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Insect Innate Immune Memory

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Advances in Comparative Immunology

Abstract

Recent years have seen a surge in studies on insect immune memory. Here we provide an overview of the current state of evidence for immune memory mechanisms in insects. This group of animals is very heterogeneous, and understanding of the molecular mechanisms behind immune memory remains fragmentary. We discuss the role of DNA synthesis and endoreplication as a basis for retaining information gathered from previous contacts with pathogens and novel mechanisms to confront different pathogenic challenges. Finally, we discuss the ecological perspective of insect immune memory.

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References

  • Barribeau SM, Schmid-Hempel P, Sadd BM (2016) Royal decree: gene expression in trans-generationally immune primed bumblebee workers mimics a primary immune response. PLoS One 11:e0159635

    PubMed  PubMed Central  Google Scholar 

  • Bolte S, Roth O, Philipp EE, Saphörster J, Rosenstiel P, Reusch TB (2013) Specific immune priming in the invasive ctenophore Mnemiopsis leidyi. Biol Lett 9:20130864

    PubMed  PubMed Central  Google Scholar 

  • Boman HG, Nilsson I, Rasmuson B (1972) Inducible antibacterial defence system in Drosophila. Nature 237:232–235

    CAS  PubMed  Google Scholar 

  • Buonocore F, Gerdol M (2016) Alternative adaptive immunity strategies: coelacanth, cod and shark immunity. Mol Immunol 69:157–169

    CAS  PubMed  Google Scholar 

  • BrehĂ©lin M, Roch P (2008) Specificity, learning and memory in the innate immune response. Inv Surv J 5:103–109

    Google Scholar 

  • Boraschi D, Italiani P (2018) Innate immune memory: time for adopting a correct terminology. Front Immunol 9:799

    PubMed  PubMed Central  Google Scholar 

  • Cadavid LF (2009) La evoluciĂłn de sistemas complejos: el caso del sistema inmune en animales. Acta Biol Colomb 14(S):247–254

    Google Scholar 

  • Castro-Vargas C, Linares-LĂłpez C, LĂłpez-Torres A, Wrobel K, Torres-Guzmán JC, Hernández GA, Wrobel K, Lanz-Mendoza H, Contreras-Garduño J (2017) Methylation on RNA: a potential mechanism related to immune priming within but not across generations. Front Microbiol 8:473

    PubMed  PubMed Central  Google Scholar 

  • Christofi T, Apidianakis Y (2013) Drosophila immune priming against Pseudomonas aeruginosa is short-lasting and depends on cellular and humoral immunity. F1000Research 2:1–13

    Google Scholar 

  • Cong M, Song L, Wang L, Zhao J, Qiu L, Li L, Zhang H (2008) The enhanced immune protection of Zhikong scallop Chlamys farreri on the secondary encounter with Listonella anguillarum. Comp Biochem Physiol B: Biochem Mol Biol 151(2):191–196

    Google Scholar 

  • Contreras-Garduño J, RodrĂ­guez MC, Hernández-MartĂ­nez S, MartĂ­nez-Barnetche J, Alvarado-Delgado A, Izquierdo J, Herrera-Ortiz A, Moreno-GarcĂ­a M, Velazquez-Meza ME, Valverde V, Argotte-Ramos R, RodrĂ­guez MH, Lanz-Mendoza H (2015) Plasmodium berghei induced priming in Anopheles albimanus independently of bacterial co-infection. Dev Comp Immunol 52:172–181

    PubMed  Google Scholar 

  • Cooper EL (1992) Overview of immunoevolution. Bolletino di Zoologia 59:119–128

    Google Scholar 

  • Cooper EL, Roch P (1986) Second-set allograft responses in the earthworm Lumbricus terrestris. Kinetics and characteristics. Transplantation 41:514–520

    CAS  PubMed  Google Scholar 

  • Cooper EL (2016) Commentary: blurring borders: innate immunity with adaptive features. Front Microbiol 7:358

    PubMed  PubMed Central  Google Scholar 

  • Chigasaki J (1925) Sur l’immunisation de Galleria aux differents stades de sa vie. Compt Rend Soc Biol 93:573–574

    Google Scholar 

  • Contreras-Garduño J, RodrĂ­guez MC, RodrĂ­gue MH, Alvarado-Delgado A, Lanz-Mendoza H (2014) Cost of immune priming within generations:trade-off between infection and reproduction. Mic Infec 16:261–267

    Google Scholar 

  • Contreras-Garduño J, Lanz-mendoza H, Franco B, Nava A, Pedraza-Reyes M, JorgecanaleS-Lazcano (2016) Insect immune priming: ecology and experimental evidences. Ecol Entomol 41(4):351–366

    Google Scholar 

  • Dhinaut J, Chogne M, Moret Y (2018) Immune priming specificity within and across generations reveals the range of pathogens affecting evolution of immunity in an insect. J Anim Ecol 87:448–463

    PubMed  Google Scholar 

  • Dubovskiy IM, Whitten MMA, Yaroslavtseva ON, Greig C, Kryukov VY, Kryukov VY, Grizanova EV, Mukherjee K, Vilcinskas A, Glupov VV (2013) Can insects develop resistance to insect pathogenic fungi? PLoS One 8:e60248

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dubuffet A, Zanchi C, Boutet G, Moreau J, Teixeira M, Moret Y (2015) Trans-generational immune priming protects the eggs only against gram-positive bacteria in the mealworm beetle. PLoS Pathog 11(10):e1005178

    PubMed  PubMed Central  Google Scholar 

  • Duneau D, Ebert D, Du Pasquier L (2016) Infections by Pasteuria do not protect its natural host Daphnia magna from subsequent infections. Dev Comp Immunol 57:120–125

    PubMed  Google Scholar 

  • Edgar BA, Zielke N, Gutierrez C (2014) Endocycles: a recurrent evolutionary innovation for pst-mitotic cell growth. Nat Rev Mol Cell Biol 15:197–210

    PubMed  Google Scholar 

  • Eggert H, Kurtz J, Diddens-de Buhr MF (2014) Different effects of paternal trans-generational immune priming on survival and immunity in step and genetic offspring. Proc R Soc B Biol Sci 281:20142089

    Google Scholar 

  • Eggert H, Diddens-de Buhr MF, Kurtz J (2015) A temperature shock can lead to trans-generational immune priming in the Red Flour Beetle, Tribolium castaneum. Ecol Evol 5:1318–1326

    PubMed  PubMed Central  Google Scholar 

  • Elrod-Erickson M, Mishra S, Schneider D (2000) Interactions between the cellular and humoral immune responses in Drosophila. Curr Biol 10:781–784

    CAS  PubMed  Google Scholar 

  • Faulhaber LM, Karp RD (1992) A diphasic immune response against bacteria in the American cockroach. Immunology 75:378–381

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fisher JJ, Hajek AE (2015) Maternal exposure of a beetle to pathogens protects offspring against fungal disease. PLoS One 10:e0125197

    PubMed  PubMed Central  Google Scholar 

  • Freitak D, Schmidtberg H, Dickel F, Lochnit G, Vogel H, Vilcinskas A (2014) The maternal transfer of bacteria can mediate trans-generational immune priming in insects. Virulence 5:547–554

    PubMed  PubMed Central  Google Scholar 

  • Futo M, Armitage SA, Kurtz J (2016) Microbiota plays a role in oral immune priming in Tribolium castaneum. Front Microbiol 6:1383

    PubMed  PubMed Central  Google Scholar 

  • Gálvez D, Chapuisat M (2014) Immune priming and pathogen resistance in ant queens. Ecol Evol 4(10):1761–1767

    PubMed  PubMed Central  Google Scholar 

  • Garbutt JS, O'Donoghue AJ, McTaggart SJ, Wilson PJ, Little TJ (2014) The development of pathogen resistance in Daphnia magna: implications for disease spread in age-structured populations. J Exp Biol 217:3929–3934

    PubMed  PubMed Central  Google Scholar 

  • Gomez HM, Rivas GA, Hernández-Quintero A, Hernández AG, Guzmán JCT, Mendoza HL, Contreras-Garduño J (2018) The occurrence of immune priming can be species-specific in entomopathogens. Microb Pathog 118:361–364

    Google Scholar 

  • Green TJ, Helbig K, Speck P, Raftos DA (2016) Primed for success: oyster parents treated with poly (I: C) produce offspring with enhanced protection against Ostreid herpesvirus type I infection. Mol Immunol 78:113–120

    CAS  PubMed  Google Scholar 

  • Greenwood JM, Milutinović B, PeuĂź R, Behrens S, Esser D, Rosenstiel P, Kennedy M, Kurtz J (2017) Oral immune priming with bacillus thuringiensis induces a shift in the gene expression of Tribolium castaneum larvae. BMC Genomics 18:329

    PubMed  PubMed Central  Google Scholar 

  • Hartman RS, Karp RD (1989) Short-term immunological memory in the allograft response of the american cockroach, Periplaneta americana. Transplantation 47:920–922

    CAS  PubMed  Google Scholar 

  • Hauton C, Smith VJ (2007) Adaptive immunity in invertebrates: a straw house without a mechanistic foundation. BioEssays 29:1138–1146

    CAS  PubMed  Google Scholar 

  • Hernández-LĂłpez J, Schuehly W, Crailsheim K, Riessberger-GallĂ© U (2014) Trans-generationalimmune priming in honeybees. Proc R Soc B Biol Sci 281:20140454

    Google Scholar 

  • Hernández-MartĂ­nez S, Román-MartĂ­nez U, MartĂ­nez-Bartneche J, RodrĂ­guez M, Lanz-Mendoza H (2006) Induction of DNA synthesis in Anopheles albimanus tissue cultures by Saccharomyces cerevisiae. Arch. Insect Biochem Physiol 63:147–158

    PubMed  Google Scholar 

  • Hernández-MartĂ­nez P, Naseri B, Navarro-Cerrillo G, Escriche B, FerrĂ© J, Herrero S Increase in midgut microbiota load induces an apparent immune priming and increases tolerance to Bacillus thuringiensis. Environ Microbiol:no–no

    Google Scholar 

  • Hildemann WH, Raison RL, Cheung G, Hull CJ, Akaka L, Okamoto J (1977) Immunological specificity and memory in a scleractinian coral. Nature 270:219–223

    CAS  PubMed  Google Scholar 

  • Herrin BR, Cooper MD (2010) Alternative adaptive immunity in jawless vertebrates. J Immunol 185:1367–1374

    CAS  PubMed  Google Scholar 

  • Heitmueller M, Billion A, Dobrindt U, Vilcinskas A, Mukherjee K (2017) Epigenetic mechanisms regulate innate immunity against uropathogenic and commensal-like Escherichia coli in the surrogate insect model Galleria mellonella. Infect Immun 85(10):e00336–e00317

    CAS  PubMed  PubMed Central  Google Scholar 

  • Karp RD (1990) Cell-mediated immunity in invertebrates. Bioscience 40:732–737

    Google Scholar 

  • Khan I, Prakash A, Agashe D (2016) Divergent immune priming responses across flour beetle life stages and populations. Ecol Evol 6:7847–7855

    PubMed  PubMed Central  Google Scholar 

  • Khan I, Prakash A, Agashe D (2017) Experimental evolution of insect immune memory versus pathogen resistance. Proc R Soc B 2017 284 20171583

    Google Scholar 

  • Kurtz J (2005) Specific memory within innate immune systems. Trends Immunol 26(4):186–192

    CAS  PubMed  Google Scholar 

  • Kurtz J, Armitage SA (2017) Dissecting the dynamics of trans-generational immune priming. Mol Ecol 26:3857–3859

    CAS  PubMed  Google Scholar 

  • Kurtz J, Franz K (2003) Innate defense: evidence for memory in invertebrate immunity. Nature 425:37–38

    CAS  PubMed  Google Scholar 

  • Lackie AM (1983) Immunological recognition of cuticular transplants in insects. Dev Comp Immunol 7:41–50

    CAS  PubMed  Google Scholar 

  • Lafont M, Petton B, Vergnes A, Pauletto M, Segarra A, Gourbal B, Montagnani C (2017) Long-lasting antiviral innate immune priming in the Lophotrochozoan Pacific oyster, Crassostrea gigas. Sci Rep 7:13143

    PubMed  PubMed Central  Google Scholar 

  • Lin YC, Chen JC, Morni WZ, Putra DF, Huang CL, Li CC, Hsieh JF (2013) Vaccination enhances early immune responses in white shrimp Litopenaeus vannamei after secondary exposure to Vibrio alginolyticus. PLoS One 8:e69722

    CAS  PubMed  PubMed Central  Google Scholar 

  • Little TJ, Colegrave N, Sadd BM, Schmid-Hempel P (2008) Studying immunity at the whole organism level. BioEssays 30(4):404–405

    PubMed  Google Scholar 

  • Little TJ, Kraaijeveld AR (2004) Ecological and evolutionary implications of immunological priming in invertebrates. Trends Ecol Evol 19:58–60

    PubMed  Google Scholar 

  • Little TJ, O’Connor B, Colegrave N, Watt K, Read AF (2003) Maternal transfer of strain-speci c immunity in an invertebrate. Curr Biol 13:489–492

    CAS  PubMed  Google Scholar 

  • Longdon B, Cao C, Martinez J, Jiggins FM (2013) Previous exposure to an RNA virus does not protect against subsequent infection in Drosophila melanogaster. PLoS One 8(9):e73833

    CAS  PubMed  PubMed Central  Google Scholar 

  • Masri L, Cremer S (2014) Individual and social immunisation in insects. Trends Immunol 35(10):471–482

    CAS  PubMed  Google Scholar 

  • McNamara KB, Lieshout E, Simmons LW (2014) The effect of maternal and paternal immune challenge on offspring immunity and reproduction in a cricket. J Evol Biol 27:1020–1028

    CAS  PubMed  Google Scholar 

  • McTaggart SJ, Wilson PJ, Little TJ (2012) Daphnia magna shows reduced infection upon secondary exposure to a pathogen. Biol Lett 8:972–975

    PubMed  PubMed Central  Google Scholar 

  • Metalnikow S (1920) ImmunitĂ© naturelle ou acquise des chenilles de Galleria mellonella. CR Acad Sci Paris 83:817–820

    Google Scholar 

  • Mikonranta L, Mappes J, Kaukoniitty M, Freitak D (2014) Insect immunity: oral exposure to a bacterial pathogen elicits free radical response and protects from a recurring infection. Front Zool 11:23

    PubMed  PubMed Central  Google Scholar 

  • Milutinovic B, Kurtz J (2016) Immune memory in invertebrates. Semin Immunol 28:328–342

    CAS  PubMed  Google Scholar 

  • Milutinović B, Fritzlar S, Kurtz J (2014) Increased survival in the red flour beetle after oral priming with bacteria-conditioned media. J Innate Immun 6:306–314

    PubMed  Google Scholar 

  • Miyashita A, Kizaki H, Kawasaki K, Sekimizu K, Kaito C (2014) Primed immune responses to gram-negative peptidoglycans confer infection resistance in silkworms. J Biol Chem 289:14412–14421

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moreno-GarcĂ­a M, Vargas V, RamĂ­rez-Bello I, Hernández-MartĂ­nez G, Lanz-Mendoza H (2015) Bacterial exposure at the larval stage induced sexual immune dimorphism and priming in adult Aedes aegypti mosquitoes. PLoS One 10(7):e0133240

    PubMed  PubMed Central  Google Scholar 

  • Moret Y (2006) Trans-generational immune priming: specific enhancement of the antimicrobial immune response in the mealworm beetle, Tenebrio molitor. Proc R Soc Lond Ser B 273:1399–1405

    CAS  Google Scholar 

  • Mukherjee K, Grizanova E, Chertkova E, Lehmann R, Dubovskiy I, Vilcinskas A (2017) Experimental evolution of resistance against in the insect model host results in epigenetic modifications. Virulence 8(8):1618–1630

    CAS  PubMed  PubMed Central  Google Scholar 

  • Netea MG, Quintin J, van der Meer JWM (2011) Trained immunity:a memory for innate host defense. Cell Host Microbe 9(5):355–361

    CAS  PubMed  Google Scholar 

  • Netea MG, van der Meer JW (2017) Trained immunity: an ancient way of remembering. Cell Host Microbe 21:297–300

    CAS  PubMed  Google Scholar 

  • Ng TH, Hung HY, Chiang YA, Lin JH, Chen YN, Chuang YC, Wang HC (2014) WSSV-induced crayfish Dscam shows durable immune behavior. Fish Shellfish Immunol 40:78–90

    CAS  PubMed  Google Scholar 

  • Norouzitallab P, Baruah K, Vandegehuchte M, Van Stappen G, Catania F, Bussche JV, Sorgeloos P, Bossier P (2014) Environmental heat stress induces epigenetic transgenerational inheritance of robustness in parthenogenetic Artemia model. FASEB J 28:3552–3563

    CAS  PubMed  Google Scholar 

  • Paust S, von Andrian UH (2011) Natural killer cell memory. Nat Immunol 12(6):500–508

    CAS  PubMed  Google Scholar 

  • Pham LN, Schneider DS (2008) Evidence for specificity and memory in the insect innate immune response. In: Beckage N (ed) Insect immunology. Elsevier AP, London, pp 120–121

    Google Scholar 

  • Pham LN, Dionne MS, Shirasu-Hiza M, Schneider DS (2007) A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog 3(3):e26. https://doi.org/10.1371/journal.ppat.0030026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pope EC, Powell A, Roberts EC, Shields RJ, Wardle R, Rowley AF (2011) Enhanced cellular immunity in shrimp (Litopenaeus vannamei) after vaccination. PLoS One 6:e20960

    CAS  PubMed  PubMed Central  Google Scholar 

  • Portela J, Duval D, Rognon A, Galinier R, Boissier J, Coustau C, Mitta G, ThĂ©ron A, Gourbal B (2013) Evidence for specific genotype-dependet immune priming in the Lophotrochozoan Biomphalaria glabrata snail. J Innate Immun 5:261–276

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pradeu T, Du Pasquier L (2018) Immunological memory: What’s in a name? Immunol Rev 283:7–20

    CAS  PubMed  Google Scholar 

  • Ramirez J, Garver LS, Brayner FA, Alves LC, Rodrigues J, Molina-Cruz A et al (2014) The role of hemocytes in Anopheles gambiae antiplasmodial immunity. J Innate Immun 6:119–128

    CAS  PubMed  Google Scholar 

  • Ramirez JL, de Almeida Oliveira G, Calvo E, Dalli J, Colas RA, Serhan CN (2015) A mosquito lipoxin/lipocalin complex mediates innate immune priming in Anopheles gambiae. Nat Commun 6:7403

    CAS  PubMed  Google Scholar 

  • Reber A, Chapuisat M (2012) No evidence for immune priming in ants exposed to a fungal pathogen. PLoS One 7:e35372

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rodrigues J, Brayner FA, Alves LC, Dixit R, Barillas-Mury C (2010) Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 329:1353–1355

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rosengaus RB, Malak T, MacKintosh C (2013) Immune-priming in ant larvae: social immunity does not undermine individual immunity. Biol Lett 9:20130563

    PubMed  PubMed Central  Google Scholar 

  • Roth O, Sadd BM, Schmid-Hempel P, Kurtz J (2009) Strain-specific immune priming in the red flour beetle, Tribolium castaneum. Proc R Soc Lond Ser B 276:145–151

    Google Scholar 

  • 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. J Anim Ecol 79(2):403–413

    PubMed  Google Scholar 

  • Ruppert EE, Barnes RD (1996) ZoologĂ­a de los invertebrados. McGraw Hill-Interamericana. 6a ediciĂłn. p 2

    Google Scholar 

  • Sadd BM, Schmid-Hempel P (2006) Insect immunity shows specificity in protection upon secondary pathogen exposure. Curr Biol 16:1206–1210

    CAS  PubMed  Google Scholar 

  • Sadd BM, Schmid-Hempel P (2009a) Ecological and evolutionary implications of specific immune responses. In: Rolff J, Reynolds SE (eds) Insect infection and immunity. Evolution, ecology and mechanism. Oxford University Press, Oxford, UK

    Google Scholar 

  • Sadd BM, Schmid-Hempel P (2009b) A distinct infection cost associated with trans-generational priming of antibacterial immunity in bumble-bees. Biol Lett 5:798–801

    PubMed  PubMed Central  Google Scholar 

  • Schmid-Hempel P (2011) Evolutionary parasitology. Oxford University Press, Oxford, UK

    Google Scholar 

  • Serrato-Salas J, Hernández-MartĂ­nez S, Martinez-Barnetche J, Conde R, Alvarado-Delgado A, Zumaya-Estrada F, Lanz-Mendoza H (2018a) De novo DNA synthesis in Aedes aegypti midgut cells as complementary strategy to limitit Dengue viral replication. Front Microbiol 9:801

    Google Scholar 

  • Serrato-Salas S, Izquierdo-Sánchez J, ArgĂĽello M, Conde R, Alvarado-Delgado A, Lanz-Mendoza H (2018b) Aedes aegypti antiviral adaptive response against DENV-2. Dev Comp Immunol 84:28–36

    CAS  Google Scholar 

  • Shi ZH, Lin YT, Hou YM (2014) Mother-derived trans-generational immune priming in the red palm weevil, Rhynchophorus ferrugineus Olivier (Coleoptera, Dryophthoridae). Bull Entomol Res 104:742–750

    CAS  PubMed  Google Scholar 

  • Shikano I, Hua KN, Cory JS (2016) Baculovirus-challenge and poor nutrition inflict within-generation fitness costs without triggering transgenerational immune priming. J Invertebr Pathol 136:35–42

    PubMed  Google Scholar 

  • Sun JC, Beilke JN, Lanier LL (2009) Adaptive immune features of natural killer cells. Nature 457(7229):557–561

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun J, Deng W-M (2007) Hindsight mediates the role of notch in suppressing hedgehog signaling and cell proliferation. Dev Cell 12:431–442

    CAS  PubMed  PubMed Central  Google Scholar 

  • Spoel SH, Dong X (2012) How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol 12(2):89–100

    CAS  PubMed  Google Scholar 

  • Tassetto M, Kunitomi M, Andino R (2017) Circulating immune cells mediate a systemic RNAi-based adaptive antiviral response in Drosophila. Cell 169:314–325

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tate AT, Graham AL (2015) 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 29:1059–1069

    Google Scholar 

  • Tate AT, Rudolf VHW (2012) Immune priming across life stages and generations: implications for infectious disease dynamics in insects. Oikos 121:1083–1092

    Google Scholar 

  • Tate AT, Andolfatto P, Demuth JP, Graham AL (2017) The within-host dynamics of infection in trans-generationally primed flour beetles. Mol Ecol 26(14):3794–3807

    CAS  PubMed  PubMed Central  Google Scholar 

  • Theopold U, Ekengren S, Hultmark D (1996) HLH106, a Drosophila transcription factor with similarity to the vertebrate sterol responsive element binding protein. PNAS 93:1195–1199

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas AM, Rudolf VH (2010) Challenges of metamorphosis in invertebrate hosts: maintaining parasite resistance across life-history stages. Ecol Entomol 35:200–205

    Google Scholar 

  • Tidbury HJ, Pedersen AB, Boots M (2011) Within and transgenerational immune priming in an insect to a DNA virus. Proc R Soc Lond Ser B 278:871–876

    Google Scholar 

  • Valdez A, Yepiz-Plascencia G, Ricca E, Olmos J (2014) First Litopenaeus vannamei WSSV 100% oral vaccination protection using CotC::Vp26 fusion protein displayed on Bacillus subtilis spores surface. J Appl Microbiol 117:347–357

    CAS  PubMed  Google Scholar 

  • Vantaux A, DabirĂ© KR, Cohuet A, Lefèvre T (2014) A heavy legacy: offspring of malaria-infected mosquitoes show reduced disease resistance. Malar J 13:442

    PubMed  PubMed Central  Google Scholar 

  • Vargas V, Moreno-GarcĂ­a M, Duarte-Elguea E, Lanz-Mendoza H (2016) Limited specificity in the injury and infection priming against bacteria in Aedes aegypti mosquitoes. Front Microbiol 7:975

    Google Scholar 

  • Vorburger C, Gegenschatz SE, Ranieri G, Rodriguez P (2008) Limited scope for maternal effects in aphid defence against parasitoids. Ecol Entomol 33(2):189–196

    Google Scholar 

  • Wilson K, Graham RI (2015) Transgenerational effects modulate density-dependent prophylactic resistance to viral infection in a lepidopteran pest. Biol Lett 11:20150012

    PubMed  PubMed Central  Google Scholar 

  • Witteveldt J, Cifuentes CC, Vlak JM, van Hulten MCW (2004) Protection of Penaeus monodon against white spot syndrome virus by oral vaccination. J Virol 78:2057–2061

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu G, Zhao Z, Liu C, Qiu L (2014) Priming Galleria mellonella (Lepidoptera: Pyralidae) larvae with heat-killed bacterial cells induced an enhanced immune protection against Photorhabdus luminescens TT01 and the role of innate immunity in the process. J Econ Entomol 107:559–569

    PubMed  Google Scholar 

  • Wu G, Xu L, Yi Y (2016) Galleria mellonella larvae are capable of sensing the extent of priming agent and mounting proportionatal cellular and humoral immune responses. Immunol Lett 174:45–52

    CAS  PubMed  Google Scholar 

  • Wu G, Li M, Liu Y, Ding Y and Yi Y (2015a) The specificity of immune priming in silkworm, Bombyx mori, is mediated by the phagocytic ability of granular cells. J Insect Physiol 81: 60–68

    CAS  PubMed  Google Scholar 

  • Wu G, Yi Y, Sun J, Li M, Qiu L (2015b) No evidence for priming response in Galleria mellonella larvae exposed to toxin protein PirA 2 B 2 from Photorhabdus luminescens TT01: an association with the inhibition of the host cellular immunity. Vaccine 33:6307–6313

    CAS  PubMed  Google Scholar 

  • Wu G, Yi Y, Lv Y, Li M, Wang J, Qiu L (2015c) The lipopolysaccharide (LPS) of Photorhabdus luminescens TT01 can elicit dose-and time-dependent immune priming in Galleria mellonella larvae. J Invertebr Pathol 127:63–72

    CAS  PubMed  Google Scholar 

  • Yue F, Zhou Z, Wang L, Ma Z, Wang J, Wang M, Zhang H, Song L (2013) Maternal transfer of immunity in scallop Chlamys farreri and its trans-generational immune protection to offspring against bacterial challenge. Dev Comp Immunol 41:569–577

    CAS  PubMed  Google Scholar 

  • Zhang T, Qiu L, Sun Z, Wang L, Zhou Z, Liu R, Yue F, Sun R, Song L (2014) The specifically enhanced cellular immune responses in Pacific oyster (Crassostrea gigas) against secondary challenge with Vibrio splendidus. Dev Comp Immunol 45(1):141–150

    CAS  PubMed  Google Scholar 

  • Zhao Z, Wu G, Wang J, Liu C, Qiu L (2013) Next-generation sequencing-based transcriptome analysis of Helicoverpa armigera larvae immune-primed with Photorhabdus luminescens TT01. PLoS One 8:e80146

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

To Prof. Edwin L. Cooper for his kind invitation. One anonymous reviewer and E. Cooper provided substantial comments that improved somewhat initially this chapter. JCG received grants from CONACYT (Laboratorios nacionales 2017-280505) and UNAM (PAPIT IA205318).

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Correspondence to Humberto Lanz-Mendoza .

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Glossary: Key Definitions Regarding Immune Priming Theory

Priming:

A challenge that activates the immune response and that may favor host molecule recognition.

Immune priming:

Host-improved protection in terms of immune response, parasite elimination, and survival after been able to respond to a parasite, pathogen, or immune challenge following a first specific exposure; recognized within and across generations.

Immune enhancement or enhanced protection:

A condition where an immune response is activated by artificial methods such as adding probiotics or exposure to nonharming immune-stimulant molecules, rendering an immune response over the physiological levels or keeping pathogens at bay (microbiota effect on many pathogens) but without exhibiting specificity and memory. This may occur within and across generations, and the protection against a second challenge after a first challenge could be due to a sustained immune response or an unspecific biphasic response.

Specificity:

In invertebrate biology, it is difficult to determine specificity against an epitope of a given antigen. However, many molecules recognize molecular patterns such as Scavenger receptors, Toll-like receptors, and Nod-like receptors (NLRs), which bind and transduce specific signals to molecules present in pathogens without exhibiting high specificity as vertebrate immunoglobulins. At a functional level, immune protection should occur, for example, in homologous (similar) challenges with the same parasite or pathogen species or strains rather than in heterologous (dissimilar) challenges. This means that the secondary response should only be elicited by homologous challenges or should be stronger and faster than heterologous challenges.

Nonspecific immune response:

Humoral and cellular responses not directly linked to a given pathogen’s structure. For example, a first challenge with a fungus may protect against Gram-positive bacteria, nematodes, or yeasts.

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Lanz-Mendoza, H., Garduño, J.C. (2018). Insect Innate Immune Memory. In: Cooper, E. (eds) Advances in Comparative Immunology. Springer, Cham. https://doi.org/10.1007/978-3-319-76768-0_9

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