Evolutionary plasticity of insect immunity

Journal of Insect Physiology

Volumn 59, Issue 2, 2013, Pages 123-129

  Vilcinskas, Andreas ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Antimicrobial peptides; Evolutionary ecology; Fitness costs; Genomics; Immunity; Insects

Indexed keywords

ANTIMICROBIAL CATIONIC PEPTIDE; INSECT PROTEIN; PROTEINASE INHIBITOR;

ANTIMICROBIAL ACTIVITY; BEETLE; ENDOSYMBIONT; EVOLUTIONARY BIOLOGY; FITNESS; GENOMICS; IMMUNITY; LIFE HISTORY TRAIT; PHENOTYPIC PLASTICITY; SECONDARY METABOLITE; TRADE-OFF;

ANIMAL; ARTICLE; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; INSECT; METABOLISM; MOLECULAR EVOLUTION;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; EVOLUTION, MOLECULAR; IMMUNITY, INNATE; INSECT PROTEINS; INSECTS; PROTEASE INHIBITORS;

APOIDEA; COLEOPTERA; HEXAPODA;

EID: 84873569115     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2012.08.018     Document Type: Article

References (81)

1. Adekoya O., Sylte I. The thermolysin family (M4) of enzymes: therapeutic and biotechnological potential. Chem. Biol. Drug Des. 2009, 73:7-16.
2. Altincicek B., Vilcinskas A. Analysis of the immune-related transcriptome from microbial stress resistant, rat-tailed maggots of the drone fly Eristalis tenax. BMC Genomics 2007, 8:326.
3. Altincicek B., Vilcinskas A. Identification of immune-related genes from an apterygote insect, the firebrat Thermobia domestica. Insect Biochem. Mol. Biol. 2007, 37:726-731.
4. Altincicek B., Vilcinskas A. Septic injury inducible genes in medicinal maggots of the blowfly Lucilia sericata. Insect Mol. Biol. 2009, 18:119-125.
5. 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.
6. Altincicek B., Knorr E., Vilcinskas A. Beetle immunity: identification of immune-inducible genes from the model insect Tribolium castaneum. Dev. Comp. Immunol. 2008, 32:585-595.
7. Armstrong P.B. Proteases and protease inhibitors: a balance of activities in host-pathogen interaction. Immunobiology 2006, 211:263-281.
8. Arolas, J.L., Botelho, T.O., Vilcinskas, A., Gomis-Rüth, F.X., 2011. Structural evidence for standard-mechanism inhibition in metallopeptidases from a complex poised to resynthesize a peptide bond. Angewandte Chemie, International Edition 50, 10357-10360.
9. Bulet P., Stöcklin R. Insect antimicrobial peptides: structures, properties and gene regulation. Protein Pept. Lett. 2005, 12:3-11.
10. Bulmer M.S., Crozier R.H. Duplication and diversifying selection among termite antifungal peptides. Mol. Biol. Evol. 2004, 21:2256-2264.
11. Chambers M.S., Schneider D.S. Pioneering immunology: insect style. Curr. Opin. Immunol. 2012, 24:10-14.
12. Christophides G.K., Zdobnov E., Barillas-Mury C., Birney E., Blandin S., Blass C., Brey P.T., Collins F.H., Danielli A., Dimopoulos G., Hetru C., Hoa N.T., Hoffmann J.A., Kanzok S.M., Letunic I., Levashina E.A., Loukeris T.G., Lycett G., Meister S., Michel K., Moita L.F., Müller H.M., Osta M.A., Paskewitz S.M., Reichhart J.M., Rzhetsky A., Troxler L., Vernick K.D., Vlachou D., Volz J., von Mering C., Xu J., Zheng L., Bork P., Kafatos F.C. Immunity-related genes and gene families in Anopheles gambiae. Science 2002, 298:159-165.
13. Clermont A., Wedde M., Seitz V., Podsiadlowski L., Hummel M., Vilcinskas A. Cloning and expression of an inhibitor against microbial metalloproteinases from insects (IMPI) contributing to innate immunity. Biochem. J. 2004, 382:315-322.
14. Degenkolb T., Düring R.-A., Vilcinskas V. Secondary metabolites released by the burying beetle Nicrophorus vespilloides: chemical analyses and possible ecological functions. J. Chem. Ecol. 2011, 37:724-735.
15. Dessanayake R.S., Silva Gunawardene Y.I., Tobe S.S. Evolutionary selective trends of insect/mosquito antimicrobial defensin peptides containing cysteine-stabilized α/ß motivs. Peptides 2007, 28:62-75.
16. Easton D.M., Nijnik A., Mayer M.L., Hancock R.E. Potential of immunomodulatory host defense peptides as novel anti-infectives. Trends Biotechnol. 2009, 27:582-590.
17. Evans J.D., Schwarz R.S. Bees brought to their kness: microbes affecting honey bee health. Trends Microbiol. 2011, 19:614-620.
18. Evans J.D., Aronstein K., Chen Y.P., Hetru C., Imler J.L., Jiang H., Kanost M., Thompson G.J., Zou Z., Hultmark D. Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol. Biol. 2006, 15:645-656.
19. Freitak D., Wheat C.W., Heckel D.G., Vogel H. Immune system responses and fitness costs associated with consumption of bacteria in larvae of Trichoplusia ni. BMC Biol. 2007, 5:56.
20. Freitak D., Heckel D.G., Vogel H. Bacterial feeding induces changes in immune-related gene expression and has trans-generatioal impacts in the cabbage looper Trichoplusia ni. Front. Zool. 2009, 6:7.
21. Freitak D., Knorr E., Vogel H., Vilcinskas A. Gender- and stressor-specific microRNA expression in Tribolium castaneum. Biology Letters 2012, 8:860-863.
22. Froy O., Gurevitz M. Arthropod and mollusk defensins - evolution by exon-shuffling. Trends Genet. 2003, 19:684-687.
23. Fullaondo A., Lee S.Y. Identification of putative miRNA involved in Drosophila melanogaster immune response. Dev. Comp. Immunol. 2012, 36:267-273.
24. Gerardo N., Altincicek B., Anselme C., Atamian H., Barribeau S., de Vos M., Evans J., Gabaldón T., Ghanim M., Heddi A., Kaloshian I., Latorre A., Monegat C., Moya A., Nakabachi A., Parker B., Pérez-Brocal V., Pignatelli M., Rahbé Y., Ramsey J., Tamames J., Tamarit D., Tamborindeguy C., Vilcinskas A. Immunity and other defenses in pea aphids Acyrthosiphon pisum. Genome Biol. 2010, 11(2):R21.
25. Gross J., Schuhmacher K., Schmidtberg H., Vilcinskas A. Protected by fumigants: beetles perfumes in antimicrobial defence. J. Chem. Ecol. 2008, 34:179-188.
26. Guani-Guerra E., Santos-Mendoza T., Lugo-Reyes S.O., Teran L.M. Antimicrobial peptides: general overview and clinical implications in human health and disease. Clin. Immunol. 2010, 135:1-11.
27. Hahn M.W., Han M.V., Han S.G. Gene family evolution across 12 Drosophila genomes. PLoS Genet. 2007, 3(11):e197.
28. Haine E.R. Symbiont-mediated protection. Proc. Royal Soc. B 2008, 275:353-358.
29. Haine E.R., Morte Y., Siva-Jothy M.T., Rolff J. Antimcrobial defense and persistent infection in insects. Science 2008, 322:1257-1259.
30. Honeybee genome sequencing consortium. 2006. Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443, 931-949.
31. International aphid genomics consortium. 2010. Genome Sequence of the Pea Aphid Acyrthosiphon pisum. PLoS Biology 8(2), e1000313.
32. Innan H., Kondrashov F. The evolution of gene duplications: classifying and distinguishing between models. Nat. Rev. Genet. 2010, 11:97-108.
33. Kaneko T., Silverman N. Bacterial recognition and signalling by the Drosophila IMD pathway. Cell Microbiol. 2005, 7:461-469.
34. Kirsch R., Vogel H., Muck A., Vilcinskas A., Pasteels J.M., Boland W. To be or not to be convergent in salicin-based defence in chrysomeline leaf beetle larvae: evidence from Phratora vitellinae salicyl alcohol oxidase. Proc. Royal Soc. B 2011, 278:3225-3232.
35. Langen G., Imani J., Altincicek B., Kieseritzky G., Kogel K.-H., Vilcinskas A. Transgenic expression of gallerimycin, a novel antifungal insect defensin from the greater wax moth Galleria mellonella, confers resistance against pathogenic fungi in tobacco. Biol. Chem. 2006, 387:549-557.
36. Lazzaro B. Natural selection on the Drosophila antimicrobial immune system. Curr. Opin. Microbiol. 2008, 11:284-289.
37. Lazzaro B.P., Little T.J. Immunity in a variable world. Philos. Trans. Royal Soc. B 2009, 364:15-26.
38. Le Conte Y., Alaux C., Martin J.-F., Harbo J.R., Harris J.W., Dantec C., Severac D., Cros-Arteil S., Navajas M. Social immunity in honeybees (Apis mellifera): transcriptome analysis of varroa-hygienic behavior. Insect Mol. Biol. 2011, 20:399-408.
39. Levashina E.A., Ohresser S., Bulet P., Reichhart J.M., Hetru C., Hoffmann J.A. Metchnikowin, a novel immune-inducible proline-rich peptide from Drosophila with antibacterial and antifungal properties. Eur. J. Biochem. 1995, 233:694-700.
40. Little T.J., ÓConnor B., Colegrave N., Watt K., Read A.F. Maternal transfer of strain-specific immunity in an invertebrate. Curr. Biol. 2003, 13:489-492.
41. Little T.J., Shuker D.M., Colegrave N., Day T., Graham A.L. The coevolution of virulence. tolerance in perspective. PLoS Pathog. 2010, 6(9):e1001006.
42. Login F.H., Balmand S., Vallier A., Vincent-Monégat C., Vigneron A., Weiss-Gayet M., Rochat D., Heddi A. Antimicrobial peptides keep insect endosymbionts under control. Science 2011, 334:362-365.
43. McKean K.A., Yourth C.P., Lazzaro B.P., Clark A.G. The evolutionary costs of immunological maintenance and deployment. BMC Evol. Biol. 2008, 8:76.
44. Moore A.D., Bornber-Bauer E. The dynamics and evolutionary potential of domain loss and emergence. Mol. Biol. Evol. 2012, 29:787-792.
45. Moore A.D., Björklund A.K., Ekman D., Bornberg-Bauer E., Elofsson A. Arrangements in the modular evolution of proteins. Trend Biochem. Sci. 2008, 33:444-451.
46. Moret Y. " Trans-generational immune priming" : specific enhancement of the antimicrobial immune response in the mealworm beetle, Tenebrio molitor. Proc. Royal Soc. B 2006, 273:1399-1405.
47. Oliver K.M., Moran N.A., Hunter M.S. Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc. Natl. Acad. Sci. USA 2005, 102:12795-12800.
48. Potempa J., Robert N.P. Corruption of innate immunity by bacterial proteases. J. Innate Immun. 2009, 1:70-87.
49. Pulido D., Nogues V., Boix E., Torrent M. Lipopolysaccharide neutralization by antimicrobial peptides: a gambit in the innate host defense strategy. J. Innate Immun. 2012, 4:327-336.
50. Rahnamaeian M., Langen G., Imani J., Altincicek B., von Wettstein D., Kogel K.-H., Vilcinskas A. Insect peptide metchnikowin confers on barley a selective capacity for resistance to ascomycota fungal pathogens. J. Exp. Bot. 2009, 60:4105-4114.
51. Ratcliffe N.A., Mello C.B., Garcia E.S., Butt T.M., Azambuja P. Insect natural products and processes: new treatments for human disease. Insect Biochem. Mol. Biol. 2011, 41:747-769.
52. Rawlings N.D., Tolle D.P., Barret A.J. Evolutionary families of peptidase inhibitors. Biochem. J. 2004, 378:705-716.
53. Riedl S., Zweytick D., Lohner K. Membrane-active host defense peptides - challenges and perspectives for the development of novel anticancer drugs. Chem. Phys. Lipids 2011, 164:766-781.
54. Röhrich C.R., Ngwa C.J., Wiesner J., Schmidtberg H., Degenkolb T., Kollewe C., Fischer R., Pradel G., Vilcinskas A. Harmonine, a defence compound from the harlequin ladybird, inhibits mycobacterial growth and demonstrates multi-stage antimalarial activity. Biol. Lett. 2012, 8:308-311.
55. Roth O., Sadd B.M., Schmid-Hempel P., Kurtz J. Strain-specific priming of resistance in the red flour beetle, Tribolium castaneum. Proc. Royal Soc. B 2009, 276:145-151.
56. Sackton T.B., Lazzaro B.P., Schlenke T.A., Evans J.D., Hultmark D., Clark A.G. Dynamic evolution of the innate immune system in Drosophila. Nat. Genet. 2007, 39:1461-1468.
57. Sadd B., Kleinlogel Y., Schmid-Hempel R., Schmid-Hempel P. Transgenerational immune priming an social insect. Biol. Lett. 2005, 1:386-388.
58. Scarborough C.L., Ferrari J., Godfray H.C. Aphid protected from pathogen by endosymbiont. Science 2005, 310:1781.
59. Schmid-Hempel P. Evolutionary ecology of insect immune defenses. Ann. Rev. Entomol. 2005, 50:529-551.
60. Schmid-Hempel P. Parasite immune evasion: a momentous molecular war. Trends Ecol. Evol. 2008, 23:318-326.
61. Schmid-Hempel P. Evolutionary Parasitology - The Integrated Study of Infections, Immunology, Ecology, and Genetics 2011, Oxford University Press.
62. Schulte R., Makus C., Hasert B., Michiels N.K., Schulenburg H. Multiple reciprocal adaptations and rapid genetic change upon experimental coevolution of an animal host and its microbial parasite. Proc. Natl. Acad. Sci002E USA 2010, 107:7346-7359.
63. Suen G., Teiling C., Li L., Holt C., Abouheif E., Bornberg-Bauer E., Bouffard P., Caldera E.J., Cash E., Cavanaugh A., Denas O., Elhaik E., Favé M.J., Gadau J., Gibson J.D., Graur D., Grubbs K.J., Hagen D.E., Harkins T.T., Helmkampf M., Hu H., Johnson B.R., Kim J., Marsh S.E., Moeller J.A., Muñoz-Torres M.C., Murphy M.C., Naughton M.C., Nigam S., Overson R., Rajakumar R., Reese J.T., Scott J.J., Smith C.R., Tao S., Tsutsui N.D., Viljakainen L., Wissler L., Yandell M.D., Zimmer F., Taylor J., Slater S.C., Clifton S.W., Warren W.C., Elsik C.G., Smith C.D., Weinstock G.M., Gerardo, N M., Currie C.R. The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle. PLoS Genet. 2011, 7(2):e1002007.
64. Tian C., Gao B., Ye G., Zhu S. Antimicrobial peptide-like genes in Nasonia vitripennis: a genomic perspective. BMC Genom. 2010, 11:187.
65. Tribolium genome sequencing consortium. 2008. The genome of the developmental model beetle and pest Tribolium castaneum. Nature 425, 949-955.
66. Tzou P., Reichhart J.-M., Lemaitre B. Constitutive expression of a single antimicrobial peptide can restore wild-type resistance to infection in immunodeficient Drosophila mutants. Proc. Natl. Acad. Sci. USA 2002, 99:2152-2157.
67. Ulgevig L., Cremer S. Social prophylaxis: group interaction promotes collective immunity in ant colonies. Curr. Biol. 2007, 17:1967-1971.
68. Vilcinskas A. Coevolution between pathogen-derived proteinases and proteinase inhibitors of host insects. Virulence 2010, 1:206-214.
69. Vilcinskas A. Anti-infective therapeutics from the Lepidopteran model host Galleria mellonella. Curr. Pharm. Des. 2011, 17:1240-1245.
70. Vilcinskas A., Gross J. Drugs from bugs: the use of insects as a valuable source of transgenes with potential in modern plant protection strategies. J. Pest. Sci. 2005, 78:187-191.
71. Vilcinskas A., Wedde M. Insect inhibitors of metalloproteinases. IUBMB Life 2002, 54:339-343.
72. Vogel H., Altincicek B., Glöckner G., Vilcinskas A. A comprehensive transcriptome and immune-gene repertoire of the Lepidopteran model host Galleria mellonella. BMC Genom. 2011, 12:308.
73. Vogel H., Badapanda C., Vilcinskas A. Identification of immunity-related genes in the burying beetle Nicrophorus vespilloides by suppression subtractive hybridization. Insect Mol. Biol. 2011, 20:787-800.
74. Waterhouse R.M., Kriventseva E.V., Meister S., Xi Z., Alvarez K.S., Bartholomay L.C., Barillas-Mury C., Bian G., Blandin S., Christensen B.M., Dong Y., Jiang H., Kanost M.R., Koutsos A.C., Levashina E.A., Li J., Ligoxygakis P., Maccallum R.M., Mayhew G.F., Mendes A., Michel K., Osta M.A., Paskewitz S., Shin S.W., Vlachou D., Wang L., Wei W., Zheng L., Zou Z., Severson D.W., Raikhel A.S., Kafatos F.C., Dimopoulos G., Zdobnov E.M., Christophides G.K. Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 2007, 316:1738-1743.
75. Wedde M., Weise C., Nuck C., Altincicek B., Vilcinskas A. The insect metalloproteinase inhibitor gene of the Lepidopteran Galleria mellonella encodes two distinct inhibitors. Biol. Chem. 2007, 388:119-127.
76. Wiesner J., Vilcinskas A. Antimicrobial peptides: the ancient arm of the human immune system. Virulence 2010, 1(5):440-464.
77. Wolinska J., King K. Environement can alter selection in host-parasite interactions. Trends Parasitol. 2009, 25:236-244.
78. Xu P., Shi M., Chen X.X. Antimicrobial peptide evolution in the Asiatic honey bee Apis cerana. PLoS ONE 2009, 4(1):e4239.
79. Yang W., Cheng T., Ye M., Deng X., Yi H., Huang Y., Tan X., Han D., Wang B., Xiang Z., Xia Q. Functional divergence among silkworm antimicrobial peptide paralogs by the activities of recombinant proteins and the induced expression profiles. PLoS ONE 2011, 6(3):e18109.
80. Yeung A.T., Gellatly S.L., Hancock R.E. Multifunctional cationic host defense peptides and their clinical applications. Cell. Mol. Life Sci. 2011, 68:2161-2176.
81. Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 2002, 415:389-395.