Plasmodium yoelii sporozoites with simultaneous deletion of P52 and P36 are completely attenuated and confer sterile immunity against infection

Infection and Immunity

Volumn 75, Issue 8, 2007, Pages 3758-3768

  Labaied, Mehdi ^a   Harupa, Anke ^a   Dumpit, Ronald F ^a   Coppens, Isabelle ^b   Mikolajczak, Sebastian A ^a   Kappe, Stefan H I ^a,c  

^a SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIVE VACCINE; MALARIA VACCINE; PROTOZOAL PROTEIN; PROTOZOAL PROTEIN P36; PROTOZOAL PROTEIN P52; UNCLASSIFIED DRUG;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MOTILITY; CELL VACUOLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; FEMALE; GENE DELETION; GENETIC MANIPULATION; HUMAN; HUMAN CELL; IMMUNITY; IMMUNIZATION; IMMUNOFLUORESCENCE; MALARIA; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE DEVELOPMENT; PARASITE TRANSMISSION; PARASITE VIRULENCE; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; PLASMODIUM YOELII; PRIORITY JOURNAL; PROTEIN FUNCTION; SALIVARY GLAND; SPOROZOITE;

ANIMALS; CULICIDAE; CYTOPLASM; DISEASE MODELS, ANIMAL; FEMALE; GENE DELETION; GENE TARGETING; HEPATOCYTES; MALARIA; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; PLASMODIUM YOELII; PROTOZOAN PROTEINS; RATS; RATS, WISTAR; SPOROZOITES; VACUOLES;

EID: 34547621806     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00225-07     Document Type: Article

References (36)

1. Baer, K., M. Roosevelt, A. B. Clarkson, Jr., N. van Rooijen, T. Schnieder, and U. Frevert. 2007. Kupffer cells are obligatory for Plasmodium yoelii sporozoite infection of the liver. Cell. Microbiol. 9:397-412.
2. Belmonte, M., T. R. Jones, M. Lu, R. Arcilla, T. Smalls, A. Belmonte, J. Rosenbloom, D. J. Carucci, and M. Sedegah. 2003. The infectivity of Plasmodium yoelii in different strains of mice. J. Parasitol. 89:602-603.
3. Carter, R., A. Coulson, S. Bhatti, B. J. Taylor, and J. F. Elliott. 1995. Predicted disulfide-bonded structures for three uniquely related proteins of Plasmodium falciparum, Pfs230, Pfs48/45 and Pf12. Mol. Biochem. Parasitol. 71:203-210.
4. Eksi, S., B. Czesny, G. J. van Gemert, R. W. Sauerwein, W. Eling, and K. C. Williamson. 2006. Malaria transmission-blocking antigen, Pfs230, mediates human red blood cell binding to exflagellating male parasites and oocyst production. Mol. Microbiol. 61:991-998.
5. Frevert, U., S. Engelmann, S. Zougbede, J. Stange, B. Ng, K. Matuschewski, L. Liebes, and H. Yee. 2005. Intravital observation of Plasmodium berghei sporozoite infection of the liver. PLoS Biol. 3:e192.
6. Frevert, U., I. Usynin, K. Baer, and C. Klotz. 2006. Nomadic or sessile: can Kupffer cells function as portals for malaria sporozoites to the liver? Cell. Microbiol. 8:1537-1546.
7. Gerloff, D. L., A. Creasey, S. Maslau, and R. Carter. 2005. Structural models for the protein family characterized by gamete surface protein Pfs230 of Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 102:13598-13603.
8. Good, M. F. 2005. Genetically modified Plasmodium highlights the potential of whole parasite vaccine strategies. Trends Immunol. 26:295-297.
9. Ishino, T., Y. Chinzei, and M. Yuda. 2005. A Plasmodium sporozoite protein with a membrane attack complex domain is required for breaching the liver sinusoidal cell layer prior to hepatocyte infection. Cell. Microbiol. 7:199-208.
10. Ishino, T., Y. Chinzei, and M. Yuda. 2005. Two proteins with 6-Cys motifs are required for malarial parasites to commit to infection of the hepatocyte. Mol. Microbiol. 58:1264-1275.
11. Ishino, T., K. Yano, Y. Chinzei, and M. Yuda. 2004. Cell-passage activity is required for the malarial parasite to cross the liver sinusoidal cell layer. PLoS Biol. 2:E4.
12. Kaiser, K., N. Camargo, I. Coppens, J. M. Morrisey, A. B. Vaidya, and S. H. Kappe. 2004. A member of a conserved Plasmodium protein family with membrane-attack complex/perforin (MACPF)-like domains localizes to the micronemes of sporozoites. Mol. Biochem. Parasitol. 133:15-26.
13. Kaiser, K., K. Matuschewski, N. Camargo, J. Ross, and S. H. Kappe. 2004. Differential transcriptome profiling identifies Plasmodium genes encoding preerythrocytic stage-specific proteins. Mol. Microbiol. 51:1221-1232.
14. Kappe, S. H., C. A. Buscaglia, and V. Nussenzweig. 2004. Plasmodium sporozoite molecular cell biology. Annu. Rev. Cell Dev. Biol. 20:29-59.
15. Kappe, S. H., M. J. Gardner, S. M. Brown, J. Ross, K. Matuschewski, J. M. Ribeiro, J. H. Adams, J. Quackenbush, J. Cho, D. J. Carucci, S. L. Hoffman, and V. Nussenzweig. 2001. Exploring the transcriptome of the malaria sporozoite stage. Proc. Natl. Acad. Sci. USA 98:9895-9900.
16. Kariu, T., T. Ishino, K. Yano, Y. Chinzei, and M. Yuda. 2006. CelTOS, a novel malarial protein that mediates transmission to mosquito and vertebrate hosts. Mol. Microbiol. 59:1369-1379.
17. Ménard, R., and C. Janse. 1997. Gene targeting in malaria parasites. Methods 13:148-157.
18. Menard, R., A. A. Sultan, C. Cortes, R. Altszuler, M. R. van Dijk, C. J. Janse, A. P. Waters, R. S. Nussenzweig, and V. Nussenzweig. 1997. Circumsporozoite protein is required for development of malaria sporozoites in mosquitoes. Nature 385:336-340.
19. Mikolajczak, S. A., and S. H. Kappe. 2006. A clash to conquer: the malaria parasite liver infection. Mol. Microbiol. 62:1499-1506.
20. Mota, M. M., G. Pradel, J. P. Vanderberg, J. C. Hafalla, U. Frevert, R. S. Nussenzweig, V. Nussenzweig, and A. Rodriguez. 2001. Migration of Plasmodium sporozoites through cells before infection. Science 291:141- 144.
21. Mueller, A. K., N. Camargo, K. Kaiser, C. Andorfer, U. Frevert, K. Matuschewski, and S. H. Kappe. 2005. Plasmodium liver stage developmental arrest by depletion of a protein at the parasite-host interface. Proc. Natl. Acad. Sci. USA 102:3022-3027.
22. Mueller, A. K., M. Labaied, S. H. Kappe, and K. Matuschewski. 2005. Genetically modified Plasmodium parasites as a protective experimental malaria vaccine. Nature 433:164-167.
23. Ponnudurai, T., A. H. Lensen, G. J. van Gemert, M. G. Bolmer, and J. H. Meuwissen. 1991. Feeding behaviour and sporozoite ejection by infected Anopheles stephensi. Trans. R. Soc. Trop. Med. Hyg. 85:175-180.
24. Prudencio, M., A. Rodriguez, and M. M. Mota. 2006. The silent path to thousands of merozoites: the Plasmodium liver stage. Nat. Rev. Microbiol. 4:849-856.
25. Quittnat, F., Y. Nishikawa, T. T. Stedman, D. R. Voelker, J. Y. Choi, M. M. Zahn, R. C. Murphy, R. M. Barkley, M. Pypaert, K. A. Joiner, and I. Coppens. 2004. On the biogenesis of lipid bodies in ancient eukaryotes: synthesis of triacylglycerols by a Toxoplasma DGAT1-related enzyme. Mol. Biochem. Parasitol. 138:107-122.
26. Renia, L., A. C. Gruner, M. Mauduit, and G. Snounou. 2006. Vaccination against malaria with live parasites. Expert Rev. Vaccines 5:473-481.
27. Renia, L., F. Miltgen, Y. Charoenvit, T. Ponnudurai, J. P. Verhave, W. E. Collins, and D. Mazier. 1988. Malaria sporozoite penetration. A new approach by double staining. J. Immunol. Methods 112:201-205.
28. Silvie, O., C. Greco, J. F. Franetich, A. Dubart-Kupperschmitt, L. Hannoun, G. J. van Gemert, R. W. Sauerwein, S. Levy, C. Boucheix, E. Rubinstein, and D. Mazier. 2006. Expression of human CD81 differently affects host cell susceptibility to malaria sporozoites depending on the Plasmodium species. Cell. Microbiol. 8:1134-1146.
29. Sultan, A. A., V. Thathy, U. Frevert, K. J. Robson, A. Crisanti, V. Nussenzweig, R. S. Nussenzweig, and R. Menard. 1997. TRAP is necessary for gliding motility and infectivity of Plasmodium sporozoites. Cell 90: 511-522.
30. Tarun, A. S., R. F. Dumpit, N. Camargo, M. Labaied, P. Liu, A. Takagi, R. Wang, and S. H. Kappe. 2007. Protracted sterile protection with Plasmodium yoelii pre-erythrocytic GAP malaria vaccines is independent of significant liver stage persistence and is mediated by CD8+ T cells. J. Infect. Dis., in press.
31. Templeton, T. J., and D. C. Kaslow. 1999. Identification of additional members define a Plasmodium falciparum gene superfamily which includes Pfs48/45 and Pfs230. Mol. Biochem. Parasitol. 101:223-227.
32. Tomas, A. M., G. Margos, G. Dimopoulos, L. H. van Lin, T. F. de Koning-Ward, R. Sinha, P. Lupetti, A. L. Beetsma, M. C. Rodriguez, M. Karras, A. Hager, J. Mendoza, G. A. Butcher, F. Kafatos, C. J. Janse, A. P. Waters, and R. E. Sinden. 2001. P25 and P28 proteins of the malaria ookinete surface have multiple and partially redundant functions. EMBO J. 20:3975-3983.
33. Ungureanu, E., R. Killick-Kendrick, P. C. Garnham, P. Branzei, C. Romanescu, and P. G. Shute. 1977. Prepatent periods of a tropical strain of Plasmodium vivax after inoculations of tenfold dilutions of sporozoites. Trans. R. Soc. Trop. Med. Hyg. 70:482-483.
34. Vanderberg, J. P., and U. Frevert. 2004. Intravital microscopy demonstrating antibody-mediated immobilisation of Plasmodium berghei sporozoites injected into skin by mosquitoes. Int. J. Parasitol. 34:991-996.
35. van Dijk, M. R., B. Douradinha, B. Franke-Fayard, V. Heussler, M. W. van Dooren, B. van Schaijk, G. J. van Gemert, R. W. Sauerwein, M. M. Mota, A. P. Waters, and C. J. Janse. 2005. Genetically attenuated, P36p-deficient malarial sporozoites induce protective immunity and apoptosis of infected liver cells. Proc. Natl. Acad. Sci. USA 102:12194-12199.
36. van Dijk, M. R., C. J. Janse, J. Thompson, A. P. Waters, J. A. Braks, H. J. Dodemont, H. G. Stunnenberg, G. J. van Gemert, R. W. Sauerwein, and W. Eling. 2001. A central role for P48/45 in malaria parasite male gamete fertility. Cell 104:153-164.