Two step male release strategy using transgenic mosquito lines to control transmission of vector-borne diseases

Acta Tropica

Volumn 132, Issue 1, 2014, Pages

  Carvalho, Danilo Oliveira ^a,b   Costa da Silva, André Luis ^a,b   Lees, Rosemary Susan ^c   Capurro, Margareth Lara ^a,b  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c Polo d'Innovazione Genomica Genetica e Biologia SCaRL Edificio D 4 piano Polo Unico di Medicina 'Santa Maria della Misericordia'   (Italy)

Author keywords

Dengue; Malaria; Transgenic; Two step release; Vector control

Indexed keywords

CLIMATE CONDITIONS; DENGUE FEVER; DISEASE CONTROL; DISEASE TRANSMISSION; INTEGRATED APPROACH; MALARIA; MOSQUITO; PATHOGEN;

ARTICLE; BIOLOGICAL PEST CONTROL; CLIMATE CHANGE; CONTROL STRATEGY; DISEASE TRANSMISSION; DNA MODIFICATION; ENVIRONMENTAL FACTOR; ENVIRONMENTAL TEMPERATURE; INSECT CONTROL; MALARIA CONTROL; NONHUMAN; TRANSGENIC ANIMAL; TWO STEP RELEASE STRATEGY; VECTOR CONTROL;

HEXAPODA;

DENGUE; MALARIA; TRANSGENIC; TWO STEP RELEASE; VECTOR CONTROL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CULICIDAE; DENGUE; FEMALE; INSECT VECTORS; MALARIA; MALE; MOSQUITO CONTROL; PEST CONTROL, BIOLOGICAL;

EID: 84896542794     PISSN: 0001706X     EISSN: 18736254     Source Type: Journal    
DOI: 10.1016/j.actatropica.2013.09.023     Document Type: Article

References (89)

1. Alphey L. Re-engineering the sterile insect technique. Insect Biochem. Mol. Biol. 2002, 32:1243-1247.
2. Alphey L., Andreasen M. Dominant lethality and insect population control. Mol. Biochem. Parasitol. 2002, 121:173-178.
3. Alphey L., Benedict M.Q., Bellini R., Clark G.G., Dame D.A., Service M.W., Dobson S.L. Sterile-insect methods for control of mosquito-borne diseases: an analysis. Vector Borne Zoonotic Dis. 2010, 10:295-311.
4. Adelman Z.N., Anderson M.A.E., Wiley M.R., Murreddu M.G., Samuel G.H., Morazzani M.E., Myles K.M. Cooler temperatures destabilize RNA interference and increase susceptibility of disease vector mosquitoes to viral infection. PLoS Negl. Trop. Dis. 2013, 7(5):e2239. doi:10.1371/journal.pntd.0002239.
5. Andraud M., Hens N., Marais C., Beutels P. Dynamic epidemiological models for dengue transmission: a systematic review of structural approaches. PLoS One 2012, 7:e49085.
6. Bakri A., Mehta K., Lance D.R. Sterilizing Insects with Ionizing Radiation in: Sterile Insect Technique 2005, 233-268. Springer, Netherlands.
7. Benedict M.Q. The first releases of transgenic mosquitoes: an argument for the sterile insect technique. Trends Parasitol. 2003, 19:349-355.
8. Berg H., vd Mutero C.M., Ichimori K. Guidance on policy-making for Integrated Vector Management 2012, Wolrd Health Organization - WHO, Geneva.
9. Bermudez S.E., Espinosa J.D., Cielo A.B., Clavel F., Subia J., Barrios S., Medianero E. Incidence of myiasis in Panama during the eradication of Cochliomyia hominivorax (Coquerel 1858, Diptera: Calliphoridae) (2002-2005). Mem. Inst. Oswaldo Cruz 2007, 102:675-679.
10. Bhatt S., Gething P.W., Brady O.J., Messina J.P., Farlow A.W., Moyes C.L., Drake J.M., Brownstein J.S., Hoen A.G., Sankoh O., Myers M.F., George D.B., Jaenisch T., Wint G.R.W., Simmons C.P., Scott T.W., Farrar J.J., Hay S.I. The global distribution and burden of dengue. Nature 2013, 496:504-507.
11. Bracco J.E., Dalbon M., Marinotti O., Barata J.M.S. Resistência a inseticidas organofosforados e carbamatos em população de Culex quinquefasciatus. Rev. Saude Publica 1997, 31:182-183.
12. Brinton M.A. The molecular biology of West Nile Virus: a new invader of the western hemisphere. Annu. Rev. Microbiol. 2002, 56:371-402.
13. Bryant B., Blair C.D., Olson K.E., Clem R.J. Annotation and expression profiling of apoptosis-related genes in the yellow fever mosquito, Aedes aegypti. Insect Biochem. Mol. Biol. 2008, 38:331-345.
14. Capurro M.L., Coleman J., Beerntsen B.T., Myles K.M., Olson K.E., Rocha E., Krettli A.U., James A.A. Virus-expressed, recombinant single-chain antibody blocks sporozoite infection of salivary glands in Plasmodium gallinaceum-infected Aedes aegypti. Am. J. Trop. Med. Hyg. 2000, 62:427-433.
15. Carrington L.B., Armijos M.V., Lambrechts L., Scott T.W. Fluctuations at a low mean temperature accelerate dengue virus transmission by Aedes aegypti. PLoS Negl. Trop. Dis. 2013, 7:e2190.
16. Catteruccia F., Crisanti A., Wimmer E.A. Transgenic technologies to induce sterility. Malar. J. 2009, 8(Suppl 2):S7.
17. Cazelles B., Chavez M., McMichael A.J., Hales S. Nonstationary influence of El Niño on the synchronous dengue epidemics in Thailand. PLoS Med. 2005, 2:e106.
18. Chen C., Huang H., Ward C.M., Su J.T., Schaeffer L.V., Guo M., Hay B.A. A synthetic maternal-effect selfish genetic element drives population replacement in Drosophila. Science 2007, 316:597-600.
19. Consoli R.A.G.B., Lourenço-de-Oliveira R. Principais Mosquitos de Importância Sanitária no Brasil 1998, Fundação Oswaldo Cruz, Rio de Janeiro. 1 ed.
20. Costa-da-Silva A.L., Capurro M.L., Bracco J.E. Genetic lineages in the yellow fever mosquito Aedes (Stegomyia) aegypti (Diptera-: Culicidae) from Peru. Mem. Inst. Oswaldo Cruz 2005, 100:539-544.
21. Craig G.B., Vandehey R.C., Hickey W.A. Genetic Variability in Populations of Aedes aegypti. Bull. World Health Organ. 1961, 24:527-539.
22. Darriet F., Marcombe S., Etienne M., Yébakima A., Agnew P., Yp-Tcha M., Corbel V. Field evaluation of pyriproxyfen and spinosad mixture for the control of insecticide resistant Aedes aegypti in Martinique (French West Indies). Parasit. Vectors 2010, 3:88.
23. Enayati A., Hemingway J. Malaria management: past, present, and future. Annu. Rev. Entomol. 2010, 55:569-591.
24. Focks D.A., Barrera R. Dengue transmission dynamics: assessment and implications for control 2007.
25. Forattini O.P. Culicidologia médica-identificação, biologia e epidemiologia. 1st ed, Culicidologia Médica. Edusp, São Paulo 2002.
26. Franz A.W.E., Sanchez-Vargas I., Adelman Z.N., Blair C.D., Beaty B.J., James A.A., Olson K.E. Engineering RNA interference-based resistance to dengue virus type 2 in genetically modified Aedes aegypti. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:4198-4203.
27. Franz A.W.E., Sanchez-Vargas I., Piper J., Smith M.R., Khoo C.C.H., James A.A., Olson K.E. Stability and loss of a virus resistance phenotype over time in transgenic mosquitoes harbouring an antiviral effector gene. Insect Mol. Biol. 2009, 18:661-672.
28. Garcia L.S. Malaria. Clin. Lab. Med. 2010, 30:93-129.
29. Godfray H.C.J. Mosquito ecology and control of malaria. J. Anim. Ecol. 2013, 82:15-25.
30. Gong P., Epton M.J., Fu G., Scaife S., Hiscox A., Condon K.C., Condon G.C., Morrison N.I., Kelly D.W., Dafa'alla T.H., Coleman P.G., Alphey L. A dominant lethal genetic system for autocidal control of the mediterranean fruitfly. Nat. Biotechnol. 2005, 23:453-456.
31. Gould F., Schliekelman P. Population genetics of autocidal control and strain replacement. Annu. Rev. Entomol. 2004, 49:193-217.
32. Gubler D.J. Dengue and dengue hemorrhagic fever. Clin. Microbiol. Rev. 1998, 11:480-496.
33. Gubler D.J. The Global Threat of Emergent/Re-emergent Vector-Borne Diseases. Vector Biology, Ecology and Control. Netherlands 2010, 39-62. Springer. P.W. Atkinson (Ed.).
34. Harris A.F., McKemey A.R., Nimmo D., Curtis Z., Black I., Morgan S., Oviedo M.N., Lacroix R., Naish N., Morrison N.I., Collado A., Stevenson J., Scaife S., Dafa'alla T., Fu G., Phillips C., Miles A., Raduan N., Kelly N., Beech C., Donnelly C., Petrie W.D., Alphey L. Successful suppression of a field mosquito population by sustained release of engineered male mosquitoes. Nat. Biotechnol. 2012, 30:828-830.
35. Harris A.F., Rajatileka S., Ranson H. Pyrethroid resistance in Aedes aegypti from Grand Cayman. Am. J. Trop. Med. Hyg. 2010, 83:277-284.
36. Hay B.A., Chen C., Ward C.M., Huang H., Su J.T., Guo M. Engineering the genomes of wild insect populations: challenges, and opportunities provided by synthetic Medea selfish genetic elements. J. Insect Physiol. 2010, 56:1402-1413.
37. Helinski M.E.H., Hassan M.M., El-motasim W.M., Malcolm C.A., Knols B.G.J., El-sayed B. Towards a sterile insect technique field release of Anopheles arabiensis mosquitoes in Sudan-: Irradiation, transportation, and field cage experimentation. Malar. J. 2008, 7:1-10.
38. Hendrichs J., Robinson A.S., Cayol J.P., Enkerlin W. Medfly areawide sterile insect technique programs for prevention, suppression or eradication: the importance of mating behavior studies. Fla. Entomol. 2002, 85:1-13.
39. Hoffmann A.A., Montgomery B.L., Popovici J., Iturbe-Ormaetxe I., Johnson P.H., Muzzi F., Greenfield M., Durkan M., Leong Y.S., Dong Y., Cook H., Axford J., Callahan A.G., Kenny N., Omodei C., McGraw E.A., Ryan P., a Ritchie S.A., Turelli M., O'Neill S.L. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 2011, 476:454-457.
40. Honorio N.A., Castro M.G., Barros F.S.M., Magalhaes M.A.F.M., Sabroza P.C. The spatial distribution of Aedes aegypti and Aedes albopictus in a transition zone, Rio de Janeiro, Brazil. Cad. Saude Publica 2009, 25:1203-1214.
41. Hopp M.J., Foley J.A. Worldwide fluctuations in dengue fever cases related to climate variability. Clin. Res. 2003, 25:85-94.
42. Howell P.I., Knols B.G.J. Male mating biology. Malar. J. 2009, 8:S8.
43. Isaacs A.T., Jasinskiene N., Tretiakov M., Thiery I., Zettor A., Bourgouin C., James A.A. Transgenic Anopheles stephensi coexpressing single-chain antibodies resist Plasmodium falciparum development. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E1922-E1930.
44. Kaiser P.E., Bailey D.L., Lowe R.E., Seawright J.A., Dame D.A. Mating competitiveness of chemosterilized males of a genetic sexing strain of Anopheles albimanus in laboratory and field tests. Mosq. News 1979, 39:768-775.
45. Kantele A., Jokiranta T.S. Review of cases with the emerging fifth human malaria parasite Plasmodium knowlesi. Clin. Infect. Dis. 2011, 52:1356-1362.
46. Killeen G.F., Fillinger U., Kiche I., Gouagna L.C., Knols B.G.J. Eradication of Anopheles gambiae from Brazil: lessons for malaria control in Africa?. Lancet Infect. Dis. 2002, 2:618-627.
47. Kilpatrick A.M., Meola M.A., Moudy R.M., Kramer L.D. Temperature, viral genetics, and the transmission of West Nile virus by Culex pipiens mosquitoes. PLoS Pathog. 2008, 4:e1000092.
48. Knipling E.F. Possibilities of insect control or eradication through the use of sexually sterile males. J. Econ. Entomol. 1955, 48:459-462.
49. Kokoza V., Ahmed A., Shin S.W., Okafor N., Zou Z., Raikhel A.S. Blocking of Plasmodium transmission by cooperative action of cecropin A and defensin A in transgenic Aedes aegypti mosquitoes. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:8111-8116.
50. Labbe G.M., Scaife S., Morgan S.A., Curtis Z.H., Alphey L. Female-specific flightless (fsRIDL) phenotype for control of Aedes albopictus. PLoS Negl. Trop. Dis. 2012, 6:e1724.
51. Lima J.B.P., Da-Cunha M.P., Silva R.C.J., Galardo A.K.R., Soares S.S., Braga I.A., Ramos R.P., Valle D. Resistance of Aedes aegypti to organophosphates in several municipalities in the State of Rio de Janeiro and Espírito Santo, Brazil. Am. J. Trop. Med. Hyg. 2003, 68:233-329.
52. Lounibos L.P. Invasion by insect vectors of human disease. Annu. Rev. Entomol. 2002, 47:233-266.
53. Lycett G.J., Kafatos F.C., Loukeris T.G. Conditional expression in the malaria mosquito Anopheles stephensi with Tet-On and Tet-Off systems. Genetics 2004, 167:1781-1790.
54. Maciel C., Oliveira V.X., Fázio M.A., Nacif-Pimenta R., Miranda A., Pimenta P.F.P., Capurro M.L. Anti-plasmodium activity of angiotensin II and related synthetic peptides. PLoS One 2008, 3:e3296.
55. Macoris M.L., Andrighetti M.T., Takaku L., Glasser C.M., Garbeloto V.C., Cirino V.B. Alteration in susceptibility response of Aedes aegypti to organophosphates in cities in the state of S. Paulo, Brazil. Rev. Saude Publica 1999, 33:521-522.
56. Marshall J.M. The effect of gene drive on containment of transgenic mosquitoes. J. Theor. Biol. 2009, 258:250-265.
57. Marshall J.M., Taylor C. Malaria control with transgenic mosquitoes. PLoS Med. 2009, 6:e1000020.
58. Martens W.J.M., Jetten T.H., Rotmans J. Climate change and diseases - a global modelling perspective. Glob. Environ. Change 1995, 5:195-209.
59. Mirzaian E., Durham M.J., Hess K., Goad J.A. Mosquito-borne illnesses in travelers: a review of risk and prevention. Pharmacotherapy 2010, 30:1031-1043.
60. Monath T.P. Dengue: the risk to developed and developing countries. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:2395-2400.
61. Morand S., Owers K.A., Waret-Szkuta A., McIntyre K.M., Baylis M. Climate variability and outbreaks of infectious diseases in Europe. Sci. Rep. 2013, 3:1774.
62. Muir W.M., Howard R.D. Possible ecological risks of transgenic organism release when transgenes affect mating success: sexual selection and the Trojan gene hypothesis. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:13853-13856.
63. Nirmala X., James A.A. Engineering Plasmodium-refractory phenotypes in mosquitoes. Trends Parasitol. 2003, 19:384-387.
64. Oki M., Yamamoto T. Climate change, population immunity, and hyperendemicity in the transmission threshold of dengue. PLoS One 2012, 7:e48258.
65. Olson K.E., Adelman Z.N., Travanty E.A., Sanchez-Vargas I., Beaty B.J., Blair C.D. Developing arbovirus resistance in mosquitoes. Insect Biochem. Mol. Biol. 2002, 32:1333-1343.
66. Palaniyandi M. The role of remote sensing and GIS for spatial prediction of vector-borne diseases transmission: a systematic review. J. Vector Borne Dis. 2012, 49:197-204.
67. Paris M., Tetreau G., Laurent F., Lelu M., Despres L., David J. Persistence of Bacillus thuringiensis israelensis (Bti) in the environment induces resistance to multiple Bti toxins in mosquitoes. Pest Manag. Sci. 2010, 67:122-128.
68. Paupy C., Brengues C., Ndiath O., Toty C., Herve J.P., Simard F. Morphological and genetic variability within Aedes aegypti in Niakhar, Senegal. Infect. Genet. Evol. 2010, 10:473-480.
69. Phuc H.K., Andreasen M.H., Burton R.S., Vass C., Epton M.J., Pape G., Fu G., Condon K.C., Scaife S., Donnelly C.A., Coleman P.G., White-Cooper H., Alphey L. Late-acting dominant lethal genetic systems and mosquito control. BMC Biol. 2007, 5:11.
70. Rajatileka S., Burhani J., Ranson H. Mosquito age and susceptibility to insecticides. Trans. R. Soc. Trop. Med. Hyg. 2011, 105:247-253.
71. Ribeiro J.M., Kidwell M.G. Transposable elements as population drive mechanisms: specification of critical parameter values. J. Med. Entomol. 1994, 31:10-16.
72. Rivero A., Vezilier J., Weill M., Read A.F., Gandon S. Insecticide control of vector-borne diseases: when is insecticide resistance a problem?. PLoS Pathog. 2010, 6:e1001000.
73. Robert M.A., Okamoto K., Lloyd A.L., Gould F. A reduce and replace strategy for suppressing vector-borne diseases: insights from a deterministic model. PLoS One 2013, 8(9):e73233. doi: 10.1371/journal.pone.0073233.
74. Sinkins S.P., Gould F. Gene drive systems for insect disease vectors. Nat. Rev. Genet. 2006, 7:427-435.
75. Smith C.N. Possible use of the sterile-male technique for control of Aedes aegypti. Bull. World Health Organ. 1967, 36:633-635.
76. Smith R., Walter M.F., Hice R.H., O'Brochta D.A., Atkinson P.W. Testis-specific expression of the beta2 tubulin promoter of Aedes aegypti and its application as a genetic sex-separation marker. Insect Mol. Biol. 2007, 16:61-71.
77. Sperança M.A., Capurro M.L. Perspectives in the control of infectious diseases by transgenic mosquitoes in the post-genomic era: a review. Mem. Inst. Oswaldo Cruz 2007, 102:425-433.
78. Staples J.E., Breiman R.F., Powers A.M. Chikungunya fever: an epidemiological review of a re-emerging infectious disease. Clin. Infect. Dis. 2009, 49:942-948.
79. Sutherst R.W. Global Change and Human Vulnerability to Vector-Borne Diseases. Clin. Microbiol. Rev. 2004, 17:136-173.
80. Takken W., Costantini C., Dolo G., Hassanali A., Sagnon N.F., Osir E. Mosquito mating behaviour. Bridging Laboratory and Field Research for Genetic Control of Disease Vectors. 2006, 183-188. Springer, Dordrecht. B.G.J. Knols, C. Louis (Eds.).
81. Tatem A.J., Huang Z., Das A., Qi Q., Roth J., Qiu Y. Air travel and vector-borne disease movement. Parasitology 2012, 139:1816-1830.
82. Tauil P.L. Critical aspects of dengue control in Brazil. Cad. Saude Publica 2002, 18:867-871.
83. Thomas D.D., Donnelly C.A., Wood R.J., Alphey L. Insect population control using a dominant, repressible, lethal genetic system. Science 2000, 287:2474-2476.
84. Toure Y.T., Manga L. Ethical legal and social issues in the use of genetically modified vectors for disease control. Bridging Laboratory and Field Research for Genetic Control of Disease Vectors. 2006, 221-225. Springer, Dordrecht. B.G.J. Knols, C. Louis (Eds.).
85. Travanty E.A., Adelman Z.N., Franz A.W.E., Keene K.M., Beaty B.J., Blair C.D., James A.A., Olson K.E. Using RNA interference to develop dengue virus resistance in genetically modified Aedes aegypti. Insect Biochem. Mol. Biol. 2004, 34:607-613.
86. 2009. Progress and prospects for the use of genetically modified mosquitoes to inhibit disease transmission. Geneva.
87. 2010. Health topics-Dengue [WWW Document]. URL http://www.who.int/topics/dengue/en/.
88. Yahara K., Fukuyo M., Sasaki A., Kobayashi I. Evolutionary maintenance of selfish homing endonuclease genes in the absence of horizontal transfer. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:18861-18866.
89. Yoshida S., Matsuoka H., Luo E., Iwai K., Arai M., Sinden R.E., Ishii A. A single-chain antibody fragment specific for the Plasmodium berghei ookinete protein Pbs21 confers transmission blockade in the mosquito midgut. Mol. Biochem. Parasitol. 1999, 104:195-204.