Reduction of malaria transmission by transgenic mosquitoes expressing an antisporozoite antibody in their salivary glands

Insect Molecular Biology

Volumn 22, Issue 1, 2013, Pages 41-51

  Sumitani, M ^a   Kasashima, K ^b   Yamamoto, D S ^b   Yagi, K ^b   Yuda, M ^c   Matsuoka, H ^b   Yoshida, S ^d  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b JICHI MEDICAL UNIVERSITY   (Japan)

^c MIE UNIVERSITY   (Japan)

^d KANAZAWA UNIVERSITY   (Japan)

Author keywords

circumsporozoite protein; malaria; salivary glands; single chain antibody fragment; transgenic mosquito

Indexed keywords

CIRCUMSPOROZOITE PROTEIN, PROTOZOAN; PROTOZOAL PROTEIN; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY;

ANIMAL; ANOPHELES; ARTICLE; CELL LINE; DISEASE MODEL; DISEASE TRANSMISSION; DRUG EFFECT; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; INSTITUTE FOR CANCER RESEARCH MOUSE; MALARIA; METABOLISM; MOLECULAR GENETICS; MOUSE; NUCLEOTIDE SEQUENCE; PARASITOLOGY; PHYSIOLOGY; PLASMODIUM FALCIPARUM; SALIVARY GLAND; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANOPHELES; CELL LINE; DISEASE MODELS, ANIMAL; MALARIA; MICE; MICE, INBRED ICR; MOLECULAR SEQUENCE DATA; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; SALIVARY GLANDS; SINGLE-CHAIN ANTIBODIES;

ANOPHELES STEPHENSI; MUS; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; RODENTIA;

EID: 84872618698     PISSN: 09621075     EISSN: 13652583     Source Type: Journal    
DOI: 10.1111/j.1365-2583.2012.01168.x     Document Type: Article

References (38)

1. Burkot, T.R., Da, Z.W., Geysen, H.M., Wirtz, R.A., and, Saul, A., (1991) Fine specificities of monoclonal antibodies against the Plasmodium falciparum circumsporozoite protein: recognition of both repetitive and non-repetitive regions. Parasite Immunol 13: 161-170.
2. Catteruccia, F., (2007) Malaria vector control in the third millennium: progress and perspectives of molecular approaches. Pest Manag Sci 63: 634-640.
3. Catteruccia, F., Nolan, T., Loukeris, T.G., Blass, C., Savakis, C., Kafatos, F.C., et al. (2000) Stable germline transformation of the malaria mosquito Anopheles stephensi. Nature 405: 959-962.
4. Chen, X.G., Mathur, G., and, James, A.A., (2008) Gene expression studies in mosquitoes. Adv Genet 64: 19-50.
5. Coppi, A., Pinzon-Ortiz, C., Hutter, C., and, Sinnis, P., (2005) The Plasmodium circumsporozoite protein is proteolytically processed during cell invasion. J Exp Med 201: 27-33.
6. Dessens, J.T., Mendoza, J., Claudianos, C., Vinetz, J.M., Khater, E., Hassard, S., et al. (2001) Knockout of the rodent malaria parasite chitinase pbCHT1 reduces infectivity to mosquitoes. Infect Immun 69: 4041-4047.
7. Dong, Y., Das, S., Cirimotich, C., Souza-Neto, J.A., McLean, K.J., and, Dimopoulos, G., (2011) Engineered Anopheles immunity to Plasmodium infection. PLoS Pathog 7: e1002458.
8. Frischknecht, F., Baldacci, P., Martin, B., Zimmer, C., Thiberge, S., Olivo-Marin, J.C., et al. (2004) Imaging movement of malaria parasites during transmission by Anopheles mosquitoes. Cell Microbiol 6: 687-694.
9. Hollingdale, M.R., Nardin, E.H., Tharavanij, S., Schwartz, A.L., and, Nussenzweig, R.S., (1984) Inhibition of entry of Plasmodium falciparum and P. vivax sporozoites into cultured cells; an in vitro assay of protective antibodies. J Immunol 132: 909-913.
10. Horn, C., and, Wimmer, E.A., (2000) A versatile vector set for animal transgenesis. Dev Genes Evol 210: 630-637.
11. Isaacs, A.T., Li, F., Jasinskiene, N., Chen, X., Nirmala, X., Marinotti, O., et al. (2011) Engineered resistance to Plasmodium falciparum development in transgenic Anopheles stephensi. PLoS Pathog 7: e1002017.
12. Isaacs, A.T., Jasinskiene, N., Tretiakov, M., Thiery, I., Aettor, A., Bourgouin, C., et al. (2012) Transgenic Anopheles stephensi coexpressing single-chain antibodies resist Plasmodium falciparum development. Proc Natl Acad Sci U S A 109: 11070-11071.
13. Ito, J., Ghosh, A., Moreira, L.A., Wimmer, E.A., and, Jacobs-Lorena, M., (2002) Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite. Nature 417: 452-455.
14. Jacobs-Lorena, M., (2003) Interrupting malaria transmission by genetic manipulation of anopheline mosquitoes. J Vect Borne Dis 40: 73-77.
15. Jasinskiene, N., Coleman, J., Ashikyan, A., Salampessy, M., Marinotti, O., and, James, A.A., (2007) Genetic control of malaria parasite transmission: threshold levels for infection in an avian model system. Am J Trop Med Hyg 76: 1072-1078.
16. Kokoza, V., Ahmed, A., Cho, W.L., Jasinskiene, N., James, A.A., and, Raikhel, A., (2000) Engineering blood meal-activated systemic immunity in the yellow fever mosquito, Aedes aegypti. Proc Natl Acad Sci U S A 97: 9144-9149.
17. Kokoza, V., Ahmed, A., Woon Shin, S., Okafor, N., Zou, Z., and, Raikhel, A.S., (2010) 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 107: 8111-8116.
18. Matsuoka, H., Ikezawa, T., and, Hirai, M., (2010) Production of a transgenic mosquito expressing circumsporozoite protein, a malarial protein, in the salivary gland of Anopheles stephensi (Diptera: Culicidae). Acta Med Okayama 64: 233-241.
19. Ménard, R., (2000) The journey of the malaria sporozoite through its hosts: two parasite proteins lead the way. Microbes Infect 2: 633-642.
20. Moreira, L.A., Edwards, M.J., Adhami, F., Jasinskiene, N., James, A.A., and, Jacobs-Lorena, M., (2000) Robust gut-specific gene expression in transgenic Aedes aegypti mosquitoes. Proc Natl Acad Sci U S A 97: 10895-10898.
21. Moreira, L.A., Ito, J., Ghosh, A., Devenport, M., Zieler, H., Abraham, E.G., et al. (2002) Bee venom phospholipase inhibits malaria parasite development in transgenic mosquitoes. J Biol Chem 277: 40839-40843.
22. Nolan, T., Papathanos, P., Windbichler, N., Magnusson, K., Benton, J., Catteruccia, F., et al. (2011) Development transgenic Anopheles mosquitoes for the sterile insect technique. Genetica 139: 33-39.
23. Persson, C., Oliveira, G.A., Sultan, A.A., Bhanot, P., Nussenzweig, V., and, Nardin, E., (2002) Cutting edge: a new tool to evaluate human pre-erythrocytic malaria vaccines: rodent parasites bearing a hybrid Plasmodium falciparum circumsporozoite protein. J Immunol 169: 6681-6685.
24. Ramirez, J.L., Garver, L.S., and, Dimopoulos, G., (2009) Challenges and approaches for mosquito targeted malaria control. Curr Mol Med 9: 116-130.
25. Sambrook, J., Fritsch, E.F., and, Maniatis, T., (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
26. Sinden, R.E., (1997) Infection of mosquitoes with rodent malaria. In Moleculer Biology of Insect Disease Vectors: A Methods Manual (, Crampton, J.M., Beard, C.B., and, Louis, C., eds), pp. 67-91. Chapman and Hall, London.
27. Sinnis, P., and, Coppi, A., (2007) A long and winding road: the Plasmodium sporozoite's journey in the mammalian host. Parasitol Int 56: 171-178.
28. Sinnis, P., and, Nardin, E., (2002) Sporozoite antigens: biology and immunology of the circumsporozoite protein and thrombospondin-related anonymous protein. Chem Immunol 80: 70-96.
29. Terenius, O., Marinotti, O., Sieglaff, D., and, James, A.A., (2008) Molecular genetic manipulation of vector mosquitoes. Cell Host Microbe 4: 417-423.
30. Tewari, R., Spaccapelo, R., Bistoni, F., Holder, A., and, Crisanti, A., (2002) Function of region I and II adhesive motifs of Plasmodium falciparum circumsporozoite protein in sporozoite motility and infectivity. J Biol Chem 277: 47613-47618.
31. Waters, A.P., Thomas, A.W., van, Dijk, M.R., and, Janse, C.J., (1997) Transfection of malaria parasites. Methods 13: 134-147.
32. Yamamoto, D.S., Nagumo, H., and, Yoshida, S., (2010) Flying vaccinator; a transgenic mosquito delivers a Leishmania vaccine via blood feeding. Insect Mol Biol 19: 391-398.
33. Yamamoto, D.S., Sumitani, M., Nagumo, H., Yoshida, S., and, Matsuoka, H., (2012) Induction of antisporozoite antibodies by biting of transgenic Anopheles stephensi delivering malarial antigen via blood feeding. Insect Mol Biol 21: 223-233.
34. Yoshida, S., and, Watanabe, H., (2006) Robust salivary gland-specific transgene expression in Anopheles stephensi mosquito. Insect Mol Biol 15: 403-410.
35. Yoshida, S., Matsuoka, H., Luo, E., Iwai, K., Arai, M., Sinden, R.E., et al. (1999) A single-chain antibody fragment specific for the Plasmodium berghei ookinete protein Pbs21 confers transmission blockade in the mosquito midgut. Mol Biochem Parasitol 104: 195-204.
36. Yoshida, S., Kobayashi, T., Matsuoka, H., Seki, C., Gosnell, W.L., Chang, S.P., et al. (2003) T-cell activation and cytokine production via a bispecific single-chain antibody fragment targeted to blood-stage malaria parasites. Blood 101: 2300-2306.
37. Yoshida, S., Shimada, Y., Kondoh, D., Kouzuma, Y., Ghosh, A.K., Jacobs-Lorena, M., et al. (2007) Hemolytic C-type lectin CEL-III from sea cucumber expressed in transgenic mosquitoes impairs malaria parasite development. PLoS Pathog 3: e192.
38. Yoshida, S., Sudo, T., Niimi, M., Tao, L., Sun, B., Kambayashi, J., et al. (2008) Inhibition of collagen-induced platelet aggregation by anopheline antiplatelet protein, a saliva protein from a malaria vector mosquito. Blood 111: 2007-2014.