Minimal role for the circumsporozoite protein in the induction of sterile immunity by vaccination with live rodent malaria sporozoites

Infection and Immunity

Volumn 78, Issue 5, 2010, Pages 2182-2188

  Mauduit, Marjorie ^a,b,c   Tewari, Rita ^d,e   Depinay, Nadya ^b,c   Kayibanda, Michèle ^b,c   Lallemand, Eliette ^b,c   Chavatte, Jean Marc ^f   Snounou, Georges ^f,g,h   Rénia, Laurent ^a,b,c   Grüner, Anne Charlotte ^a,b,c  

^a AGENCY FOR SCIENCE   (Singapore)

^b INSTITUT COCHIN   (France)

^c INSERM   (France)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^f MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^g PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^h SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROQUINE; CIRCUMSPOROZOITE PROTEIN; MALARIA VACCINE; SPOROZOITE VACCINE;

ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; FEMALE; IMMUNE RESPONSE; IMMUNITY; MALARIA; MOUSE; NONHUMAN; PLASMODIUM BERGHEI; PLASMODIUM YOELII; PRIORITY JOURNAL; TRANSGENIC ORGANISM;

ANIMALS; FEMALE; INTERFERON-GAMMA; LEUKOCYTES, MONONUCLEAR; LIVER; MALARIA; MALARIA VACCINES; MICE; MICE, INBRED BALB C; PLASMODIUM BERGHEI; PLASMODIUM YOELII; PROTOZOAN PROTEINS; SPLEEN; SPOROZOITES;

EID: 77951227194     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01415-09     Document Type: Article

References (32)

1. Ballou, W. R. 2009. The development of the RTS, S malaria vaccine candidate: challenges and lessons. Parasite Immunol. 31:492-500.
2. Beaudoin, R. L., C. P. Strome, F. Mitchell, and T. A. Tubergen. 1977. Plasmodium berghei: immunization of mice against the ANKA strain using the unaltered sporozoite as an antigen. Exp. Parasitol. 42:1-5.
3. Belnoue, E., F. T. Costa, T. Frankenberg, A. M. Vigario, T. Voza, N. Leroy, M. M. Rodrigues, I. Landau, G. Snounou, and L. Rénia. 2004. Protective T cell immunity against malaria liver stage after vaccination with live sporozoites under chloroquine treatment. J. Immunol. 172:2487-2495. (Pubitemid 38182399)
4. Clyde, D. F., V. C. McCarthy, R. M. Miller, and W. E. Woodward. 1975. Immunization of man against falciparum and vivax malaria by use of attenuated sporozoites. Am. J. Trop. Med. Hyg. 24:397-401.
5. de Koning-Ward, T. F., R. A. O'Donnell, D. R. Drew, R. Thomson, T. P. Speed, and B. S. Crabb. 2003. A new rodent model to assess blood stage immunity to the Plasmodium falciparum antigen merozoite surface protein 119 reveals a protective role for invasion inhibitory antibodies. J. Exp. Med. 198:869-875.
6. Douradinha, B., M. R. Van Dijk, R. Ataide, G. J. van Gemert, J. Thompson, J. F. Franetich, D. Mazier, A. J. F. Luty, R. W. Sauerwein, C. J. Janse, A. P. Waters, and M. M. Mota. 2007. Genetically attenuated P36p-deficient Plasmodium berghei sporozoites confer long-lasting and partial cross-species protection. Int. J. Parasitol. 37:1511-1519.
7. Franke-Fayard, B., H. Trueman, J. Ramesar, J. Mendoza, M. van der Keur, R. van der Linden, R. E. Sinden, A. P. Waters, and C. J. Janse. 2004. A Plasmodium berghei reference line that constitutively expresses GFP at a high level throughout the complete life cycle. Mol. Biochem. Parasitol. 137:23-33.
8. Grillot, D., M. Michel, I. Muller, C. Tougne, L. Rénia, D. Mazier, G. Corradin, P. H. Lambert, J. A. Louis, and G. Del Guidice. 1990. Immune responses to defined epitopes of the circumsporozoite protein of the murine malaria parasite, Plasmodium yoelii. Eur. J. Immunol. 20:1215-1222. (Pubitemid 20206083)
9. Grüner, A. C., S. Hez-Deroubaix, G. Snounou, N. Hall, C. Bouchier, F. Letourneur, I. Landau, and P. Druilhe. 2005. Insights into the P. y. yoelii hepatic stage transcriptome reveal complex transcriptional patterns. Mol. Biochem. Parasitol. 142:184-192.
10. Grüner, A. C., M. Mauduit, R. Tewari, J. F. Romero, N. Depinay, M. Kayibanda, E. Lallemand, J. M. Chavatte, A. Crisanti, P. Sinnis, D. Mazier, G. Corradin, G. Snounou, and L. Rénia. 2007. Sterile protection against malaria is independent of immune responses to the circumsporozoite protein. PLoS One 2:e1371. (Pubitemid 351760771)
11. Grüner, A. C., G. Snounou, K. Brahimi, F. Letourneur, L. Rénia, and P. Druilhe. 2003. Pre-erythrocytic antigens of Plasmodium falciparum: from rags to riches? Trends Parasitol. 19:74-78.
12. Hoffman, S. L., L. M. Goh, T. C. Luke, I. Schneider, T. P. Le, D. L. Doolan, J. Sacci, P. de la Vega, M. Dowler, C. Paul, D. M. Gordon, J. A. Stoute, L. W. Church, M. Sedegah, D. G. Heppner, W. R. Ballou, and T. L. Richie. 2002. Protection of humans against malaria by immunization with radiation-attenuated Plasmodium falciparum sporozoites. J. Infect. Dis. 185:1155-1164.
13. Kumar, K. A., G. Sano, S. Boscardin, R. S. Nussenzweig, M. C. Nussenzweig, F. Zavala, and V. Nussenzweig. 2006. The circumsporozoite protein is an immunodominant protective antigen in irradiated sporozoites. Nature 444:937-940.
14. Lopez, J. A., M. A. Roggero, O. Duombo, J. M. Gonzalez, R. Tolle, O. Koita, M. Arevalo-Herrera, S. Herrera, and G. Corradin. 1996. Recognition of synthetic 104-mer and 102-mer peptides corresponding to N- and C-terminal nonrepeat regions of the Plasmodium falciparum circumsporozoite protein by sera from human donors. Am. J. Trop. Med. Hyg. 55:424-429.
15. Mauduit, M., A. C. Gruner, R. Tewari, N. Depinay, M. Kayibanda, J. M. Chavatte, J. F. Franetich, A. Crisanti, D. Mazier, G. Snounou, and L. Renia. 2009. A role for immune responses against non-CS components in the cross-species protection induced by immunization with irradiated malaria sporozoites. PLoS One 4:e7717.
16. 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.
17. Murhandarwati, E. E., L. Wang, H. D. de Silva, C. Ma, M. Plebanski, C. G. Black, and R. L. Coppel. 2009. Growth-inhibitory antibodies are not necessary for protective immunity to malaria infection. Infect. Immun. 78:680-687.
18. Nardin, E. H., and R. S. Nussenzweig. 1993. T cell responses to pre-erythrocytic stages of malaria: role in protection and vaccine development against pre-erythrocytic stages. Annu. Rev. Immunol. 11:687-727.
19. Nussenzweig, R. S., J. Vanderberg, G. L. Spitalny, C. I. Rivera, C. Orton, and H. Most. 1972. Sporozoite-induced immunity in mammalian malaria. A review. Am. J. Trop. Med. Hyg. 21:722-728.
20. O'Donnell, R. A., A. Saul, A. F. Cowman, and B. S. Crabb. 2000. Functional conservation of the malaria vaccine antigen MSP-119 across distantly related Plasmodium species. Nat. Med. 6:91-95.
21. Rénia, 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.
22. Rieckmann, K. H., P. E. Carson, R. L. Beaudoin, J. S. Cassells, and K. W. Sell. 1974. Sporozoite induced immunity in man against an Ethiopian strain of Plasmodium falciparum. Trans. R. Soc. Trop. Med. Hyg. 68:258-259.
23. Roestenberg, M., M. McCall, J. Hopman, J. Wiersma, A. J. Luty, G. J. van Gemert, M. van de Vegte-Bolmer, B. van Schaijk, K. Teelen, T. Arens, L. Spaarman, Q. de Mast, W. Roeffen, G. Snounou, L. Rénia, A. van der Ven, C. C. Hermsen, and R. Sauerwein. 2009. Protection against a malaria challenge by sporozoite inoculation. N. Engl. J. Med. 361:468-477.
24. Sacci, J. B., Jr., J. M. Ribeiro, F. Huang, U. Alam, J. A. Russell, P. L. Blair, A. Witney, D. J. Carucci, A. F. Azad, and J. C. Aguiar. 2005. Transcriptional analysis of in vivo Plasmodium yoelii liver stage gene expression. Mol. Biochem. Parasitol. 142:177-183.
25. Scheller, L. F., and A. F. Azad. 1995. Maintenance of protective immunity against malaria by persistent hepatic parasites derived from irradiated sporozoites. Proc. Natl. Acad. Sci. U. S. A. 92:4066-4068.
26. Sedegah, M., W. W. Weiss, and S. L. Hoffman. 2007. Cross-protection between attenuated Plasmodium berghei and P. yoelii sporozoites. Parasite Immunol. 29:559-565.
27. Snounou, G., A. C. Grüner, C. D. Müller-Graf, D. Mazier, and L. Renia. 2005. The Plasmodium sporozoite survives RTS,S vaccination. Trends Parasitol. 21:456-461. (Pubitemid 41297748)
28. Tarun, A. S., X. Peng, R. F. Dumpit, Y. Ogata, H. Silva-Rivera, N. Camargo, T. M. Daly, L. W. Bergman, and S. H. Kappe. 2008. A combined transcriptome and proteome survey of malaria parasite liver stages. Proc. Natl. Acad. Sci. U. S. A. 105:305-310.
29. Tewari, R., D. Rathore, and A. Crisanti. 2005. Motility and infectivity of Plasmodium berghei sporozoites expressing avian Plasmodium gallinaceum circumsporozoite protein. Cell Microbiol. 7:699-707.
30. VanBuskirk, K. M., M. T. O'Neill, P. De La Vega, A. G. Maier, U. Krzych, J. Williams, M. G. Dowler, J. B. Sacci, Jr., N. Kangwanrangsan, T. Tsuboi, N. M. Kneteman, D. G. Heppner, Jr., B. A. Murdock, S. A. Mikolajczak, A. S. Aly, A. F. Cowman, and S. H. Kappe. 2009. Preerythrocytic, live-attenuated Plasmodium falciparum vaccine candidates by design. Proc. Natl. Acad. Sci. U. S. A. 106:13004-13009.
31. 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. U. S. A. 102:12194-12199.
32. Wang, Q., S. Brown, D. S. Roos, V. Nussenzweig, and P. Bhanot. 2004. Transcriptome of axenic liver stages of Plasmodium yoelii. Mol. Biochem. Parasitol. 137:161-168.