Transgenesis as a Tool to Reduce Parasite -Vector Interaction: a Review on the Progress for the Use of Genetically Manipulated Anopheles Mosquitoes to Control Malaria

Authors

  • Rania Ali El Hadi Mohamed
  • Wafa Abdullah Al-Megrin

Keywords:

Transgenic mosquitoes, vector competence, Anopheles, Plasmodium, symbiotic bacteria

Abstract

Malaria kills millions of people every year, imposing major economic and social burdens. Despite many efforts the classical control interventions which focus mainly on vector management and treatment of affected individuals with drugs. These interventions have proven inadequate to stop the transmission of Plasmodium parasites, subsequently the spread of malaria by Anopheles mosquitoes. The progressive numbers of insecticide-resistant insects and drug-resistant parasites have led to the search for a novel arsenal of strategies for inhibiting Plasmodium infection of mosquitoes. This work reviews current knowledge on genetic manipulation in mosquitoes that holds promise for development of transgenic mosquito refractory to malaria parasites transmission.

References

Marcia and Margareth. Perspectives in the control of infectious diseases by transgenic mosquitoes in the post-genomic era

Hay SI, Guerra CA, Gething PW, Patil AP, Tatem AJ, Noor AM, Kabaria CW, Manh BH, Elyazar IR, Brooker. A world malaria map: Plasmodium falciparum endemicity in 2007. PLoS Me 2007; 6e1000048.

Sachs JD. A new global effort to control malaria. Sciences 2002; 298:122

World Health Organization. First meeting report on planning: Technical consultation on current status and planning for future development of genetically modified mosquitoes for malaria and dengue control 2009; DOI 10.2471/TDR.10.978-924-1599238: 4-64.

Bin Dajem SM, Al-Farsi HM, Al-Hashami ZS, Al-Sheikh AAH, Al-Qahtani A, and Babiker HA. Distribution of Drug Resistance Genotypes in Plasmodium falciparum in an Area of Limited Parasite Diversity in Saudi Arabia. The American Society of Tropical Medicine and Hygiene 2012; 86:782

Ghosh AK and Lorena MJ. Plasmodium sporozoite invasion of the mosquito salivary gland. Curr Opin Microbiol 2009; 12:394

Catteruccia F, Holan T, Loukeris TG. Stable germline transformation of the malaria mosquito Anopheles stephensi. Nature 2012; 405: 959

Perera OP, Harrell RA, and Handler AM. Germline transformation of the South American malaria vector, Anopheles albimanus, with a piggyBac/EGFP transposon vector is routine and highly efficient. Insect Molecular Biology 2002; 11: 291

Cirimotich CM, April Clayton AM, and Dimopoulos G. Low- and High-Tech Approaches to Control Plasmodium Parasite Transmission by Anopheles Mosquitoes. Journal of Tropical Medicine 2011; doi:10.1155/2011/891342.

Carter, R. Transmission blocking malaria vaccines. Vaccine 2001; 19: 2309- 2314.

Duffy, P. E. and Kaslow, D. C. A novel malaria protein, Pfs28, and Pfs25 are genetically linked and synergistic as falciparum malaria transmission-blocking vaccines. Infect. Immun 1997; 65: 1109-1113.

Healer, J., McGuinness, D., Carter, R. and Riley, E. Transmission blocking immunity to Plasmodium falciparum in malaria-immune individuals is associated with antibodies to the gamete surface protein Pfs230. Parasitol 1999; 119: 425-433.

Ramasamy, M. S. and Ramasamy, R. Effect of anti-mosquito antibodies on the infectivity of the rodent malaria parasite Plasmodium berghei to Anopheles farauti. Med. Vet. Entomol 1990; 4, 161-166.

Jacobs-Lorena, M. and Lemos, F. J. Immunological strategies for control of insect disease vectors: a critical assessment. Parasitol Today 1995; 11: 144-147.

Riehle MA, Srinivasan P, Moreira CK and Lorena MJ. Towards genetic manipulation of wild mosquito populations to combat malaria: advances and challenges. The Journal of Experimental Biology 2003; 206: 3809-3816. doi:10.1242/jeb.00609.

Beerntsen, B., James, A. A. and Christensen, B. Genetics of mosquito vector competence. Microbiol. Mol. Biol. Rev 2000; 64: 115-137.

Golenda, C. F., Starkweather, W. H. and Wirtz, R. A. The distribution of circumsporozoite protein (CS) in Anopheles stephensi mosquitoes infected with Plasmodium falciparum malaria. J. Histochem. Cytochem 1990; 38: 475-481.

Rosenberg, R. Inability of Plasmodium knowlesi sporozoites to invade Anopheles freeborni salivary glands. Am. J. Trop. Med. Hyg 1985; 34: 687-691.

Nussenzweig, V. and Nussenzweig, R. S. Circumsporozoite proteins of malaria parasites. Bull. Mem. Acad. R. Med. Belg 1998; 144: 493-504.

Warburg, A., Touray, M., Krettli, AU., Miller, LH. Plasmodium gallinaceum: antibodies to circumsporozoite protein prevent sporozoites from invading the salivary glands of Aedes aegypti. Exp. Parasitol 1992; 75, 303-307.

Ito J, Ghosh A, Moreira LA, Wimmer EA, and Jacobs-Lorena M. Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite. Nature 2002; 417: 6887: 452

Abraham EG, Donnelly-Doman M, Fujioka H, Ghosh A, Moreira L, and Jacobs-Lorena M. Driving midgut-specific expression and secretion of a foreign protein in transgenic mosquitoes with AgPer1 regulatory elements. Insect Molecular Biology 2005; 14:3: 271

Nolan T, Petris E, Muller HM, Cronin A, Catteruccia F, and Crisanti A. Analysis of two novel midgut-specific promoters driving transgene expression in Anopheles stephensi mosquitoes. PLoS One 2011; 2. DOI e16471.

Chen XG, Marinotti O, Whitman L, Jasinskiene N, and James AA. The Anopheles gambiae vitellogenin gene (VGT2) promoter directs persistent accumulation of a reported gene product in transgenic Anopheles stephensi following multiple blood meals. American Journal of Tropical Medicine and Hygiene 2007; 76: 6: 1118

Lombardo F, Lycett GJ, Lanfrancotti A, Coluzzi M, and Arc B. Analysis of apyrase 5_ upstream region validates improved Anopheles gambiae transformation technique,

Yoshida S and Watanabe H. Robust salivary gland-specific transgene expression in Anopheles stephensi mosquito. Insect Molecular Biology 2006; 15: 4: 403

Lycett GJ, Kafatos FC, and Loukeris TG. Conditional expression in the malaria mosquito Anopheles stephensi with Tet-on and Tet-off systems. Genetics 2004; 167:1781

Yoshida S, Shimada Y, Kondoh D. Hemolytic C-type lectin CEL-III from sea cucumber expressed in transgenic mosquitoes impairs malaria parasite development. PLoS Pathogens 2007; 3: 192- 197.

Meredith JM, S. Basu and Nimmo DD. Site-specific integration and expression of an anti-malarial gene in transgenic Anopheles gambiae significantly reduces Plasmodium infections. PLoS One 2011; 6: 1: DOI e14587.

Corby-Harris V, Drexler A, de Jong LW. Activation of Akt signaling reduces the prevalence and intensity of malaria parasite infection and lifespan in Anopheles stephensi mosquitoes. PLoS Pathogens 2010; 6: 7: DOI e1001003.

Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 2005; 2: 214

Breman JG, Egan A, Keusch GT. The intolerable burden of malaria: a new look at the numbers. Am J Trop Med Hyg 2001; 64: 1

Hemingway J, Field L, Vontas J. An overview of insecticide resistance. Science 2002; 298: 96

Christian Epp, Raskolnikov D and Deitsch KW. A regulatable transgene expression system for cultured Plasmodium falciparum parasites. Malaria journal 2008; 7:8: doi: 10.1186/1475-2875-7-86.

Hill J, Lines J, Rowland M. Insecticide-treated nets. Adv Parasitol 2006; 61: 77

Maharaj R, Mthembu DJ, Sharp BL. Impact of DDT reintroduction on malaria transmission in KwaZulu-Natal. S Afr Med J 2005; 95: 871

Killeen GF, Seyoum A, Knols BGJ. Rationalizing historical successes of malaria control in Africa in terms of mosquito resource availability management. Am J Trop Med Hyg 2004; 71: 87

Gu W, Novak RJ. Habitat-based modeling of impacts of mosquito larval interventions on entomological inoculation rates, incidence, and prevalence of malaria. Am J Trop Med Hyg 2005; 73: 546

Sinkins SP and Gould F. Gene drive systems for insect disease vectors. Nature Reviews Genetics 2006; 7: 427

Fuchs S, Nolan T, Crisanti A. Mosquito transgenic technologies to reduce Plasmodium transmission. Methods in Molecular Biology 2013; 923: 601-622

O

Windbichler N, Papathanos PA, Catteruccia F, Ranson H, Burt A, and Crisanti. Homing endonuclease mediated gene targeting in Anopheles gambiae cells and embryos. Nucleic Acids Research 2007; 35: 5922

Windbichler N, Menichelli M, Papathanos PA. A synthetic homing endonuclease-based gene drive system in the human malaria mosquito. Nature 2011; 473: 212- 219.

Chen CH, Huang H, Ward CM. A synthetic maternal-effect selfish genetic element drives population replacement in Drosophila. Science 2007; 316: 597

Papathanos PA, Windbichler N, Menichelli M, Burt A, and Crisanti A. The vasa regulatory region mediates germline expression and maternal transmission of proteins in the malaria mosquito Anopheles gambiae: a versatile tool for genetic control strategies. BMC Molecular Biology 2009; 10: 29-36.

Chen XG, Mathur G, and James AA. Chapter 2 Gene expression studies in mosquitoes, Advances in Geneticsm2008; 64: 19

Nolan T. piggyBac- mediated germline transformation of the malaria mosquito Anopheles stephensi using the red fluorescent protein dsRED as a selectable marker. J Biol Chem 2002; 277:8759

Perera OP. Germ-line transformation of the South American malaria vector, Anopheles albimanus, with a piggyBac /EGFP transposon vector is routine and highly efficient. Insect Mol Biol 2002; 11:291

Meredith JM. Site-specific integration and expression of an anti-malarial gene in transgenic Anopheles gambiae significantly reduces Plasmodium infections. PLOS One 2011; 6: DOI e14587.

Windbichler N. Targeting the X chromosome during spermatogenesis induces Y chromosome transmission ratio distortion and early dominant embryo lethality in Anopheles gambiae. PLoS Genet 2008; 4: DOI e1000291.

Lobo NF. High efficiency germline transformation of mosquitoes. Nat Protoc 2006; 1:1312

Chater KF. Dispensable sequences and packaging constraints of DNA from the Streptomyces temperate phage phi C31. Gene 1981; 15:249

Li C, Marrelli MT, Yan G, and Jacobs-Lorena M. Fitness of transgenic Anopheles stephensi mosquitoes expressing the SM1 peptide under the control of a vitellogenin promoter. Journal of Heredity 2008; 99: 275

Moreira LA, Wang J, Collins FH, and Jacobs-Lorena M. Fitness of anopheling mosquitoes expressing transgenes that inhibit Plasmodium development. Genetics 2004; 166: 1337

C. M. Cirimotich CM, Dong Y, Clayton AM. Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae. Science 2011; 332: 6031:855.

Dong Y, Manfredini F, and Dimopoulos G. Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathogens 2009; 5: 5 DOI: e1000423.

Gonzales-Ceron L, Santillan F, Rodriguez MH, Mendez D, and Hernandez-Avila JE. Bacteria in midguts of field collected Anopheles albimanus block Plasmodium vivax sporogonic development. Journal of Medical Entomology 2003; 40: 371

Pumpuni CB, Beier MS, Nataro JP, Guers LD, and Davis JR. Plasmodium falciparum: inhibition of sporogonic development in Anopheles stephensi by gram-negative bacteria. Experimental Parasitology 1993; 77:195

Straif SC, Mbogo CN, Toure AM. Midgut bacteria in Anopheles gambiae and An. Funestus (Diptera: Culicidae) from Kenya and Mali. Journal of Medical Entomology 1998; 35: 222

Tour

Ho. M.W. Genetic engineering: dream or nightmare? Gateway Books, London 1998.

TDR. Scientific Working Group on Insect Disease Vectors and Human Health, Geneva, WHO/HQ, 12

Macer D. Ethical, legal and social issues of genetically modified disease vectors in public health. UNDP/World Bank/ WHO Special program for Research and Training in Tropical Diseases (TDR), Geneva 2003.

Macer D. Ethical, legal and social issues of genetically modifying insect vectors for public health. Insect Biochemistry and Molecular Biology 2005; 35: 649

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Published

2015-08-02

How to Cite

El Hadi Mohamed, R. A., & Al-Megrin, W. A. (2015). Transgenesis as a Tool to Reduce Parasite -Vector Interaction: a Review on the Progress for the Use of Genetically Manipulated Anopheles Mosquitoes to Control Malaria. International Journal of Sciences: Basic and Applied Research (IJSBAR), 24(1), 83–94. Retrieved from https://gssrr.org/index.php/JournalOfBasicAndApplied/article/view/4256

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