Insights from natural host-parasite interactions: The Drosophila model

Developmental and Comparative Immunology

Volumn 42, Issue 1, 2014, Pages 111-123

  Keebaugh, Erin S ^a   Schlenke, Todd A ^a  

^a EMORY UNIVERSITY   (United States)

Author keywords

Coevolution; Drosophila immunity; Natural pathogens

Indexed keywords

PIWI INTERACTING RNA;

ANOPHELES GAMBIAE; ARTICLE; AUTOPHAGY; CYTOKINE PRODUCTION; DROSOPHILA; GLYCOSYLATION; HEMOLYMPH; HOMEOSTASIS; HOST PARASITE INTERACTION; HUMORAL IMMUNITY; IMMUNE RESPONSE; INNATE IMMUNITY; MOLECULAR EVOLUTION; NONHUMAN; PARASITE VIRULENCE; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN INTERACTION; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; RNA INTERFERENCE; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

COEVOLUTION; DROSOPHILA IMMUNITY; NATURAL PATHOGENS;

ANIMALS; BIOLOGICAL EVOLUTION; DROSOPHILA MELANOGASTER; HOST-PARASITE INTERACTIONS; HUMANS; IMMUNITY, INNATE; MODELS, ANIMAL; NUCLEAR PROTEINS; OPPORTUNISTIC INFECTIONS; PLANT PROTEINS; PLANTS; SYMBIOSIS; VIRULENCE FACTORS;

EID: 84886098627     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2013.06.001     Document Type: Article

References (175)

1. Adams M.D., Celniker S.E., Holt R.A., Evans C.A., Gocayne J.D., Amanatides P.G., Scherer S.E., Li P.W., Hoskins R.A., Galle R.F., George R.A., Lewis S.E., Richards S., Ashburner M., Henderson S.N., Sutton G.G., Wortman J.R., Yandell M.D., Zhang Q., Chen L.X., Brandon R.C., Rogers Y.H., Blazej R.G., Champe M., Pfeiffer B.D., Wan K.H., Doyle C., Baxter E.G., Helt G., Nelson C.R., Gabor G.L., Abril J.F., Agbayani A., An H.J., Andrews-Pfannkoch C., Baldwin D., Ballew R.M., Basu A., Baxendale J., Bayraktaroglu L., Beasley E.M., Beeson K.Y., Benos P.V., Berman B.P., Bhandari D., Bolshakov S., Borkova D., Botchan M.R., Bouck J., Brokstein P., Brottier P., Burtis K.C., Busam D.A., Butler H., Cadieu E., Center A., Chandra I., Cherry J.M., Cawley S., Dahlke C., Davenport L.B., Davies P., de Pablos B., Delcher A., Deng Z., Mays A.D., Dew I., Dietz S.M., Dodson K., Doup L.E., Downes M., Dugan-Rocha S., Dunkov B.C., Dunn P., Durbin K.J., Evangelista C.C., Ferraz C., Ferriera S., Fleischmann W., Fosler C., Gabrielian A.E., Garg N.S., Gelbart W.M., Glasser K., Glodek A., Gong F., Gorrell J.H., Gu Z., Guan P., Harris M., Harris N.L., Harvey D., Heiman T.J., Hernandez J.R., Houck J., Hostin D., Houston K.A., Howland T.J., Wei M.H., Ibegwam C., Jalali M., Kalush F., Karpen G.H., Ke Z., Kennison J.A., Ketchum K.A., Kimmel B.E., Kodira C.D., Kraft C., Kravitz S., Kulp D., Lai Z., Lasko P., Lei Y., Levitsky A.A., Li J., Li Z., Liang Y., Lin X., Liu X., Mattei B., McIntosh T.C., McLeod M.P., McPherson D., Merkulov G., Milshina N.V., Mobarry C., Morris J., Moshrefi A., Mount S.M., Moy M., Murphy B., Murphy L., Muzny D.M., Nelson D.L., Nelson D.R., Nelson K.A., Nixon K., Nusskern D.R., Pacleb J.M., Palazzolo M., Pittman G.S., Pan S., Pollard J., Puri V., Reese M.G., Reinert K., Remington K., Saunders R.D., Scheeler F., Shen H., Shue B.C., Siden-Kiamos I., Simpson M., Skupski M.P., Smith T., Spier E., Spradling A.C., Stapleton M., Strong R., Sun E., Svirskas R., Tector C., Turner R., Venter E., Wang A.H., Wang X., Wang Z.Y., Wassarman D.A., Weinstock G.M., Weissenbach J., Williams S.M., Worley T., Woodage K.C., Wu D., Yang S., Yao Q.A., Ye J., Yeh R.F., Zaveri J.S., Zhan M., Zhang G., Zhao Q., Zheng L., Zheng X.H., Zhong F.N., Zhong W., Zhou X., Zhu S., Zhu X., Smith H.O., Gibbs R.A., Myers E.W., Rubin G.M., Venter J.C. The genome sequence of Drosophila melanogaster. Science 2000, 287:2185-2195.
2. Allemand R., Lemaitre C., Frey F., Bouletreau M., Vavre F., Nordlander G., van Alphen J., Carton Y. Phylogeny of six African Leptopilina species (Hymenoptera: cynipoidea: figitidae), parasitoids of Drosophila, with description of three new species. Ann. Soc. Entomol. F 2002, 39:319-332.
3. Aminetzach Y.T., Macpherson J.M., Petrov D.A. Pesticide resistance via transposition-mediated adaptive gene truncation in Drosophila. Science 2005, 309:764-767.
4. Anthony R.M., Rutitzky L.I., Urban J.F., Stadecker M.J., Gause W.C. Protective immune mechanisms in helminth infection. Nat. Rev. Immunol. 2007, 7:975-987.
5. Asai T., Tena G., Plotnikova J., Willmann M.R., Chiu W.L., Gomez-Gomez L., Boller T., Ausubel F.M., Sheen J. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 2002, 415:977-983.
6. Bangham J., Obbard D.J., Kim K.W., Haddrill P.R., Jiggins F.M. The age and evolution of an antiviral resistance mutation in Drosophila melanogaster. Proc. R. Soc. London B Biol. Sci. 2007, 274:2027-2034.
7. Becher P.G., Bengtsson M., Hansson B.S., Witzgall P. Flying the fly: long-range flight behavior of Drosophila melanogaster to attractive odors. J. Chem. Ecol. 2010, 36:599-607.
8. Bem R.A., Domachowske J.B., Rosenberg H.F. Animal models of human respiratory syncytial virus disease. Am. J. Physiol. Lung Cell. Mol. Physiol. 2011, 301:L148-156.
9. Boete C. Malaria parasites in mosquitoes: laboratory models, evolutionary temptation and the real world. Trends Parasitol. 2005, 21:445-447.
10. Bosinger S.E., Jacquelin B., Benecke A., Silvestri G., Muller-Trutwin M. Systems biology of natural simian immunodeficiency virus infections. Curr. Opin. HIV AIDS 2012, 7:71-78.
11. Boulanger N., Ehret-Sabatier L., Brun R., Zachary D., Bulet P., Imler J.L. Immune response of Drosophila melanogaster to infection with the flagellate parasite Crithidia spp. Insect Biochem. Mol. Biol. 2001, 31:129-137.
12. Boulanger N., Brun R., Ehret-Sabatier L., Kunz C., Bulet P. Immunopeptides in the defense reactions of Glossina morsitans to bacterial and Trypanosoma brucei brucei infections. Insect Biochem. Mol. Biol. 2002, 32:369-375.
13. Bouletreau M., David J.R. Sexually dimorphic response to host habitat toxicity in Drosophila parasitic wasps. Evolution 1981, 35:395-399.
14. Bourtzis K., Nirgianaki A., Markakis G., Savakis C. Wolbachia infection and cytoplasmic incompatibility in Drosophila species. Genetics 1996, 144:1063-1073.
15. Boutros M., Agaisse H., Perrimon N. Sequential activation of signaling pathways during innate immune responses in Drosophila. Dev. Cell 2002, 3:711-722.
16. Brennecke J., Aravin A.A., Stark A., Dus M., Kellis M., Sachidanandam R., Hannon G.J. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 2007, 128:1089-1103.
17. Brennecke J., Malone C.D., Aravin A.A., Sachidanandam R., Stark A., Hannon G.J. An epigenetic role for maternally inherited piRNAs in transposon silencing. Science 2008, 322:1387-1392.
18. Brun G., Plus N. The viruses of Drosophila. The Genetics and Biology of Drosophila 1980, 625-702. Academic Press, London. M. Ashburner, R. Wright (Eds.).
19. Buchon N., Broderick N.A., Chakrabarti S., Lemaitre B. Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes Dev. 2009, 23:2333-2344.
20. Carpenter J., Hutter S., Baines J.F., Roller J., Saminadin-Peter S.S., Parsch J., Jiggins F.M. The transcriptional response of Drosophila melanogaster to infection with the sigma virus (Rhabdoviridae). PLoS ONE 2009, 4:e6838.
21. Carton Y., Bouletreau M., Van Alphen J.J.M., Lenteren J.C. The Drosophila parasitic wasps. The Genetics and Biology of Drosophila 1986, 347-394. Academic Press, London.
22. Carton Y., Poirie M., Nappi A.J. Insect immune resistance to parasitoids. Insect Sci. 2008, 15:67-87.
23. Chakrabarti S., Liehl P., Buchon N., Lemaitre B. Infection-induced host translational blockage inhibits immune responses and epithelial renewal in the Drosophila gut. Cell Host Microbe 2012, 12:60-70.
24. Chandler J.A., James P.M. Discovery of trypanosomatid parasites in globally distributed Drosophila species. PLoS ONE 2013, 8:e61937.
25. Chandler J.A., Lang J.M., Bhatnagar S., Eisen J.A., Kopp A. Bacterial communities of diverse Drosophila species: ecological context of a host-microbe model system. PLoS Genet. 2011, 7:e1002272.
26. Chandler J.A., Eisen J.A., Kopp A. Yeast communities of diverse Drosophila species: comparison of two symbiont groups in the same hosts. Appl. Environ. Microbiol. 2012, 78:7327-7336.
27. Chatton E., Alilaire E. Coexistence d'un Leptomonas (Herpetomonas) et d'un Trypanosoma chez un muscide non vulnerant, D. confusa Staeger. Comptes Rendus des Seances de la Societe de la Biologie 1908, 64:1004-1006.
28. Chisholm S.T., Coaker G., Day B., Staskawicz B.J. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 2006, 124:803-814.
29. Cohuet A., Osta M.A., Morlais I., Awono-Ambene P.H., Michel K., Simard F., Christophides G.K., Fontenille D., Kafatos F.C. Anopheles and Plasmodium: from laboratory models to natural systems in the field. EMBO Rep. 2006, 7:1285-1289.
30. Colinet D., Schmitz A., Depoix D., Crochard D., Poirie M. Convergent use of RhoGAP toxins by eukaryotic parasites and bacterial pathogens. PLoS Pathog. 2007, 3:e203.
31. Colinet D., Dubuffet A., Cazes D., Moreau S., Drezen J.M., Poirie M. A serpin from the parasitoid wasp Leptopilina boulardi targets the Drosophila phenoloxidase cascade. Dev. Comp. Immunol. 2009, 33:681-689.
32. Colinet D., Cazes D., Belghazi M., Gatti J.L., Poirie M. Extracellular superoxide dismutase in insects: characterization, function, and interspecific variation in parasitoid wasp venom. J. Biol. Chem. 2011, 286:40110-40121.
33. Colinet D., Deleury E., Anselme C., Cazes D., Poulain J., Azema-Dossat C., Belghazi M., Gatti J.L., Poirie M. Extensive inter- and intraspecific venom variation in closely related parasites targeting the same host: the case of Leptopilina parasitoids of Drosophila. Insect Biochem. Mol. Biol. 2013, 43:601-611.
34. Corby-Harris V., Pontaroli A.C., Shimkets L.J., Bennetzen J.L., Habel K.E., Promislow D.E. Geographical distribution and diversity of bacteria associated with natural populations of Drosophila melanogaster. Appl. Environ. Microbiol. 2007, 73:3470-3479.
35. Corwin R.M. A study of Trypanosomatids in Drosophila 1962, Master's Thesis, University of Georgia, Athens, GA.
36. Crozatier M., Ubeda J.M., Vincent A., Meister M. Cellular immune response to parasitization in Drosophila requires the EBF orthologue collier. PLoS Biol. 2004, 2:E196.
37. Dawkins R., Krebs J.R. Arms races between and within species. Proc. R. Soc. London B Biol. Sci. 1979, 205:489-511.
38. De Gregorio E., Spellman P.T., Tzou P., Rubin G.M., Lemaitre B. The Toll and Imd pathways are the major regulators of the immune response in Drosophila. EMBO J. 2002, 21:2568-2579.
39. Degnan P.H., Moran N.A. Diverse phage-encoded toxins in a protective insect endosymbiont. Appl. Environ. Microbiol. 2008, 74:6782-6791.
40. Degnan P.H., Moran N.A. Evolutionary genetics of a defensive facultative symbiont of insects: exchange of toxin-encoding bacteriophage. Mol. Ecol. 2008, 17:916-929.
41. Degnan P.H., Yu Y., Sisneros N., Wing R.A., Moran N.A. Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc. Natl. Acad. Sci. USA 2009, 106:9063-9068.
42. DeYoung B.J., Innes R.W. Plant NBS-LRR proteins in pathogen sensing and host defense. Nat. Immunol. 2006, 7:1243-1249.
43. Dodds P.N., Lawrence G.J., Catanzariti A.M., Teh T., Wang C.I., Ayliffe M.A., Kobe B., Ellis J.G. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc. Natl. Acad. Sci. USA 2006, 103:8888-8893.
44. Domachowske J.B., Bonville C.A., Gao J.L., Murphy P.M., Easton A.J., Rosenberg H.F. MIP-1alpha is produced but it does not control pulmonary inflammation in response to respiratory syncytial virus infection in mice. Cell. Immunol. 2000, 206:1-6.
45. Dong Y., Aguilar R., Xi Z., Warr E., Mongin E., Dimopoulos G. Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog. 2006, 2:e52.
46. Dostert C., Jouanguy E., Irving P., Troxler L., Galiana-Arnoux D., Hetru C., Hoffmann J.A., Imler J.L. The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of Drosophila. Nat. Immunol. 2005, 6:946-953.
47. Dubuffet A., Colinet D., Anselme C., Dupas S., Carton Y., Poirie M. Variation of Leptopilina boulardi success in Drosophila hosts: what is inside the black box?. Adv. Parasitol. 2009, 70:147-188.
48. Dyer K.D., Garcia-Crespo K.E., Glineur S., Domachowske J.B., Rosenberg H.F. The Pneumonia virus of mice (PVM) model of acute respiratory infection. Viruses 2012, 4:3494-3510.
49. Ebbert M.A., Marlowe J.L., Burkholder J.J. Protozoan and intracellular fungal gut endosymbionts in Drosophila: prevalence and fitness effects of single and dual infections. J. Invertebr. Pathol. 2003, 83:37-45.
50. Fang M., Cheng H., Dai Z., Bu Z., Sigal L.J. Immunization with a single extracellular enveloped virus protein produced in bacteria provides partial protection from a lethal orthopoxvirus infection in a natural host. Virology 2006, 345:231-243.
51. Ferguson H.M., Read A.F. Why is the effect of malaria parasites on mosquito survival still unresolved?. Trends Parasitol. 2002, 18:256-261.
52. Fleuriet A. Comparison of various physiological traits in flies (Drosophila melanogaster) of wild origin, infected or uninfected by the hereditary Rhabdovirus sigma. Arch. Virol. 1981, 69:261-272.
53. Flor H.H. Current status of the gene-for-gene concept. Ann. Rev. Phytopathol. 1971, 9:275-296.
54. Francois S., Vidick S., Sarlet M., Michaux J., Koteja P., Desmecht D., Stevenson P.G., Vanderplasschen A., Gillet L. Comparative study of murid gammaherpesvirus 4 infection in mice and in a natural host, bank voles. J. Gen. Virol. 2010, 91:2553-2563.
55. Futerman P.H., Layen S.J., Kotzen M.L., Franzen C., Kraaijeveld A.R., Godfray H.C. Fitness effects and transmission routes of a microsporidian parasite infecting Drosophila and its parasitoids. Parasitology 2006, 132:479-492.
56. Galiana-Arnoux D., Dostert C., Schneemann A., Hoffmann J.A., Imler J.L. Essential function in vivo for dicer-2 in host defense against RNA viruses in Drosophila. Nat. Immunol. 2006, 7:590-597.
57. Ghildiyal M., Zamore P.D. Small silencing RNAs: an expanding universe. Nat. Rev. Genet. 2009, 10:94-108.
58. Goecks J., Mortimer N.T., Mobley J.A., Bowersock G.J., Taylor J., Schlenke T.A. Integrative approach reveals composition of endoparasitoid wasp venoms. PLoS ONE 2013, 5:e64125.
59. Haas D., Defago G. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat. Rev. Microbiol. 2005, 3:307-319.
60. Habayeb M.S., Ekengren S.K., Hultmark D. Nora virus, a persistent virus in Drosophila, defines a new picorna-like virus family. J. Gen. Virol. 2006, 87:3045-3051.
61. Habayeb M.S., Ekstrom J.O., Hultmark D. Nora virus persistent infections are not affected by the RNAi machinery. PLoS ONE 2009, 4:e5731.
62. Harris A.N., Macdonald P.M. Aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C. Development 2001, 128:2823-2832.
63. Haselkorn T.S., Markow T.A., Moran N.A. Multiple introductions of the Spiroplasma bacterial endosymbiont into Drosophila. Mol. Ecol. 2009, 18:1294-1305.
64. Heavner M.E., Gueguen G., Rajwani R., Pagan P.E., Small C., Govind S. Partial venom gland transcriptome of a Drosophila parasitoid wasp, Leptopilina heterotoma, reveals novel and shared bioactive profiles with stinging Hymenoptera. Gene 2013, 10.1016/j.gene.2013.04.080.
65. Hedges L.M., Brownlie J.C., O'Neill S.L., Johnson K.N. Wolbachia and virus protection in insects. Science 2008, 322:702.
66. Hedges L.M., Yamada R., O'Neill S.L., Johnson K.N. The small interfering RNA pathway is not essential for Wolbachia-mediated antiviral protection in Drosophila melanogaster. Appl. Environ. Microbiol. 2012, 78:6773-6776.
67. Houck M.A., Clark J.B., Peterson K.R., Kidwell M.G. Possible horizontal transfer of Drosophila genes by the mite Proctolaelaps regalis. Science 1991, 253:1125-1128.
68. Hu Y., Aksoy S. An antimicrobial peptide with trypanocidal activity characterized from Glossina morsitans morsitans. Insect Biochem. Mol. Biol. 2005, 35:105-115.
69. Hughes D.J., Kipar A., Sample J.T., Stewart J.P. Pathogenesis of a model gammaherpesvirus in a natural host. J. Virol. 2010, 84:3949-3961.
70. Hughes D.J., Kipar A., Leeming G.H., Bennett E., Howarth D., Cummerson J.A., Papoula-Pereira R., Flanagan B.F., Sample J.T., Stewart J.P. Chemokine binding protein M3 of murine gammaherpesvirus 68 modulates the host response to infection in a natural host. PLoS Pathog. 2011, 7:e1001321.
71. Hughes D.J., Kipar A., Leeming G., Sample J.T., Stewart J.P. Experimental infection of laboratory-bred bank voles (Myodes glareolus) with murid herpesvirus 4. Arch. Virol. 2012, 157:2207-2212.
72. Huszar T., Imler J.L. Drosophila viruses and the study of antiviral host-defense. Adv. Virus Res. 2008, 72:227-265.
73. Hwang R.Y., Zhong L., Xu Y., Johnson T., Zhang F., Deisseroth K., Tracey W.D. Nociceptive neurons protect Drosophila larvae from parasitoid wasps. Curr. Biol. 2007, 17:2105-2116.
74. Irving P., Ubeda J.M., Doucet D., Troxler L., Lagueux M., Zachary D., Hoffmann J.A., Hetru C., Meister M. New insights into Drosophila larval haemocyte functions through genome-wide analysis. Cell. Microbiol. 2005, 7:335-350.
75. Itami T., Takahashi Y., Nakamura Y. Efficacy of vaccination against vibriosis in cultured kuruma prawns Penaeus japonicus. J. Aquat. Anim. Health 1989, 1:238-242.
76. Jaenike J. Mycophagous Drosophila and their nematode parasites. Am. Nat. 1992, 139:893-906.
77. Jiang H.Q., Patel P.H., Kohlmaier A., Grenley M.O., McEwen D.G., Edgar B.A. Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell 2009, 137:1343-1355.
78. Jones J.D., Dangl J.L. The plant immune system. Nature 2006, 444:323-329.
79. Kacsoh B.Z., Lynch Z.R., Mortimer N.T., Schlenke T.A. Fruit flies medicate offspring after seeing parasites. Science 2013, 339:947-950.
80. Kaminker J.S., Bergman C.M., Kronmiller B., Carlson J., Svirskas R., Patel S., Frise E., Wheeler D.A., Lewis S.E., Rubin G.M., Ashburner M., Celniker S.E. The transposable elements of the Drosophila melanogaster euchromatin: a genomics perspective. Genome Biol. 2002, 3:1-20.
81. Kapun M., Nolte V., Flatt T., Schlotterer C. Host range and specificity of the Drosophila C virus. PLoS ONE 2010, 5:e12421.
82. Kemp C., Imler J.L. Antiviral immunity in drosophila. Curr. Opin. Immunol. 2009, 21:3-9.
83. Kemp C., Mueller S., Goto A., Barbier V., Paro S., Bonnay F., Dostert C., Troxler L., Hetru C., Meignin C., Pfeffer S., Hoffmann J.A., Imler J.L. Broad RNA interference-mediated antiviral immunity and virus-specific inducible responses in Drosophila. J. Immunol. 2013, 190:650-658.
84. Knowles S.C., Fenton A., Pedersen A.B. Epidemiology and fitness effects of wood mouse herpesvirus in a natural host population. J. Gen. Virol. 2012, 93:2447-2456.
85. Koppang E.O., Haugarvoll E., Hordvik I., Aune L., Poppe T.T. Vaccine-associated granulomatous inflammation and melanin accumulation in Atlantic salmon, Salmo salar L., white muscle. J. Fish Dis. 2005, 28:13-22.
86. Kurtz J., Franz K. Innate defence: evidence for memory in invertebrate immunity. Nature 2003, 425:37-38.
87. Labrosse C., Eslin P., Doury G., Drezen J.M., Poirie M. Haemocyte changes in D. melanogaster in response to long gland components of the parasitoid wasp Leptopilina boulardi: a Rho-GAP protein as an important factor. J. Insect Physiol. 2005, 51:161-170.
88. Labrosse C., Stasiak K., Lesobre J., Grangeia A., Huguet E., Drezen J.M., Poirie M. A RhoGAP protein as a main immune suppressive factor in the Leptopilina boulardi (Hymenoptera, Figitidae)-Drosophila melanogaster interaction. Insect Biochem. Mol. Biol. 2005, 35:93-103.
89. Lazzaro B.P. Natural selection on the Drosophila antimicrobial immune system. Curr. Opin. Microbiol. 2008, 11:284-289.
90. Lazzaro B.P., Clark A.G. Molecular population genetics of inducible antibacterial peptide genes in Drosophila melanogaster. Mol. Biol. Evol. 2003, 20:914-923.
91. Lecuit M., Dramsi S., Gottardi C., Fedor-Chaiken M., Gumbiner B., Cossart P. A single amino acid in E-cadherin responsible for host specificity towards the human pathogen Listeria monocytogenes. EMBO J. 1999, 18:3956-3963.
92. Lefevre T., de Roode J.C., Kacsoh B.Z., Schlenke T.A. Defence strategies against a parasitoid wasp in Drosophila: fight or flight?. Biol. Lett. 2012, 8:230-233.
93. Lemaitre B., Hoffmann J. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 2007, 25:697-743.
94. Liehl P., Blight M., Vodovar N., Boccard F., Lemaitre B. Prevalence of local immune response against oral infection in a Drosophila/Pseudomonas infection model. PLoS Pathog. 2006, 2:e56.
95. Longdon B., Jiggins F.M. Vertically transmitted viral endosymbionts of insects: do sigma viruses walk alone?. Proc. Biol. Sci. 2012, 279:3889-3898.
96. Lushbaugh W.B., Rowton E.D., McGhee R.B. Parasitic yeastlike fungus from the intestinal epithelium of Drosophila melanogaster. J. Invertebr. Pathol. 1976, 28:93-107.
97. MacLeod E.T., Maudlin I., Darby A.C., Welburn S.C. Antioxidants promote establishment of trypanosome infections in tsetse. Parasitology 2007, 134:827-831.
98. Magwire M.M., Bayer F., Webster C.L., Cao C.A., Jiggins F.M. Successive increases in the resistance of Drosophila to viral infection through a transposon insertion followed by a duplication. PLoS Genet. 2011, 7:e1002337.
99. Magwire M.M., Fabian D.K., Schweyen H., Cao C., Longdon B., Bayer F., Jiggins F.M. Genome-wide association studies reveal a simple genetic basis of resistance to naturally coevolving viruses in Drosophila melanogaster. PLoS Genet. 2012, 8:e1003057.
100. McTaggart S.J., Wilson P.J., Little T.J. Daphnia magna shows reduced infection upon secondary exposure to a pathogen. Biol. Lett. 2012, 8:972-975.
101. Megosh H.B., Cox D.N., Campbell C., Lin H. The role of PIWI and the miRNA machinery in Drosophila germline determination. Curr. Biol. 2006, 16:1884-1894.
102. Michel K., Suwanchaichinda C., Morlais I., Lambrechts L., Cohuet A., Awono-Ambene P.H., Simard F., Fontenille D., Kanost M.R., Kafatos F.C. Increased melanizing activity in Anopheles gambiae does not affect development of Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 2006, 103:16858-16863.
103. Milan N.F., Kacsoh B.Z., Schlenke T.A. Alcohol consumption as self-medication against blood-borne parasites in the fruit fly. Curr. Biol. 2012, 22:488-493.
104. Mitsui H., Van Achterberg K., Nordlander G., Kimura M.T. Geographical distributions and host associations of larval parasitoids of frugivorous Drosophilidae in Japan. J. Nat. Hist. 2007, 41:1731-1738.
105. Moran N.A., Degnan P.H., Santos S.R., Dunbar H.E., Ochman H. The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. Proc. Natl. Acad. Sci. USA 2005, 102:16919-16926.
106. Mortimer N.T., Kacsoh B.Z., Keebaugh E.S., Schlenke T.A. Mgat1-dependent N-glycosylation of membrane components primes Drosophila melanogaster blood cells for the cellular encapsulation response. PLoS Pathog. 2012, 8:e1002819.
107. Mortimer N.T., Goecks J., Kacsoh B.Z., Mobley J.A., Bowersock G.J., Taylor J., Schlenke T.A. Parasitoid wasp venom SERCA regulates Drosophila calcium levels and inhibits cellular immunity. Proc. Natl. Acad. Sci. USA 2013, 110:9427-9432.
108. Mukhopadhyay S., Farver C.F., Vaszar L.T., Dempsey O.J., Popper H.H., Mani H., Capelozzi V.L., Fukuoka J., Kerr K.M., Zeren E.H., Iyer V.K., Tanaka T., Narde I., Nomikos A., Gumurdulu D., Arava S., Zander D.S., Tazelaar H.D. Causes of pulmonary granulomas: a retrospective study of 500 cases from seven countries. J. Clin. Pathol. 2012, 65:51-57.
109. Munks R.J., Sant'Anna M.R., Grail W., Gibson W., Igglesden T., Yoshiyama M., Lehane S.M., Lehane M.J. Antioxidant gene expression in the blood-feeding fly Glossina morsitans morsitans. Insect Mol. Biol. 2005, 14:483-491.
110. Nappi A., Poirie M., Carton Y. The role of melanization and cytotoxic by-products in the cellular immune responses of Drosophila against parasitic wasps. Adv. Parasitol. 2009, 70:99-121.
111. Nezis I.P. Selective autophagy in Drosophila. Int. J. Cell Biol. 2012, 2012:146767.
112. Novkovic B., Mitsui H., Suwito A., Kimura M.T. Taxonomy and phylogeny of Leptopilina species (Hymenoptera: Cynipoidea: Figitidae) attacking frugivorous drosophilid flies in Japan, with description of three new species. Entomol. Sci. 2011, 14:333-346.
113. Nurnberger T., Brunner F., Kemmerling B., Piater L. Innate immunity in plants and animals: striking similarities and obvious differences. Immunol. Rev. 2004, 198:249-266.
114. Obbard D.J., Welch J.J., Kim K.W., Jiggins F.M. Quantifying adaptive evolution in the Drosophila immune system. PLoS Genet. 2009, 5:e1000698.
115. 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.
116. Opota O., Vallet-Gely I., Vincentelli R., Kellenberger C., Iacovache I., Gonzalez M.R., Roussel A., van der Goot F.G., Lemaitre B. Monalysin, a novel beta-pore-forming toxin from the Drosophila pathogen Pseudomonas entomophila, contributes to host intestinal damage and lethality. PLoS Pathog. 2011, 7:e1002259.
117. Osborne S.E., Leong Y.S., O'Neill S.L., Johnson K.N. Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans. PLoS Pathog. 2009, 5:e1000656.
118. Panteleev D., Goriacheva I.I., Andrianov B.V., Reznik N.L., Lazebnyi O.E., Kulikov A.M. The endosymbiotic bacterium Wolbachia enhances the nonspecific resistance to insect pathogens and alters behavior of Drosophila melanogaster. Genetika 2007, 43:1277-1280.
119. Parham P. The Immune System 2009, Garland Publishing, New York.
120. Plus N., Duthoit J.L. A new Drosophila melanogaster virus, the P virus. C. R. Acad. Sci. Hebd. Seances Acad. Sci. D 1969, 268:2313-2315.
121. Plus N., Croizier G., Duthoit J.L., David J., Anxolabehere D., Periquet G. The discovery, in Drosophila, of viruses belonging to three new groups. C. R. Acad. Sci. Hebd. Seances Acad. Sci. D 1975, 280:1501-1504.
122. Plus N., Croizier G., Jousset F.X., David J. Picornaviruses of laboratory and wild Drosophila melanogaster: geographical distribution and serotypic composition. Ann. Microbiol. (Paris) 1975, 126:107-117.
123. Plus N., Croizier G., Veyrunes J.C., David J. A comparison of buoyant density and polypeptides of Drosophila P, C and A viruses. Intervirology 1976, 7:346-350.
124. Polak M. Ectoparasitic effects on host survival and reproduction: the Drosophila-Macrocheles association. Ecology 1996, 77:1379-1389.
125. Polak M. Heritability of resistance against ectoparasitism in the Drosophila-Macrocheles system. J. Evol. Biol. 2003, 16:74-82.
126. 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 2011, 6:e20960.
127. Presgraves D.C. A genetic test of the mechanism of Wolbachia-induced cytoplasmic incompatibility in Drosophila. Genetics 2000, 154:771-776.
128. Rahme L.G., Stevens E.J., Wolfort S.F., Shao J., Tompkins R.G., Ausubel F.M. Common virulence factors for bacterial pathogenicity in plants and animals. Science 1995, 268:1899-1902.
129. Revilla Y., Callejo M., Rodriguez J.M., Culebras E., Nogal M.L., Salas M.L., Vinuela E., Fresno M. Inhibition of nuclear factor kappaB activation by a virus-encoded IkappaB-like protein. J. Biol. Chem. 1998, 273:5405-5411.
130. Richards D.T., Hoole D., Lewis J.W., Ewens E., Arme C. Ultrastructural observations on the cellular response of carp, Cyprinus carpio L., to eggs of the blood fluke Sanguinicola inermis Plehn, 1905 (Trematoda: Sanguinicolidae). J. Fish Dis. 1996, 17:439-443.
131. Riegler M., Sidhu M., Miller W.J., O'Neill S.L. Evidence for a global Wolbachia replacement in Drosophila melanogaster. Curr. Biol. 2005, 15:1428-1433.
132. Rotger M., Dalmau J., Rauch A., McLaren P., Bosinger S.E., Martinez R., Sandler N.G., Roque A., Liebner J., Battegay M., Bernasconi E., Descombes P., Erkizia I., Fellay J., Hirschel B., Miro J.M., Palou E., Hoffmann M., Massanella M., Blanco J., Woods M., Gunthard H.F., de Bakker P., Douek D.C., Silvestri G., Martinez-Picado J., Telenti A. Comparative transcriptomics of extreme phenotypes of human HIV-1 infection and SIV infection in sooty mangabey and rhesus macaque. J. Clin. Invest. 2011, 121:2391-2400.
133. Roth O., Sadd B.M., Schmid-Hempel P., Kurtz J. Strain-specific priming of resistance in the red flour beetle, Tribolium castaneum. Proc. Biol. Sci. 2009, 276:145-151.
134. Rottschaefer S.M., Lazzaro B.P. No effect of Wolbachia on resistance to intracellular infection by pathogenic bacteria in Drosophila melanogaster. PLoS ONE 2012, 7:e40500.
135. Rowton E.D., Mcghee R.B. Population-dynamics of Herpetomonas-Ampelophilae, with a note on systematics of Herpetomonas from Drosophila Spp. J. Protozool. 1978, 25:232-235.
136. Rubin G.M., Kidwell M.G., Bingham P.M. The molecular basis of P-M hybrid dysgenesis: the nature of induced mutations. Cell 1982, 29:987-994.
137. Russo J., Dupas S., Frey F., Carton Y., Brehelin M. Insect immunity: early events in the encapsulation process of parasitoid (Leptopilina boulardi) eggs in resistant and susceptible strains of Drosophila. Parasitology 1996, 112:135-142.
138. Ryu J.H., Kim S.H., Lee H.Y., Bai J.Y., Nam Y.D., Bae J.W., Lee D.G., Shin S.C., Ha E.M., Lee W.J. Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science 2008, 319:777-782.
139. 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.
140. Schesser K., Spiik A.K., Dukuzumuremyi J.M., Neurath M.F., Pettersson S., Wolf-Watz H. The yopJ locus is required for yersinia-mediated inhibition of NF-kappaB activation and cytokine expression: YopJ contains a eukaryotic SH2-like domain that is essential for its repressive activity. Mol. Microbiol. 1998, 28:1067-1079.
141. Schlenke T.A., Begun D.J. Natural selection drives Drosophila immune system evolution. Genetics 2003, 164:1471-1480.
142. Schlenke T.A., Morales J., Govind S., Clark A.G. Contrasting infection strategies in generalist and specialist wasp parasitoids of Drosophila melanogaster. PLoS Pathog. 2007, 3:1486-1501.
143. Secombes C.J., Chappell L.H. Fish immune responses to experimental and natural infection with helminth parasites. Annu. Rev. Fish Dis. 1996, 6:167-177.
144. Senti K.A., Brennecke J. The piRNA pathway: a fly's perspective on the guardian of the genome. Trends Genet. 2010, 26:499-509.
145. Shelly S., Lukinova N., Bambina S., Berman A., Cherry S. Autophagy is an essential component of Drosophila immunity against vesicular stomatitis virus. Immunity 2009, 30:588-598.
146. Silva J.C., Loreto E.L., Clark J.B. Factors that affect the horizontal transfer of transposable elements. Curr. Iss. Mol. Biol. 2004, 6:57-71.
147. Sodora D.L., Allan J.S., Apetrei C., Brenchley J.M., Douek D.C., Else J.G., Estes J.D., Hahn B.H., Hirsch V.M., Kaur A., Kirchhoff F., Muller-Trutwin M., Pandrea I., Schmitz J.E., Silvestri G. Toward an AIDS vaccine: lessons from natural simian immunodeficiency virus infections of African nonhuman primate hosts. Nat. Med. 2009, 15:861-865.
148. Sorrentino R.P., Melk J.P., Govind S. Genetic analysis of contributions of dorsal group and JAK-Stat92E pathway genes to larval hemocyte concentration and the egg encapsulation response in Drosophila. Genetics 2004, 166:1343-1356.
149. Spoel S.H., Dong X. How do plants achieve immunity? Defence without specialized immune cells. Nat. Rev. Immunol. 2012, 12:89-100.
150. Starmer W.T., Weir A. Laboulbeniales associated with the Drosophila affinis subgroup in central New York. Drosophila Inf. Serv. 2001, 84:22-24.
151. Stensmyr M.C., Dweck H.K., Farhan A., Ibba I., Strutz A., Mukunda L., Linz J., Grabe V., Steck K., Lavista-Llanos S., Wicher D., Sachse S., Knaden M., Becher P.G., Seki Y., Hansson B.S. A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell 2012, 151:1345-1357.
152. Swartz J.M., Bystrom J., Dyer K.D., Nitto T., Wynn T.A., Rosenberg H.F. Plasminogen activator inhibitor-2 (PAI-2) in eosinophilic leukocytes. J. Leukoc. Biol. 2004, 76:812-819.
153. Tahar R., Boudin C., Thiery I., Bourgouin C. Immune response of Anopheles gambiae to the early sporogonic stages of the human malaria parasite Plasmodium falciparum. EMBO J. 2002, 21:6673-6680.
154. Teixeira L., Ferreira A., Ashburner M. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol. 2008, 6:e2.
155. Thomas-Orillard M. Interaction between a picornavirus and a wild population of Drosophila melanogaster. Oecologia 1988, 75:516-520.
156. Tidbury H.J., Pedersen A.B., Boots M. Within and transgenerational immune priming in an insect to a DNA virus. Proc. Biol. Sci. 2011, 278:871-876.
157. Tripet F. Ecological immunology of mosquito-malaria interactions: of non-natural versus natural model systems and their inferences. Parasitology 2009, 136:1935-1942.
158. Tsai C.W., McGraw E.A., Ammar E.D., Dietzgen R.G., Hogenhout S.A. Drosophila melanogaster mounts a unique immune response to the Rhabdovirus sigma virus. Appl. Environ. Microbiol. 2008, 74:3251-3256.
159. Unckless R.L. A DNA virus of Drosophila. PLoS ONE 2011, 6:e26564.
160. Vallet-Gely I., Opota O., Boniface A., Novikov A., Lemaitre B. A secondary metabolite acting as a signalling molecule controls Pseudomonas entomophila virulence. Cell. Microbiol. 2010, 12:1666-1679.
161. van der Wilk F., Dullemans A.M., Verbeek M., van den Heuvel J. Isolation and characterization of APSE-1, a bacteriophage infecting the secondary endosymbiont of Acyrthosiphon pisum. Virology 1999, 262:104-113.
162. van Rij R.P., Saleh M.C., Berry B., Foo C., Houk A., Antoniewski C., Andino R. The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster. Genes Dev. 2006, 20:2985-2995.
163. Vodovar N., Vinals M., Liehl P., Basset A., Degrouard J., Spellman P., Boccard F., Lemaitre B. Drosophila host defense after oral infection by an entomopathogenic Pseudomonas species. Proc. Natl. Acad. Sci. USA 2005, 102:11414-11419.
164. Vodovar N., Vallenet D., Cruveiller S., Rouy Z., Barbe V., Acosta C., Cattolico L., Jubin C., Lajus A., Segurens B., Vacherie B., Wincker P., Weissenbach J., Lemaitre B., Medigue C., Boccard F. Complete genome sequence of the entomopathogenic and metabolically versatile soil bacterium Pseudomonas entomophila. Nat. Biotechnol. 2006, 24:673-679.
165. Weeks A.R., Turelli M., Harcombe W.R., Reynolds K.T., Hoffmann A.A. From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol. 2007, 5:997-1005.
166. Wilfert L., Longdon B., Ferreira A.G., Bayer F., Jiggins F.M. Trypanosomatids are common and diverse parasites of Drosophila. Parasitology 2011, 18:1-8.
167. Williams M.J., Ando I., Hultmark D. Drosophila melanogaster Rac2 is necessary for a proper cellular immune response. Genes Cells 2005, 10:813-823.
168. Wong Z.S., Hedges L.M., Brownlie J.C., Johnson K.N. Wolbachia-mediated antibacterial protection and immune gene regulation in Drosophila. PLoS ONE 2011, 6:e25430.
169. Wu J.L., Nishioka T., Mori K., Nishizawa T., Muroga K. A time-course study on the resistance of Penaeus japonicus induced by artificial infection with white spot syndrome virus. Fish Shellfish Immunol. 2002, 13:391-403.
170. Xie J., Vilchez I., Mateos M. Spiroplasma bacteria enhance survival of Drosophila hydei attacked by the parasitic wasp Leptopilina heterotoma. PLoS ONE 2010, 5:e12149.
171. Xie J., Tiner B., Vilchez I., Mateos M. Effect of the Drosophila endosymbiont spiroplasma on parasitoid wasp development and on the reproductive fitness of wasp-attacked fly survivors. Evol. Ecol. 2011, 25:1065-1079.
172. Zambon R.A., Vakharia V.N., Wu L.P. RNAi is an antiviral immune response against a dsRNA virus in Drosophila melanogaster. Cell. Microbiol. 2006, 8:880-889.
173. Zettervall C.J., Anderl I., Williams M.J., Palmer R., Kurucz E., Ando I., Hultmark D. A directed screen for genes involved in Drosophila blood cell activation. Proc. Natl. Acad. Sci. USA 2004, 101:14192-14197.
174. Zheng Y., Ren P.P., Wang J.L., Wang Y.F. Wolbachia-induced cytoplasmic incompatibility is associated with decreased Hira expression in male Drosophila. PLoS ONE 2011, 6:e19512.
175. Zheng Y., Wang J.L., Liu C., Wang C.P., Walker T., Wang Y.F. Differentially expressed profiles in the larval testes of Wolbachia infected and uninfected Drosophila. BMC Genomics 2011, 12:595.