: insect style. Curr. Opin. Immunol. 24 (2012), 10–14.
13. Contreras-Garduño, J., Rodríguez, M.C., Rodríguez, M.H., Alvarado-Delgado, A., Lanz-Mendoza, H., Cost of immune priming within generations: trade-off between infection and reproduction. Microbes Infect. 16 (2014), 261–267.
14. Contreras-Garduño, J., Rodríguez, M.C., Hernández-Martínez, S., Martínez-Barnetche, J., Alvarado-Delgado, A., Izquierdo, J., Herrera-Ortiz, A., Moreno-García, M., Velazquez-Meza, M.E., Valverde, V., Argotte-Ramos, R., Rodríguez, M.H., Lanz-Mendoza, H., Plasmodium bergheiinduced priming in Anopheles albimanus independently of bacterial co-infection. Dev. Comp. Immunol. 52 (2015), 172–181.
15. Criscitiello, M.F., de Figueiredo, P., Fifty shades of immune defense. PLoS Pathog., 9, 2013, e1003110.
16. Dönitz, J., Schmitt-Engel, C., Grossmann, D., Gerischer, L., Tech, M., Schoppmeier, M., Klingler, M., Bucher, G., iBeetle-Base: a database for RNAi phenotypes in the red flour beetle Tribolium castaneum. Nucleic Acids Res. 43 (2014), D720–D725.
17. Dong, Y., Taylor, H.E., Dimopoulos, G., AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biol., 4, 2006, e229.
18. Dong, Y., Cirimotich, C.M., Pike, A., Chandra, R., Dimopoulos, G., Anopheles NF-κB-regulated splicing factors direct pathogen-specific repertoires of the hypervariable pattern recognition receptor AgDscam. Cell Host Microbe 12 (2012), 521–530.
19. Du Pasquier, L., Germline and somatic diversification of immune recognition elements in Metazoa. Immunol. Lett. 104 (2006), 2–17.
20. Dubuffet, A., Zanchi, C., Boutet, G., Moreau, J., Teixeira, M., Moret, Y., Trans-generational immune priming protects the eggs only against gram-positive bacteria in the mealworm beetle. PLoS Pathog., 11, 2015, e1005178.
21. Eggert, H., Kurtz, J., Diddens-de Buhr, M.F., Different effects of paternal trans-generational immune priming on survival and immunity in step and genetic offspring. Proc. R. Soc. B 281 (2014), 2014–2089.
22. 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.
23. Fairlie-Clarke, K.J., Shuker, D.M., Graham, A.L., Why do adaptive immune responses cross-react?. Evol. Appl. 2 (2009), 122–131.
24. Feis, M.E., Goedknegt, M.A., Thieltges, D.W., Buschbaum, C., Wegner, K.M., Biological invasions and host–parasite coevolution: different coevolutionary trajectories along separate parasite invasion fronts. Zoology 119 (2016), 366–374.
25. Frank, S.A., Immunology and Evolution of Infectious Disease. 2002, Princeton University Press, Princeton.
26. Freitak, D., Heckel, D.G., Vogel, H., Bacterial feeding induces changes in immune-related gene expression and has trans-generational impacts in the cabbage looper (Trichoplusia ni). Front. Zool., 6, 2009, 7.
27. Futo, M., Armitage, S.A., Kurtz, J., Microbiota plays a role in oral immune priming in Tribolium castaneum. Front. Microbiol., 6, 2015, 1383.
28. Gerardo, N.M., Altincicek, B., Anselme, C., Atamian, H., Barribeau, S.M., de Vos, M., Duncan, E.J., Evans, J.D., Gabaldón, T., Ghanim, M., Heddi, A., Kaloshian, I., Latorre, A., Moya, A., Nakabachi, A., Parker, B.J., Pérez-Brocal, V., Pignatelli, M., Rahbé, Y., Ramsey, J.S., Spragg, C.J., Tamames, J., Tamarit, D., Tamborindeguy, C., Vincent-Monegat, C., Vilcinskas, A., Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol., 11, 2010, R21.
29. Gilles, A.F., Schinko, J.B., Averof, M., Efficient CRISPR-mediated gene targeting and transgene replacement in the beetle Tribolium castaneum. Development 142 (2015), 2832–2839.
30. Graveley, B.R., Mutually exclusive splicing of the insect Dscam pre-mRNA directed by competing intronic RNA secondary structures. Cell 123 (2005), 65–73.
31. Greenwood, J., 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.
32. Haine, E.R., Moret, Y., Siva-Jothy, M.T., Rolff, J., Antimicrobial defense and persistent infection in insects. Science 322 (2008), 1257–1259.
33. Johnston, P.R., Rolff, J., Immune- and wound-dependent differential gene expression in an ancient insect. Dev. Comp. Immunol. 40 (2013), 320–324.
34. Kerstes, N.A., Bérénos, C., Martin, O.Y., Coevolving parasites and population size shape the evolution of mating behaviour. BMC Evol. Biol., 13, 2013, 29.
35. Knorr, E., Schmidtberg, H., Arslan, D., Bingsohn, L., Vilcinskas, A., Translocation of bacteria from the gut to the eggs triggers maternal transgenerational immune priming in Tribolium castaneum. Biol. Lett., 11, 2015, 20150885.
36. Kurtz, J., Memory in the innate and adaptive immune systems. Microbes Infect. 6 (2004), 1410–1417.
37. Kurtz, J., Specific memory within innate immune systems. Trends Immunol. 26 (2005), 186–192.
38. Kurtz, J., Armitage, S.A.O., Alternative adaptive immunity in invertebrates. Trends Immunol. 27 (2006), 493–496.
39. Kurtz, J., Franz, K., Innate defence: evidence for memory in invertebrate immunity. Nature 425 (2003), 37–38.
40. Kurtz, J., Sauer, K., The immunocompetence handicap hypothesis: testing the genetic predictions. Proc. R. Soc. B 266 (1999), 2515–2522.
41. Kutzer, M.A.M., Armitage, S.A.O., Maximising fitness in the face of parasites: a review of host tolerance. Zoology 119 (2016), 281–289.
42. Lazzaro, B.P., Genetic basis of natural variation in D. melanogaster antibacterial immunity. Science 303 (2004), 1873–1876.
43. Le Bourg, E., Massou, I., Gobert, V., Cold stress increases resistance to fungal infection throughout life in Drosophila melanogaster. Biogerontology 10 (2009), 613–625.
44. Lemaitre, B., Hoffmann, J., The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25 (2007), 697–743.
45. Little, T.J., Kraaijeveld, A.R., Ecological and evolutionary implications of immunological priming in invertebrates. Trends Ecol. Evol. 19 (2004), 58–60.
46. 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.
47. Little, T.J., Hultmark, D., Read, A.F., Invertebrate immunity and the limits of mechanistic immunology. Nat. Immunol. 6 (2005), 651–654.
48. Loker, E., Adema, C., Zhang, S., Kelper, T., Invertebrate immune systems – not homogeneous, not simple, not well understood. Immunol. Rev. 198 (2004), 10–24.
49. Martins, N.E., Faria, V.G., Teixeira, L., Magalhães, S., Sucena, É., Host adaptation is contingent upon the infection route taken by pathogens. PLoS Pathog., 9, 2013, e1003601.
50. Milutinović, B., Stolpe, C., Peuß, R., Armitage, S.A.O., Kurtz, J., The red flour beetle as a model for bacterial oral infections. PLoS One, 8, 2013, e64638.
51. Milutinović, B., Fritzlar, S., Kurtz, J., Increased survival in the red flour beetle after oral priming with bacteria-conditioned media. J. Innate Immun. 6 (2014), 306–314.
52. Milutinović, B., Höfling, C., Futo, M., Scharsack, J.P., Kurtz, J., Infection of Tribolium castaneum with Bacillus thuringiensis: quantification of bacterial replication within cadavers, transmission via cannibalism, and inhibition of spore germination. Appl. Environ. Microbiol. 81 (2015), 8135–8144.
53. Moret, Y., Siva-Jothy, M.T., Adaptive innate immunity? Responsive-mode prophylaxis in the mealworm beetle, Tenebrio molitor. Proc. Biol. Sci. 270 (2003), 2475–2480.
54. Murphy, K.P., Janeway, C.A., Mowat, A., Janeway's Immunobiology. 8th ed., 2012, Garland Science, New York.
55. Netea, M.G., Quintin, J., van der Meer, J.W.M., Trained immunity: a memory for innate host defense. Cell Host Microbe 9 (2011), 355–361.
56. Ng, T.H., Chiang, Y.A., Yeh, Y.C., Wang, H.C., Review of Dscam-mediated immunity in shrimp and other arthropods. Dev. Comp. Immunol. 46 (2014), 129–138.
57. Pedrini, N., Ortiz-Urquiza, A., Huarte-Bonnet, C., Fan, Y., Juárez, M.P., Keyhani, N.O., Tenebrionid secretions and a fungal benzoquinone oxidoreductase form competing components of an arms race between a host and pathogen. Proc. Natl. Acad. Sci. USA 112 (2015), E3651–E3660.
58. Peuß, R., Eggert, H., Armitage, S.A.O., Kurtz, J., Downregulation of the evolutionary capacitor Hsp90 is mediated by social cues. Proc. R. Soc. B, 282, 2015, 20152041.
59. Peuß, R., Wensing, K.U., Woestmann, L., Eggert, H., Milutinović, B., Sroka, M., Scharsack, J.P., Kurtz, J., Armitage, S.A.O., Down syndrome cell adhesion molecule 1: testing for a role in insect immunity, behaviour and reproduction. R. Soc. Open Sci., 3, 2016, 160138.
60. Pham, L.N., Dionne, M.S., Shirasu-Hiza, M., Schneider, D.S., A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog., 3, 2007, e26.
61. Pigliucci, M., Evolution of phenotypic plasticity: where are we going now?. Trends Ecol. Evol 20 (2005), 481–486.
62. Pinaud, S., Portela, J., Duval, D., Nowacki, F.C., Olive, M.-A., Allienne, J.-F., Galinier, R., Dheilly, N.M., Kieffer-Jaquinod, S., Mitta, G., Théron, A., Gourbal, B., A shift from cellular to humoral responses contributes to innate immune memory in the vector snail Biomphalaria glabrata. PLoS Pathog., 12, 2016, e1005361.
63. Pope, E.C., Powell, A., Roberts, E.C., Shields, R.J., Wardle, R., Rowley, A.F., Enhanced cellular immunity in shrimp (Litopenaeus vannamei) after vaccination. PLoS One, 6, 2011, e20960.
64. Rafaluk, C., Gildenhard, M., Mitschke, A., Telschow, A., Schulenburg, H., Joop, G., Rapid evolution of virulence leading to host extinction under host–parasite coevolution. BMC Evol. Biol., 15, 2015, 112.
65. Rahman, M.M., Roberts, H.L.S., Sarjan, M., Asgari, S., Schmidt, O., Induction and transmission of Bacillus thuringiensis tolerance in the flour moth Ephestia kuehniella. Proc. Natl. Acad. Sci. USA 101 (2004), 2696–2699.
66. Rahnamaeian, M., Cytryńska, M., Zdybicka-Barabas, A., Dobslaff, K., Wiesner, J., Twyman, R.M., Zuchner, T., Sadd, B.M., Regoes, R.R., Schmid-Hempel, P., Vilcinskas, A., Insect antimicrobial peptides show potentiating functional interactions against Gram-negative bacteria. Proc. Biol. Sci., 282, 2015, 20150293.
67. Ramirez, J.L., de Almeida Oliveira, G., Calvo, E., Dalli, J., Colas, R.A., Serhan, C.N., Ribeiro, J.M., Barillas-Mury, C., A mosquito lipoxin/lipocalin complex mediates innate immune priming in Anopheles gambiae. Nat. Commun., 6, 2015, 7403.
68. Raymond, B., Wyres, K.L., Sheppard, S.K., Ellis, R.J., Bonsall, M.B., Environmental factors determining the epidemiology and population genetic structure of the Bacillus cereus group in the field. PLoS Pathog., 6, 2010, e1000905.
69. Rodrigues, J., Brayner, F.A., Alves, L.C., Dixit, R., Barillas-Mury, C., Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 329 (2010), 1353–1355.
70. Roth, O., Kurtz, J., The stimulation of immune defence accelerates development in the red flour beetle (Tribolium castaneum). J. Evol. Biol. 21 (2008), 1703–1710.
71. Roth, O., Kurtz, J., Phagocytosis mediates specificity in the immune defence of an invertebrate, the woodlouse Porcellio scaber (Crustacea: Isopoda). Dev. Comp. Immunol. 33 (2009), 1151–1155.
72. Roth, O., Sadd, B.M., Schmid-Hempel, P., Kurtz, J., Strain-specific priming of resistance in the red flour beetle, Tribolium castaneum. Proc. R. Soc. B 276 (2009), 145–151.
73. 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.
74. Sadd, B.M., Schmid-Hempel, P., Insect immunity shows specificity in protection upon secondary pathogen exposure. Curr. Biol. 16 (2006), 1206–1210.
75. Schmid-Hempel, P., Evolutionary Parasitology: The Integrated Study of Infections, Immunology. Ecology and Genetics, 2011, Oxford University Press, New York.
76. Schmid-Hempel, P., Ebert, D., On the evolutionary ecology of specific immune defence. Trends Ecol. Evol. 18 (2003), 27–32\.
77. Schmucker, D., Clemens, J.C., Shu, H., Worby, C.A., Xiao, J., Muda, M., Dixon, J.E., Zipursky, S.L., Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101 (2000), 671–684.
78. Schulenburg, H., Boehnisch, C., Michiels, N.K., How do invertebrates generate a highly specific innate immune response?. Mol. Immunol. 44 (2007), 3338–3344.
79. Sheldon, B.C., Verhulst, S., Ecological immunology—costly parasite defenses and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11 (1996), 317–321.
80. Shudo, E., Iwasa, Y., Inducible defense against pathogens and parasites: optimal choice among multiple options. J. Theor. Biol. 209 (2001), 233–247.
81. Tate, A.T., Graham, A.L., Trans-generational priming of resistance in wild flour beetles reflects the primed phenotypes of laboratory populations and is inhibited by co-infection with a common parasite. Funct. Ecol. 29 (2015), 1059–1069.
82. Tidbury, H.J., Pedersen, A.B., Boots, M., Within and transgenerational immune priming in an insect to a DNA virus. Proc. Biol. Sci. 278 (2011), 871–876.
83. Uttenweiler-Joseph, S., Moniatte, M., Lagueux, M., Van Dorsselaer, A., Hoffmann, J.A., Bulet, P., Differential display of peptides induced during the immune response of Drosophila: a matrix-assisted laser desorption ionization time-of-flight mass spectrometry study. Proc. Natl. Acad. Sci. USA 95 (1998), 11342–11347.
84. Vilcinskas, A., The role of epigenetics in host–parasite coevolution: lessons from the model host insects Galleria mellonella and Tribolium castaneum. Zoology 119 (2016), 273–280.
85. Vilcinskas, A., Mukherjee, K., Vogel, H., Expansion of the antimicrobial peptide repertoire in the invasive ladybird Harmonia axyridis. Proc. R. Soc. B, 280, 2012, 20122113.
86. Watson, F.L., Püttmann-Holgado, R., Thomas, F., Lamar, D.L., Hughes, M., Kondo, M., Rebel, V.I., Schmucker, D., Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 309 (2005), 1874–1878.
87. Watthanasurorot, A., Jiravanichpaisal, P., Liu, H., Söderhäll, I., Söderhäll, K., Bacteria-induced Dscam isoforms of the crustacean, Pacifastacus leniusculus. PLoS Pathog., 7, 2011, e1002062.
88. Wegner, K.M., Berenos, C., Schmid-Hempel, P., Host genetic architecture in single and multiple infections. J. Evol. Biol. 22 (2009), 396–404.
89. Witteveldt, J., Cifuentes, C.C., Vlak, J.M., van Hulten, M.C.W., Protection of Penaeus monodon against white spot syndrome virus by oral vaccination. J. Virol. 78 (2004), 2057–2061.
90. 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.
91. Wu, G., Yi, Y., Lv, Y., Li, M., Wang, J., Qiu, L., The lipopolysaccharide (LPS) of Photorhabdus luminescens TT01 can elicit dose- and time-dependent immune priming in Galleria mellonella larvae. J. Invertebr. Pathol. 127 (2015), 63–72.
92. Zanchi, C., Troussard, J.P., 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. 80 (2011), 1174–1183.
93. Zasloff, M., Antimicrobial peptides of multicellular organisms. Nature 415 (2002), 389–395.