The Toll-Dorsal Pathway Is Required for Resistance to Viral Oral Infection in
Pathogenic microbes can enter their hosts through different routes. This can have a strong impact on which host defensive mechanisms are elicited and in disease outcome. We used the model organism Drosophila melanogaster to understand how resistance to viruses differs between infection by direct virus entry into the body cavity and infection through feeding on food with the virus. We show that the Toll pathway is required to resist oral infection with different RNA viruses. On the other hand this pathway does not influence the outcome of viral infection performed by injection. Together our results show that the Toll pathway has a route-specific general antiviral effect. Our work expands the role of this classical innate immunity pathway and contributes to a better understanding of viral oral infection resistance in insects. This is particularly relevant because insect vectors of emerging human viral diseases, like dengue, are infected through feeding on contaminated hosts.
Vyšlo v časopise:
The Toll-Dorsal Pathway Is Required for Resistance to Viral Oral Infection in. PLoS Pathog 10(12): e32767. doi:10.1371/journal.ppat.1004507
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004507
Souhrn
Pathogenic microbes can enter their hosts through different routes. This can have a strong impact on which host defensive mechanisms are elicited and in disease outcome. We used the model organism Drosophila melanogaster to understand how resistance to viruses differs between infection by direct virus entry into the body cavity and infection through feeding on food with the virus. We show that the Toll pathway is required to resist oral infection with different RNA viruses. On the other hand this pathway does not influence the outcome of viral infection performed by injection. Together our results show that the Toll pathway has a route-specific general antiviral effect. Our work expands the role of this classical innate immunity pathway and contributes to a better understanding of viral oral infection resistance in insects. This is particularly relevant because insect vectors of emerging human viral diseases, like dengue, are infected through feeding on contaminated hosts.
Zdroje
1. LeggettHC, CornwallisCK, WestSA (2012) Mechanisms of pathogenesis, infective dose and virulence in human parasites. PLoS Pathog 8: e1002512 doi:10.1371/journal.ppat.1002512
2. MartinsNE, FariaVG, TeixeiraL, MagalhãesS, SucenaÉ (2013) Host adaptation is contingent upon the infection route taken by pathogens. PLoS Pathog 9: e1003601 doi:10.1371/journal.ppat.1003601
3. ClaytonDH, TompkinsDM (1994) Ectoparasite virulence is linked to mode of transmission. Proc Biol Sci 256: 211–217 doi:10.1098/rspb.1994.0072
4. AgnewP, KoellaJC (1997) Virulence, parasite mode of transmission, and host fluctuating asymmetry. Proc Biol Sci 264: 9–15 doi:10.1098/rspb.1997.0002
5. TeixeiraL (2012) Whole-genome expression profile analysis of Drosophila melanogaster immune responses. Brief Funct Genomics 11: 375–386 doi:10.1093/bfgp/els043
6. LemaitreB, MeisterM, GovindS, GeorgelP, StewardR, et al. (1995) Functional analysis and regulation of nuclear import of dorsal during the immune response in Drosophila. EMBO J 14: 536–545.
7. LemaitreB, NicolasE, MichautL, ReichhartJM, HoffmannJA (1996) The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86: 973–983 doi:10.1016/S0092-8674(00)80172-5
8. KylstenP, SamakovlisC, HultmarkD (1990) The cecropin locus in Drosophila; a compact gene cluster involved in the response to infection. EMBO J 9: 217–224.
9. WickerC, ReichhartJM, HoffmannD, HultmarkD, SamakovlisC, et al. (1990) Insect immunity. Characterization of a Drosophila cDNA encoding a novel member of the diptericin family of immune peptides. J Biol Chem 265: 22493–22498.
10. TzouP, OhresserS, FerrandonD, CapovillaM, ReichhartJ-M, et al. (2000) Tissue-Specific Inducible Expression of Antimicrobial Peptide Genes in Drosophila Surface Epithelia. Immunity 13: 737–748 doi:10.1016/S1074-7613(00)00072-8
11. Zaidman-RémyA, HervéM, PoidevinM, Pili-FlouryS, KimM, et al. (2006) The Drosophila amidase PGRP-LB modulates the immune response to bacterial infection. Immunity 24: 463–473 doi:10.1016/j.immuni.2006.02.012
12. Bosco-DrayonV, PoidevinM, BonecaIG, Narbonne-ReveauK, RoyetJ, et al. (2012) Peptidoglycan sensing by the receptor PGRP-LE in the Drosophila gut induces immune responses to infectious bacteria and tolerance to microbiota. Cell Host Microbe 12: 153–165 doi:10.1016/j.chom.2012.06.002
13. BuchonN, BroderickNA, PoidevinM, PradervandS, LemaitreB (2009) Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe 5: 200–211 doi:10.1016/j.chom.2009.01.003
14. VodovarN, VinalsM, LiehlP, BassetA, DegrouardJ, et al. (2005) Drosophila host defense after oral infection by an entomopathogenic Pseudomonas species. Proc Natl Acad Sci U S A 102: 11414–11419 doi:10.1073/pnas.0502240102
15. NehmeNT, LiégeoisS, KeleB, GiammarinaroP, PradelE, et al. (2007) A model of bacterial intestinal infections in Drosophila melanogaster. PLoS Pathog 3: e173 doi:10.1371/journal.ppat.0030173
16. YueC, GenerschE (2005) RT-PCR analysis of Deformed wing virus in honeybees (Apis mellifera) and mites (Varroa destructor). J Gen Virol 86: 3419–3424 doi:10.1099/vir.0.81401-0
17. ShenM, YangX, Cox-FosterD, CuiL (2005) The role of varroa mites in infections of Kashmir bee virus (KBV) and deformed wing virus (DWV) in honey bees. Virology 342: 141–149 doi:10.1016/j.virol.2005.07.012
18. ChenY, EvansJ, FeldlauferM (2006) Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. J Invertebr Pathol 92: 152–159 doi:10.1016/j.jip.2006.03.010
19. MerklingSH, van RijRP (2013) Beyond RNAi: antiviral defense strategies in Drosophila and mosquito. J Insect Physiol 59: 159–170 doi:10.1016/j.jinsphys.2012.07.004
20. SabinLR, HannaSL, CherryS (2010) Innate antiviral immunity in Drosophila. Curr Opin Immunol 22: 4–9 doi:10.1016/j.coi.2010.01.007
21. KempC, ImlerJ-L (2009) Antiviral immunity in drosophila. Curr Opin Immunol 21: 3–9 doi:10.1016/j.coi.2009.01.007
22. Brun N, Plus N (1980) The viruses of Drosophila. In: Ashburner and M, Wright TRF, editors. The genetics and Biology of Drosophila. New York: Academic Press. pp. 625–702.
23. HabayebMS, EkengrenSK, HultmarkD (2006) Nora virus, a persistent virus in Drosophila, defines a new picorna-like virus family. J Gen Virol 87: 3045–3051 doi:10.1099/vir.0.81997-0
24. HabayebMS, CanteraR, CasanovaG, EkströmJ-O, AlbrightS, et al. (2009) The Drosophila Nora virus is an enteric virus, transmitted via feces. J Invertebr Pathol 101: 29–33 doi:10.1016/j.jip.2009.02.003
25. JoussetFX, PlusN (1975) [Study of the vertical transmission and horizontal transmission of “Drosophila melanogaster” and “Drosophila immigrans” picornavirus (author's transl)]. Ann Microbiol (Paris) 126: 231–249.
26. Gomariz-ZilberE, PorasM, Thomas-OrillardM (1995) Drosophila C virus: experimental study of infectious yields and underlying pathology in Drosophila melanogaster laboratory populations. J Invertebr Pathol 65: 243–247 doi:10.1006/jipa.1995.1037
27. FilipeD, Thomas-orillardM (1998) Experimental study of a Drosophila melanogaster laboratory population infected by food contamination. Endocytobiosis Cell Res 12: 163–176.
28. Roxström-LindquistK, TereniusO, FayeI (2004) Parasite-specific immune response in adult Drosophila melanogaster: a genomic study. EMBO Rep 5: 207–212 doi:10.1038/sj.embor.7400073
29. XuJ, HopkinsK, SabinL, YasunagaA, SubramanianH, et al. (2013) ERK signaling couples nutrient status to antiviral defense in the insect gut. Proc Natl Acad Sci U S A 110: 15025–15030 doi:10.1073/pnas.1303193110
30. Van RijRP, SalehM, BerryB, FooC, HoukA, et al. (2006) The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster. Genes Dev 20: 2985–2995 doi:10.1101/gad.1482006
31. Galiana-ArnouxD, DostertC, SchneemannA, HoffmannJA, ImlerJ-L (2006) Essential function in vivo for Dicer-2 in host defense against RNA viruses in drosophila. Nat Immunol 7: 590–597 doi:10.1038/ni1335
32. WangX-H, AliyariR, LiW-X, LiH-W, KimK, et al. (2006) RNA interference directs innate immunity against viruses in adult Drosophila. Science 312: 452–454 doi:10.1126/science.1125694
33. ZambonRA, VakhariaVN, WuLP (2006) RNAi is an antiviral immune response against a dsRNA virus in Drosophila melanogaster. Cell Microbiol 8: 880–889 doi:10.1111/j.1462-5822.2006.00688.x
34. BronkhorstAW, van CleefKWR, VodovarN, InceIA, BlancH, et al. (2012) The DNA virus Invertebrate iridescent virus 6 is a target of the Drosophila RNAi machinery. Proc Natl Acad Sci U S A 109: E3604–13 doi:10.1073/pnas.1207213109
35. KempC, MuellerS, GotoA, BarbierV, ParoS, et al. (2013) Broad RNA interference-mediated antiviral immunity and virus-specific inducible responses in Drosophila. J Immunol 190: 650–658 doi:10.4049/jimmunol.1102486
36. LiH, LiWX, DingSW (2002) Induction and suppression of RNA silencing by an animal virus. Science 296: 1319–1321 doi:10.1126/science.1070948
37. TeixeiraL, FerreiraA, AshburnerM (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6: e2 doi:10.1371/journal.pbio.1000002
38. HedgesLM, BrownlieJC, O'NeillSL, JohnsonKN (2008) Wolbachia and virus protection in insects. Science 322: 702 doi:10.1126/science.1162418
39. RancèsE, YeYH, WoolfitM, McGraw Ea, O'NeillSL (2012) The relative importance of innate immune priming in Wolbachia-mediated dengue interference. PLoS Pathog 8: e1002548 doi:10.1371/journal.ppat.1002548
40. GlaserRL, MeolaMA (2010) The native Wolbachia endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to West Nile virus infection. PLoS ONE 5: e11977 doi:10.1371/journal.pone.0011977
41. DostertC, JouanguyE, IrvingP, TroxlerL, Galiana-ArnouxD, et al. (2005) The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of drosophila. Nat Immunol 6: 946–953 doi:10.1038/ni1237
42. CostaA, JanE, SarnowP, SchneiderD (2009) The Imd pathway is involved in antiviral immune responses in Drosophila. PLoS ONE 4: e7436 doi:10.1371/journal.pone.0007436
43. AvadhanulaV, WeasnerBP, HardyGG, KumarJP, HardyRW (2009) A novel system for the launch of alphavirus RNA synthesis reveals a role for the Imd pathway in arthropod antiviral response. PLoS Pathog 5: e1000582 doi:10.1371/journal.ppat.1000582
44. SabatierL, JouanguyE, DostertC, ZacharyD, DimarcqJ-L, et al. (2003) Pherokine-2 and -3. Eur J Biochem 270: 3398–3407 doi:10.1046/j.1432-1033.2003.03725.x
45. IpYT, ReachM, EngstromY, KadalayilL, CaiH, et al. (1993) Dif, a dorsal-related gene that mediates an immune response in Drosophila. Cell 75: 753–763.
46. MengX, KhanujaBS, IpYT (1999) Toll receptor-mediated Drosophila immune response requires Dif, an NF-kappaB factor. Genes Dev 13: 792–797.
47. ManfruelliP, ReichhartJM, StewardR, HoffmannJA, LemaitreB (1999) A mosaic analysis in Drosophila fat body cells of the control of antimicrobial peptide genes by the Rel proteins Dorsal and DIF. EMBO J 18: 3380–3391 doi:10.1093/emboj/18.12.3380
48. ZambonRA, NandakumarM, VakhariaVN, WuLP (2005) The Toll pathway is important for an antiviral response in Drosophila. Proc Natl Acad Sci U S A 102: 7257–7262 doi:10.1073/pnas.0409181102
49. NazziF, BrownSP, AnnosciaD, Del PiccoloF, Di PriscoG, et al. (2012) Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathog 8: e1002735 doi:10.1371/journal.ppat.1002735
50. XiZ, RamirezJL, DimopoulosG (2008) The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathog 4: e1000098 doi:10.1371/journal.ppat.1000098
51. JohnsonKN, ChristianPD (1998) The novel genome organization of the insect picorna-like virus Drosophila C virus suggests this virus belongs to a previously undescribed virus family. J Gen Virol 79 (Pt 1) 191–203.
52. RyderE, BlowsF, AshburnerM, Bautista-LlacerR, CoulsonD, et al. (2004) The DrosDel collection: a set of P-element insertions for generating custom chromosomal aberrations in Drosophila melanogaster. Genetics 167: 797–813 doi:10.1534/genetics.104.026658
53. RutschmannS, JungAC, HetruC, ReichhartJ-M, HoffmannJA, et al. (2000) The Rel Protein DIF Mediates the Antifungal but Not the Antibacterial Host Defense in Drosophila. Immunity 12: 569–580 doi:10.1016/S1074-7613(00)80208-3
54. RutschmannS, KilincA, FerrandonD (2002) Cutting edge: the toll pathway is required for resistance to gram-positive bacterial infections in Drosophila. J Immunol 168: 1542–1546.
55. LigoxygakisP, PelteN, HoffmannJA, ReichhartJ-M (2002) Activation of Drosophila Toll during fungal infection by a blood serine protease. Science 297: 114–116 doi:10.1126/science.1072391
56. GobertV, GottarM, MatskevichAA, RutschmannS, RoyetJ, et al. (2003) Dual activation of the Drosophila toll pathway by two pattern recognition receptors. Science 302: 2126–2130 doi:10.1126/science.1085432
57. MoreiraLA, Iturbe-OrmaetxeI, JefferyJA, LuG, PykeAT, et al. (2009) A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 139: 1268–1278 doi:10.1016/j.cell.2009.11.042
58. PanX, ZhouG, WuJ, BianG, LuP, et al. (2012) Wolbachia induces reactive oxygen species (ROS)-dependent activation of the Toll pathway to control dengue virus in the mosquito Aedes aegypti. Proc Natl Acad Sci U S A 109: E23–31 doi:10.1073/pnas.1116932108
59. RancèsE, JohnsonTK, PopoviciJ, Iturbe-OrmaetxeI, ZakirT, et al. (2013) The toll and Imd pathways are not required for wolbachia-mediated dengue virus interference. J Virol 87: 11945–11949 doi:10.1128/JVI.01522-13
60. TateJ, LiljasL, ScottiP, ChristianP, LinT, et al. (1999) The crystal structure of cricket paralysis virus: the first view of a new virus family. Nat Struct Biol 6: 765–774 doi:10.1038/11543
61. ScottiPD, DearingS, MossopDW (1983) Flock House virus: a nodavirus isolated from Costelytra zealandica (White) (Coleoptera: Scarabaeidae). Arch Virol 75: 181–189 doi:10.1007/BF01315272
62. WhalenAM, StewardR (1993) Dissociation of the dorsal-cactus complex and phosphorylation of the dorsal protein correlate with the nuclear localization of dorsal. J Cell Biol 123: 523–534.
63. MichelT, ReichhartJM, HoffmannJA, RoyetJ (2001) Drosophila Toll is activated by Gram-positive bacteria through a circulating peptidoglycan recognition protein. Nature 414: 756–759 doi:10.1038/414756a
64. ReichhartJM, GeorgelP, MeisterM, LemaitreB, KapplerC, et al. (1993) Expression and nuclear translocation of the rel/NF-kappa B-related morphogen dorsal during the immune response of Drosophila. C R Acad Sci III 316: 1218–1224.
65. GrossI, GeorgelP, Oertel-BuchheitP, SchnarrM, ReichhartJM (1999) Dorsal-B, a splice variant of the Drosophila factor Dorsal, is a novel Rel/NF-kappaB transcriptional activator. Gene 228: 233–242.
66. MatovaN, Anderson KV (2006) Rel/NF-kappaB double mutants reveal that cellular immunity is central to Drosophila host defense. Proc Natl Acad Sci U S A 103: 16424–16429 doi:10.1073/pnas.0605721103
67. HanZS, IpYT (1999) Interaction and specificity of Rel-related proteins in regulating Drosophila immunity gene expression. J Biol Chem 274: 21355–21361.
68. TanjiT, YunE-Y, IpYT (2010) Heterodimers of NF-kappaB transcription factors DIF and Relish regulate antimicrobial peptide genes in Drosophila. Proc Natl Acad Sci U S A 107: 14715–14720 doi:10.1073/pnas.1009473107
69. MatovaN, AndersonKV (2010) Drosophila Rel proteins are central regulators of a robust, multi-organ immune network. J Cell Sci 123: 627–633 doi:10.1242/jcs.060731
70. Nüsslein-VolhardC, Lohs-SchardinM, SanderK, CremerC (1980) A dorso-ventral shift of embryonic primordia in a new maternal-effect mutant of Drosophila. Nature 283: 474–476 doi:10.1038/283474a0
71. RoseD, ZhuX, KoseH, HoangB, ChoJ, et al. (1997) Toll, a muscle cell surface molecule, locally inhibits synaptic initiation of the RP3 motoneuron growth cone in Drosophila. Development 124: 1561–1571.
72. HalfonMS, HashimotoC, KeshishianH (1995) The Drosophila toll gene functions zygotically and is necessary for proper motoneuron and muscle development. Dev Biol 169: 151–167 doi:10.1006/dbio.1995.1134
73. HalfonMS, KeshishianH (1998) The Toll pathway is required in the epidermis for muscle development in the Drosophila embryo. Dev Biol 199: 164–174 doi:10.1006/dbio.1998.8915
74. SutcliffeB, ForeroMG, ZhuB, RobinsonIM, HidalgoA (2013) Neuron-type specific functions of DNT1, DNT2 and Spz at the Drosophila neuromuscular junction. PLoS One 8: e75902 doi:10.1371/journal.pone.0075902
75. HeckscherES, FetterRD, MarekKW, AlbinSD, DavisGW (2007) NF-kappaB, IkappaB, and IRAK control glutamate receptor density at the Drosophila NMJ. Neuron 55: 859–873 doi:10.1016/j.neuron.2007.08.005
76. QiuP, PanPC, GovindS (1998) A role for the Drosophila Toll/Cactus pathway in larval hematopoiesis. Development 125: 1909–1920.
77. GottarM, GobertV, Matskevich Aa, ReichhartJ-M, WangC, et al. (2006) Dual detection of fungal infections in Drosophila via recognition of glucans and sensing of virulence factors. Cell 127: 1425–1437 doi:10.1016/j.cell.2006.10.046
78. El ChamyL, LeclercV, CaldelariI, ReichhartJ-M (2008) Sensing of “danger signals” and pathogen-associated molecular patterns defines binary signaling pathways “upstream” of Toll. Nat Immunol 9: 1165–1170 doi:10.1038/ni.1643
79. ParisiF, StefanatosRK, StrathdeeK, YuY, VidalM (2014) Transformed epithelia trigger non-tissue-autonomous tumor suppressor response by adipocytes via activation of Toll and Eiger/TNF signaling. Cell Rep 6: 855–867 doi:10.1016/j.celrep.2014.01.039
80. MingM, ObataF, KuranagaE, MiuraM (2014) Persephone/Spätzle pathogen sensors mediate the activation of Toll receptor signaling in response to endogenous danger signals in apoptosis-deficient Drosophila. J Biol Chem 289: 7558–7568 doi:10.1074/jbc.M113.543884
81. DeddoucheS, MattN, BuddA, MuellerS, KempC, et al. (2008) The DExD/H-box helicase Dicer-2 mediates the induction of antiviral activity in drosophila. Nat Immunol 9: 1425–1432 doi:10.1038/ni.1664
82. NakamotoM, MoyRH, XuJ, BambinaS, YasunagaA, et al. (2012) Virus recognition by Toll-7 activates antiviral autophagy in Drosophila. Immunity 36: 658–667 doi:10.1016/j.immuni.2012.03.003
83. HabayebMS, EkströmJ-O, HultmarkD (2009) Nora virus persistent infections are not affected by the RNAi machinery. PLoS One 4: e5731 doi:10.1371/journal.pone.0005731
84. Di PasqualeG, ChioriniJA (2006) AAV transcytosis through barrier epithelia and endothelium. Mol Ther 13: 506–516 doi:10.1016/j.ymthe.2005.11.007
85. OuzilouL, CaliotE, PelletierI, PrévostM-C, PringaultE, et al. (2002) Poliovirus transcytosis through M-like cells. J Gen Virol 83: 2177–2182.
86. WangY, Gosselin GrenetAS, CastelliI, CermenatiG, RavallecM, et al. (2013) Densovirus crosses the insect midgut by transcytosis and disturbs the epithelial barrier function. J Virol 87: 12380–12391 doi:10.1128/JVI.01396-13
87. LiuB, BehuraSK, ClemRJ, SchneemannA, BecnelJ, et al. (2013) P53-mediated rapid induction of apoptosis conveys resistance to viral infection in Drosophila melanogaster. PLoS Pathog 9: e1003137 doi:10.1371/journal.ppat.1003137
88. VaidyanathanR, ScottTW (2006) Apoptosis in mosquito midgut epithelia associated with West Nile virus infection. Apoptosis 11: 1643–1651 doi:10.1007/s10495-006-8783-y
89. MorganNS, SkovronskyDM, Artavanis-TsakonasS, MoosekerMS (1994) The molecular cloning and characterization of Drosophila melanogaster myosin-IA and myosin-IB. J Mol Biol 239: 347–356 doi:10.1006/jmbi.1994.1376
90. AndersonKV, Nüsslein-VolhardC (1984) Information for the dorsal–ventral pattern of the Drosophila embryo is stored as maternal mRNA. Nature 311: 223–227 doi:10.1038/311223a0
91. AndersonKV, JürgensG, Nüsslein-VolhardC (1985) Establishment of dorsal-ventral polarity in the Drosophila embryo: genetic studies on the role of the Toll gene product. Cell 42: 779–789.
92. HechtPM, AndersonKV (1993) Genetic characterization of tube and pelle, genes required for signaling between Toll and dorsal in the specification of the dorsal-ventral pattern of the Drosophila embryo. Genetics 135: 405–417.
93. Nüsslein-Volhard C (1979) Maternal effect mutations that alter the saptial coordinates of Drosophila melanogaster. In: Subtelny S, Konigsberg IR, editors. Determinats of Spatial Organization. New York: Academic Press. pp. 185–211.
94. RynesJ, DonohoeCD, FrommoltP, BrodesserS, JindraM, et al. (2012) Activating transcription factor 3 regulates immune and metabolic homeostasis. Mol Cell Biol 32: 3949–3962 doi:10.1128/MCB.00429-12
95. OsterwalderT, YoonKS, WhiteBH, KeshishianH (2001) A conditional tissue-specific transgene expression system using inducible GAL4. Proc Natl Acad Sci U S A 98: 12596–12601 doi:10.1073/pnas.221303298
96. BuchonN, OsmanD, DavidFPA, FangHY, BoqueteJ-P, et al. (2013) Morphological and molecular characterization of adult midgut compartmentalization in Drosophila. Cell Rep 3: 1725–1738 doi:10.1016/j.celrep.2013.04.001
97. O'BrienLE, SolimanSS, LiX, BilderD (2011) Altered modes of stem cell division drive adaptive intestinal growth. Cell 147: 603–614 doi:10.1016/j.cell.2011.08.048
98. ShiaAKH, GlittenbergM, ThompsonG, WeberAN, ReichhartJ-M, et al. (2009) Toll-dependent antimicrobial responses in Drosophila larval fat body require Spätzle secreted by haemocytes. J Cell Sci 122: 4505–4515 doi:10.1242/jcs.049155
99. NiJ-Q, ZhouR, CzechB, LiuL-P, HolderbaumL, et al. (2011) A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat Methods 8: 405–407 doi:10.1038/nmeth.1592
100. ChrostekE, MarialvaMSP, EstevesSS, WeinertLA, MartinezJ, et al. (2013) Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: a phenotypic and phylogenomic analysis. PLoS Genet 9: e1003896 doi:10.1371/journal.pgen.1003896
101. ScottiPD (1977) End-point dilution and plaque assay methods for titration of cricket paralysis virus in cultured Drosophila cells. J Gen Virol 35: 393–396.
102. SchindelinJ, Arganda-CarrerasI, FriseE, KaynigV, LongairM, et al. (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9: 676–682 doi:10.1038/nmeth.2019
103. ChuDT, KlymkowskyMW (1989) The appearance of acetylated alpha-tubulin during early development and cellular differentiation in Xenopus. Dev Biol 136: 104–117.
104. PfafflMW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29: e45.
105. SharonG, SegalD, RingoJM, HefetzA, Zilber-RosenbergI, et al. (2010) Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci U S A 107: 20051–20056 doi:10.1073/pnas.1009906107
106. RyuJ-H, KimS-H, LeeH-Y, BaiJY, NamY-D, et al. (2008) Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science 319: 777–782 doi:10.1126/science.1149357
107. R Development Core Team RFFSC (2008) R: A Language and Environment for Statistical Computing. Vienna Austria R Found Stat Comput 1: 2673.
108. Zar JH (1999) Biostatistical Analysis. Prentice Hall, New Jersey, 663 pp.
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2014 Číslo 12
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Plasma Membrane-Located Purine Nucleotide Transport Proteins Are Key Components for Host Exploitation by Microsporidian Intracellular Parasites
- Emergence of MERS-CoV in the Middle East: Origins, Transmission, Treatment, and Perspectives
- Experimental Cerebral Malaria Pathogenesis—Hemodynamics at the Blood Brain Barrier
- Unique Features of HIV-1 Spread through T Cell Virological Synapses