Parasitoid wasp virulence: A window into fly immunity

Fly

Volumn 7, Issue 4, 2013, Pages

  Mortimer, Nathan T ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

Calcium; Drosophila; Encapsulation; Ganaspis; Immunity; Parasitoid; SERCA

Indexed keywords

DROSOPHILA MELANOGASTER; GANASPIS; MAMMALIA;

WASP VENOM;

ANIMAL; CALCIUM SIGNALING; CELLULAR IMMUNITY; DROSOPHILA MELANOGASTER; DRUG EFFECTS; FEMALE; HOST PARASITE INTERACTION; IMMUNOLOGY; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY; VIRULENCE; WASP;

ANIMALS; CALCIUM SIGNALING; DROSOPHILA MELANOGASTER; FEMALE; HOST-PARASITE INTERACTIONS; IMMUNITY, CELLULAR; VIRULENCE; WASP VENOMS; WASPS;

EID: 84887432801     PISSN: 19336934     EISSN: 19336942     Source Type: Journal    
DOI: None     Document Type: Article

References (66)

1. Hoffmann JA, Kafatos FC, Janeway CA, Ezekowitz RA. Phylogenetic perspectives in innate immunity. Science 1999; 284:1313-8; http:// dx.doi.org /10.1126/ scienc e.284.5418.1313; PMID:10334979
2. Khush RS, Lemaitre B. Genes that fight infection: what the Drosophila genome says about animal immunity. Trends Genet 2000; 16:442-9; http:// dx.doi.org/10.1016/S0168-9525(00)02095-3; PMID:11050330
3. Brandt SM, Jaramillo-Gutierrez G, Kumar S, Barillas-Mury C, Schneider DS. Use of a Drosophila model to identify genes regulating Plasmodium growth in the mosquito. Genetics 2008; 180:1671-8; http://dx.doi.org/10.1534/genetics.108.089748; PMID:18791251
4. Tzou P, De Gregorio E, Lemaitre B. How Drosophila combats microbial infection: a model to study innate immunity and host-pathogen interactions. Curr Opin Microbiol 2002; 5:102-10; http:// dx.doi.org/10.1016/S1369-5274(02) 00294-1; PMID:11834378
5. Lemaitre B, Hoffmann J. The host defense of Drosophila melanogaster. Annu Rev Immunol 2007; 25:697-743; http://dx.doi.org/10.1146/annurev. immunol.25.022106.141615; PMID:17201680
6. Brennan CA, Anderson KV. Drosophila: the genetics of innate immune recognition and response. Annu Rev Immunol 2004; 22:457-83; http://dx.doi. org/10.1146/annurev.immunol.22.012703.104626; PMID:15032585
7. Lemaitre B, Kromer-Metzger E, Michaut L, Nicolas E, Meister M, Georgel P, Reichhart JM, Hoffmann JA. A recessive mutation, immune deficiency (imd), defines two distinct control pathways in the Drosophila host defense. Proc Natl Acad Sci U S A 1995; 92:9465-9; http://dx.doi.org/10.1073/ pnas.92.21.9465; PMID:7568155
8. Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA. The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 1996; 86:973-83; http://dx.doi.org/10.1016/S0092-8674(00)80172-5; PMID:8808632
9. Lemaitre B, Reichhart JM, Hoffmann JA. Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc Natl Acad Sci U S A 1997; 94:14614-9; http://dx.doi.org/10.1073/ pnas.94.26.14614; PMID:9405661
10. Stuart LM, Ezekowitz RA. Phagocytosis and comparative innate immunity: learning on the fly. Nat Rev Immunol 2008; 8:131-41; http://dx.doi. org/10.1038/nri2240; PMID:18219310
11. Meister M, Lagueux M. Drosophila blood cells. Cell Microbiol 2003; 5:573-80; http:// dx.doi.org/10.1046/j.1462-5822.2003.00302.x; PMID:12925127
12. Williams MJ. Drosophila hemopoiesis and cellular immunity. J Immunol 2007; 178:4711-6; PMID:17404248
13. Carton Y, Bouletreau M, van Alphen JJM, van Lenteren JC. The Drosophila parasitic wasps. In: Ashburner M, Carson L, Thompson JN, eds. The Genetics and Biology of Drosophila. London: Academic Press, 1986:347-94.
14. Keebaugh ES, Schlenke TA. Insights from natural host-parasite interactions: The Drosophila model. Dev Comp Immunol 2013; http://dx.doi. org/10.1016/j.dci.2013.06.001; PMID:23764256
15. Carton Y, Nappi AJ. Drosophila cellular immunity against parasitoids. Parasitol Today 1997; 13:218-27; http://dx.doi.org/10.1016/S0169-4758(97)01058-2; PMID:15275074
16. 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; 112:135-42; http://dx.doi. org/10.1017/S0031182000065173; PMID:8587797
17. Mortimer NT, Kacsoh BZ, Keebaugh ES, Schlenke TA. Mgat1-dependent N-glycosylation of membrane components primes Drosophila melanogaster blood cells for the cellular encapsulation response. PLoS Pathog 2012; 8:e1002819; http://dx.doi.org/10.1371/ journal.ppat.1002819; PMID:22829770
18. Mortimer NT, Goecks J, Kacsoh BZ, Mobley JA, Bowersock GJ, Taylor J, Schlenke TA. Parasitoid wasp venom SERCA regulates Drosophila calcium levels and inhibits cellular immunity. Proc Natl Acad Sci U S A 2013; 110:9427-32; http://dx.doi.org/10.1073/ pnas.1222351110; PMID:23690612
19. Williams MJ, Ando I, Hultmark D. Drosophila melanogaster Rac2 is necessary for a proper cellular immune response. Genes Cells 2005; 10:813-23; http://dx.doi.org/10.1111/j.1365-2443.2005.00883.x; PMID:16098145
20. Williams MJ. The Drosophila cell adhesion molecule Neuroglian regulates Lissencephaly-1 localisation in circulating immunosurveillance cells. BMC Immunol 2009; 10:17; http://dx.doi.org/10.1186/1471-2172-10-17; PMID:19320973
21. Lanot R, Zachary D, Holder F, Meister M. Postembryonic hematopoiesis in Drosophila. Dev Biol 2001; 230:243-57; http://dx.doi.org/10.1006/ dbio.2000.0123; PMID:11161576
22. Sorrentino RP, Carton Y, Govind S. Cellular immune response to parasite infection in the Drosophila lymph gland is developmentally regulated. Dev Biol 2002; 243:65-80; http://dx.doi.org/10.1006/ dbio.2001.0542; PMID:11846478
23. Márkus R, Laurinyecz B, Kurucz E, Honti V, Bajusz I, Sipos B, Somogyi K, Kronhamn J, Hultmark D, Andó I. Sessile hemocytes as a hematopoietic compartment in Drosophila melanogaster. Proc Natl Acad Sci U S A 2009; 106:4805-9; http://dx.doi. org/10.1073/pnas.0801766106; PMID:19261847
24. Nappi A, Poirié 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; http://dx.doi.org/10.1016/S0065-308X(09)70004-1; PMID:19773068
25. Fauvarque MO, Williams MJ. Drosophila cellular immunity: a story of migration and adhesion. J Cell Sci 2011; 124:1373-82; http://dx.doi.org/10.1242/ jcs.064592; PMID:21502134
26. Howell L, Sampson CJ, Xavier MJ, Bolukbasi E, Heck MM, Williams MJ. A directed miniscreen for genes involved in the Drosophila anti-parasitoid immune response. Immunogenetics 2012; 64:155-61; http://dx.doi.org/10.1007/s00251-011-0571-3; PMID:21947570
27. Kaeslin M, Pfister-Wilhelm R, Lanzrein B. Influence of the parasitoid Chelonus inanitus and its polydnavirus on host nutritional physiology and implications for parasitoid development. J Insect Physiol 2005; 51:1330-9; http://dx.doi.org/10.1016/j. jinsphys.2005.08.003; PMID:16203013
28. Weisel-Eichler A, Haspel G, Libersat F. Venom of a parasitoid wasp induces prolonged grooming in the cockroach. J Exp Biol 1999; 202:957-64; PMID:10085268
29. Schlenke TA, Morales J, Govind S, Clark AG. Contrasting infection strategies in generalist and specialist wasp parasitoids of Drosophila melanogaster. PLoS Pathog 2007; 3:1486-501; http://dx.doi.org/10.1371/journal.ppat.0030158; PMID:17967061
30. Carton Y, Frey F, Nappi AJ. Parasite-induced changes in nitric oxide levels in Drosophila paramelanica. J Parasitol 2009; 95:1134-41; http://dx.doi. org/10.1645/GE-2091.1; PMID:19388790
31. Rizki TM, Rizki RM, Carton Y. Leptopilina heterotoma and L. boulardi: strategies to avoid cellular defense responses of Drosophila melanogaster. Exp Parasitol 1990; 70:466-75; http://dx.doi.org/10.1016/0014-4894(90)90131-U; PMID:2108875
32. Moreau SJ, Eslin P, Giordanengo P, Doury G. Comparative study of the strategies evolved by two parasitoids of the genus Asobara to avoid the immune response of the host, Drosophila melanogaster. Dev Comp Immunol 2003; 27:273-82; http:// dx.doi.org/10.1016/S0145-305X(02) 00101-5; PMID:12590961
33. Poirié M, Carton Y, Dubuffet A. Virulence strategies in parasitoid Hymenoptera as an example of adaptive diversity. C R Biol 2009; 332:311-20; http://dx.doi. org/10.1016/j.crvi.2008.09.004; PMID:19281961
34. Eslin P, Giordanengo P, Fourdrain Y, Prevost G. Avoidance of encapsulation in the absence of VLP by a braconid parasitoid of Drosophila larvae: an ultrastructural study. Can J Zool 1996; 74:2193-8; http://dx.doi.org/10.1139/z96-248
35. Monconduit H, Prevost G. Avoidance of encapsulation by Asobara tabida, a larval parasitoid of Drosophila species. Nor J Agric Sci 1994; (Supplement 16): 301-9
36. Eslin P, Prévost G. Racing against host's immunity defenses: a likely strategy for passive evasion of encapsulation in Asobara tabida parasitoids. J Insect Physiol 2000; 46:1161-7; http://dx.doi.org/10.1016/ S0022-1910(99)00227-9; PMID:10818243
37. Rizki TM, Rizki RM. Developmental analysis of a temperature-sensitive melanotic tumor mutant in Drosophila melanogaster. Wilhelm Roux's Archives 1980; 189:197-206; http://dx.doi.org/10.1007/ BF00868678
38. Labrosse C, Eslin P, Doury G, Drezen JM, Poirié 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; 51:161-70; http://dx.doi.org/10.1016/j.jinsphys.2004.10.004; PMID:15749101
39. Colinet D, Schmitz A, Depoix D, Crochard D, Poirié M. Convergent use of RhoGAP toxins by eukaryotic parasites and bacterial pathogens. PLoS Pathog 2007; 3:e203; http://dx.doi.org/10.1371/journal. ppat.0030203; PMID:18166080
40. Rizki RM, Rizki TM. Selective destruction of a host blood cell type by a parasitoid wasp. Proc Natl Acad Sci U S A 1984; 81:6154-8; http://dx.doi. org/10.1073/pnas.81.19.6154; PMID:6435126
41. Rizki RM, Rizki TM. Parasitoid virus-like particles destroy Drosophila cellular immunity. Proc Natl Acad Sci U S A 1990; 87:8388-92; http://dx.doi. org/10.1073/pnas.87.21.8388; PMID:2122461
42. Morales J, Chiu H, Oo T, Plaza R, Hoskins S, Govind S. Biogenesis, structure, and immune-suppressive effects of virus-like particles of a Drosophila parasitoid, Leptopilina victoriae. J Insect Physiol 2005; 51:181-95; http://dx.doi.org/10.1016/j. jinsphys.2004.11.002; PMID:15749103
43. Chiu H, Govind S. Natural infection of D. melanogaster by virulent parasitic wasps induces apoptotic depletion of hematopoietic precursors. Cell Death Differ 2002; 9:1379-81; http://dx.doi. org/10.1038/sj.cdd.4401134; PMID:12478476
44. Mabiala-Moundoungou AD, Doury G, Eslin P, Cherqui A, Prévost G. Deadly venom of Asobara japonica parasitoid needs ovarian antidote to regulate host physiology. J Insect Physiol 2010; 56:35-41; http://dx.doi.org/10.1016/j.jinsphys.2009.09.001; PMID:19769980
45. Colinet D, Dubuffet A, Cazes D, Moreau S, Drezen JM, Poirié M. A serpin from the parasitoid wasp Leptopilina boulardi targets the Drosophila phenoloxidase cascade. Dev Comp Immunol 2009; 33:681-9; http://dx.doi.org/10.1016/j. dci.2008.11.013; PMID:19109990
46. Colinet D, Cazes D, Belghazi M, Gatti JL, Poirié M. Extracellular superoxide dismutase in insects: characterization, function, and interspecific variation in parasitoid wasp venom. J Biol Chem 2011; 286:40110-21; http://dx.doi.org/10.1074/jbc. M111.288845; PMID:21937434
47. Labrosse C, Stasiak K, Lesobre J, Grangeia A, Huguet E, Drezen JM, 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; http://dx.doi.org/10.1016/j. ibmb.2004.10.004; PMID:15681220
48. Moreau SJ, Cherqui A, Doury G, Dubois F, Fourdrain Y, Sabatier L, Bulet P, Saarela J, Prévost G, Giordanengo P. Identification of an aspartylglucosaminidase-like protein in the venom of the parasitic wasp Asobara tabida (Hymenoptera: Braconidae). Insect Biochem Mol Biol 2004; 34:485-92; http://dx.doi.org/10.1016/j.ibmb.2004.03.001; PMID:15110870
49. Heavner ME, Gueguen G, Rajwani R, Pagan PE, 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; 526:195-204; http://dx.doi.org/10.1016/j. gene.2013.04.080; PMID:23688557
50. Goecks J, Mortimer NT, Mobley JA, Bowersock GJ, Taylor J, Schlenke TA. Integrative approach reveals composition of endoparasitoid wasp venoms. PLoS One 2013; 8:e64125; http://dx.doi.org/10.1371/ journal.pone.0064125; PMID:23717546
51. Colinet D, Deleury E, Anselme C, Cazes D, Poulain J, Azema-Dossat C, Belghazi M, Gatti JL, Poirié 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; 43:601-11; http://dx.doi. org/10.1016/j.ibmb.2013.03.010; PMID:23557852
52. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney SA, Schreiter ER, et al. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 2009; 6:875-81; http:// dx.doi.org/10.1038/nmeth.1398; PMID:19898485
53. Lytton J, Westlin M, Hanley MR. Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps. J Biol Chem 1991; 266:17067-71; PMID:1832668
54. Vet LEM. Host-habitat location through olfactory cues by Leptopilina clavipes (Hartig) (Hym, Eucoilidae), a parasitoid of fungivorous Drosophila-the influence of conditioning. Neth J Zool 1983; 33:225-48; http://dx.doi.org/10.1163/002829683X00101
55. Harrisingh MC, Wu Y, Lnenicka GA, Nitabach MN. Intracellular Ca2+ regulates free-running circadian clock oscillation in vivo. J Neurosci 2007; 27:12489-99; http://dx.doi.org/10.1523/ JNEUROSCI.3680-07.2007; PMID:18003827
56. Clapham DE. Calcium signaling. Cell 2007; 131:1047-58; http://dx.doi.org/10.1016/j. cell.2007.11.028; PMID:18083096
57. Vig M, Kinet JP. Calcium signaling in immune cells. Nat Immunol 2009; 10:21-7; http://dx.doi. org/10.1038/ni.f.220; PMID:19088738
58. Cuttell L, Vaughan A, Silva E, Escaron CJ, Lavine M, Van Goethem E, Eid JP, Quirin M, Franc NC. Undertaker, a Drosophila Junctophilin, links Draper-mediated phagocytosis and calcium homeostasis. Cell 2008; 135:524-34; http://dx.doi.org/10.1016/j. cell.2008.08.033; PMID:18984163
59. Sanyal S, Consoulas C, Kuromi H, Basole A, Mukai L, Kidokoro Y, Krishnan KS, Ramaswami M. Analysis of conditional paralytic mutants in Drosophila sarco-endoplasmic reticulum calcium ATPase reveals novel mechanisms for regulating membrane excitability. Genetics 2005; 169:737-50; http://dx.doi.org/10.1534/genetics.104.031930; PMID:15520268
60. Venkiteswaran G, Hasan G. Intracellular Ca2+ signaling and store-operated Ca2+ entry are required in Drosophila neurons for flight. Proc Natl Acad Sci U S A 2009; 106:10326-31; http://dx.doi. org/10.1073/pnas.0902982106; PMID:19515818
61. Salt GW. The cellular defense reactions of insects. Cambridge University Press, 1970.
62. Williams MJ, Wiklund ML, Wikman S, Hultmark D. Rac1 signalling in the Drosophila larval cellular immune response. J Cell Sci 2006; 119:2015-24; http://dx.doi.org/10.1242/jcs.02920; PMID:16621891
63. Dode L, Andersen JP, Leslie N, Dhitavat J, Vilsen B, Hovnanian A. Dissection of the functional differences between sarco(endo)plasmic reticulum Ca2+-ATPase (SERCA) 1 and 2 isoforms and characterization of Darier disease (SERCA2) mutants by steady-state and transient kinetic analyses. J Biol Chem 2003; 278:47877-89; http://dx.doi.org/10.1074/jbc. M306784200; PMID:12975374
64. Vangheluwe P, Raeymaekers L, Dode L, Wuytack F. Modulating sarco(endo)plasmic reticulum Ca2+ ATPase 2 (SERCA2) activity: cell biological implications. Cell Calcium 2005; 38:291-302; ht tp: //dx. doi.org/10.1016/j.ceca.2005.06.033; PMID:16105684
65. Chiu H, Morales J, Govind S. Identification and immuno-electron microscopy localization of p40, a protein component of immunosuppressive virus-like particles from Leptopilina heterotoma, a virulent parasitoid wasp of Drosophila. J Gen Virol 2006; 87:461-70; http://dx.doi.org/10.1099/vir.0.81474-0; PMID:16432035
66. Gueguen G, Rajwani R, Paddibhatla I, Morales J, Govind S. VLPs of Leptopilina boulardi share biogenesis and overall stellate morphology with VLPs of the heterotoma clade. Virus Res 2011; 160:159-65; http://dx.doi.org/10.1016/j.virusres.2011.06.005; PMID:21704090