Dengue Virus Infection of Requires a Putative Cysteine Rich Venom Protein

1. Kao CL, King CC, Chao DY, Wu HL, Chang GJ (2005) Laboratory diagnosis of dengue virus infection: current and future perspectives in clinical diagnosis and public health. J Microbiol Immunol Infect 38 : 5–16. 15692621

2. Overgaard HJ, Alexander N, Matiz MI, Jaramillo JF, Olano VA, et al. (2012) Diarrhea and dengue control in rural primary schools in Colombia: study protocol for a randomized controlled trial. Trials 13 : 182. doi: 10.1186/1745-6215-13-182 23034084

3. Gubler DJ (2002) Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. Trends Microbiol 10 : 100–103. 11827812

4. Guzman MG, Halstead SB, Artsob H, Buchy P, Farrar J, et al. (2010) Dengue: a continuing global threat. Nat Rev Microbiol 8: S7–16. doi: 10.1038/nrmicro2460 21079655

5. Hales S, de Wet N, Maindonald J, Woodward A (2002) Potential effect of population and climate changes on global distribution of dengue fever: an empirical model. Lancet 360 : 830–834. 12243917

6. Kyle JL, Harris E (2008) Global spread and persistence of dengue. Annu Rev Microbiol 62 : 71–92. doi: 10.1146/annurev.micro.62.081307.163005 18429680

7. Gubler DJ (1998) Dengue and dengue hemorrhagic fever. Clin Microbiol Rev 11 : 480–496. 9665979

8. Gubler DJ, Clark GG (1995) Dengue/dengue hemorrhagic fever: the emergence of a global health problem. Emerg Infect Dis 1 : 55–57. 8903160

9. Guzman MG, Alvarez M, Halstead SB (2013) Secondary infection as a risk factor for dengue hemorrhagic fever/dengue shock syndrome: an historical perspective and role of antibody-dependent enhancement of infection. Arch Virol 158 : 1445–1459. doi: 10.1007/s00705-013-1645-3 23471635

10. van den Berg H, Velayudhan R, Ebol A, Catbagan BH Jr., Turingan R, et al. (2012) Operational efficiency and sustainability of vector control of malaria and dengue: descriptive case studies from the Philippines. Malar J 11 : 269. doi: 10.1186/1475-2875-11-269 22873707

11. Jansen CC, Beebe NW (2010) The dengue vector Aedes aegypti: what comes next. Microbes Infect 12 : 272–279. doi: 10.1016/j.micinf.2009.12.011 20096802

12. Miller M BS, Henderson DA. Control and Eradication. (2006) Disease Control Priorities in Developing Countries. In: Jamison DT BJ, Measham AR, et al., editors., editor. 2nd edition ed. Washington (DC): World Bank; 2006. Chapter 62.: Washington (DC): World Bank; 2006. Chapter 62.

13. Pinheiro FP, Corber SJ (1997) Global situation of dengue and dengue haemorrhagic fever, and its emergence in the Americas. World Health Stat Q 50 : 161–169. 9477544

14. Wilder-Smith A, Macary P (2014) Dengue: challenges for policy makers and vaccine developers. Curr Infect Dis Rep 16 : 404. doi: 10.1007/s11908-014-0404-2 24781826

15. Scott RM, Nisalak A, Eckels KH, Tingpalapong M, Harrison VR, et al. (1980) Dengue-2 vaccine: viremia and immune responses in rhesus monkeys. Infect Immun 27 : 181–186. 6766903

16. Miller BR, Beaty BJ, Aitken TH, Eckels KH, Russell PK (1982) Dengue-2 vaccine: oral infection, transmission, and lack of evidence for reversion in the mosquito, Aedes aegypti. Am J Trop Med Hyg 31 : 1232–1237. 7149108

17. Kochel TJ, Raviprakash K, Hayes CG, Watts DM, Russell KL, et al. (2000) A dengue virus serotype-1 DNA vaccine induces virus neutralizing antibodies and provides protection from viral challenge in Aotus monkeys. Vaccine 18 : 3166–3173. 10856796

18. Hoffmann AA, Montgomery BL, Popovici J, Iturbe-Ormaetxe I, Johnson PH, et al. (1038) Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476 : 454–457. doi: 10.1038/nature10356 21866160

19. Johnson AJ, Roehrig JT (1999) New mouse model for dengue virus vaccine testing. J Virol 73 : 783–786. 9847388

20. Guirakhoo F, Weltzin R, Chambers TJ, Zhang ZX, Soike K, et al. (2000) Recombinant chimeric yellow fever-dengue type 2 virus is immunogenic and protective in nonhuman primates. J Virol 74 : 5477–5485. 10823852

21. Fink K, Shi PY (2014) Live attenuated vaccine: the first clinically approved dengue vaccine? Expert Rev Vaccines 13 : 185–188. doi: 10.1586/14760584.2014.870888 24350687

22. Sabchareon A, Wallace D, Sirivichayakul C, Limkittikul K, Chanthavanich P, et al. (2012) Protective efficacy of the recombinant, live-attenuated, CYD tetravalent dengue vaccine in Thai schoolchildren: a randomised, controlled phase 2b trial. Lancet 380 : 1559–1567. doi: 10.1016/S0140-6736(12)61428-7 22975340

23. Guzman MG, Hermida L, Bernardo L, Ramirez R, Guillen G Domain III of the envelope protein as a dengue vaccine target. Expert Rev Vaccines 9 : 137–147.

24. Kliks SC, Nisalak A, Brandt WE, Wahl L, Burke DS (1989) Antibody-dependent enhancement of dengue virus growth in human monocytes as a risk factor for dengue hemorrhagic fever. Am J Trop Med Hyg 40 : 444–451. 2712199

25. Nikin-Beers R, Ciupe SM (2015) The role of antibody in enhancing dengue virus infection. Math Biosci 263 : 83–92. doi: 10.1016/j.mbs.2015.02.004 25707916

26. Flipse J, Wilschut J, Smit JM (2013) Molecular mechanisms involved in antibody-dependent enhancement of dengue virus infection in humans. Traffic 14 : 25–35. doi: 10.1111/tra.12012 22998156

27. Burke DS, Kliks S (2006) Antibody-dependent enhancement in dengue virus infections. J Infect Dis 193 : 601–603; author reply 603–604.

28. Halstead SB (2003) Neutralization and antibody-dependent enhancement of dengue viruses. Adv Virus Res 60 : 421–467. 14689700

29. Villar L, Dayan GH, Arredondo-Garcia JL, Rivera DM, Cunha R, et al. (2015) Efficacy of a tetravalent dengue vaccine in children in Latin America. N Engl J Med 372 : 113–123. doi: 10.1056/NEJMoa1411037 25365753

30. Kay BH, Kemp DH (1994) Vaccines against arthropods. Am J Trop Med Hyg 50 : 87–96. 8024089

31. Carter R (2001) Transmission blocking malaria vaccines. Vaccine 19 : 2309–2314. 11257353

32. Coutinho-Abreu IV, Ramalho-Ortigao M (2010) Transmission blocking vaccines to control insect-borne diseases: a review. Mem Inst Oswaldo Cruz 105 : 1–12. 20209323

33. Wang P, Conrad JT, Shahabuddin M (2001) Localization of midgut-specific protein antigens from Aedes aegypti (Diptera: Culicidae) using monoclonal antibodies. J Med Entomol 38 : 223–230. 11296827

34. 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

35. Colpitts TM, Cox J, Vanlandingham DL, Feitosa FM, Cheng G, et al. (2011) Alterations in the Aedes aegypti transcriptome during infection with West Nile, dengue and yellow fever viruses. PLoS Pathog 7: e1002189. doi: 10.1371/journal.ppat.1002189 21909258

36. Chisenhall DM, Londono BL, Christofferson RC, McCracken MK, Mores CN (2014) Effect of dengue-2 virus infection on protein expression in the salivary glands of Aedes aegypti mosquitoes. Am J Trop Med Hyg 90 : 431–437. doi: 10.4269/ajtmh.13-0412 24445208

37. Chisenhall DM, Christofferson RC, McCracken MK, Johnson AM, Londono-Renteria B, et al. (2014) Infection with dengue-2 virus alters proteins in naturally expectorated saliva of Aedes aegypti mosquitoes. Parasit Vectors 7 : 252. doi: 10.1186/1756-3305-7-252 24886023

38. Baron OL, Ursic-Bedoya RJ, Lowenberger CA, Ocampo CB (2010) Differential gene expression from midguts of refractory and susceptible lines of the mosquito, Aedes aegypti, infected with Dengue-2 virus. J Insect Sci 10 : 41. doi: 10.1673/031.010.4101 20572793

39. Behura SK, Gomez-Machorro C, deBruyn B, Lovin DD, Harker BW, et al. (2014) Influence of mosquito genotype on transcriptional response to dengue virus infection. Funct Integr Genomics 14 : 581–589. doi: 10.1007/s10142-014-0376-1 24798794

40. Campbell CL, Harrison T, Hess AM, Ebel GD (2014) MicroRNA levels are modulated in Aedes aegypti after exposure to Dengue-2. Insect Mol Biol 23 : 132–139. doi: 10.1111/imb.12070 24237456

41. Zhang M, Zheng X, Wu Y, Gan M, He A, et al. (2013) Differential proteomics of Aedes albopictus salivary gland, midgut and C6/36 cell induced by dengue virus infection. Virology 444 : 109–118. doi: 10.1016/j.virol.2013.06.001 23816433

42. Bonizzoni M, Dunn WA, Campbell CL, Olson KE, Marinotti O, et al. (2012) Complex modulation of the Aedes aegypti transcriptome in response to dengue virus infection. PLoS One 7: e50512. doi: 10.1371/journal.pone.0050512 23209765

43. Behura SK, Severson DW (2012) Intrinsic features of Aedes aegypti genes affect transcriptional responsiveness of mosquito genes to dengue virus infection. Infect Genet Evol 12 : 1413–1418. doi: 10.1016/j.meegid.2012.04.027 22579482

44. Sim S, Ramirez JL, Dimopoulos G (2012) Dengue virus infection of the Aedes aegypti salivary gland and chemosensory apparatus induces genes that modulate infection and blood-feeding behavior. PLoS Pathog 8: e1002631. doi: 10.1371/journal.ppat.1002631 22479185

45. Dai J, Narasimhan S, Zhang L, Liu L, Wang P, et al. (2010) Tick histamine release factor is critical for Ixodes scapularis engorgement and transmission of the lyme disease agent. PLoS Pathog 6: e1001205. doi: 10.1371/journal.ppat.1001205 21124826

46. Arca B, Lombardo F, Francischetti IM, Pham VM, Mestres-Simon M, et al. (2007) An insight into the sialome of the adult female mosquito Aedes albopictus. Insect Biochem Mol Biol 37 : 107–127. 17244540

47. 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

48. Calvo E, Pham VM, Lombardo F, Arca B, Ribeiro JM (2006) The sialotranscriptome of adult male Anopheles gambiae mosquitoes. Insect Biochem Mol Biol 36 : 570–575. 16835022

49. Ribeiro JM, Charlab R, Pham VM, Garfield M, Valenzuela JG (2004) An insight into the salivary transcriptome and proteome of the adult female mosquito Culex pipiens quinquefasciatus. Insect Biochem Mol Biol 34 : 543–563. 15147756

50. Conway MJ, Watson AM, Colpitts TM, Dragovic SM, Li Z, et al. (2014) Mosquito saliva serine protease enhances dissemination of dengue virus into the mammalian host. J Virol 88 : 164–175. doi: 10.1128/JVI.02235-13 24131723

51. Furuta T, Murao LA, Lan NT, Huy NT, Huong VT, et al. (2012) Association of mast cell-derived VEGF and proteases in Dengue shock syndrome. PLoS Negl Trop Dis 6: e1505. doi: 10.1371/journal.pntd.0001505 22363824

52. Bonizzoni M, Britton M, Marinotti O, Dunn WA, Fass J, et al. (2013) Probing functional polymorphisms in the dengue vector, Aedes aegypti. BMC Genomics 14 : 739. doi: 10.1186/1471-2164-14-739 24168143

53. Gulley MM, Zhang X, Michel K (2013) The roles of serpins in mosquito immunology and physiology. J Insect Physiol 59 : 138–147. doi: 10.1016/j.jinsphys.2012.08.015 22960307

54. 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

55. Brackney DE, Foy BD, Olson KE (2008) The effects of midgut serine proteases on dengue virus type 2 infectivity of Aedes aegypti. Am J Trop Med Hyg 79 : 267–274. 18689635

56. Paingankar MS, Gokhale MD, Deobagkar DN (2010) Dengue-2-virus-interacting polypeptides involved in mosquito cell infection. Arch Virol 155 : 1453–1461. doi: 10.1007/s00705-010-0728-7 20571839

57. Kuadkitkan A, Wikan N, Fongsaran C, Smith DR (2010) Identification and characterization of prohibitin as a receptor protein mediating DENV-2 entry into insect cells. Virology 406 : 149–161. doi: 10.1016/j.virol.2010.07.015 20674955

58. Gibbs GM, O'Bryan MK (2007) Cysteine rich secretory proteins in reproduction and venom. Soc Reprod Fertil Suppl 65 : 261–267. 17644967

59. Udby L, Calafat J, Sorensen OE, Borregaard N, Kjeldsen L (2002) Identification of human cysteine-rich secretory protein 3 (CRISP-3) as a matrix protein in a subset of peroxidase-negative granules of neutrophils and in the granules of eosinophils. J Leukoc Biol 72 : 462–469. 12223513

60. Parkinson NM, Conyers C, Keen J, MacNicoll A, Smith I, et al. (2004) Towards a comprehensive view of the primary structure of venom proteins from the parasitoid wasp Pimpla hypochondriaca. Insect Biochem Mol Biol 34 : 565–571. 15147757

61. Arensburger P, Megy K, Waterhouse RM, Abrudan J, Amedeo P, et al. (2010) Sequencing of Culex quinquefasciatus establishes a platform for mosquito comparative genomics. Science 330 : 86–88. doi: 10.1126/science.1191864 20929810

62. Schambony A, Hefele JA, Gentzel M, Wilm M, Wedlich D (2003) A homologue of cysteine-rich secretory proteins induces premature degradation of vitelline envelopes and hatching of Xenopus laevis embryos. Mech Dev 120 : 937–948. 12963113

63. Tchankouo-Nguetcheu S, Bourguet E, Lenormand P, Rousselle JC, Namane A, et al. (2012) Infection by chikungunya virus modulates the expression of several proteins in Aedes aegypti salivary glands. Parasit Vectors 5 : 264. doi: 10.1186/1756-3305-5-264 23153178

64. Ribeiro JM, Arca B, Lombardo F, Calvo E, Phan VM, et al. (2007) An annotated catalogue of salivary gland transcripts in the adult female mosquito, Aedes aegypti. BMC Genomics 8 : 6. 17204158

65. Gibbs GM, Roelants K, O'Bryan MK (2008) The CAP superfamily: cysteine-rich secretory proteins, antigen 5, and pathogenesis-related 1 proteins—roles in reproduction, cancer, and immune defense. Endocr Rev 29 : 865–897. doi: 10.1210/er.2008-0032 18824526

66. Ribeiro JM, Arca B, Lombardo F, Calvo E, Phan VM, et al. (2007) An annotated catalogue of salivary gland transcripts in the adult female mosquito, Aedes aegypti. BMC Genomics 8 : 6. 17204158

67. Londono-Renteria B, Cardenas JC, Cardenas LD, Christofferson RC, Chisenhall DM, et al. (2013) Use of anti-Aedes aegypti salivary extract antibody concentration to correlate risk of vector exposure and dengue transmission risk in Colombia. PLoS One 8: e81211. doi: 10.1371/journal.pone.0081211 24312537

68. Londono-Renteria BL, Eisele TP, Keating J, James MA, Wesson DM (2010) Antibody response against Anopheles albimanus (Diptera: Culicidae) salivary protein as a measure of mosquito bite exposure in Haiti. J Med Entomol 47 : 1156–1163. 21175067

69. Ameri M, Wang X, Wilkerson MJ, Kanost MR, Broce AB (2008) An immunoglobulin binding protein (antigen 5) of the stable fly (Diptera: Muscidae) salivary gland stimulates bovine immune responses. J Med Entomol 45 : 94–101. 18283948

70. Suzuki M, Itoh T, Anuruddhe BM, Bandaranayake IK, Shirani Ranasinghe JG, et al. (2010) Molecular diversity in venom proteins of the Russell's viper (Daboia russellii russellii) and the Indian cobra (Naja naja) in Sri Lanka. Biomed Res 31 : 71–81. 20203422

71. Plotnick MI, Mayne L, Schechter NM, Rubin H (1996) Distortion of the active site of chymotrypsin complexed with a serpin. Biochemistry 35 : 7586–7590. 8652540

72. Wei A, Rubin H, Cooperman BS, Christianson DW (1994) Crystal structure of an uncleaved serpin reveals the conformation of an inhibitory reactive loop. Nat Struct Biol 1 : 251–258. 7656054

73. Han J, Zhang H, Min G, Kemler D, Hashimoto C (2000) A novel Drosophila serpin that inhibits serine proteases. FEBS Lett 468 : 194–198. 10692585

74. Rizvi N, Chaturvedi UC, Mathur A (1991) Inhibition of the presentation of dengue virus antigen by macrophages to B cells by serine-protease inhibitors. Int J Exp Pathol 72 : 23–29. 1888663

75. Morrow IC, Parton RG (2005) Flotillins and the PHB domain protein family: rafts, worms and anaesthetics. Traffic 6 : 725–740. 16101677

76. McClung JK, Danner DB, Stewart DA, Smith JR, Schneider EL, et al. (1989) Isolation of a cDNA that hybrid selects antiproliferative mRNA from rat liver. Biochem Biophys Res Commun 164 : 1316–1322. 2480116

77. Kuadkitkan A, Smith DR, Berry C (2012) Investigation of the Cry4B-prohibitin interaction in Aedes aegypti cells. Curr Microbiol 65 : 446–454. doi: 10.1007/s00284-012-0178-4 22767320

78. Sharma A, Qadri A (2004) Vi polysaccharide of Salmonella typhi targets the prohibitin family of molecules in intestinal epithelial cells and suppresses early inflammatory responses. Proc Natl Acad Sci U S A 101 : 17492–17497. 15576509

79. Kolonin MG, Saha PK, Chan L, Pasqualini R, Arap W (2004) Reversal of obesity by targeted ablation of adipose tissue. Nat Med 10 : 625–632. 15133506

80. Grotendorst CA, Carter R (1987) Complement effects of the infectivity of Plasmodium gallinaceum to Aedes aegypti mosquitoes. II. Changes in sensitivity to complement-like factors during zygote development. J Parasitol 73 : 980–984. 3116195

81. Margos G, Navarette S, Butcher G, Davies A, Willers C, et al. (2001) Interaction between host complement and mosquito-midgut-stage Plasmodium berghei. Infect Immun 69 : 5064–5071. 11447187

82. Chugh M, Adak T, Sehrawat N, Gakhar SK (2011) Effect of anti-mosquito midgut antibodies on development of malaria parasite, Plasmodium vivax and fecundity in vector mosquito Anopheles culicifacies (Diptera: culicidae). Indian J Exp Biol 49 : 245–253. 21614887

83. Ramasamy MS, Sands M, Kay BH, Fanning ID, Lawrence GW, et al. (1990) Anti-mosquito antibodies reduce the susceptibility of Aedes aegypti to arbovirus infection. Med Vet Entomol 4 : 49–55. 1966777

84. Cheng G, Liu L, Wang P, Zhang Y, Zhao YO, et al. (2011) An in vivo transfection approach elucidates a role for Aedes aegypti thioester-containing proteins in flaviviral infection. PloS one 6: e22786. doi: 10.1371/journal.pone.0022786 21818390

85. Colpitts TM, Cox J, Nguyen A, Feitosa F, Krishnan MN, et al. (2011) Use of a tandem affinity purification assay to detect interactions between West Nile and dengue viral proteins and proteins of the mosquito vector. Virology 417 : 179–187. doi: 10.1016/j.virol.2011.06.002 21700306