Bioengineering of malaria vectors, anopheles mosquitoes (Diptera: Culicidae) as a control strategy: An overview

Kayode David Ileke and Isaac Omotayo Olabimi

Abstract
Disease in any form is undesirable in any human population. Malaria is a communicable disease that is vectored by female Anopheles mosquitoes. It is the leading vector transmitted disease in terms of the number of morbidity and mortality accounting for over 200 million cases annually. Several control measures have been employed by man over the years to control the vector which will in turn lead to the control of the diseases with the popular ones involving the use of insecticidal nets and indoor residual spraying of insecticides. However, these control measures have their various pitfalls. The use of genetically modified mosquitoes (GMMs) through bioengineering may be a promising method of reducing malaria vector population in our environment. This process involves population replacement technique (PRT) and population suppression techniques (PST). With proper integration of GMMs into the already existing control measures employed in the management of mosquitoes, a remarkable decrease in the prevalence of malaria is envisaged.

Keywords
Bioengineering; Genetically modified mosquitoes (GMMs); Population replacement technique (PRT); Population suppression techniques (PST).

DOI
10.21472/bjbs.061204

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References
Alphey, L. Re-engineering the sterile insect technique. Insect Biochemistry and Molecular Biology, v. 32, p. 1243-1247, 2002.

Alphey, L.; Andrew, M.; Derric N.; Marco, N. O.; Renaud, L.; Kelly, M.; Camilla, B. Genetic control of Aedes mosquitoes. Pathogen and Global Health, v. 107, no. 4, p. 170-179, 2013.

Atkinson, P. W.; Michel, K. What's buzzing? Mosquito genomics and transgenic mosquitoes. Genesis, v. 32, p. 42-48, 2002.

Barclay, H. J. Mathematical models for the use of sterile insects. Dyck, V. A.; Hendrichs, J.; Robinson, A. S. (Eds.). Sterile insect technique: Principles and practice in area-wide integrated pest management. New York: Springer, 2005. p. 147-174.

Barnes, J. M. Toxic hazards of pesticides. Bulletin World Health Organization, v. 8, p. 419-490, 1953.

Beard, C. B.; Mason, P. W.; Aksoy, S.; Tesh, R. B.; Richards, F. F. Transformation of an insect symbiont and expression of a foreign gene in the Chagas disease vector Rhodnius prolixus. American Journal of Tropical Medicine Hygiene, v. 46, p. 195-200, 1992.

Beard, C. B.; O'Neill, S. L.; Tesh, R. B.; Richards, F. F.; Aksoy, S. Modification of arthropod vector competence via symbiotic bacteria. Parasitology Today, v. 9, p. 179-183, 1993.

Bibikova, M.; Carroll, D.; Segal, D. J.; Trautman, J. K.; Smith, J.; Kim, Y. G.; Chandrasegaran, S. Stimulation of homologous recombination through targeted cleavage by chimeric nucleases. Molecular and Cell Biology, v. 21, p. 289-297, 2001.

Brelsfoard, C. L.; Sechan, Y.; Dobson, S. L. Interspecific hybridization yields strategy for South Pacific filariasis vector elimination. Public Library of Science Neglected Tropical Diseases, v. 2, e. 129, 2008.

Catteruccia, F. Malaria vector control in the third millennium: Progress and perspectives of molecular approaches. Pest Management Science, v. 63, p. 634-640, 2007.

Chalfie, M.; Tu, Y.; Euskirchen, G.; Ward, W. W.; Prasher, D. C. Green fluorescent protein as a marker for gene expression. Science, v. 263, p. 802-805, 1994.

Chevalier, B. S.; Stoddard, B. L. Homing endonucleases: Structural and functional insight into the catalysts of intron/intein mobility. Nucleic Acid Research, v. 29, p. 3757-3774, 2001.

Coates, C. J.; Jasinskiene, N.; Miyashiro, L.; James, A. A. Mariner transposition and transformation of the yellow fever mosquito, Aedes aegypti. Proceedings of the National Academy of Sciences USA, v. 95, p. 3748-3751, 1998.

Franz, A. W.; 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. Proceedings of the National Academy of Sciences USA, v. 103, p. 4198-4203, 2006.

Fu, G.; Lees, R. S.; Nimmo, D.; Aw, D.; Jin, L.; Gray, P. Female-specific flightless phenotype for mosquito control. Proceedings of the National Academy of Sciences USA, v. 107, p. 4550-4554, 2010.

Gabrieli, P.; Smidler, A.; Catteruccia, F. Engineering the control of mosquito-borne infectious diseases. Genome Biology, v. 15, p. 535, 2014.

Gaio, A. O.; Gusmão, D. S.; Santos, A. V.; Berbert-Molina, M. A.; Pimenta P. F.; Lemos F. J. Contribution of midgut bacteria to blood digestion and egg production in Aedes aegypti (Diptera: culicidae). Parasites and Vectors, v. 14, p. 94-105, 2011.

Grissa, I.; Vergnaud, G.; Pourcel, C. The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinformatics, v. 8, p. 1-10, 2007.

Grossman, G. L.; Rafferty, C. S.; Clayton, J. R.; Stevens, T. K.; Mukabayire, O.; Benedict M. Q Germline transformation of the malaria vector, Anopheles gambiae, with the piggy Bac transposable element. Insect Molecular Biology, v. 10, p. 597-604, 2001.

Hahn, M. W.; Nuzhdin, S. V. The fixation of malaria refractoriness in mosquitoes. Current Biology, v. 14, p. 264-265, 2004.

Heinrich, J. L.; Scott, M. J. A repressible female-specific lethal genetic system for making transgenic insect strains suitable for a sterile-release program. Proceedings of the National Academy of Sciences USA, v. 97, p. 8229-8232, 2000.

Hendrichs, J.; Robinson, A. S.; Cayol, J. P.; Enkerlin, W. Medfly areawide sterile insect technique programmes for prevention, suppression or eradication: The importance of mating behavior studies. Florida Entomology, v. 85, p. 1-13, 2002.

Ito, J.; Ghosh, A.; Moreira, L. A.; Wimmer, E. A.; Jacobs-Lorena, M. Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite. Nature, v. 417, p. 452-455, 2002.

Jinek, M.; Chylinski, K.; Fonfara, I.; Hauer, M.; Doudna, J. A.; Charpentier, E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, v. 337, p. 816-821, 2012.

John, W.; Kathy, L.; Scot, L.; Sherryl, T.; Marcia, J. G. A Monthly Bulletin on Epidemiology and Public Health Practice in Washington. epiTrends, v. 20, p. 3, 2015.

Kim, W.; Koo, H.; Richman, A. M.; Seeley, D.; Vizioli, J.; Klocko, A. D.; O’Brochta, D. A. Ectopic expression of a cecropin transgene in the human malaria vector mosquito Anopheles gambiae (Diptera: Culicidae): Effects on susceptibility to Plasmodium. Journal of Medical Entomology, v. 41, p. 447-455, 2004.

Kim, Y. G.; Cha, J; Chandrasegaran, S. Hybrid restriction enzymes: Zinc finger fusions to Fok I cleavage domain. Proceedings of the National Academy of Sciences USA, v. 93, p. 1156-1160, 1996.

Knipling, E. F. Possibilities of insect control or eradication through the use of sexually sterile males. Journal of Economic Entomology, v. 48, p. 902-904, 1995.

Knols, B. G. J.; Bossin, H. C.; Mukabana, W. R.; Robinson, A. S. Transgenic mosquitoes and the fight against malaria: Managing technology push in a turbulent GMO world. America Journal of Tropical Medicine and Hygiene, v. 77, no. 6, p. 232-242, 2007.

Kokoza, V.; Ahmed, A.; Wimmer, E. A.; Raikhel, A. S. Efficient transformation of the yellow fever mosquito Aedes aegypti using the piggyBac transposable element vector pBac[3xP3-EGFP afm]. Insect Biochemical and Molecular Biology, v. 31, p. 1137-1143, 2001.

Macer, D. R. J. Ethical, legal and social issues of genetically modified disease vectors in public health. Geneva: UNDP/World Bank/WHO, 2003.

Marrelli, M. T.; Moreira, C. K.; Kelly, D.; Alphey, L.; Jacobs-Lorena, M. Mosquito transgenesis: What is the fitness cost? Trends in Parasitology, v. 22, p. 197-202, 2006.

Moreira, L. A; Edwards, M. J.; Adhami, F.; Jasinskiene, N.; James, A. A.; Jacobs-Lorena, M. Robust gut-specific gene expression in transgenic Aedes aegypti mosquitoes. Proceedings of the National Academy of Sciences USA, v. 97, p. 10895-10898, 2000.

Mussolino, C.; Cathomen, T. TALE nucleases: Tailored genome engineering made easy. Current Opinion in Biotechnology, v. 23, p. 644-650, 2012.

Najera, J. A.; Gonzalez-Silva, M; Alonso, P. L. Some lessons for the future from the global malaria eradication programme (1955-1969). Public Library of Science Medicine, v. 8, no. 1, e. 1000412, 2011.

Oxitec. Oxitec's Genetically Modified Mosquitoes: Ready to roll out?. Gene watch UK. 2017.

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 Bioinformatics, v. 5, p. 11, 2007.

Reegan, D. A.; Ceasar, A. S.; Paulraj, G. M.; Ignacimuthu, S.; Al-Dhabi N. A. Current status of genome editing in vector mosquitoes: A review. Bioscience Trends, p. 1-9, 2016.

Reiter, P. Oviposition, dispersal and survival in Aedes aegypti: Implications for the efficacy of control strategies. Vector-Borne Zoonotic Diseases, v. 7, p. 261-73, 2007.

Reyon, D.; Tsai, S. Q.; Khayter, C.; Foden, J. A.; Sander J. D.; Joung J. K. FLASH assembly of TALENs for high-throughput genome editing. Nature Biotechnology, v. 30, p. 460-465, 2012.

Riehle, M. A.; Jacobs-Lorena, M. Using bacteria to express and display anti-parasite molecules in mosquitoes: Current and future strategies. Insect Biochemistry and Molecular Biology, v. 35, p. 699-707, 2005.

Riehle, M. A.; Moreira, C. K.; Lampe, D.; Lauzon, C.; Jacobs-Lorena, M. Using bacteria to express and display anti-Plasmodium molecules in the mosquito midgut. International Journal of Parasitology, v. 37, p. 595-603, 2007.

Sakuma, T.; Woltjen, K. Nuclease-mediated genome editing: At the front-line of functional genomics technology. Development Growth and Differentiation, v. 56, p. 2-13, 2014.

Thomas, D. D.; Donnelly, C. A.; Wood, R. J.; Alphey, L. S. Insect population control using a dominant, repressible, lethal genetic system. Science, v. 287, p. 2474-2476, 2000.

Volna, P.; Jarjour, J.; Baxter, S.; Roffler, S. R.; Monnat, J., Jr.; Stoddard, B. L. Flow cytometric analysis of DNA binding and cleavage by cell surface-displayed homing endonucleases. Nucleic Acid Research, v. 35, p. 2748-2758, 2007.

WHO - World Health Organization. A framework for malaria elimination. Geneva, Switzerland: WHO, 2017.

WHO - World Health Organization. Achieving the malaria millennium development goal target: Reversing the Incidence of Malaria 2000-2015. Geneva, Switzerland: WHO, 2015.

WHO - World Health Organization. Malaria elimination: A field manual for low and moderate endemic countries. Geneva, Switzerland: WHO, 2007.

WHO - World Health Organization. Progress and prospects for the use of genetically modified mosquitoes to inhibit disease transmission. Geneva, Switzerland: WHO, 2009.

WHO - World Health Organization. Vector control. Geneva, Switzerland: WHO, 2001.

Wilke, A. B.; Gomes, A. C.; Natal, D.; Marrelli, M. T. Control of vector populations using genetically modified mosquitoes. Revista de Saúde Pública, v. 43, p.869-874, 2009.

Wolfe, S. A.; Nekludova, L.; Pabo, C. O. DNA recognition by Cys2His2 zinc finger proteins. Annual Review of Biophysics and Biomolecular Structure, v. 29, p. 183-212, 2001.

Wyss, J. H. Screwworm eradication in the Americas. Annals of the New York Academy of Science, v. 916, p. 186-193, 2000.

Yoshida, S.; Ioka, D.; Matsuoka, H.; Endo, H.; Ishii, A. Bacteria expressing singlechain immunotoxin inhibit malaria parasite development in mosquitoes. Molecular and Biochemical Parasitology, v. 113, p. 89-96, 2001.