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Infection and Immunity, December 2009, p. 5496-5500, Vol. 77, No. 12
0019-9567/09/$08.00+0     doi:10.1128/IAI.00640-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Malaria Ookinete Surface Protein-Based Vaccination via the Intranasal Route Completely Blocks Parasite Transmission in both Passive and Active Vaccination Regimens in a Rodent Model of Malaria Infection {triangledown}

Takeshi Arakawa,1,2 Mayumi Tachibana,3 Takeshi Miyata,1 Tetsuya Harakuni,1 Hideyasu Kohama,1 Yasunobu Matsumoto,4 Naotoshi Tsuji,5 Hajime Hisaeda,6,{dagger} Anthony Stowers,6,{ddagger} Motomi Torii,3 and Takafumi Tsuboi7*

Molecular Microbiology Group, COMB, Tropical Biosphere Research Center, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa 903-0213, Japan,1 Division of Host Defense and Vaccinology, Graduate School of Medicine, University of the Ryukyus, 207 Uehara, Nishihara, Okinawa 903-0215, Japan,2 Department of Molecular Parasitology, Ehime University School of Medicine, Shigenobu-cho, Ehime 791-0295, Japan,3 Laboratory of Global Animal Resource Science, Department of Global Agricultural Sciences, Graduate School of Agricultural and Life Sciences, University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan,4 National Institute of Animal Health, National Agricultural Research Organization, 3-1-5 Kannondai, Tsukuba, Ibaraki 305-0856, Japan,5 Malaria Vaccine Development Unit, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland,6 Cell-Free Science and Technology Research Center, Ehime University, Matsuyama, Ehime 790-8577, Japan7

Received 5 June 2009/ Returned for modification 6 July 2009/ Accepted 6 September 2009

Malaria vaccines based on ookinete surface proteins (OSPs) of the malaria parasites block oocyst development in feeding mosquitoes and hence disrupt the parasite life cycle and prevent the disease from being transmitted to other individuals. To investigate whether a noninvasive mucosal vaccination regimen effectively blocks parasite transmission in vivo, Plasmodium yoelii Pys25, a homolog of the Pfs25 and Pvs25 OSPs of Plasmodium falciparum and Plasmodium vivax, respectively, was intranasally (i.n.) administered using a complement-deficient DBA/2 mouse malaria infection model, in which a highly elevated level of oocysts develops in feeding mosquitoes. Vaccinated mice developed a robust antibody response when the vaccine antigen was given together with cholera toxin adjuvant. The induced immune serum was passively transferred to DBA/2 mice 3 days after infection with P. yoelii 17XL, and Anopheles stephensi mosquitoes were allowed to feed on the infected mice before or after serum transfusion. This passive immunization completely blocked oocyst development; however, immune serum induced by the antigen or adjuvant alone did not have such a profound antiparasite effect. Further, when i.n. vaccinated mice were infected with the parasite and then mosquitoes were allowed to directly feed on the infected mice, complete blockage of transmission was again observed. To our knowledge, this is the first time that mucosal vaccination has been demonstrated to be efficacious for directly preventing parasite transmission from vaccinated animals to mosquitoes, and the results may provide important insight into rational design of nonparenteral vaccines for use against human malaria.

* Corresponding author. Mailing address: Cell-Free Science and Technology Research Center, Ehime University, 3 Bunkyo-cho, Matsuyama, Ehime 790-8577, Japan. Phone: 81-89-927-8277. Fax: 81-89-927-9941. E-mail: tsuboi{at}ccr.ehime-u.ac.jp

{triangledown} Published ahead of print on 14 September 2009.

Editor: W. A. Petri, Jr.

{dagger} Present address: Department of Immunology and Parasitology, Faculty of Medical Sciences, Kyushu University, Fukuoka, Fukuoka 812-8582, Japan.

{ddagger} Present address: CSL Limited A.C.N. 051 588 348, 45 Poplar Road, Parkville, Victoria 3052, Australia.

Infection and Immunity, December 2009, p. 5496-5500, Vol. 77, No. 12
0019-9567/09/$08.00+0     doi:10.1128/IAI.00640-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.





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