Role of the vector in arbovirus transmission

Annual Review of Virology

Volumn 1, Issue 1, 2014, Pages 71-88

  Conway, Michael J ^a   Colpitts, Tonya M ^b   Fikrig, Erol ^c,d  

^a Children's Hospital of Michigan   (United States)

^b TULANE UNIVERSITY   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Host; Immune response; Mosquito; Saliva protein

Indexed keywords

INSECT REPELLENT; VIRUS VECTOR;

AEDES AEGYPTI; AEDES ALBOPICTUS; ARBOVIRAL DISEASE; ARBOVIRUS; ARTICLE; CULEX; DISEASE CARRIER; GENOMICS; HOST; HOST PARASITE INTERACTION; HUMAN; INFECTION; INFECTION CONTROL; LETHAL GENE; MICROORGANISM; MOSQUITO; PREVALENCE; PRIORITY JOURNAL; PROTEOMICS; SALIVA; SALIVARY GLAND; TRANSGENIC MOSQUITO; VIRUS INFECTION; VIRUS TRANSMISSION; WEST NILE VIRUS; WOLBACHIA;

ARBOVIRUS;

EID: 85017019954     PISSN: 2327056X     EISSN: 23270578     Source Type: Journal    
DOI: 10.1146/annurev-virology-031413-085513     Document Type: Article

References (116)

1. Anderson JR,Rico-Hesse R. 2006. Aedes aegypti vectorial capacity is determined by the infecting genotype of dengue virus. Am. J. Trop. Med. Hyg. 75:886-92
2. Bhatt S,Gething PW, Brady OJ, Messina JP, Farlow AW, et al. 2013. The global distribution and burden of dengue. Nature 496:504-7
3. Guzman MG,Halstead SB, ArtsobH, Buchy P, Farrar J, et al. 2010. Dengue: a continuing global threat. Nat. Rev. Microbiol. 8:S7-16
4. Kilpatrick AM, Randolph SE. 2012. Drivers, dynamics, and control of emerging vector-borne zoonotic diseases. Lancet 380:1946-55
5. Lindsey NP, Lehman JA, Staples JE, Fischer M. 2013. West Nile virus and other arboviral diseases-United States, 2012. CDC Morb. Mortal. Wkly. Rep. 62:513-17. http://www.cdc.gov/mmwr/preview/ mmwrhtml/mm6225a1.htm
6. Petersen LR,Carson PJ, Biggerstaff BJ,Custer B, Borchardt SM, Busch MP. 2012. Estimated cumulative incidence of West Nile virus infection in US adults, 1999-2010. Epidemiol. Infect. 141:591-95
7. Murray KO, Ruktanonchai D, Hesalroad D, Fonken E, Nolan MS. 2013. West Nile virus, Texas, USA, 2012. Emerg. Infect. Dis. 19 doi: 10.3201/eid1911.130768
8. Murray KO, Rodriguez LF, Herrington E, Kharat V, Vasilakis N, et al. 2013. Identification of dengue fever cases in Houston, Texas, with evidence of autochthonous transmission between 2003 and 2005. Vector Borne Zoonotic Dis. 13:835-45
9. Eisen L,Moore CG. 2013. Aedes (Stegomyia) aegypti in the continental United States: a vector at the cool margin of its geographic range. J. Med. Entomol. 50:467-78
10. Rezza G. 2012. Aedes albopictus and the reemergence of dengue. BMC Public Health 12:72
11. Mitchell CJ, Niebylski ML, Smith GC, Karabatsos N,Martin D, et al. 1992. Isolation of eastern equine encephalitis virus from Aedes albopictus in Florida. Science 257:526-27
12. Hanson SM, Craig GB Jr. 1995. Aedes albopictus (Diptera: Culicidae) eggs: field survivorship during northern Indiana winters. J. Med. Entomol. 32:599-604
13. Swanson J, Lancaster M, Anderson J, Crandell M, Haramis L, et al. 2000. Overwintering and establishment of Aedes albopictus (Diptera: Culicidae) in an urban La Crosse virus enzootic site in Illinois. J. Med. Entomol. 37:454-60
14. Hawley WA, Pumpuni CB, Brady RH, Craig GB Jr. 1989. Overwintering survival of Aedes albopictus (Diptera: Culicidae) eggs in Indiana. J. Med. Entomol. 26:122-29
15. Lambrechts L, Scott TW, Gubler DJ. 2010. Consequences of the expanding global distribution of Aedes albopictus for dengue virus transmission. PLoS Negl. Trop. Dis. 4:e646
16. Bargielowski IE, Lounibos LP, Carrasquilla MC. 2013. Evolution of resistance to satyrization through reproductive character displacement in populations of invasive dengue vectors. Proc. Natl. Acad. Sci. USA 110:2888-92
17. Tripet F, Lounibos LP, Robbins D, Moran J, Nishimura N, Blosser EM. 2011. Competitive reduction by satyrization? Evidence for interspecific mating in nature and asymmetric reproductive competition between invasive mosquito vectors. Am. J. Trop. Med. Hyg. 85:265-70
18. Kilpatrick AM, Kramer LD, Jones MJ, Marra PP, Daszak P. 2006. West Nile virus epidemics in North America are driven by shifts in mosquito feeding behavior. PLoS Biol. 4:e82
19. Kilpatrick AM, Daszak P, Jones MJ, Marra PP, Kramer LD. 2006. Host heterogeneity dominates West Nile virus transmission. Proc. R. Soc. B 273:2327-33
20. 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
21. Kato N, Mueller CR, Fuchs JF, McElroy K,Wessely V, et al. 2008. Evaluation of the function of a type I peritrophic matrix as a physical barrier for midgut epithelium invasion by mosquito-borne pathogens in Aedes aegypti. Vector Borne Zoonotic Dis. 8:701-12
22. 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. 79:267-74
23. Oliveira JH, Goncalves RL, Lara FA, Dias FA, Gandara AC, et al. 2011. Blood meal-derived heme decreases ROS levels in the midgut of Aedes aegypti and allows proliferation of intestinal microbiota. PLoS Pathog. 7:e1001320
24. Forrester NL, Guerbois M, Seymour RL, Spratt H, Weaver SC. 2012. Vector-borne transmission imposes a severe bottleneck on an RNA virus population. PLoS Pathog. 8:e1002897
25. Tsetsarkin KA, Weaver SC. 2011. Sequential adaptive mutations enhance efficient vector switching by chikungunya virus and its epidemic emergence. PLoS Pathog. 7:e1002412
26. 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
27. Bonizzoni M, Dunn WA, Campbell CL, Olson KE,Marinotti O, James AA. 2012. Complex modulation of the Aedes aegypti transcriptome in response to dengue virus infection. PLoS ONE 7:e50512
28. Luplertlop N, Surasombatpattana P, Patramool S, 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
29. Bartholomay LC, Waterhouse RM, Mayhew GF, Campbell CL, Michel K, et al. 2010. Pathogenomics of Culex quinquefasciatus and meta-analysis of infection responses to diverse pathogens. Science 330:88-90
30. 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 106:17841-46
31. Brackney DE, Beane JE, Ebel GD. 2009. RNAi targeting of West Nile virus in mosquito midguts promotes virus diversification. PLoS Pathog. 5:e1000502
32. Keene KM, Foy BD, Sanchez-Vargas I, Beaty BJ, Blair CD, Olson KE. 2004. RNA interference acts as a natural antiviral response to o'nyong-nyong virus (Alphavirus; Togaviridae) infection of Anopheles gambiae. Proc. Natl. Acad. Sci. USA 101:17240-45
33. Xu J, Hopkins K, Sabin L, Yasunaga A, Subramanian H, et al. 2013. ERK signaling couples nutrient status to antiviral defense in the insect gut. Proc. Natl. Acad. Sci. USA 110:15025-30
34. Girard YA, Klingler KA, Higgs S. 2004. West Nile virus dissemination and tissue tropisms in orally infected Culex pipiens quinquefasciatus. Vector Borne Zoonotic Dis. 4:109-22
35. Salazar MI,Richardson JH, Sanchez-Vargas I,Olson KE,Beaty BJ. 2007. Dengue virus type 2: replication and tropisms in orally infected Aedes aegypti mosquitoes. BMC Microbiol. 7:9
36. Weaver SC, BraultAC, KangW,Holland JJ. 1999. Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells. J. Virol. 73:4316-26
37. Vasilakis N, Deardorff ER, Kenney JL, Rossi SL, Hanley KA, Weaver SC. 2009. Mosquitoes put the brake on arbovirus evolution: experimental evolution reveals slower mutation accumulation in mosquito than vertebrate cells. PLoS Pathog. 5:e1000467
38. Coffey LL, Vasilakis N, Brault AC, Powers AM, Tripet F, Weaver SC. 2008. Arbovirus evolution in vivo is constrained by host alternation. Proc. Natl. Acad. Sci. USA 105:6970-75
39. Cologna R, Armstrong PM, Rico-Hesse R. 2005. Selection for virulent dengue viruses occurs in humans and mosquitoes. J. Virol. 79:853-59
40. Greenwalt DE,Goreva YS, Siljeström SM, RoseT,Harbach RE. 2013. Hemoglobin-derived porphyrins preserved in a Middle Eocene blood-engorged mosquito. Proc. Natl. Acad. Sci. USA. In press. doi: 10.1073/pnas.1310885110
41. Cook S, Moureau G, Harbach RE, Mukwaya L, Goodger K, et al. 2009. Isolation of a novel species of flavivirus and a new strain of Culex flavivirus (Flaviviridae) from a natural mosquito population in Uganda. J. Gen. Virol. 90:2669-78
42. Cook S, Moureau G, Kitchen A, Gould EA, de Lamballerie X, et al. 2012. Molecular evolution of the insect-specific flaviviruses. J. Gen. Virol. 93:223-34
43. Edman JD, Strickman D, Kittayapong P, Scott TW. 1992. Female Aedes aegypti (Diptera: Culicidae) in Thailand rarely feed on sugar. J. Med. Entomol. 29:1035-38
44. Foster WA. 1995. Mosquito sugar feeding and reproductive energetics. Annu. Rev. Entomol. 40:443-74
45. Vinogradova EB, Karpova SG. 2006. Cultivation of the mosquito Culex pipiens pipiens f. molestus (Diptera, Culicidae) without blood feeding. Parazitologiia 40:306-11
46. O'Meara GF, Edman JD. 1975. Autogenous egg production in the salt-marsh mosquito, Aedes taeniorhynchus. Biol. Bull. 149:384-96
47. Foster WA, Hancock RG. 1994. Nectar-related olfactory and visual attractants for mosquitoes. J. Am. Mosq. Control Assoc. 10:288-96
48. DeGennaro M, McBride CS, Seeholzer L, Nakagawa T, Dennis EJ, et al. 2013. orco mutant mosquitoes lose strong preference for humans and are not repelled by volatile DEET. Nature 498:487-91
49. Dormont L, Bessiere JM, McKey D, Cohuet A. 2013. New methods for field collection of human skin volatiles and perspectives for their application in the chemical ecology of human-pathogen-vector interactions. J. Exp. Biol. 216:2783-88
50. Verhulst NO, Beijleveld H, Knols BG, Takken W, Schraa G, et al. 2009. Cultured skin microbiota attracts malaria mosquitoes. Malar. J. 8:302
51. Smallegange RC, Knols BG, TakkenW. 2010. Effectiveness of synthetic versus natural human volatiles as attractants for Anopheles gambiae (Diptera: Culicidae) sensu stricto. J. Med. Entomol. 47:338-44
52. Bohbot JD, Durand NF, Vinyard BT,Dickens JC. 2013. Functional development of the octenol response in Aedes aegypti. Front. Physiol. 4:39
53. Tauxe GM, MacWilliam D, Boyle SM, Guda T, Ray A. 2013. Targeting a dual detector of skin and CO2 to modify mosquito host seeking. Cell 155:1365-79
54. Turell MJ, Tammariello RF, Spielman A. 1995. Nonvascular delivery of St. Louis encephalitis and Venezuelan equine encephalitis viruses by infected mosquitoes (Diptera: Culicidae) feeding on a vertebrate host. J. Med. Entomol. 32:563-68
55. Turell MJ, Spielman A. 1992. Nonvascular delivery of Rift Valley fever virus by infected mosquitoes. Am. J. Trop. Med. Hyg. 47:190-94
56. Styer LM, Kent KA, Albright RG, Bennett CJ, Kramer LD, Bernard KA. 2007. Mosquitoes inoculate high doses of West Nile virus as they probe and feed on live hosts. PLoS Pathog. 3:1262-70
57. Thangamani S, Higgs S, Ziegler S, Vanlandingham D, Tesh R,Wikel S. 2010. Host immune response to mosquito-transmitted chikungunya virus differs from that elicited by needle inoculated virus. PLoS ONE 5:e12137
58. Ader DB, Celluzzi C, Bisbing J,Gilmore L,Gunther V, et al. 2004. Modulation of dengue virus infection of dendritic cells by Aedes aegypti saliva. Viral Immunol. 17:252-65
59. Schneider BS, Soong L, Zeidner NS, Higgs S. 2004. Aedes aegypti salivary gland extracts modulate anti-viral and TH1/TH2 cytokine responses to Sindbis virus infection. Viral Immunol. 17:565-73
60. Schneider BS, Soong L, Girard YA, Campbell G, Mason P, Higgs S. 2006. Potentiation of West Nile encephalitis by mosquito feeding. Viral Immunol. 19:74-82
61. Styer LM, Lim PY, Louie KL, Albright RG, Kramer LD, Bernard KA. 2011. Mosquito saliva causes enhancement ofWest Nile virus infection in mice. J. Virol. 85:1517-27
62. Surasombatpattana P, Ekchariyawat P, HamelR, Patramool S, Thongrungkiat S, et al. 2013. Aedes aegypti saliva contains a prominent 34-kDa protein that strongly enhances dengue virus replication in human keratinocytes. J. Investig. Dermatol. 134:281-84
63. 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. 88:164-75
64. Le Coupanec A, Babin D, Fiette L, Jouvion G, Ave P, et al. 2013. Aedes mosquito saliva modulates Rift Valley fever virus pathogenicity. PLoS Negl. Trop. Dis. 7:e2237
65. Limesand KH, Higgs S, Pearson LD, Beaty BJ. 2000. Potentiation of vesicular stomatitis New Jersey virus infection in mice by mosquito saliva. Parasite Immunol. 22:461-67
66. Osorio JE, Godsey MS, Defoliart GR, Yuill TM. 1996. La Crosse viremias in white-tailed deer and chipmunks exposed by injection or mosquito bite. Am. J. Trop. Med. Hyg. 54:338-42
67. Reisen WK, Chiles RE, Kramer LD, Martinez VM, Eldridge BF. 2000. Method of infection does not alter response of chicks and house finches to western equine encephalomyelitis and St. Louis encephalitis viruses. J. Med. Entomol. 37:250-58
68. Schneider BS,Higgs S. 2008. The enhancement of arbovirus transmission and disease by mosquito saliva is associated with modulation of the host immune response. Trans. R. Soc. Trop. Med. Hyg. 102:400-8
69. Cox J,Mota J, Sukupolvi-Petty S, DiamondMS, Rico-Hesse R. 2012. Mosquito bite delivery of dengue virus enhances immunogenicity and pathogenesis in humanized mice. J. Virol. 86:7637-49
70. Christofferson RC, McCracken MK, Johnson AM, Chisenhall DM, Mores CN. 2013. Development of a transmission model for dengue virus. Virol. J. 10:127
71. McCracken MK, Christofferson RC, Chisenhall DM, Mores CN. 2014. Analysis of early dengue viral infection in mice as modulated by Aedes aegypti probing. J. Virol. 88:1881-89
72. Schneider BS, McGee CE, Jordan JM, Stevenson HL, Soong L, Higgs S. 2007. Prior exposure to uninfected mosquitoes enhances mortality in naturally-transmitted West Nile virus infection. PLoS ONE 2:e1171
73. Limesand KH, Higgs S, Pearson LD, Beaty BJ. 2003. Effect of mosquito salivary gland treatment on vesicular stomatitis New Jersey virus replication and interferon α/βexpression in vitro. J. Med. Entomol. 40:199-205
74. Surasombatpattana P, Patramool S, Luplertlop N, Yssel H,Misse D. 2012. Aedes aegypti saliva enhances dengue virus infection of human keratinocytes by suppressing innate immune responses. J. Investig. Dermatol. 132:2103-5
75. Edwards JF, Higgs S, Beaty BJ. 1998. Mosquito feeding-induced enhancement of Cache Valley virus (Bunyaviridae) infection in mice. J. Med. Entomol. 35:261-65
76. 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
77. Calvo E, Sanchez-Vargas I, Favreau AJ, Barbian KD, Pham VM, et al. 2010. An insight into the sialotranscriptome of the West Nile mosquito vector, Culex tarsalis. BMC Genomics 11:51
78. Reagan KL, Machain-Williams C, Wang T, Blair CD. 2012. Immunization of mice with recombinant mosquito salivary protein D7 enhances mortality from subsequent West Nile virus infection viamosquito bite. PLoS Negl. Trop. Dis. 6:e1935
79. Jacobs JJ, Lehe CL,HasegawaH, Elliott GR,Das PK. 2006. Skin irritants and contact sensitizers induce Langerhans cell migration and maturation at irritant concentration. Exp. Dermatol. 15:432-40
80. Ouwehand K, Oosterhoff D, BreetveldM, Scheper RJ, deGruijlTD, Gibbs S. 2011. Irritant-induced migration of Langerhans cells coincides with an IL-10-dependent switch to a macrophage-like phenotype. J. Investig. Dermatol. 131:418-25
81. Price AA, Cumberbatch M, Kimber I, Ager A. 1997. α6 integrins are required for Langerhans cell migration from the epidermis. J. Exp. Med. 186:1725-35
82. Hammad H, Lambrecht BN. 2008. Dendritic cells and epithelial cells: linking innate and adaptive immunity in asthma. Nat. Rev. Immunol. 8:193-204
83. Zeidner NS, Higgs S, Happ CM, Beaty BJ, Miller BR. 1999. Mosquito feeding modulates Th1 and Th2 cytokines in flavivirus susceptible mice: an effect mimicked by injection of sialokinins, but not demonstrated in flavivirus resistant mice. Parasite Immunol. 21:35-44
84. Wu SJ, Grouard-Vogel G, Sun W, Mascola JR, Brachtel E, et al. 2000. Human skin Langerhans cells are targets of dengue virus infection. Nat. Med. 6:816-20
85. Fink K, Ng C, Nkenfou C, Vasudevan SG, van Rooijen N, Schul W. 2009. Depletion of macrophages in mice results in higher dengue virus titers and highlights the role of macrophages for virus control. Eur. J. Immunol. 39:2809-21
86. Farrance CE, Chichester JA, Musiychuk K, Shamloul M, Rhee A, et al. 2011. Antibodies to plantproduced Plasmodium falciparum sexual stage protein Pfs25 exhibit transmission blocking activity. Hum. Vaccines 7(Suppl.):191-98
87. Mathias DK, Plieskatt JL, Armistead JS, Bethony JM, Abdul-Majid KB, et al. 2012. Expression, immunogenicity, histopathology, and potency of a mosquito-based malaria transmission-blocking recombinant vaccine. Infect. Immun. 80:1606-14
88. Miyata T, Harakuni T, Sugawa H, Sattabongkot J, Kato A, et al. 2011. Adenovirus-vectored Plasmodium vivax ookinete surface protein, Pvs25, as a potential transmission-blocking vaccine. Vaccine 29:2720-26
89. Williams AR, Zakutansky SE, Miura K, Dicks MD, Churcher TS, et al. 2013. Immunisation against a serine protease inhibitor reduces intensity of Plasmodium berghei infection in mosquitoes. Int. J. Parasitol. 43:869-74
90. Kamhawi S,Ramalho-OrtigaoM, PhamVM, Kumar S, Lawyer PG, et al. 2004. A role for insect galectins in parasite survival. Cell 119:329-41
91. Gomes R,Oliveira F, TeixeiraC,Meneses C, GilmoreDC, et al. 2012. Immunity to sand fly salivary protein LJM11 modulates host response to vector-transmitted leishmania conferring ulcer-free protection. J. Investig. Dermatol. 132:2735-43
92. Gomes R, Teixeira C, Teixeira MJ, Oliveira F, Menezes MJ, et al. 2008. Immunity to a salivary protein of a sand fly vector protects against the fatal outcome of visceral leishmaniasis in a hamster model. Proc. Natl. Acad. Sci. USA 105:7845-50
93. Jones PL, Pask GM, Rinker DC, Zwiebel LJ. 2011. Functional agonism of insect odorant receptor ion channels. Proc. Natl. Acad. Sci. USA 108:8821-25
94. Taylor RW, Romaine IM, Liu C, Murthi P, Jones PL, et al. 2012. Structure-activity relationship of a broad-spectrum insect odorant receptor agonist. ACS Chem. Biol. 7:1647-52
95. Laven H. 1967. Eradication of Culex pipiens fatigans through cytoplasmic incompatibility. Nature 216:383-84
96. Dobson SL, Fox CW, Jiggins FM. 2002. The effect of Wolbachia-induced cytoplasmic incompatibility on host population size in natural and manipulated systems. Proc. R. Soc. B 269:437-45
97. Mousson L, Zouache K, Arias-Goeta C, Raquin V,Mavingui P, Failloux AB. 2012. The native Wolbachia symbionts limit transmission of dengue virus in Aedes albopictus. PLoS Negl. Trop. Dis. 6:e1989
98. Glaser RL, Meola MA. 2010. The native Wolbachia endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to West Nile virus infection. PLoS ONE 5:e11977
99. Blagrove MS, Arias-Goeta C, Di Genua C, Failloux AB, Sinkins SP. 2013. A Wolbachia wMel transinfection in Aedes albopictus is not detrimental to host fitness and inhibits chikungunya virus. PLoS Negl. Trop. Dis. 7:e2152
100. Xi Z, Khoo CC, Dobson SL. 2005. Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science 310:326-28
101. McMeniman CJ, Lane RV, Cass BN, Fong AW, Sidhu M, et al. 2009. Stable introduction of a lifeshortening Wolbachia infection into the mosquito Aedes aegypti. Science 323:141-44
102. Walker T, Johnson PH, Moreira LA, Iturbe-Ormaetxe I, Frentiu FD, et al. 2011. The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 476:450-53
103. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, et al. 2009. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, chikungunya, and Plasmodium. Cell 139:1268-78
104. Bian G, Xu Y, Lu P, Xie Y, Xi Z. 2010. The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti. PLoS Pathog. 6:e1000833
105. Hoffmann AA, Montgomery BL, Popovici J, Iturbe-Ormaetxe I, Johnson PH, et al. 2011. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476:454-57
106. Burivong P, Pattanakitsakul SN, Thongrungkiat S, Malasit P, Flegel TW. 2004. Markedly reduced severity of dengue virus infection in mosquito cell cultures persistently infected with Aedes albopictus densovirus (AalDNV). Virology 329:261-69
107. Hirunkanokpun S, Carlson JO, Kittayapong P. 2008. Evaluation ofmosquito densoviruses for controlling Aedes aegypti (Diptera: Culicidae): variation in efficiency due to virus strain and geographic origin of mosquitoes. Am. J. Trop. Med. Hyg. 78:784-90
108. Afanasiev BN, Kozlov YV, Carlson JO, Beaty BJ. 1994. Densovirus of Aedes aegypti as an expression vector in mosquito cells. Exp. Parasitol. 79:322-39
109. Fu G, Lees RS, Nimmo D, Aw D, Jin L, et al. 2010. Female-specific flightless phenotype for mosquito control. Proc. Natl. Acad. Sci. USA 107:4550-54
110. Phuc HK, Andreasen MH, Burton RS, Vass C, Epton MJ, et al. 2007. Late-acting dominant lethal genetic systems and mosquito control. BMC Biol. 5:11
111. Bargielowski I, Nimmo D, Alphey L, Koella JC. 2011. Comparison of life history characteristics of the genetically modified OX513A line and a wild type strain of Aedes aegypti. PLoS ONE 6:e20699
112. Harris AF, McKemey AR, Nimmo D, Curtis Z, Black I, et al. 2012. Successful suppression of a field mosquito population by sustained release of engineered male mosquitoes. Nat. Biotechnol. 30:828-30
113. Franz AW, Sanchez-Vargas I, Adelman ZN, Blair CD, Beaty BJ, et al. 2006. Engineering RNA interference-based resistance to dengue virus type 2 in genetically modified Aedes aegypti. Proc. Natl. Acad. Sci. USA 103:4198-203
114. Deredec A,GodfrayHC, Burt A. 2011. Requirements for effectivemalaria control with homing endonuclease genes. Proc. Natl. Acad. Sci. USA 108:E874-80
115. Traver BE, Anderson MA, Adelman ZN. 2009. Homing endonucleases catalyze double-stranded DNA breaks and somatic transgene excision in Aedes aegypti. Insect. Mol. Biol. 18:623-33
116. Cheng G, Cox J, Wang P, Krishnan MN, Dai J, et al. 2010. A C-type lectin collaborates with a CD45 phosphatase homolog to facilitateWest Nile virus infection of mosquitoes. Cell 142:714-25