Genetic Dissection of Gut Epithelial Responses to
In malaria vector mosquitoes, the presence of bacteria and malaria parasites is tightly linked. Bacteria that are part of the mosquito gut ecosystem are critical modulators of the immune response elicited during infection with malaria parasites. Furthermore, responses against oral bacterial infections can affect malaria parasites. Here, we combined mosquito gut infections with the enterobacterium Serratia marcescens with genome-wide discovery and phenotypic analysis of genes involved in antibacterial responses to characterize molecular processes that control gut bacterial infections thus possibly affecting the mosquito susceptibility to infection by malaria parasites. Our data reveal complex genetic networks controlling the gut bacterial infection load and ecosystem homeostasis. These networks appear to exhibit much higher specificity toward specific classes of bacteria than previously thought and include behavioral response circuits involved in antibacterial immunity.
Vyšlo v časopise:
Genetic Dissection of Gut Epithelial Responses to. PLoS Pathog 10(3): e32767. doi:10.1371/journal.ppat.1003897
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Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1003897
Souhrn
In malaria vector mosquitoes, the presence of bacteria and malaria parasites is tightly linked. Bacteria that are part of the mosquito gut ecosystem are critical modulators of the immune response elicited during infection with malaria parasites. Furthermore, responses against oral bacterial infections can affect malaria parasites. Here, we combined mosquito gut infections with the enterobacterium Serratia marcescens with genome-wide discovery and phenotypic analysis of genes involved in antibacterial responses to characterize molecular processes that control gut bacterial infections thus possibly affecting the mosquito susceptibility to infection by malaria parasites. Our data reveal complex genetic networks controlling the gut bacterial infection load and ecosystem homeostasis. These networks appear to exhibit much higher specificity toward specific classes of bacteria than previously thought and include behavioral response circuits involved in antibacterial immunity.
Zdroje
1. HarrisC, LambrechtsL, RoussetF, AbateL, NsangoSE, et al. (2010) Polymorphisms in Anopheles gambiae immune genes associated with natural resistance to Plasmodium falciparum. PLoS Pathog 6: e1001112.
2. WhiteBJ, LawniczakMK, ChengC, CoulibalyMB, WilsonMD, et al. (2011) Adaptive divergence between incipient species of Anopheles gambiae increases resistance to Plasmodium. Proc Natl Acad Sci U S A 108: 244–249.
3. RiehleMM, MarkianosK, NiareO, XuJ, LiJ, et al. (2006) Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science 312: 577–579.
4. GarverLS, BahiaAC, DasS, Souza-NetoJA, ShiaoJ, et al. (2012) Anopheles imd pathway factors and effectors in infection intensity-dependent anti-Plasmodium action. PLoS Pathog 8: e1002737.
5. MeisterS, AgianianB, TurlureF, RelogioA, MorlaisI, et al. (2009) Anopheles gambiae PGRPLC-mediated defense against bacteria modulates infections with malaria parasites. PLoS Pathog 5: e1000542.
6. SchnitgerAK, YassineH, KafatosFC, OstaMA (2009) Two C-type lectins cooperate to defend Anopheles gambiae against Gram-negative bacteria. J Biol Chem 284: 17616–17624.
7. GrossmanSR, AndersenKG, ShlyakhterI, TabriziS, WinnickiS, et al. (2013) Identifying recent adaptations in large-scale genomic data. Cell 152: 703–713.
8. SangareI, MichalakisY, YameogoB, DabireR, MorlaisI, et al. (2013) Studying fitness cost of Plasmodium falciparum infection in malaria vectors: validation of an appropriate negative control. Malar J 12: 2.
9. RaniA, SharmaA, RajagopalR, AdakT, BhatnagarRK (2009) Bacterial diversity analysis of larvae and adult midgut microflora using culture-dependent and culture-independent methods in lab-reared and field-collected Anopheles stephensi-an Asian malarial vector. BMC Microbiol 9: 96.
10. Gonzalez-CeronL, SantillanF, RodriguezMH, MendezD, Hernandez-AvilaJE (2003) Bacteria in midguts of field-collected Anopheles albimanus block Plasmodium vivax sporogonic development. J Med Entomol 40: 371–374.
11. Gendrin M, Christophides GK (2013) The Anopheles Mosquito Microbiota and Their Impact on Pathogen Transmission. In Manguin S, Ed. Anopheles mosquitoes - New insights into malaria vectors
12. BoissièreA, TchioffoMT, BacharD, AbateL, MarieA, et al. (2012) Midgut Microbiota of the Malaria Mosquito Vector Anopheles gambiae and Interactions with Plasmodium falciparum Infection. PLoS Pathogens 8: e1002742.
13. WangY, GilbreathTM3rd, KukutlaP, YanG, XuJ (2011) Dynamic Gut Microbiome across Life History of the Malaria Mosquito Anopheles gambiae in Kenya. PLoS One 6: e24767.
14. Osei-PokuJ, MbogoCM, PalmerWJ, JigginsFM (2012) Deep sequencing reveals extensive variation in the gut microbiota of wild mosquitoes from Kenya. Mol Ecol 21: 5138–5150.
15. KumarS, Molina-CruzA, GuptaL, RodriguesJ, Barillas-MuryC (2010) A peroxidase/dual oxidase system modulates midgut epithelial immunity in Anopheles gambiae. Science 327: 1644–1648.
16. DongY, ManfrediniF, DimopoulosG (2009) Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog 5: e1000423.
17. RodriguesJ, BraynerFA, AlvesLC, DixitR, Barillas-MuryC (2010) Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 329: 1353–1355.
18. CirimotichCM, DongY, ClaytonAM, SandifordSL, Souza-NetoJA, et al. (2011) Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae. Science 332: 855–858.
19. LemaitreB, HoffmannJ (2007) The host defense of Drosophila melanogaster. Annu Rev Immunol 25: 697–743.
20. KanekoT, GoldmanWE, MellrothP, SteinerH, FukaseK, et al. (2004) Monomeric and polymeric gram-negative peptidoglycan but not purified LPS stimulate the Drosophila IMD pathway. Immunity 20: 637–649.
21. ChoeKM, LeeH, AndersonKV (2005) Drosophila peptidoglycan recognition protein LC (PGRP-LC) acts as a signal-transducing innate immune receptor. Proc Natl Acad Sci U S A 102: 1122–1126.
22. MailletF, BischoffV, VignalC, HoffmannJ, RoyetJ (2008) The Drosophila peptidoglycan recognition protein PGRP-LF blocks PGRP-LC and IMD/JNK pathway activation. Cell Host Microbe 3: 293–303.
23. LhocineN, RibeiroPS, BuchonN, WepfA, WilsonR, et al. (2008) PIMS modulates immune tolerance by negatively regulating Drosophila innate immune signaling. Cell Host Microbe 4: 147–158.
24. HaEM, OhCT, BaeYS, LeeWJ (2005) A direct role for dual oxidase in Drosophila gut immunity. Science 310: 847–850.
25. CroninSJ, NehmeNT, LimmerS, LiegeoisS, PospisilikJA, et al. (2009) Genome-wide RNAi screen identifies genes involved in intestinal pathogenic bacterial infection. Science 325: 340–343.
26. 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.
27. BuchonN, BroderickNA, KuraishiT, LemaitreB (2010) Drosophila EGFR pathway coordinates stem cell proliferation and gut remodeling following infection. BMC Biol 8: 152.
28. RyuJH, KimSH, LeeHY, BaiJY, NamYD, et al. (2008) Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science 319: 777–782.
29. LeeKA, KimSH, KimEK, HaEM, YouH, et al. (2013) Bacterial-derived uracil as a modulator of mucosal immunity and gut-microbe homeostasis in Drosophila. Cell 153: 797–811.
30. HergardenAC, TaylerTD, AndersonDJ (2012) Allatostatin-A neurons inhibit feeding behavior in adult Drosophila. Proc Natl Acad Sci U S A 109: 3967–3972.
31. AdamoSA (2005) Parasitic suppression of feeding in the tobacco hornworm, Manduca sexta: parallels with feeding depression after an immune challenge. Arch Insect Biochem Physiol 60: 185–197.
32. ChakrabartiS, LiehlP, BuchonN, LemaitreB (2012) Infection-induced host translational blockage inhibits immune responses and epithelial renewal in the Drosophila gut. Cell Host Microbe 12: 60–70.
33. LiehlP, BlightM, VodovarN, BoccardF, LemaitreB (2006) Prevalence of local immune response against oral infection in a Drosophila/Pseudomonas infection model. PLoS Pathog 2: e56.
34. MiyamotoT, SloneJ, SongX, AmreinH (2012) A Fructose Receptor Functions as a Nutrient Sensor in the Drosophila Brain. Cell 151: 1113–1125.
35. MoonSJ, LeeY, JiaoY, MontellC (2009) A Drosophila gustatory receptor essential for aversive taste and inhibiting male-to-male courtship. Curr Biol 19: 1623–1627.
36. MaslowskiKM, VieiraAT, NgA, KranichJ, SierroF, et al. (2009) Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461: 1282–1286.
37. BandoH, OkadoK, GuelbeogoWM, BadoloA, AonumaH, et al. (2013) Intra-specific diversity of Serratia marcescens in Anopheles mosquito midgut defines Plasmodium transmission capacity. Sci Rep 3: 1641.
38. LawniczakMK, EmrichSJ, HollowayAK, RegierAP, OlsonM, et al. (2010) Widespread divergence between incipient Anopheles gambiae species revealed by whole genome sequences. Science 330: 512–514.
39. NeafseyDE, LawniczakMK, ParkDJ, RedmondSN, CoulibalyMB, et al. (2010) SNP genotyping defines complex gene-flow boundaries among African malaria vector mosquitoes. Science 330: 514–517.
40. GottarM, GobertV, MichelT, BelvinM, DuykG, et al. (2002) The Drosophila immune response against Gram-negative bacteria is mediated by a peptidoglycan recognition protein. Nature 416: 640–644.
41. ChoeKM, WernerT, StovenS, HultmarkD, AndersonKV (2002) Requirement for a peptidoglycan recognition protein (PGRP) in Relish activation and antibacterial immune responses in Drosophila. Science 296: 359–362.
42. LinH, ZhangL, LunaC, HoNT, ZhengL (2007) A splice variant of PGRP-LC required for expression of antimicrobial peptides in Anopheles gambiae. Insect Science 14: 185–192.
43. WatsonFL, Puttmann-HolgadoR, ThomasF, LamarDL, HughesM, et al. (2005) Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 309: 1874–1878.
44. DongY, TaylorHE, DimopoulosG (2006) AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biol 4: e229.
45. WatthanasurorotA, JiravanichpaisalP, LiuH, SoderhallI, SoderhallK (2011) Bacteria-Induced Dscam Isoforms of the Crustacean, Pacifastacus leniusculus. PLoS Pathog 7: e1002062.
46. WojtowiczWM, WuW, AndreI, QianB, BakerD, et al. (2007) A vast repertoire of Dscam binding specificities arises from modular interactions of variable Ig domains. Cell 130: 1134–1145.
47. DongY, CirimotichCM, PikeA, ChandraR, DimopoulosG (2012) Anopheles NF-kappaB-Regulated Splicing Factors Direct Pathogen-Specific Repertoires of the Hypervariable Pattern Recognition Receptor AgDscam. Cell Host Microbe 12: 521–530.
48. SmithPH, MwangiJM, AfraneYA, YanG, ObbardDJ, et al. (2011) Alternative splicing of the Anopheles gambiae Dscam gene in diverse Plasmodium falciparum infections. Malar J 10: 156.
49. ClaytonAM, CirimotichCM, DongY, DimopoulosG (2012) Caudal is a negative regulator of the Anopheles IMD Pathway that controls resistance to P. falciparum infection. Dev Comp Immunol 39 (4) 323–32.
50. XinN, BenchabaneH, TianA, NguyenK, KlofasL, et al. (2011) Erect Wing facilitates context-dependent Wnt/Wingless signaling by recruiting the cell-specific Armadillo-TCF adaptor Earthbound to chromatin. Development 138: 4955–4967.
51. DitchLM, ShirangiT, PitmanJL, LathamKL, FinleyKD, et al. (2005) Drosophila retained/dead ringer is necessary for neuronal pathfinding, female receptivity and repression of fruitless independent male courtship behaviors. Development 132: 155–164.
52. ShirangiTR, TaylorBJ, McKeownM (2006) A double-switch system regulates male courtship behavior in male and female Drosophila melanogaster. Nat Genet 38: 1435–1439.
53. DubrovskyEB, DubrovskayaVA, BernardoT, OtteV, DiFilippoR, et al. (2011) The Drosophila FTZ-F1 nuclear receptor mediates juvenile hormone activation of E75A gene expression through an intracellular pathway. J Biol Chem 286: 33689–33700.
54. FunkhouserJD, AronsonNNJr (2007) Chitinase family GH18: evolutionary insights from the genomic history of a diverse protein family. BMC Evol Biol 7: 96.
55. Dela CruzCS, LiuW, HeCH, JacobyA, GornitzkyA, et al. (2012) Chitinase 3-like-1 Promotes Streptococcus pneumoniae Killing and Augments Host Tolerance to Lung Antibacterial Responses. Cell Host Microbe 12: 34–46.
56. VolzJ, MullerHM, ZdanowiczA, KafatosFC, OstaMA (2006) A genetic module regulates the melanization response of Anopheles to Plasmodium. Cell Microbiol 8: 1392–1405.
57. VolzJ, OstaMA, KafatosFC, MullerHM (2005) The roles of two clip domain serine proteases in innate immune responses of the malaria vector Anopheles gambiae. J Biol Chem 280: 40161–40168.
58. PovelonesM, BhagavatulaL, YassineH, TanLA, UptonLM, et al. (2013) The CLIP-Domain Serine Protease Homolog SPCLIP1 Regulates Complement Recruitment to Microbial Surfaces in the Malaria Mosquito Anopheles gambiae. PLoS Pathog 9: e1003623.
59. DongY, AguilarR, XiZ, WarrE, MonginE, et al. (2006) Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog 2: e52.
60. WaterhouseRM, PovelonesM, ChristophidesGK (2010) Sequence-structure-function relations of the mosquito leucine-rich repeat immune proteins. BMC Genomics 11: 531.
61. PovelonesM, UptonLM, SalaKA, ChristophidesGK (2011) Structure-Function Analysis of the Anopheles gambiae LRIM1/APL1C Complex and its Interaction with Complement C3-Like Protein TEP1. PLoS Pathog 7: e1002023.
62. PovelonesM, WaterhouseRM, KafatosFC, ChristophidesGK (2009) Leucine-rich repeat protein complex activates mosquito complement in defense against Plasmodium parasites. Science 324: 258–261.
63. OstaMA, ChristophidesGK, KafatosFC (2004) Effects of mosquito genes on Plasmodium development. Science 303: 2030–2032.
64. KazuraJW, ZouZ, Souza-NetoJ, XiZ, KokozaV, et al. (2011) Transcriptome Analysis of Aedes aegypti Transgenic Mosquitoes with Altered Immunity. PLoS Pathogens 7: e1002394.
65. ValanneS, WangJH, RametM (2011) The Drosophila Toll signaling pathway. J Immunol 186: 649–656.
66. GarverLS, DongY, DimopoulosG (2009) Caspar controls resistance to Plasmodium falciparum in diverse anopheline species. PLoS Pathog 5: e1000335.
67. VaishnavaS, YamamotoM, SeversonKM, RuhnKA, YuX, et al. (2011) The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science 334: 255–258.
68. DongY, DimopoulosG (2009) Anopheles fibrinogen-related proteins provide expanded pattern recognition capacity against bacteria and malaria parasites. J Biol Chem 284: 9835–9844.
69. PaceKE, BaumLG (2004) Insect galectins: roles in immunity and development. Glycoconj J 19: 607–614.
70. MendesAM, Awono-AmbenePH, NsangoSE, CohuetA, FontenilleD, et al. (2011) Infection intensity dependent responses of Anopheles gambiae to African malaria parasites Plasmodium falciparum. Infect Immun 79 (11) 4708–15.
71. StyerKL, SinghV, MacoskoE, SteeleSE, BargmannCI, et al. (2008) Innate immunity in Caenorhabditis elegans is regulated by neurons expressing NPR-1/GPCR. Science 322: 460–464.
72. ReddyKC, AndersenEC, KruglyakL, KimDH (2009) A polymorphism in npr-1 is a behavioral determinant of pathogen susceptibility in C. elegans. Science 323: 382–384.
73. CirilloC, Vanden BergheP, TackJ (2011) Role of serotonin in gastrointestinal physiology and pathology. Minerva Endocrinol 36: 311–324.
74. KhanWI, GhiaJE (2010) Gut hormones: emerging role in immune activation and inflammation. Clin Exp Immunol 161: 19–27.
75. BaganzNL, BlakelyRD (2013) A dialogue between the immune system and brain, spoken in the language of serotonin. ACS Chem Neurosci 4: 48–63.
76. BecnelJ, JohnsonO, LuoJ, NasselDR, NicholsCD (2011) The serotonin 5-HT7Dro receptor is expressed in the brain of Drosophila, and is essential for normal courtship and mating. PLoS One 6: e20800.
77. JohnsonO, BecnelJ, NicholsCD (2011) Serotonin receptor activity is necessary for olfactory learning and memory in Drosophila melanogaster. Neuroscience 192: 372–381.
78. DierickHA, GreenspanRJ (2007) Serotonin and neuropeptide F have opposite modulatory effects on fly aggression. Nat Genet 39: 678–682.
79. DzitoyevaS, DimitrijevicN, ManevH (2003) Gamma-aminobutyric acid B receptor 1 mediates behavior-impairing actions of alcohol in Drosophila: adult RNA interference and pharmacological evidence. Proc Natl Acad Sci U S A 100: 5485–5490.
80. WenT, ParrishCA, XuD, WuQ, ShenP (2005) Drosophila neuropeptide F and its receptor, NPFR1, define a signaling pathway that acutely modulates alcohol sensitivity. Proc Natl Acad Sci U S A 102: 2141–2146.
81. Shohat-OphirG, KaunKR, AzanchiR, HeberleinU (2012) Sexual deprivation increases ethanol intake in Drosophila. Science 335: 1351–1355.
82. HillCA, FoxAN, PittsRJ, KentLB, TanPL, et al. (2002) G protein-coupled receptors in Anopheles gambiae. Science 298: 176–178.
83. BrayS, AmreinH (2003) A putative Drosophila pheromone receptor expressed in male-specific taste neurons is required for efficient courtship. Neuron 39: 1019–1029.
84. MiyamotoT, AmreinH (2008) Suppression of male courtship by a Drosophila pheromone receptor. Nat Neurosci 11: 874–876.
85. WatanabeK, TobaG, KoganezawaM, YamamotoD (2011) Gr39a, a highly diversified gustatory receptor in Drosophila, has a role in sexual behavior. Behav Genet 41: 746–753.
86. WangL, HanX, MehrenJ, HiroiM, BilleterJC, et al. (2011) Hierarchical chemosensory regulation of male-male social interactions in Drosophila. Nat Neurosci 14: 757–762.
87. LeeY, KimSH, MontellC (2010) Avoiding DEET through insect gustatory receptors. Neuron 67: 555–561.
88. MoonSJ, KottgenM, JiaoY, XuH, MontellC (2006) A taste receptor required for the caffeine response in vivo. Curr Biol 16: 1812–1817.
89. JonesWD, CayirliogluP, KadowIG, VosshallLB (2007) Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445: 86–90.
90. ErdelyanCN, MahoodTH, BaderTS, WhyardS (2011) Functional validation of the carbon dioxide receptor genes in Aedes aegypti mosquitoes using RNA interference. Insect Mol Biol
91. ChybS, DahanukarA, WickensA, CarlsonJR (2003) Drosophila Gr5a encodes a taste receptor tuned to trehalose. Proc Natl Acad Sci U S A 100 Suppl 2: 14526–14530.
92. UenoK, OhtaM, MoritaH, MikuniY, NakajimaS, et al. (2001) Trehalose sensitivity in Drosophila correlates with mutations in and expression of the gustatory receptor gene Gr5a. Curr Biol 11: 1451–1455.
93. DahanukarA, FosterK, van der Goes van NatersWM, CarlsonJR (2001) A Gr receptor is required for response to the sugar trehalose in taste neurons of Drosophila. Nat Neurosci 4: 1182–1186.
94. JiaoY, MoonSJ, MontellC (2007) A Drosophila gustatory receptor required for the responses to sucrose, glucose, and maltose identified by mRNA tagging. Proc Natl Acad Sci U S A 104: 14110–14115.
95. SerhanCN, ChiangN, Van DykeTE (2008) Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat Rev Immunol 8: 349–361.
96. LucasKJ, MylesKM, RaikhelAS (2013) Small RNAs: a new frontier in mosquito biology. Trends Parasitol 29: 295–303.
97. ZhouR, HuG, LiuJ, GongAY, DrescherKM, et al. (2009) NF-kappaB p65-dependent transactivation of miRNA genes following Cryptosporidium parvum infection stimulates epithelial cell immune responses. PLoS Pathog 5: e1000681.
98. SakuraiM, AokiT, YoshikawaS, SantschiLA, SaitoH, et al. (2009) Differentially expressed Drl and Drl-2 play opposing roles in Wnt5 signaling during Drosophila olfactory system development. J Neurosci 29: 4972–4980.
99. GesellchenV, KuttenkeulerD, SteckelM, PelteN, BoutrosM (2005) An RNA interference screen identifies Inhibitor of Apoptosis Protein 2 as a regulator of innate immune signalling in Drosophila. EMBO Rep 6: 979–984.
100. ChenJ, ZhangY, ShenP (2008) A protein kinase C activity localized to neuropeptide Y-like neurons mediates ethanol intoxication in Drosophila melanogaster. Neuroscience 156: 42–47.
101. ChenJ, ZhangY, ShenP (2010) Protein kinase C deficiency-induced alcohol insensitivity and underlying cellular targets in Drosophila. Neuroscience 166: 34–39.
102. YeT, TangW, ZhangX (2012) Involvement of Rab6 in the regulation of phagocytosis against virus infection in invertebrates. J Proteome Res 11: 4834–4846.
103. CoutelisJB, EphrussiA (2007) Rab6 mediates membrane organization and determinant localization during Drosophila oogenesis. Development 134: 1419–1430.
104. TianAG, TamoriY, HuangYC, MelendezNT, DengWM (2013) Efficient EGFR signaling and dorsal-ventral axis patterning requires syntaxin dependent Gurken trafficking. Dev Biol 373: 349–358.
105. Abou TayounAN, PikielnyC, DolphPJ (2012) Roles of the Drosophila SK channel (dSK) in courtship memory. PLoS One 7: e34665.
106. RustenTE, VaccariT, LindmoK, RodahlLM, NezisIP, et al. (2007) ESCRTs and Fab1 regulate distinct steps of autophagy. Curr Biol 17: 1817–1825.
107. SoukupSF, CuliJ, GubbD (2009) Uptake of the necrotic serpin in Drosophila melanogaster via the lipophorin receptor-1. PLoS Genet 5: e1000532.
108. LevashinaEA (1999) Constitutive Activation of Toll-Mediated Antifungal Defense in Serpin-Deficient Drosophila. Science 285: 1917–1919.
109. PelteN, RobertsonAS, ZouZ, BelorgeyD, DaffornTR, et al. (2006) Immune challenge induces N-terminal cleavage of the Drosophila serpin Necrotic. Insect Biochem Mol Biol 36: 37–46.
110. MarinottiO, CalvoE, NguyenQK, DissanayakeS, RibeiroJM, et al. (2006) Genome-wide analysis of gene expression in adult Anopheles gambiae. Insect Mol Biol 15: 1–12.
111. BakerDA, NolanT, FischerB, PinderA, CrisantiA, et al. (2011) A comprehensive gene expression atlas of sex- and tissue-specificity in the malaria vector, Anopheles gambiae. BMC Genomics 12: 296.
112. PittsRJ, RinkerDC, JonesPL, RokasA, ZwiebelLJ (2011) Transcriptome profiling of chemosensory appendages in the malaria vector Anopheles gambiae reveals tissue- and sex-specific signatures of odor coding. BMC Genomics 12: 271.
113. MeisterS, KanzokSM, ZhengXL, LunaC, LiTR, et al. (2005) Immune signaling pathways regulating bacterial and malaria parasite infection of the mosquito Anopheles gambiae. Proc Natl Acad Sci U S A 102: 11420–11425.
114. FelixRC, SilveiraH (2011) The Interplay between Tubulins and P450 Cytochromes during Plasmodium berghei Invasion of Anopheles gambiae Midgut. PLoS One 6: e24181.
115. BenoitJB, Lopez-MartinezG, PatrickKR, PhillipsZP, KrauseTB, et al. (2011) From the Cover: Drinking a hot blood meal elicits a protective heat shock response in mosquitoes. Proc Natl Acad Sci U S A 108: 8026–8029.
116. LiB, CalvoE, MarinottiO, JamesAA, PaskewitzSM (2005) Characterization of the c-type lysozyme gene family in Anopheles gambiae. Gene 360: 131–139.
117. ChristophidesGK, ZdobnovE, Barillas-MuryC, BirneyE, BlandinS, et al. (2002) Immunity-related genes and gene families in Anopheles gambiae. Science 298: 159–165.
118. DanielliA, LoukerisTG, LagueuxM, MullerHM, RichmanA, et al. (2000) A modular chitin-binding protease associated with hemocytes and hemolymph in the mosquito Anopheles gambiae. Proc Natl Acad Sci U S A 97: 7136–7141.
119. DinglasanRR, DevenportM, FlorensL, JohnsonJR, McHughCA, et al. (2009) The Anopheles gambiae adult midgut peritrophic matrix proteome. Insect Biochem Mol Biol 39: 125–134.
120. KuraishiT, BinggeliO, OpotaO, BuchonN, LemaitreB (2011) Genetic evidence for a protective role of the peritrophic matrix against intestinal bacterial infection in Drosophila melanogaster. Proc Natl Acad Sci U S A 108: 15966–15971.
121. BrownMR, CrimJW, ArataRC, CaiHN, ChunC, et al. (1999) Identification of a Drosophila brain-gut peptide related to the neuropeptide Y family. Peptides 20: 1035–1042.
122. StanekDM, PohlJ, CrimJW, BrownMR (2002) Neuropeptide F and its expression in the yellow fever mosquito, Aedes aegypti. Peptides 23: 1367–1378.
123. WuQ, ZhaoZ, ShenP (2005) Regulation of aversion to noxious food by Drosophila neuropeptide Y- and insulin-like systems. Nat Neurosci 8: 1350–1355.
124. ShenP, CaiHN (2001) Drosophila neuropeptide F mediates integration of chemosensory stimulation and conditioning of the nervous system by food. J Neurobiol 47: 16–25.
125. KacsohBZ, LynchZR, MortimerNT, SchlenkeTA (2013) Fruit flies medicate offspring after seeing parasites. Science 339: 947–950.
126. WangY, BrentCS, FennernE, AmdamGV (2012) Gustatory perception and fat body energy metabolism are jointly affected by vitellogenin and juvenile hormone in honey bees. PLoS Genet 8: e1002779.
127. XuJ, ShengZ, PalliSR (2013) Juvenile hormone and insulin regulate trehalose homeostasis in the red flour beetle, Tribolium castaneum. PLoS Genet 9: e1003535.
128. NoriegaFG (2004) Nutritional regulation of JH synthesis: a mechanism to control reproductive maturation in mosquitoes? Insect Biochem Mol Biol 34: 687–693.
129. Perez-HedoM, Rivera-PerezC, NoriegaFG (2013) The insulin/TOR signal transduction pathway is involved in the nutritional regulation of juvenile hormone synthesis in Aedes aegypti. Insect Biochem Mol Biol 43 (6) 495–500.
130. 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.
131. CareyAF, WangG, SuCY, ZwiebelLJ, CarlsonJR (2010) Odorant reception in the malaria mosquito Anopheles gambiae. Nature 464: 66–71.
132. MeunierN, BelgacemYH, MartinJR (2007) Regulation of feeding behaviour and locomotor activity by takeout in Drosophila. J Exp Biol 210: 1424–1434.
133. VanaphanN, DauwalderB, ZufallRA (2012) Diversification of takeout, a male-biased gene family in Drosophila. Gene 491: 142–148.
134. ParkJH, KwonJY (2011) Heterogeneous expression of Drosophila gustatory receptors in enteroendocrine cells. PLoS One 6: e29022.
135. NiareO, MarkianosK, VolzJ, OduolF, ToureA, et al. (2002) Genetic loci affecting resistance to human malaria parasites in a West African mosquito vector population. Science 298: 213–216.
136. BlandinSA, Wang-SattlerR, LamacchiaM, GagneurJ, LycettG, et al. (2009) Dissecting the genetic basis of resistance to malaria parasites in Anopheles gambiae. Science 326: 147–150.
137. Molina-CruzA, GarverLS, AlabasterA, BangioloL, HaileA, et al. (2013) The human malaria parasite Pfs47 gene mediates evasion of the mosquito immune system. Science 340: 984–987.
138. HeutinkP, OostraBA (2002) Gene finding in genetically isolated populations. Hum Mol Genet 11: 2507–2515.
139. GudmundssonJ, SulemP, GudbjartssonDF, MassonG, AgnarssonBA, et al. (2012) A study based on whole-genome sequencing yields a rare variant at 8q24 associated with prostate cancer. Nat Genet 44: 1326–1329.
140. LeeK-A, KimS-H, KimE-K, HaE-M, YouH, et al. (2013) Bacterial-Derived Uracil as a Modulator of Mucosal Immunity and Gut-Microbe Homeostasis in Drosophila. Cell 153: 797–811.
141. MeijersR, Puettmann-HolgadoR, SkiniotisG, LiuJH, WalzT, et al. (2007) Structural basis of Dscam isoform specificity. Nature 449: 487–491.
142. KolodziejPA, TimpeLC, MitchellKJ, FriedSR, GoodmanCS, et al. (1996) frazzled encodes a Drosophila member of the DCC immunoglobulin subfamily and is required for CNS and motor axon guidance. Cell 87: 197–204.
143. KiddT, BroseK, MitchellKJ, FetterRD, Tessier-LavigneM, et al. (1998) Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell 92: 205–215.
144. EvansTA, BashawGJ (2010) Axon guidance at the midline: of mice and flies. Curr Opin Neurobiol 20: 79–85.
145. KochCM, Honemann-CapitoM, Egger-AdamD, WodarzA (2009) Windei, the Drosophila homolog of mAM/MCAF1, is an essential cofactor of the H3K9 methyl transferase dSETDB1/Eggless in germ line development. PLoS Genet 5: e1000644.
146. LiuL, IshiharaK, IchimuraT, FujitaN, HinoS, et al. (2009) MCAF1/AM is involved in Sp1-mediated maintenance of cancer-associated telomerase activity. J Biol Chem 284: 5165–5174.
147. GarverLS, XiZ, DimopoulosG (2008) Immunoglobulin superfamily members play an important role in the mosquito immune system. Dev Comp Immunol 32: 519–531.
148. ZdobnovEM, von MeringC, LetunicI, TorrentsD, SuyamaM, et al. (2002) Comparative genome and proteome analysis of Anopheles gambiae and Drosophila melanogaster. Science 298: 149–159.
149. 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.
150. ParedesJC, WelchmanDP, PoidevinM, LemaitreB (2011) Negative Regulation by Amidase PGRPs Shapes the Drosophila Antibacterial Response and Protects the Fly from Innocuous Infection. Immunity 35: 770–779.
151. Crampton JM, Beard CB, Louis C, World Health Organization. (1997) The molecular biology of insect disease vectors : a methods manual. London: Chapman & Hall. xxv: , 578 p.
152. NehmeNT, LiegeoisS, KeleB, GiammarinaroP, PradelE, et al. (2007) A model of bacterial intestinal infections in Drosophila melanogaster. PLoS Pathog 3: e173.
153. FaviaG, RicciI, DamianiC, RaddadiN, CrottiE, et al. (2007) Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector. Proc Natl Acad Sci U S A 104: 9047–9051.
154. ReidenbachKR, NeafseyDE, CostantiniC, SagnonN, SimardF, et al. (2012) Patterns of genomic differentiation between ecologically differentiated M and S forms of Anopheles gambiae in West and Central Africa. Genome Biol Evol 4 (12) 1202–12.
155. LawsonD, ArensburgerP, AtkinsonP, BesanskyNJ, BruggnerRV, et al. (2009) VectorBase: a data resource for invertebrate vector genomics. Nucleic Acids Res 37: D583–587.
156. BlandinS, MoitaLF, KocherT, WilmM, KafatosFC, et al. (2002) Reverse genetics in the mosquito Anopheles gambiae: targeted disruption of the Defensin gene. EMBO Rep 3: 852–856.
157. GoecksJ, NekrutenkoA, TaylorJ, GalaxyT (2010) Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11: R86.
158. Santiago-SoteloP, Ramirez-PradoJH (2012) prfectBLAST: a platform-independent portable front end for the command terminal BLAST+ stand-alone suite. Biotechniques 53: 299–300.
159. HusonDH, MitraS, RuscheweyhHJ, WeberN, SchusterSC (2011) Integrative analysis of environmental sequences using MEGAN4. Genome Res 21: 1552–1560.
160. JaWW, CarvalhoGB, MakEM, de la RosaNN, FangAY, et al. (2007) Prandiology of Drosophila and the CAFE assay. Proc Natl Acad Sci U S A 104: 8253–8256.
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
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