Complement-Related Proteins Control the Flavivirus Infection of by Inducing Antimicrobial Peptides
Hosts are equipped with sophisticated machineries for detecting and eliminating invading viruses before they cause significant physiological damage. Unlike mammals which have both innate and adaptive immune systems, insects rely solely on the innate immune system to limit viral infection. Mosquitoes are natural vectors for many human pathogenic viruses, such as dengue virus (DENV) and yellow fever virus. Despite lacking an immunoglobulin-based humoral response, mosquitoes arm themselves with a functional complement-like system to ward off invading pathogens. Herein, we show that a system composed of complement-related factors recognizes and limits flaviviruses by inducing antimicrobial peptides expression. Understanding antiviral mechanisms in arthropods may provide novel strategies for limiting arboviral transmission in nature.
Vyšlo v časopise:
Complement-Related Proteins Control the Flavivirus Infection of by Inducing Antimicrobial Peptides. PLoS Pathog 10(4): e32767. doi:10.1371/journal.ppat.1004027
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004027
Souhrn
Hosts are equipped with sophisticated machineries for detecting and eliminating invading viruses before they cause significant physiological damage. Unlike mammals which have both innate and adaptive immune systems, insects rely solely on the innate immune system to limit viral infection. Mosquitoes are natural vectors for many human pathogenic viruses, such as dengue virus (DENV) and yellow fever virus. Despite lacking an immunoglobulin-based humoral response, mosquitoes arm themselves with a functional complement-like system to ward off invading pathogens. Herein, we show that a system composed of complement-related factors recognizes and limits flaviviruses by inducing antimicrobial peptides expression. Understanding antiviral mechanisms in arthropods may provide novel strategies for limiting arboviral transmission in nature.
Zdroje
1. WeaverSC, BarrettAD (2004) Transmission cycles, host range, evolution and emergence of arboviral disease. Nat Rev Microbiol 2: 789–801.
2. GanesanS, AggarwalK, PaquetteN, SilvermanN (2011) NF-kappaB/Rel proteins and the humoral immune responses of Drosophila melanogaster. Curr Top Microbiol Immunol 349: 25–60.
3. ShishidoSN, VarahanS, YuanK, LiX, FlemingSD (2012) Humoral innate immune response and disease. Clin Immunol 144: 142–158.
4. LevashinaEA, MoitaLF, BlandinS, VriendG, LagueuxM, et al. (2001) Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 104: 709–718.
5. BlandinS, ShiaoSH, MoitaLF, JanseCJ, WatersAP, et al. (2004) Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116: 661–670.
6. BuresovaV, HajdusekO, FrantaZ, LoosovaG, GrunclovaL, et al. (2011) Functional genomics of tick thioester-containing proteins reveal the ancient origin of the complement system. J Innate Immun 3: 623–630.
7. ChengG, LiuL, WangP, ZhangY, ZhaoYO, et al. (2011) An in vivo transfection approach elucidates a role for Aedes aegypti thioester-containing proteins in flaviviral infection. PLoS ONE 6: e22786.
8. DoddsAW, LawSK (1998) The phylogeny and evolution of the thioester bond-containing proteins C3, C4 and α2-macroglobulin. Immunol Rev 166: 15–26.
9. BlandinS, LevashinaEA (2004) Thioester-containing proteins and insect immunity. Mol Immunol 40: 903–908.
10. MoitaLF, Wang-SattlerR, MichelK, ZimmermannT, BlandinS, et al. (2005) In vivo identification of novel regulators and conserved pathways of phagocytosis in Anopheles gambiae. Immunity 23: 65–73.
11. Stroschein-StevensonSL, FoleyE, O’FarrellPH, JohnsonAD (2006) Identification of Drosophila gene products required for phagocytosis of Candida albicans. PLoS Biol 4: 87–99.
12. Bou AounR, HetruC, TroxlerL, DoucetD, FerrandonD, MattN (2011) Analysis of thioester-containing proteins during the innate immune response of Drosophila melanogaster. J Innate Immun 3: 52–64.
13. GoughPJ, GordonS (2000) The role of scavenger receptors in the innate immune system. Microbes Infect 2: 305–311.
14. RämetM, PearsonA, ManfruelliP, LiX, KozielH, et al. (2001) Drosophila scavenger receptor CI is a pattern recognition receptor for bacteria. Immunity 15: 1027–1038.
15. CasasnovasJM, LarvieM, StehleT (1999) Crystal structure of two CD46 domains reveals an extended measles virus-binding surface. EMBO J 18: 2911–2922.
16. MolinaH, BrennerC, JacobiS, GorkaJ, CarelJC, et al. (1991) Analysis of Epstein-Barr virus-binding sites on complement receptor 2 (CR2/CD21) using human-mouse chimeras and peptides. At least two distinct sites are necessary for ligand-receptor interaction. J Biol Chem 266: 12173–12179.
17. DörigRE, MarcilA, ChopraA, RichardsonCD (1993) The human CD46 molecule is a receptor for measles virus (Edmonston strain). Cell 75: 295–305.
18. StoiberH, ClivioA, DierichMP (1997) Role of complement in HIV infection. Annu Rev Immunol 15: 649–674.
19. PangburnMK (2000) Host recognition and target differentiation by factor H, a regulator of the alternative pathway of complement. Immunopharmacology 49: 149–157.
20. Rigau-PérezJG, ClarkGG, GublerDJ, ReiterP, SandersEJ, et al. (1998) Dengue and dengue haemorrhagic fever. Lancet 352: 971–977.
21. GouldEA, SolomonT (2008) Pathogenic flaviviruses. Lancet 371: 500–509.
22. RanjitS, KissoonN (2011) Dengue hemorrhagic fever and shock syndromes. Pediatr Crit Care Med 12: 90–100.
23. HalsteadSB (2008) Dengue virus-mosquito interactions. Annu Rev Entomol 53: 273–291.
24. GublerDJ (1998) Dengue and dengue hemorrhagic fever. Clin Microbiol Rev 11: 480–496.
25. NeneV, WortmanJR, LawsonD, HaasB, KodiraC, et al. (2007) Genome sequence of Aedes aegypti, a major arbovirus vector. Science 316: 1718–1723.
26. ChengG, CoxJ, WangP, KrishnanMN, DaiJ, et al. (2010) A C-type lectin collaborates with a CD45 phosphatase homolog to facilitate West Nile virus infection of mosquitoes. Cell 142: 714–725.
27. LiuY, ZhangFC, LiuJY, XiaoXP, ZhangSY, et al. (2014) Transmission-blocking antibodies against mosquito C-type lectins for dengue prevention. PLoS Pathog 10: e1003931.
28. ColpittsTM, CoxJ, VanlandinghamDL, FeitosaFM, ChengG, et al. (2011) Alterations in the Aedes aegypti transcriptome during infection with West Nile, dengue and yellow fever viruses. PLoS Pathog 7: e1002189.
29. DempseyPW, AllisonME, AkkarajuS, GoodnowCC, FearonDT (1996) C3d of complement as a molecular adjuvant, bridging innate and acquired immunity. Science 271: 348–350.
30. PanX, ZhouG, WuJ, BianG, LuP, et al. (2011) 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 USA 109: E23–31.
31. XiZ, RamirezJL, DimopoulosG (2008) The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathog 4: e1000098.
32. LuplertlopN, SurasombatpattanaP, PatramoolS, DumasE, WasinpiyamongkolL, et al. (2011) Induction of a peptide with activity against a broad spectrum of pathogens in the Aedes aegypti salivary gland, following infection with dengue virus. PLoS Pathog 7: e1001252.
33. RamirezJL, Souza-NetoJ, Torres CosmeR, RoviraJ, OrtizA, et al. (2012) Reciprocal tripartite interactions between the Aedes aegypti midgut microbiota, innate immune system and dengue virus influences vector competence. PLoS Negl Trop Dis 6: e1561.
34. WangXH, AliyariR, LiWX, LiHW, KimK, et al. (2006) RNA interference directs innate immunity against viruses in adult Drosophila. Science 312: 452–454.
35. ArjonaA, WangPH, MontgomeryRR, FikrigE (2011) Innate immune control of West Nile virus infection. Cell Microbiol 13: 1648–1658.
36. PearsonA, LuxA, KriegerM (1995) Expression cloning of dSR-CI, a class C macrophage-specific scavenger receptor from Drosophila melanogaster. Proc Natl Acad Sci USA 92: 4056–4060.
37. SchmidtCQ, HerbertAP, HockingHG, UhrínD, BarlowPN (2008) Translational mini-review series on complement factor H, structural and functional correlations for factor H. Clin Exp Immunol. 151: 14–24.
38. LeungE, BlomAM, ClemenzaL, IsenmanDE (2006) The complement regulator C4b-binding protein (C4BP) interacts with both the C4c and C4dg subfragments of the parent C4b ligand, evidence for synergy in C4BP subsite binding. Biochemistry 45: 8378–8392.
39. MillerEC, ChaseNM, DensenP, HintermeyerMK, CasperJT, et al. (2012) Autoantibody stabilization of the classical pathway C3 convertase leading to C3 deficiency and Neisserial sepsis, C4 nephritic factor revisited. Clin Immunol 145: 241–250.
40. FraitureM, BaxterRH, SteinertS, ChelliahY, FroletC, et al. (2009) Two mosquito LRR proteins function as complement control factors in the TEP1-mediated killing of Plasmodium. Cell Host Microbe 5: 273–284.
41. FuchsA, LinTY, BeasleyDW, StoverCM, SchwaebleWJ, et al. (2010) Direct complement restriction of flavivirus infection requires glycan recognition by mannose-binding lectin. Cell Host Microbe 8: 186–195.
42. AvirutnanP, HauhartRE, MarovichMA, GarredP, AtkinsonJP, et al. (2011) Complement-mediated neutralization of dengue virus requires mannose-binding lectin. MBio 2: e00276–e002711.
43. WaterhouseRM, KriventsevaEV, MeisterS, XiZ, AlvarezKS, et al. (2007) Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 316: 1738–1734.
44. HancockRE, SahlHG (2006) Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat Biotechnol 24: 1551–1557.
45. HancockRE, RobertEW, RozekA (2002) Role of membranes in the activities of antimicrobial cationic peptides. FEMS Microbiol Lett 206: 143–149.
46. DongY, AguilarR, XiZ, WarrE, MonginE, et al. (2006) Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog 2: e52.
47. GarverLS, DongY, DimopoulosG (2009) Caspar controls resistance to Plasmodium falciparum in diverse anopheline species. PLoS Pathog 5: e1000335.
48. Souza-NetoJA, SimS, DimopoulosG (2009) An evolutionary conserved function of the JAK-STAT pathway in anti-dengue defense. Proc Natl Acad Sci USA 106: 17841–17846.
49. DongY, MortonJCJr, RamirezJL, Souza-NetoJA, DimopoulosG (2012) The entomopathogenic fungus Beauveria bassiana activate toll and JAK-STAT pathway-controlled effector genes and anti-dengue activity in Aedes aegypti. Insect Biochem Mol Biol 42: 126–132.
50. LagueuxM, PerrodouE, LevashinaEA, CapovillaM, HoffmannJA (2000) Constitutive expression of a complement-like protein in toll and JAK gain-of-function mutants of Drosophila. Proc Natl Acad Sci USA 97: 11427–11432.
51. Maciel-de-FreitasR, KoellaJC, Lourenço-de-OliveiraR (2011) Lower survival rate, longevity and fecundity of Aedes aegypti (Diptera: Culicidae) females orally challenged with dengue virus serotype 2. Trans R Soc Trop Med Hyg 105: 452–458.
52. SylvestreG, GandiniM, Maciel-de-FreitasR (2013) Age-dependent effects of oral infection with dengue virus on Aedes aegypti (Diptera: Culicidae) feeding behavior, survival, oviposition success and fecundity. PLoS ONE 8: e59933.
53. VaidyanathanR, ScottTW (2006) Apoptosis in mosquito midgut epithelia associated with West Nile virus infection. Apoptosis 11: 1643–1651.
54. KellyEM, MoonDC, BowersDF (2012) Apoptosis in mosquito salivary glands: Sindbis virus-associated and tissue homeostasis. J Gen Virol 93: 2419–2424.
55. YenYT, ChenHC, LinYD, ShiehCC, Wu-HsiehBA (2008) Enhancement by tumor necrosis factor alpha of dengue virus-induced endothelial cell production of reactive nitrogen and oxygen species is key to hemorrhage development. J Virol 82: 12312–12324.
56. HenchalEA, GentryMK, McCownJM, BrandtWE (1982) Dengue virus-specific and flavivirus group determinants identified with monoclonal antibodies by indirect immunofluorescence. Am J Trop Med Hyg 31: 830–836.
57. SaitouN, NeiM (1987) The neighbor-joining method, a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425.
58. Edgar RChttp://nar.oxfordjournals.org/content/32/5/1792.short - corresp-1 (2004) MUSCLE, multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797.
59. BrackneyDE, FoyBD, OlsonKE (2008) The effects of midgut serine proteases on dengue virus type 2 infectivity of Aedes aegypti. Am J. Trop Med Hyg 79: 267–274.
60. PovelonesM, WaterhouseRM, KafatosFC, ChristophidesGK (2009) Leucine-rich repeat protein complex activates mosquito complement in defense against Plasmodium parasites. Science 324: 258–261.
61. HanYS, ChunJ, SchwartzA, NelsonS, PaskewitzSM (1999) Induction of mosquito hemolymph proteins in response to immune challenge and wounding. Dev Comp Immunol 23: 553–562.
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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