A Neuron-Specific Antiviral Mechanism Prevents Lethal Flaviviral Infection of Mosquitoes

English version České info

The central nervous system plays a predominant role in organisms associated with cognition and higher-order functions, which is key to their normal behavior and successful survival. Many mosquito-borne flaviviruses particularly invade the central nervous system in vertebrates, resulting in dramatic neural degeneration and damage. As natural vectors, mosquitoes are highly permissive to flaviviral infection that can be persistent in the mosquito nervous system. However, the infection intriguingly does neither lead to significant malignant pathological sequelae, nor dramatically influences mosquito behavior or lifespan, and thus mosquitoes can transmit viruses efficiently. Little is known about the neuron-specific resistant mechanism in viral infection of mosquitoes. Here we report that a neuron-specific factor specifically controls flaviviral replication in the mosquito nervous system by interfering with viral entry, and its activity prevents lethal flaviviral infection of mosquitoes. Our study provides insight into the sophisticated interactions between mosquito-borne viruses and their vectors, and offers an important target for arboviral limitation in nature.

Vyšlo v časopise: A Neuron-Specific Antiviral Mechanism Prevents Lethal Flaviviral Infection of Mosquitoes. PLoS Pathog 11(4): e32767. doi:10.1371/journal.ppat.1004848
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004848

Souhrn

Zdroje

1. Gould EA, Solomon T (2008) Pathogenic flaviviruses. Lancet 371: 500–509. doi: 10.1016/S0140-6736(08)60238-X 18262042

2. Cheng G, Cox J, Wang P, Krishnan MN, Dai J, 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. doi: 10.1016/j.cell.2010.07.038 20797779

3. Liu Y, Zhang F, Liu J, Xiao X, Zhang S, et al. (2014) Transmission-blocking antibodies against mosquito C-type lectins for dengue prevention. PLoS Pathog 10: e1003931. doi: 10.1371/journal.ppat.1003931 24550728

4. Girard YA, Klingler KA, Higgs S (2004) West Nile virus dissemination and tissue tropisms in orally infected Culex pipiens quinquefasciatus. Vector Borne Zoonotic Dis 4: 109–122. 15228811

5. Carrington LB, Seifert SN, Armijos MV, Lambrechts L, Scott TW (2013) Reduction of Aedes aegypti vector competence for dengue virus under large temperature fluctuations. Am J Trop Med Hyg 88: 689–697. doi: 10.4269/ajtmh.12-0488 23438766

6. Garza-Hernández JA, Rodríguez-Pérez MA, Salazar MI, Russell TL, Adeleke MA, et al. (2013) Vectorial capacity of Aedes aegypti for dengue virus type 2 is reduced with co-infection of Metarhizium anisopliae. PLoS Negl Trop Dis 7: e2013. doi: 10.1371/journal.pntd.0002013 23505581

7. Hill CL, Sharma A, Shouche Y, Severson DW (2014) Dynamics of midgut microflora and dengue virus impact on life history traits in Aedes aegypti. Acta Trop 140C: 151–157.

8. Putnam JL, Scott TW (1995) Blood-feeding behavior of dengue-2 virus-infected Aedes aegypti. Am J Trop Med Hyg 52: 225–227. 7694963

9. Hoshino M, Matsuzaki F, Nabeshima Y, Hama C (1993) Hikaru genki, a CNS-specific gene identified by abnormal locomotion in Drosophila, encodes a novel type of protein. Neuron 10: 395–407. 8461133

10. Hoshino M, Suzuki E, Nabeshima Y, Hama C (1996) Hikaru genki protein is secreted into synaptic clefts from an early stage of synapse formation in Drosophila. Development 122: 589–597. 8625810

11. Xiao X, Liu Y, Zhang X, Wang J, Li Z, et al. (2014) Complement-related proteins control the flavivirus infection of Aedes aegypti by inducing antimicrobial peptides. PLoS Pathog 10: e1004027. doi: 10.1371/journal.ppat.1004027 24722701

12. Molina H, Brenner C, Jacobi S, Gorka J, Carel JC, 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. 1712014

13. Dörig RE, Marcil A, Chopra A, Richardson CD (1993) The human CD46 molecule is a receptor for measles virus (Edmonston strain). Cell 75: 295–305. 8402913

14. Stoiber H, Clivio A, Dierich MP (1997) Role of complement in HIV infection. Annu Rev Immunol 15: 649–674. 9143703

15. Pangburn MK (2000) Host recognition and target differentiation by factor H, a regulator of the alternative pathway of complement. Immunopharmacology 49: 149–157. 10904114

16. Feng Y, Fu S, Zhang H, Li M, Zhou T, et al. (2012) Distribution of mosquitoes and mosquito-borne viruses along the China-Myanmar border in Yunnan Province. Jpn J Infect Dis 65: 215–221. 22627302

17. Nene V, Wortman JR, Lawson D, Haas B, Kodira C, et al. (2007) Genome sequence of Aedes aegypti, a major arbovirus vector. Science 316: 1718–1723. 17510324

18. Casasnovas JM, Larvie M, Stehle T (1999) Crystal structure of two CD46 domains reveals an extended measles virus-binding surface. EMBO J 18: 2911–2922. 10357804

19. Dempsey PW, Allison ME, Akkaraju S, Goodnow CC, Fearon DT (1996) C3d of complement as a molecular adjuvant, bridging innate and acquired immunity. Science 271: 348–350. 8553069

20. Snow PM, Patel NH, Harrelson AL, Goodman CS (1987) Neural-specific carbohydrate moiety shared by many surface glycoproteins in Drosophila and Grasshopper embryos. J Neurosci 7: 4137–4144. 3320283

21. Mysore K, Flister S, Müller P, Rodrigues V, Reichert H (2011) Brain development in the yellow fever mosquito Aedes aegypti: a comparative immunocytochemical analysis using cross-reacting antibodies from Drosophila melanogaster. Dev Genes Evol 221: 281–296. doi: 10.1007/s00427-011-0376-2 21956584

22. Hubálek Z (2008) Mosquito-borne viruses in Europe. Parasitol Res 103 Suppl 1: S29–S43. doi: 10.1007/s00436-008-1064-7 19030884

23. Wang H, Gort T, Boyle DL, Clem RJ (2012) Effects of manipulating apoptosis on Sindbis virus infection of Aedes aegypti mosquitoes. J Virol 86: 6546–54. doi: 10.1128/JVI.00125-12 22438551

24. Khoo CC, Piper J, Sanchez-Vargas I, Olson KE, Franz AW (2010) The RNA interference pathway affects midgut infection- and escape barriers for Sindbis virus in Aedes aegypti. BMC Microbiol 10: 130. doi: 10.1186/1471-2180-10-130 20426860

25. Campbell CL, Keene KM, Brackney DE, Olson KE, Blair CD, et al. (2008) Aedes aegypti uses RNA interference in defense against Sindbis virus infection. BMC Microbiol 8: 47. doi: 10.1186/1471-2180-8-47 18366655

26. Cirimotich CM, Scott JC, Phillips AT, Geiss BJ, Olson KE (2009) Suppression of RNA interference increases alphavirus replication and virus-associated mortality in Aedes aegypti mosquitoes. BMC Microbiol 9: 49. doi: 10.1186/1471-2180-9-49 19265532

27. Vaidyanathan R, Scott TW (2006) Apoptosis in mosquito midgut epithelia associated with West Nile virus infection. Apoptosis 11: 1643–1651. 16820968

28. Girard YA, Mayhew GF, Fuchs JF, Li H, Schneider BS, et al. (2010) Transcriptome changes in Culex quinquefasciatus (Diptera: Culicidae) salivary glands during West Nile virus infection. J Med Entomol 47: 421–435. 20496590

29. Girard YA, Schneider BS, McGee CE, Wen J, Han VC, et al. (2007) Salivary gland morphology and virus transmission during long-term cytopathologic West Nile virus infection in Culex mosquitoes. Am J Trop Med Hyg 76: 118–128. 17255239

30. Girard YA, Popov V, Wen J, Han V, Higgs S (2005) Ultrastructural study of West Nile virus pathogenesis in Culex pipiens quinquefasciatus (Diptera: Culicidae). J Med Entomol 42: 429–444. 15962797

31. Fan Y, Bergmann A (2010) The cleaved-Caspase-3 antibody is a marker of Caspase-9-like DRONC activity in Drosophila. Cell Death Differ 17: 534–539. doi: 10.1038/cdd.2009.185 19960024

32. Modis Y, Ogata S, Clements D, Harrison SC (2003) A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc Natl Acad Sci USA 100: 6986–6991. 12759475

33. Peleg J (1968) Growth of arboviruses in primary tissue culture of Aedes aegypti embryos. Am J Trop Med Hyg 17: 219–223. 4869110

34. Sim S, Dimopoulos G (2010) Dengue virus inhibits immune responses in Aedes aegypti cells. PLoS ONE 5: e10678. doi: 10.1371/journal.pone.0010678 20502529

35. Barletta AB, Silva MC, Sorgine MH (2012) Validation of Aedes aegypti Aag-2 cells as a model for insect immune studies. Parasit Vectors 5: 148. doi: 10.1186/1756-3305-5-148 22827926

36. Sessions OM, Barrows NJ, Souza-Neto JA, Robinson TJ, Hershey CL, et al. (2009) Discovery of insect and human dengue virus host factors. Nature 458: 1047–50. doi: 10.1038/nature07967 19396146

37. Wang XH, Aliyari R, Li WX, Li HW, Kim K. et al. (2006) RNA interference directs innate immunity against viruses in adult drosophila. Science 312: 452–454. 16556799

38. Arjona A, Wang PH, Montgomery RR, Fikrig E (2011) Innate immune control of West Nile virus infection. Cell Microbiol 13: 1648–1658. doi: 10.1111/j.1462-5822.2011.01649.x 21790942

39. Ramirez JL, Dimopoulos G (2010) The Toll immune signaling pathway control conserved anti-dengue defenses across diverse Aedes aegypti strains and against multiple dengue virus serotypes. Dev Comp Immunol 34: 625–629. doi: 10.1016/j.dci.2010.01.006 20079370

40. Pan X, Zhou G, Wu J, Bian G, Lu P, 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. doi: 10.1073/pnas.1116932108 22123956

41. Rodriguez-Andres J, Rani S, Varjak M, Chase-Topping ME, Beck MH, et al. (2012) Phenoloxidase activity acts as a mosquito innate immune response against infection with Semliki Forest virus. PLoS Pathog 8: e1002977. doi: 10.1371/journal.ppat.1002977 23144608

42. Cornet S, Gandon S, Rivero A (2013) Patterns of phenoloxidase activity in insecticide resistant and susceptible mosquitoes differ between laboratory-selected and wild-caught individuals. Parasit Vectors 6: 315. doi: 10.1186/1756-3305-6-315 24499651

43. Krishnan MN, Sukumaran B, Pal U, Agaisse H, Murray JL, et al. (2007) Rab 5 is required for the cellular entry of dengue and West Nile viruses. J Virol 81: 4881–4885. 17301152

44. Ryckman BJ, Chase MC, Johnson DC (2008) CMV gH/gL/UL128-131 interferes with virus entry into epithelial cells: evidence for cell type-specific receptors. Proc Natl Acad Sci USA 105: 14118–14123. doi: 10.1073/pnas.0804365105 18768787

45. Acosta EG, Castilla V, Damonte EB (2011) Infectious dengue-1 virus entry into mosquito C6/36 cells. Virus Res 160: 173–179. doi: 10.1016/j.virusres.2011.06.008 21708195

46. Clyde K, Kyle JL, Harris E (2006) Recent advances in deciphering viral and host determinants of dengue virus replication and pathogenesis. J Virol 80: 11418–11431. 16928749

47. Hidari KI, Abe T, Suzuki T (2013) Carbohydrate-related inhibitors of dengue virus entry. Viruses 5: 605–618. doi: 10.3390/v5020605 23389466

48. Zerial M, McBride H (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2: 107–117. 11252952

49. Brass AL, Huang IC, Benita Y, John SP, Krishnan MN, et al. (2009) The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 139: 1243–1254. doi: 10.1016/j.cell.2009.12.017 20064371

50. Huang IC, Bailey CC, Weyer JL, Radoshitzky SR, Becker MM, et al. (2011) Distinct patterns of IFITM-mediated restriction of filoviruses, SARS Coronavirus, and influenza A Virus. PLoS Pathog 7: e1001258. doi: 10.1371/journal.ppat.1001258 21253575

51. Amini-Bavil-Olyaee S, Choi YJ, Lee JH, Shi M, Huang IC, et al. (2013) The antiviral effector IFITM3 disrupts intracellular cholesterol homeostasis to block viral entry. Cell Host Microbe 13: 452–464. doi: 10.1016/j.chom.2013.03.006 23601107

52. Li K, Markosyan RM, Zheng YM, Golfetto O, Bungart B, et al. (2013) IFITM proteins restrict viral membrane hemifusion. PLoS Pathog 9: e1003124. doi: 10.1371/journal.ppat.1003124 23358889

53. Desai TM, Marin M, Chin CR, Savidis G, Brass AL, et al. (2014) IFITM3 restricts Influenza A virus entry by blocking the formation of fusion pores following virus-endosome hemifusion. PLoS Pathog 10: e1004048. doi: 10.1371/journal.ppat.1004048 24699674

54. Ezekowitz RA, Kuhlman M, Groopman JE, Byrn RA (1989) A human serum mannose-binding protein inhibits in vitro infection by the human immunodeficiency virus. J Exp Med 169: 185–196. 2909656

55. Ying H, Ji X, Hart ML, Gupta K, Saifuddin M, et al. (2004) Interaction of mannose-binding lectin with HIV-1 is sufficient for virus opsonization but not neutralization. AIDS Res Hum Retroviruses 20: 327–335. 15117456

56. Spear GT, Zariffard MR, Xin J, Saifuddin M (2003) Inhibition of DC-SIGN-mediated trans infection of T cells by mannose-binding lectin. Immunology 110: 80–85. 12941144

57. Ji X, Olinger GG, Aris S, Chen Y, Gewurz H, et al. (2005) Mannose-binding lectin binds to Ebola and Marburg envelope glycoproteins, resulting in blocking of virus interaction with DC-SIGN and complement-mediated virus neutralization. J Gen Virol 86: 2535–2542. 16099912

58. Brown-Augsburger P, Hartshorn K, Chang D, Rust K, Fliszar C, et al. (1996) Site-directed mutagenesis of Cys-15 and Cys-20 of pulmonary surfactant protein D. Expression of a trimeric protein with altered anti-viral properties. J Biol Chem 271: 13724–13730. 8662732

59. Hartshorn KL, White MR, Voelker DR, Coburn J, Zaner K, et al. (2000) Mechanism of binding of surfactant protein D to influenza A viruses: importance of binding to haemagglutinin to antiviral activity. Biochem J 351: 449–458. 11023831

60. Hillaire ML, van Eijk M, van Trierum SE, van Riel D, Saelens X, et al. (2011) Assessment of the antiviral properties of recombinant porcine SP-D against various influenza A viruses in vitro. PLoS ONE 6: e25005. doi: 10.1371/journal.pone.0025005 21935489

61. Tecle T, White MR, Crouch EC, Hartshorn KL (2007) Inhibition of influenza viral neuraminidase activity by collectins. Arch Virol 152: 1731–1742. 17514488

62. Hancock RE, Robert EW, Rozek A (2002) Role of membranes in the activities of antimicrobial cationic peptides. FEMS Microbiol Lett 206: 143–149. 11814654

63. Xi Z, Ramirez JL, Dimopoulos G (2008) The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathog 4: e1000098. doi: 10.1371/journal.ppat.1000098 18604274

64. Avadhanula V, Weasner BP, Hardy GG, Kumar JP, Hardy RW (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 19763182

65. Souza-Neto JA, Sim S, Dimopoulos G (2009) An evolutionary conserved function of the JAK-STAT pathway in anti-dengue defense. Proc Natl Acad Sci USA 106: 17841–17846. doi: 10.1073/pnas.0905006106 19805194

66. Luplertlop N, Surasombatpattana P, Patramool S, Dumas E, Wasinpiyamongkol L, 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. doi: 10.1371/journal.ppat.1001252 21249175

67. Schmidt RL, Trejo TR, Plummer TB, Platt JL, Tang AH (2008) Infection-induced proteolysis of PGRP-LC controls the IMD activation and melanization cascades in Drosophila. FASEB J 22: 918–929. doi: 10.1096/fj.06-7907com 18308747

68. Sabin LR, Zhou R, Gruber JJ, Lukinova N, Bambina S, et al. (2009) Ars2 regulates both miRNA-and siRNA-dependent silencing and suppresses RNA virus infection in Drosophila. Cell 138: 340–351. doi: 10.1016/j.cell.2009.04.045 19632183

69. Sánchez-Vargas I, Scott JC, Poole-Smith BK, Franz AW, Barbosa-Solomieu V, et al. (2009) Dengue virus type 2 infections of Aedes aegypti are modulated by the mosquito's RNA interference pathway. PLoS Pathog 5: e1000299. doi: 10.1371/journal.ppat.1000299 19214215

70. Pizzi M (1950) Sampling variation of the fifty percent end-point, determined by the Reed-Muench (Behrens) method. Human Biology 22: 151–190. 14778593

71. Bai F, Town T, Pradhan D, Cox J, Ashish Ledizet M, et al. (2007) Antiviral peptide targeting the West Nile virus envelope protein. J Virol 81: 2047–2055. 17151121

72. Saitou N, Nei M (1987) The neighbor-joining method, a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425. 3447015

73. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680. 7984417

74. Chang KJ, Bennett V, Cuatrecasas P (1975) Membrane receptors as general markers for plasma membrane isolation procedures. The use of 125-I-labeled wheat germ agglutinin, insulin, and cholera toxin. J Biol Chem 250: 488–500. 163229

75. Spray FJ, Christensen BM (1991) Aedes aegypti: characterization of hemocyte polypeptide synthesis during wound healing and immune response to inoculated microfilariae. Exp Parasitol 73: 481–488. 1959574

76. Ghaninia M, Hansson BS, Ignell R (2007) The antennal lobe of the African malaria mosquito, Anopheles gambiae-innervation and three-dimensional reconstruction. Arthropod Struct Dev 36: 23–39. 18089085

77. Beck MH, Strand MR (2007) A novel polydnavirus protein inhibits the insect prophenoloxidase activation pathway. Proc Natl Acad Sci USA 104: 19267–19272. 18032603

78. Jiang H, Wang Y, Yu XQ, Kanost MR (2003) Prophenoloxidase-activating proteinase-2 from hemolymph of Manduca sexta. A bacteria-inducible serine proteinase containing two clip domains. J Biol Chem 278: 3552–3561. 12456683

79. Rämet M, Pearson A, Manfruelli P, Li X, Koziel H, et al. (2001) Drosophila scavenger receptor CI is a pattern recognition receptor for bacteria. Immunity 15: 1027–1038. 11754822