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Using Insects as Models of Immunosenescence

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Handbook of Immunosenescence
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Abstract

Most organisms exhibit physiological decline with advancing age and understanding the causes of this decline is a fundamental goal of aging research. Insect models have been a key model for understanding the general process of aging (Hughes and Reynolds (Annu Rev Entomol 50:421–445, 2005); Lee et al. (Entomol Res 45:1–8, 2015)) although most studies to date have focused on understanding factors regulating life span. However, there is growing awareness that understanding the physiological and genetic basis of age-related decline in traits that influence healthspan (e.g., locomotion, and the immune response to infection) will provide new insight into the process of senescence. This chapter updates my previous review (Leips 2009) on the use of insects as models of immunosenescence. In preparing this update it became clear that while insects have provided insights into the causes of immunosenescence, they have yet to be fully exploited in this area. The hope is that by highlighting particular areas where insects have advanced our knowledge of immunosenescence, it will stimulate greater use of insects to address questions for which they are particularly well-suited.

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References

  • Abrams ET, Miller EM (2011) The roles of the immune system in women’s reproduction: evolutionary constraints and life history trade-offs. Yearb Phys Anthropol 54:134–154

    Google Scholar 

  • Acerenza L (2016) Constraints, trade-offs and the currency of fitness. J Mol Evol 82:117–127

    Article  CAS  PubMed  Google Scholar 

  • Adamo SA, Jensen M, Younger M (2001) Changes in lifetime immunocompetence in male and female Gryllus texensis (formerly G-integer): trade-offs between immunity and reproduction. Anim Behav 62:417–425

    Article  Google Scholar 

  • Adamo SA, Roberts JL, Easy RH, Ross NW (2008) Competition between immune function and lipid transport for the protein apolipophorin III leads to stress-induced immunosuppression in crickets. J Exp Biol 211:531–538

    Article  CAS  PubMed  Google Scholar 

  • Agaisse H, Petersen U, Boutros M, Mathey-Prevot B, Perrimon N (2003) Signaling role of hemocytes in Drosophila JAK/STAT-dependent response to septic injury. Dev Cell 5:441–450

    Article  CAS  PubMed  Google Scholar 

  • Agrawal A, Agrawal S, Cao JN, Su HF, Osann K, Gupta S (2007) Altered innate immune functioning of dendritic cells in elderly humans: a role of phosphoinositide 3-kinase-signaling pathway. J Immunol 178:6912–6922

    Article  CAS  PubMed  Google Scholar 

  • Alonso-Alvarez C, Bertrand S, Devevey G, Gaillard M, Prost J, Faivre B, Sorci G (2004) An experimental test of the dose-dependent effect of carotenoids and immune activation on sexual signals and antioxidant activity. Am Nat 164:651–65

    PubMed  Google Scholar 

  • Amrit FRG, Boehnisch CM, May RC (2010) Phenotypic covariance of longevity, immunity and stress resistance in the Caenorhabditis nematodes. PLoS One 5:e9978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arefin B, Kucerova L, Dobes P et al (2014) Genome-wide transcriptional analysis of Drosophila larvae infected by entomopathogenic nematodes shows involvement of complement, recognition and extracellular matrix proteins. J Innate Immun 6(2):192–204

    Article  CAS  PubMed  Google Scholar 

  • Barillas-Mury C, Han YS, Seeley D, Kafatos FC (1999) Anopheles gambiae Ag-STAT, a new insect member of the STAT family, is activated in response to bacterial infection. EMBO J 18:959–967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barrickman NL (2016) The ontogeny of encephalization: tradeoffs between brain growth, somatic growth, and life history in Hominoids and Platyrrhines. Evol Biol 43:81–95

    Article  Google Scholar 

  • Bleu J, Gamelon M, Bernt-Erik S (2016) Reproductive costs in terrestrial male vertebrates: insights from bird studies. Proc R Soc Lond B Biol Sci 283:Article: 20152600

    Article  CAS  Google Scholar 

  • Bond D, Foley E (2009) A quantitative RNAi screen for JNK modifiers identifies Pvr as a novel regulator of Drosophila immune signaling. PloS Pathog 5(11):e1000655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boulais J, Trost M, Landry CR, Diekmann R, Levy ED, Soldati T, Michnick SW, Thibault P, Desjardins M (2010) Molecular characterization of the evolution of phagosomes. Mol Syst Biol 6:423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brennan CA, Anderson KV (2004) Drosophila: the genetics of innate immune recognition and response. Annu Rev Immunol 22:457–483

    Article  CAS  PubMed  Google Scholar 

  • Brock PM, Murdock CC, Martin LB (2014) The history of ecoimmunology and its integration with disease ecology. Integr Comp Biol 54:353–362

    Article  PubMed  PubMed Central  Google Scholar 

  • Buchon N, Silverman N, Cherry S (2014) Immunity in Drosophila melanogaster – from microbial recognition to whole-organism physiology. Nat Rev Immunol 14:796–810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carroll MC, Prodeus AP (1998) Linkages of innate and adaptive immunity. Curr Opin Immunol 10:36–40

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth B (1994) Evolution in age-structured populations. Cambridge University Press, Cambridge [u.a.]

    Book  Google Scholar 

  • Cho I, Horn L, Felix TM, Foster L, Gregory G, Starz-Gaiano M, Chambers MM, De Luca M, Leips J (2010) Age- and diet-specific effects of variation at S6 kinase on life history, metabolic and immune response traits in Drosophila melanogaster. DNA Cell Biol 29:473–485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christophides GK, Zdobnov E, Barillas-Mury C et al (2002) Immunity-related genes and gene families in Anopheles gambiae. Science 298:159–165

    Article  CAS  PubMed  Google Scholar 

  • Cipriano C, Caruso C, Lio D, Giacconi R, Malavolta M, Muti E, Gasparini N, Franceschi C, Mocchegiani E (2005) The -308G/A polymorphism of TNF-alpha influences immunological parameters in old subjects affected by infectious diseases. Int J Immunogenet 32:13–18

    Article  CAS  PubMed  Google Scholar 

  • Clark R, Kupper T (2005) Old meets new: the interaction between innate and adaptive immunity. J Invest Dermatol 125:629–637

    Article  CAS  PubMed  Google Scholar 

  • Clark RI, Woodcock KJ, Geissmann F, Trouillet C, Dionne MS (2011) Multiple TGF-β superfamily signals modulate the adult Drosophila immune response. Curr Biol 21:1672–1677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cogni R, Cao C, Day JP, Bridson C, Jiggins FM (2016) The genetic architecture of resistance to virus infection in Drosophila. Mol Ecol 25:5228–5241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Cronin SJ, Nehme NT, Limmer S, Liegeois S, Pospisilik JA, Schramek D, Leibbrandt A, Simoes RD, Gruber S, Puc U, Ebersberger I, Zoranovic T, Neely GG, von Haeseler A, Ferrandon D, Penninger JM (2009) Genome-wide RNAi screen identifies genes involved in intestinal pathogenic bacterial infection. Science 325:340–343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davis MM, Engström Y (2012) Immune response in the barrier epithelia: lessons from the fruit fly Drosophila melanogaster. J Innate Immun 4:273–283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delaney JR, Stoven S, Uvell H, Anderson KV, Engstrom Y, Mlodzik M (2006) Cooperative control of Drosophila immune responses by the JNK and NF-kappa B signaling pathways. Embo J 25:3068–3077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delmastro-Greenwood MM, Piganelli JD (2013) Changing the energy of an immune response. Am J Clin Exp Immunol 2:30–54

    PubMed  PubMed Central  Google Scholar 

  • Dostert C, Jouanguy E, Irving P, Troxler L, Galiana-Arnoux D, Hetru C, Hoffmann JA, Imler JL (2005) The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of Drosophila. Nat Immunol 6:946–953

    Article  CAS  PubMed  Google Scholar 

  • Doums C, Moret Y, Benelli E, Schmid-Hempel P (2002) Senescence of immune defence in Bombus workers. Ecol Entomol 27:138–144

    Article  Google Scholar 

  • Durham MF, Magwire MM, Stone EA, Leips J (2014) Genome-wide analysis in Drosophila reveals age-specific effects of SNPs on fitness traits. Nat Commun 5:4338

    Article  CAS  PubMed  Google Scholar 

  • Ekengren S, Tryselius Y, Dushay MS, Liu G, Steiner H, Hultmark D (2001) A humoral stress response in Drosophila. Curr Biol 11:714–718

    Article  CAS  PubMed  Google Scholar 

  • Eleftherianos I, Castillo JC, Patrnogic J (2016) TGF-beta signaling regulates resistance to parasitic nematode infection in Drosophila melanogaster. Immunobiology 221:1362–1368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erler S, Popp M, Lattorff HMG (2011) Dynamics of immune system gene expression upon bacterial challenge and wounding in a social insect (Bombus terrestris). PLoS One 6:e18126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Felix TM, Hughes KA, Stone EA, Drnevich JM, Leips J (2012) Age-specific variation in immune response in Drosophila melanogaster has a genetic basis. Genetics 191:989–1002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fisher JJ, Hajek AE (2016) Influence of mating and age on susceptibility of the beetle Anoplophora glabripennis to the fungal pathogen Metarhizium brunneum. J Invertebr Pathol 136:142–148

    Article  PubMed  Google Scholar 

  • French SS, DeNardo DF, Moore MC (2007) Trade-offs between the reproductive and immune systems: facultative responses to resources or obligate responses to reproduction? Am Nat 170:79–89

    PubMed  Google Scholar 

  • Fulop T, Franceschi C, Hirokawa K, Pawalec G (2009) Handook of immunosenescence: basic understanding and clinical applications. Springer

    Google Scholar 

  • Gallo RL, Hopper LV (2012) Epithelial antimicrobial defence of the skin and intestine. Nat Rev Immunol 12:503–516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ganz T (2003) Defensins: antimicrobial peptides of innate immunity. Nat Rev Immunol 3:710–720

    Article  CAS  PubMed  Google Scholar 

  • Geng T, Lv DD, Huang XY, Hou CX, Qin GX, Guo XJ (2016) JAK/STAT signaling pathway-mediated immune response in silkworm (Bombyx mori) challenged by Beauveria bassiana. Gene 595:69–76

    Article  CAS  PubMed  Google Scholar 

  • Gilmore TD, Wolenski FS (2012) NF-kappa B: where did it come from and why? Immunol Rev 246:14–35

    Article  CAS  PubMed  Google Scholar 

  • González-Santoyo I, Córdoba-Aguilar A (2012) Phenoloxidase: a key component of the insect immune system. Entomol Exp Appl 142:1–16

    Article  CAS  Google Scholar 

  • Haine ER, Moret Y, Siva-Jothy MT, Rolff J (2008) Antimicrobial defense and persistent infection in insects. Science 322:1257–1259

    Article  CAS  PubMed  Google Scholar 

  • Harder J, Bartels J, Christophers E, Schroder JM (1997) A peptide antibiotic from human skin. Nature 387:861–861

    Article  CAS  PubMed  Google Scholar 

  • Harris C, Lambrechts L, Rousset F (2010) Polymorphisms in Anopheles gambiae immune genes associated with natural Resistance to Plasmodium falciparum. PLoS Pathog 6:e1001112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Helle S, Lummaa V, Jokela J (2004) Accelerated immunosenescence in preindustrial twin mothers. Proc Natl Acad Sci 101:12391–12396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hillyer JF (2016) Insect immunology and hematopoiesis. Dev Comp Immunol 58:102–118

    Article  CAS  PubMed  Google Scholar 

  • Hillyer JF, Schmidt SL, Fuchs JF, Boyle JP, Christensen BM (2005) Age-associated mortality in immune challenged mosoquitos Aedes aegypti correlates with a decrease in haemocyte numbers. Cell Microbiol 7:39–51

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann JA, Reichhart JM (2002) Drosophila innate immunity: an evolutionary perspective. Nat Immun 3:121–126

    Article  CAS  Google Scholar 

  • Hoffmann JA, Kafatos FC, Janeway CA, Ezekowitz RAB (1999) Phylogenetic perspectives in innate immunity. Science 284:1313–1318

    Article  CAS  PubMed  Google Scholar 

  • Horn L, Leips J, Starz-Gaiano M (2014) Phagocytic ability declines with age in adult Drosophila hemocytes. Aging Cell 13:719–728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsu H, Zhang H, Li L, Yi N, Yang P, Wu Q, Zhou J, Sun S, Xu X, Yang X, Lu L, Van Zant G, Williams RW, Allison DB, Mountz JD (2003) Age-related thymic involution in C57BL/6J x DBA/2J recombinant-inbred mice maps to mouse chromosomes 9 and 10. Genes Immun 4:402–410

    Article  CAS  PubMed  Google Scholar 

  • Hughes KA, Reynolds RM (2005) Evolutionary and mechanistic theories of aging. Annu Rev Entomol 50:421–445

    Article  CAS  PubMed  Google Scholar 

  • Hughes KA (2010) Mutation and the evolution of ageing: from biometrics to system genetics. Philos Trans R Soc B 365:1273–1279

    Article  Google Scholar 

  • Hughes KA, Leips J (2016) Pleiotropy, constraint, and modularity in the evolution of life histories: insights from genomic analyses. Ann N Y Acad Sci 1389:76–91

    Article  PubMed  PubMed Central  Google Scholar 

  • Irazoqui JE, Urbach JM, Ausubel FM (2010) Evolution of host innate defence: insights from C. elegans and primitive invertebrates. Nat Rev Immunol 10:47–58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jackson A, Galecki A, Burke D, Miller R (2003) Genetic polymorphisms in mouse genes regulating age-sensitive and age-stable T cell subsets. Genes Immun 4:30–39

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang H, Patel PH, Kohlmaier A, Grenley MO, McEwen DG, Edgar BA (2009) Cytokine/JAK/STAT signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell 137:1343–1355

    Article  PubMed  PubMed Central  Google Scholar 

  • Kemp C, Mueller S, Goto A, Barbier V, Paro S, Bonnay F, Dostert C, Troxler L, Hetru C, Meignin C, Pfeffer S, Hoffmann JA, Imler JL (2013) Broad RNA interference-mediated antiviral immunity and virus-specific inducible responses in Drosophila. J Immunol 190:650–658

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Khan I, Prakash A, Agashe D (2016b) Immunosenescence and the ability to survive bacterial infection in the red flour beetle Tribolium castaneum. J Anim Ecol 85:291–301

    Article  PubMed  Google Scholar 

  • Khush RS, Leulier F, Lemaitre B (2001) Drosophila immunity: two paths to NFĸB (2001). Trends in Immunol 22:260–264

    Article  CAS  Google Scholar 

  • King JG, Hillyer JF (2013) Spatial and temporal in vivo analysis of circulating and sessile immune cells in mosquitoes: hemocyte mitosis following infection. BMC Biol 11:55

    Article  PubMed  PubMed Central  Google Scholar 

  • Klasing KC (2004) The costs of immunity. Acta Zool Sin 50:961–969

    CAS  Google Scholar 

  • Klein SL, Nelson RJ (1998) Adaptive immune responses are linked to the mating system of arvicoline rodents. Am Nat 151:59–67

    Article  CAS  PubMed  Google Scholar 

  • Kurz CL, Tan M-W (2004) Regulation of aging and innate immunity in C. elegans. Aging Cell 3:185–193

    Article  CAS  PubMed  Google Scholar 

  • Lamiable O, Imler J-L (2014) Induced antiviral innate immunity in Drosophila. Curr Opin Microbiol 20:62–68

    Article  CAS  PubMed  Google Scholar 

  • Lazzaro BP, Sceurman BK, Clark AG (2004) Genetic basis of natural variation in D. melanogaster antibacterial immunity. Science 303:1873–1876

    Article  CAS  PubMed  Google Scholar 

  • Lee HY, Lee SH, Min KJ (2015) Insects as a model system for aging studies. Entomol Res 45:1–8

    Article  Google Scholar 

  • Leips J (2009) Insect models of immunosenescence. In: Folup T, Franceschi C, Hirokawa K, Pawalec G (eds) Handbook on immunosenescence. Springer, New York, pp 87–105

    Chapter  Google Scholar 

  • Lemaitre B, Hoffmann J (2007) The host defense of Drosophila melanogaster. Annu Rev Immunol 25:697–743

    Article  CAS  PubMed  Google Scholar 

  • Lesser KJ, Paiusi IC, Leips J (2006) Naturally occurring genetic variation in the age-specific immune response of Drosophila melanogaster. Aging Cell 5:293–295

    Article  CAS  PubMed  Google Scholar 

  • Libert S, Chao YF, Chu, XW, Pletcher SD (2006) Trade-offs between longevity and pathogen resistance in Drosophila melanogaster are mediated by NF kappa B signaling. Aging Cell 5:533–543

    Article  CAS  PubMed  Google Scholar 

  • Lord JM, Butcher S, Kllampali V, Lascelles D, Salmon M (2001) Neutrophil ageing and immunesenescence. Mech Ageing Dev 122:1521–1535

    Article  CAS  PubMed  Google Scholar 

  • Mackenzie DK, Bussiere LF, Tinsley MC (2011) Senescence of the cellular immune response in Drosophila melanogaster. Exp Gerontol 46:853–859

    Article  CAS  PubMed  Google Scholar 

  • Magwire MM, Fabian DK, Schweyen H, Cao C, Longdon B, Bayer F, Jiggins FM (2012) Genome-wide association studies reveal a simple genetic basis of resistance to naturally coevolving viruses in Drosophila melanogaster. PLoS Genet 8:e1003057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin LB, Scheuerlein A, Wikelski M (2003) Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proc R Soc B Biol Sci 270:153–158

    Article  Google Scholar 

  • McNamara KB, van Lieshout E, Jones TM, Simmons LW (2013) Age-dependent trade-offs between immunity and male, but not female, reproduction. J Anim Ecol 82:235–244

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Minakhina S, Steward R (2006) Nucleaer factor-kappa B-pathways in Drosophila. Oncogene 25:6749–6757

    Article  CAS  PubMed  Google Scholar 

  • Moret Y, Moreau J (2012) The immune role of the arthropod exoskeleton. Invertebr Surviv J 9:200–206

    Google Scholar 

  • Myllymaki H, Valanne S, Ramet M (2014) The Drosophila Imd signaling pathway. J Immunol 192:3455–3462

    Article  CAS  PubMed  Google Scholar 

  • Nizet V, Ohtake T, Lauth X, Trowbridge J, Rudisill J, Dorschner RA, Pestonjamasp V, Piraino J, Huttner K, Gallo RL (2001) Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature 414:454–457

    Article  CAS  PubMed  Google Scholar 

  • Paradkar PN, Trinidad L, Voysey R, Duchemin J-B, Walker PJ (2012) Secreted Vago restricts West Nile virus infection in Culex mosquito cells by activating the Jak–STAT pathway. Proc Natl Acad Sci USA 109:18915–18920

    Article  PubMed  PubMed Central  Google Scholar 

  • Park Y, Stanley D (2015) Physiological trade-off between cellular immunity and flight capability in the wing-dimorphic sand cricket, Gryllus firmus. J Asia-Pacific Entomol 18:553–559

    Article  CAS  Google Scholar 

  • Parsons B, Foley E (2016) Cellular immune defenses of Drosophila melanogaster. Dev Comp Immunol 58:95–101

    Article  CAS  PubMed  Google Scholar 

  • Pereira BI, Akbar AN (2016) Convergence of innate and adaptive immunity during human aging. Front Immunol 7:445

    PubMed  PubMed Central  Google Scholar 

  • Plowden J, Renshaw-Hoelscher M, Engleman C, Katz J, Sabhara S (2004) Innate immunity in aging: impact on macrophage function. Aging Cell 3:161–167

    Article  CAS  PubMed  Google Scholar 

  • Ponnappan U, Cinader B, Gerber V, Blaser K (1992) Polymorphism of age-related changes in the antibody response to the hapten phosphorylcholine. Immunol Investig 21:637–648

    Article  CAS  Google Scholar 

  • Rämet M, Lanot R, Zachary D, Manfruelli P (2002) JNK signaling pathway is required for efficient wound healing in Drosophila. Dev Biol 241:145–156

    Article  CAS  PubMed  Google Scholar 

  • Rauw WM (2012) Immune response from a resource allocation perspective. Front Genet 3:267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roberts KE, Hughes OH (2014) Immunosenescence and resistance to parasite infection in the honey bee, Apis mellifera. J Invertebr Pathol 121:1–6

    Article  CAS  PubMed  Google Scholar 

  • Rodel HG, Zapka M, Stefanski V, von Holst D (2016) Reproductive effort alters immune parameters measured post-partum in European rabbits under semi-natural conditions. Funct Ecol 30:1800–1809

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez-Carrio J, Alperi-Lopez M, Lopez P, Alonso-Castro S, Ballina-Garcia FJ, Suarez A (2015) TNF alpha polymorphism as marker of immunosenescence for rheumatoid arthritis patients. Exp Gerontol 61:123–129

    Article  CAS  PubMed  Google Scholar 

  • Sackton TB, Lazzaro BP, Clark AG (2010) Genotype and gene expression associations with immune function in Drosophila. PLoS Genet 6:e1000797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Schauber J, Gallo RL (2008) Antimicrobial peptides and the skin immune system. J Allergy Clin Immunol 122:261–266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwenke RA, Lazzaro BP, Wolfner MF (2016) Reproduction-immunity trade-offs in insects. Annu Rev Entomol 61:239–256

    Article  CAS  PubMed  Google Scholar 

  • Sen GC (2001) Viruses and interferons. Annu Rev Microbiol 55:255–281

    Article  CAS  PubMed  Google Scholar 

  • Shanley DP, Aw D, Manley NR et al (2009) An evolutionary perspective on the mechanisms of immunosenescence. Trends Immunol 30:374–381

    Article  CAS  PubMed  Google Scholar 

  • Shaw AC, Goldstein DR, Montgomery RR (2013) Age-dependent dysregulation of innate immunity. Nat Rev Immunol 13:875–887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321

    Article  CAS  PubMed  Google Scholar 

  • Smolinska S, O’Mahony L (2016) Microbiome-host immune system interactions. Semin Liver Dis 36:317–326

    Article  CAS  PubMed  Google Scholar 

  • Solana R, Tarazona R, Gayoso I, Lesur O, Dupuis G, Fulop T (2012) Innate immunosenescence: effect of aging on cells and receptors of the innate immune system in humans. Semin Immunol 24:331–341

    Article  CAS  PubMed  Google Scholar 

  • Souza-Neto JA, Sim S, Dimopoulos G (2009) An evolutionary conserved function of the JAK-STAT pathway in anti-dengue defense. Proc Natl Acad Sci USA 106:17841–17846

    Article  PubMed  PubMed Central  Google Scholar 

  • Stuart LM, Charriere GM, Hennessy EJ, Brunet S, Jutras I, Goyette G, Rondeau C, Letarte S, Huang H, Morales F, Kocks C, Bader JS, Desjardins M, Ezekowitz RAB (2007) A systems biology analysis of the Drosophila phagosome. Nature 445:95–101

    Article  CAS  PubMed  Google Scholar 

  • Subhamoy P, Wu LP (2009) Pattern recognition receptors in the fly Lessons we can learn from the Drosophila melanogaster immune system. Fly 3:121–129

    Article  Google Scholar 

  • Tjelle TE, Lovdal T, Berg T (2000) Phagosome dynamics and function. BioEssays 22:255–263

    Article  CAS  PubMed  Google Scholar 

  • Touret N, Paroutis P, Terebiznik M, Harrison RE, Trombetta S, Pypaert M, Chow A, Jiang A, Shaw J, Yip C, Moore HP, van der Wel N, Houben D, Peters PJ, de Chastellier C, Mellman I, Grinstein S (2005) Quantitative and dynamic assessment of the contribution of the ER to phagosome formation. Cell 123:157–170

    Article  CAS  PubMed  Google Scholar 

  • Tzou P, Ohresser S, Ferrandon D, Capovilla M, Reichhart JM, Lemaitre B, Hoffmann JA, Imler JL (2000) Tissue-specific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia. Immunity 13:737–748

    Article  CAS  PubMed  Google Scholar 

  • Unckless RL, Rottschaefer SM, Lazzaro BP (2015) The complex contributions of genetics and nutrition to immunity in Drosophila melanogaster. PLoS Genet 11:e1005030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vieira OV, Botelho RJ, Grinstein S (2002) Phagosome maturation: aging gracefully. Biochem J 366:689–704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Visidou I, Wood W (2015) Drosophila blood cells and their role in immune responses. FEBS J 282:1368–1382

    Article  CAS  Google Scholar 

  • Wang G (2014) Human antimicrobial peptides and proteins. Pharmaceuticals 7:545–594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu J, Cherry S (2014) Dev Comp Immunol 42:67–84

    Article  CAS  PubMed  Google Scholar 

  • Zapata HJ, Quagliarello VJ (2015) The microbiota and microbiome in aging: potential implications in health and age-related diseases. J Am Geriatr Soc 63:776–781

    Article  PubMed  PubMed Central  Google Scholar 

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Leips, J. (2019). Using Insects as Models of Immunosenescence. In: Fulop, T., Franceschi, C., Hirokawa, K., Pawelec, G. (eds) Handbook of Immunosenescence. Springer, Cham. https://doi.org/10.1007/978-3-319-99375-1_4

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