Enhanced immunity to Plasmodium falciparum circumsporozoite protein (PfCSP) by using Salmonella enterica serovar typhi expressing PfCSP and a PfCSP-encoding DNA vaccine in a heterologous prime-boost strategy

Infection and Immunity

Volumn 75, Issue 8, 2007, Pages 3769-3779

  Chinchilla, Magaly ^a,b   Pasetti, Marcela F ^a,b   Medina Moreno, Sandra ^a,b,d   Jin, Yuan Wang ^a   Gomez Duarte, Oscar G ^a,e   Stout, Rick ^c   Levine, Myron M ^a,b   Galen, James E ^a,b,d  

^a University of Maryland School of Medicine Center for Vaccine Development   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c Bioject Inc   (United States)

^d UNIVERSITY OF MARYLAND   (United States)

^e UNIVERSITY OF IOWA CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIRCUMSPOROZOITE PROTEIN; CYTOLYSIN; DNA VACCINE; GAMMA INTERFERON; IMMUNOGLOBULIN G2A; MALARIA VACCINE;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; BACTERIAL GENE; CARBOXY TERMINAL SEQUENCE; CELL LYSATE; CELLULAR IMMUNITY; CLYA GENE; CONTROLLED STUDY; DNA IMMUNIZATION; DOSE RESPONSE; DRUG DOSE ESCALATION; FEMALE; GENE; HUMORAL IMMUNITY; IMMUNITY; IMMUNOGENICITY; MOUSE; NONHUMAN; PLASMID; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTOZOAL GENETICS; SALMONELLA ENTERICA; SUPERNATANT; T CSP1 GENE; T CSP2 GENE; T LYMPHOCYTE;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, PROTOZOAN; BACTERIAL PROTEINS; CELLS, CULTURED; EPITOPES; FEMALE; GENETIC VECTORS; HEMOLYSIN PROTEINS; IMMUNITY, MUCOSAL; IMMUNIZATION, SECONDARY; INTERFERON TYPE II; LEUKOCYTES, MONONUCLEAR; MALARIA VACCINES; MICE; MICE, INBRED BALB C; MODELS, ANIMAL; MOLECULAR SEQUENCE DATA; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; RECOMBINANT FUSION PROTEINS; SALMONELLA TYPHI; VACCINES, DNA;

EID: 34547627867     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00356-07     Document Type: Article

References (60)

1. + cytotoxic T cells. J. Exp. Med. 172:1083-1090.
2. Aguiar, J. C., R. C. Hedstrom, W. O. Rogers, Y. Charoenvit, J. B. Sacci, Jr., D. E. Lanar, V. F. Majam, R. R. Stout, and S. L. Hoffman. 2001. Enhancement of the immune response in rabbits to a malaria DNA vaccine by immunization with a needle-free jet device. Vaccine 20:275-280.
3. Aidoo, M., A. Lalvani, C. E. Allsopp, M. Plebanski, S. J. Meisner, P. Krausa, M. Browning, S. Morris-Jones, F. Gotch, D. A. Fidock, M. Takiguchi, K. J. H. Robson, B. M. Greenwood, P. Druilhe, H. C. Whittle, and A. V. Hill. 1995. Identification of conserved antigenic components for a cytotoxic T lymphocyte-inducing vaccine against malaria. Lancet 345:1003-1007.
4. Aidoo, M., and V. Udhayakumar. 2000. Field studies of cytotoxic T lymphocytes in malaria infections: implications for malaria vaccine development. Parasitol. Today 16:50-56.
5. Alloueche, A., P. Milligan, D. J. Conway, M. Pinder, K. Bojang, T. Doherty, N. Tornieporth, J. Cohen, and B. M. Greenwood. 2003. Protective efficacy of the RTS,S/AS02 Plasmodium falciparum malaria vaccine is not strain specific. Am. J. Trop. Med. Hyg. 68:97-101.
6. Alonso, P. L., J. Sacarlal, J. J. Aponte, A. Leach, E. Macete, P. Aide, B. Sigauque, J. Milman, I. Mandomando, Q. Bassat, C. Guinovart, M. Espasa, S. Corachan, M. Lievens, M. M. Navia, M. C. Dubois, C. Menendez, F. Dubovsky, J. Cohen, R. Thompson, and W. R. Ballou. 2005. Duration of protection with RTS,S/AS02A malaria vaccine in prevention of Plasmodium falciparum disease in Mozambican children: single-blind extended follow-up of a randomised controlled trial. Lancet 366:2012-2018.
7. Alonso, P. L., J. Sacarlal, J. J. Aponte, A. Leach, E. Macete, J. Milman, I. Mandomando, B. Spiessens, C. Guinovart, M. Espasa, Q. Bassat, P. Aide, O. Ofori-Anyinam, M. M. Navia, S. Corachan, M. Ceuppens, M. C. Dubois, M. A. Demoitie, F. Dubovsky, C. Menendez, N. Tornieporth, W. R. Ballou, R. Thompson, and J. Cohen. 2004. Efficacy of the RTS,S/AS02A vaccine against Plasmodium falciparum infection and disease in young African children: randomised controlled trial. Lancet 364:1411-1420.
8. Calvo-Calle, J. M., J. Hammer, F. Sinigaglia, P. Clavijo, Z. R. Moya-Castro, and E. H. Nardin. 1997. Binding of malaria T cell epitopes to DR and DQ molecules in vitro correlates with immunogenicity in vivo: identification of a universal T cell epitope in the Plasmodium falciparum circumsporozoite protein. J. Immunol. 159:1362-1373.
9. + T cell responses in gene gun DNA immunization. J. Immunol. 167:5549-5557.
10. Clyde, D. F. 1975. Immunization of man against falciparum and vivax malaria by use of attenuated sporozoites. Am. J. Trop. Med. Hyg. 24:397-401.
11. Dame, J. B., J. L. Williams, T. F. McCutchan, J. L. Weber, R. A. Wirtz, W. T. Hockmeyer, W. L. Maloy, J. D. Haynes, I. Schneider, D. Roberts, G. S. Sanders, E. P. Reddy, C. Diggs, and L. H. Miller. 1984. Structure of the gene encoding the immunodominant surface antigen on the sporozoite of the human malaria parasite Plasmodium falciparum. Science 225:593-599.
12. de Groot, A. S., A. H. Johnson, W. L. Maloy, I. A. Quakyi, E. M. Riley, A. Menon, S. M. Banks, J. A. Berzofsky, and M. F. Good. 1989. Human T cell recognition of polymorphic epitopes from malaria circumsporozoite protein. J. Immunol. 142:4000-4005.
13. Doolan, D. L., S. L. Hoffman, S. Southwood, P. A. Wentworth, J. Sidney, R. W. Chesnut, E. Keogh, E. Appella, T. B. Nutman, A. A. Lai, D. M. Gordon, A. Oloo, and A. Sette. 1997. Degenerate cytotoxic T cell epitopes from P. falciparum restricted by multiple HLA-A and HLA-B supertype alleles. Immunity 7:97-112.
14. Dunachie, S. J., and A. V. Hill. 2003. Prime-boost strategies for malaria vaccine development. J. Exp. Biol. 206:3771-3779.
15. Epstein, J. E., Y. Charoenvit, K. E. Kester, R. Wang, R. Newcomer, S. Fitzpatrick, T. L. Richie, N. Tornieporth, D. G. Heppner, C. Ockenhouse, V. Majam, C. Holland, E. Abot, H. Ganeshan, M. Berzins, T. Jones, C. N. Freydberg, J. Ng, J. Norman, D. J. Carucci, J. Cohen, and S. L. Hoffman. 2004. Safety, tolerability, and antibody responses in humans after sequential immunization with a PfCSP DNA vaccine followed by the recombinant protein vaccine RTS,S/AS02A. Vaccine 22:1592-1603.
16. Frevert, U., M. R. Galinski, F. U. Hugel, N. Allon, H. Schreier, S. Smulevitch, M. Shakibaei, and P. Clavijo. 1998. Malaria circumsporozoite protein inhibits protein synthesis in mammalian cells. EMBO J. 17:3816-3826.
17. Galen, J. E., O. G. Gomez-Duarte, G. A. Losonsky, J. L. Halpern, C. S. Lauderbaugh, S. Kaintuck, M. K. Reymann, and M. M. Levine. 1997. A murine model of intranasal immunization to assess the immunogenicity of attenuated Salmonella typhi live vector vaccines in stimulating serum antibody responses to expressed foreign antigens. Vaccine 15:700-708.
18. Galen, J. E., and M. M. Levine. 2001. Can. a 'flawless' live vector vaccine strain be engineered? Trends Microbiol. 9:372-376.
19. Galen, J. E., J. Nair, J. Y. Wang, S. S. Wasserman, M. K. Tanner, M. B. Sztein, and M. M. Levine. 1999. Optimization of plasmid maintenance in the attenuated live vector vaccine strain Salmonella typhi CVD 908-htrA. Infect. Immun. 67:6424-6433.
20. Galen, J. E., L. Zhao, M. Chinchilla, J. Y. Wang, M. F. Pasetti, J. Green, and M. M. Levine. 2004. Adaptation of the endogenous Salmonella enterica serovar Typhi clyA-encoded hemolysin for antigen export enhances the immunogenicity of anthrax protective antigen domain 4 expressed by the attenuated live-vector vaccine strain CVD 908-htrA. Infect. Immun. 72:7096-7106.
21. Gomez-Duarte, O. G., M. F. Pasetti, A. Santiago, M. B. Sztein, S. L. Hoffman, and M. M. Levine. 2001. Expression, extracellular secretion, and immunogenicity of the Plasmodium falciparum sporozoite surface protein 2 in Salmonella vaccine strains. Infect. Immun. 69:1192-1198.
22. Gonzalez, C., D. Hone, F. R. Noriega, C. O. Tacket, J. R. Davis, G. Losonsky, J. P. Nataro, S. Hoffman, A. Malik, E. Nardin, M. B. Sztein, D. G. Heppner, T. R. Fouts, A. Asibasi, and M. M. Levine. 1994. Salmonella typhi vaccine strain CVD 908 expressing the circumsporozoite protein of Plasmodium falciparum: strain construction and safety and immunogenicity in humans. J. Infect. Dis. 169:927-931.
23. Hess, J., I. Gentschev, D. Miko, M. Welzel, C. Ladel, W. Goebel, and S. H. Kaufmann. 1996. Superior efficacy of secreted over somatic antigen display in recombinant Salmonella vaccine induced protection against listeriosis. Proc. Natl. Acad. Sci. USA 93:1458-1463.
24. Hill, A. V., J. Elvin, A. C. Willis, M. Aidoo, C. E. Allsopp, F. M. Gotch, X. M. Gao, M. Takiguchi, B. M. Greenwood, A. R. Townsend, A. J. McMichael, and H. C. Wittle. 1992. Molecular analysis of the association of HLA-B53 and resistance to severe malaria. Nature 360:434-439.
25. Hone, D. M., A. M. Harris, S. Chatfield, G. Dougan, and M. M. Levine. 1991. Construction of genetically defined double aro mutants of Salmonella typhi. Vaccine 9:810-816.
26. Jones, T. R., D. L. Narum, A. S. Gozalo, J. Aguiar, S. R. Fuhrmann, H. Liang, J. D. Haynes, J. K. Moch, C. Lucas, T. Luu, A. J. Magill, S. L. Hoffman, and B. K. Sim. 2001. Protection of Aotus monkeys by Plasmodium falciparum EBA-175 region II DNA prime-protein boost immunization regimen. J. Infect. Dis. 183:303-312.
27. Jongwutiwes, S., K. Tanabe, M. K. Hughes, H. Kanbara, and A. L. Hughes. 1994. Allelic variation in the circumsporozoite protein of Plasmodium falciparum from Thai field isolates. Am. J. Trop. Med. Hyg. 51:659-668.
28. Kang, H. Y., and R. Curtiss III. 2003. Immune responses dependent on antigen location in recombinant attenuated Salmonella typhimurium vaccines following oral immunization. FEMS Immunol. Med. Microbiol. 37:99-104.
29. Lange, U. G., P. Mastroeni, J. M. Blackwell, and C. B. Stober. 2004. DNA-Salmonella enterica serovar Typhimurium primer-booster vaccination biases towards T helper 1 responses and enhances protection against Leishmania major infection in mice. Infect. Immun. 72:4924-4928.
30. Londono-Arcila, P., D. Freeman, H. Kleanthous, A. M. O'Dowd, S. Lewis, A. K. Turner, E. L. Rees, T. J. Tibbitts, J. Greenwood, T. P. Monath, and M. J. Darsley. 2002. Attenuated Salmonella enterica serovar Typhi expressing urease effectively immunizes mice against Helicobacter pylori challenge as part of a heterologous mucosal priming-parenteral boosting vaccination regimen. Infect. Immun. 70:5096-5106.
31. Malik, A., J. E. Egan, R. A. Houghten, J. C. Sadoff, and S. L. Hoffman. 1991. Human cytotoxic T lymphocytes against the Plasmodium falciparum circumsporozoite protein. Proc. Natl. Acad. Sci. USA 88:3300-3304.
32. Moorthy, V. S., M. F. Good, and A. V. Hill. 2004. Malaria vaccine developments. Lancet 363:150-156.
33. Moorthy, V. S., E. B. Imoukhuede, S. Keating, M. Pinder, D. Webster, M. A. Skinner, S. C. Gilbert, G. Walraven, and A. V. Hill. 2004. Phase 1 evaluation of 3 highly immunogenic prime-boost regimens, including a 12-month reboosting vaccination, for malaria vaccination in Gambian men. J. Infect. Dis. 189:2213-2219.
34. Nardin, E. H., J. M. Calvo-Calle, G. A. Oliveira, P. Clavijo, R. Nussenzweig, R. Simon, W. Zeng, and K. Rose. 1998. Plasmodium falciparum polyoximes: highly immunogenic synthetic vaccines constructed by chemoselective ligation of repeat B-cell epitopes and a universal T-cell epitope of CS protein. Vaccine 16:590-600.
35. Nardin, E. H., G. A. Oliveira, J. M. Calvo-Calle, Z. R. Castro, R. S. Nussenzweig, B. Schmeckpeper, B. F. Hall, C. Diggs, S. Bodison, and R. Edelman. 2000. Synthetic malaria peptide vaccine elicits high levels of antibodies in vaccinees of defined HLA genotypes. J. Infect. Dis. 182: 1486-1496.
36. Narum, D. L., S. Kumar, W. O. Rogers, S. R. Fuhrmann, H. Liang, M. Oakley, A. Taye, B. K. Sim, and S. L. Hoffman. 2001. Codon optimization of gene fragments encoding Plasmodium falciparum merozoite proteins enhances DNA vaccine protein expression and immunogenicity in mice. Infect. Immun. 69:7250-7253.
37. Pasetti, M. F., R. J. Anderson, F. R. Noriega, M. M. Levine, and M. B. Sztein. 1999. Attenuated deltaguaBA Salmonella typhi vaccine strain CVD 915 as a live vector utilizing prokaryotic or eukaryotic expression systems to deliver foreign antigens and elicit immune responses. Clin. Immunol. 92:76-89.
38. Pasetti, M. F., M. M. Levine, and M. B. Sztein. 2003. Animal models paving the way for clinical trials of attenuated Salmonella enterica serovar Typhi live oral vaccines and live vectors. Vaccine 21:401-418.
39. Rathore, D., and T. F. McCutchan. 2000. The cytotoxic T-lymphocyte epitope of the Plasmodium falciparum circumsporozoite protein also modulates the efficiency of receptor-ligand interaction with hepatocytes. Infect. Immun. 68:740-743.
40. Raviprakash, K., D. Ewing, M. Simmons, K. R. Porter, T. R. Jones, C. G. Hayes, R. Stout, and G. S. Murphy. 2003. Needle-free Biojector injection of a dengue virus type 1 DNA vaccine with human immunostimulatory sequences and the GM-CSF gene increases immunogenicity and protection from virus challenge in Aotus monkeys. Virology 315:345-352.
41. Rogers, W. O., W. R. Weiss, A. Kumar, J. C. Aguiar, J. A. Tine, R. Gwadz, J. G. Harre, K. Gowda, D. Rathore, S. Kumar, and S. L. Hoffman. 2002. Protection of rhesus macaques against lethal Plasmodium knowlesi malaria by a heterologous DNA priming and poxvirus boosting immunization regimen. Infect. Immun. 70:4329-4335.
42. 4 on the surface of Salmonella enterica using the autotransporter MisL. Infect. Immun. 70:3611-3620.
43. Sadoff, J. C., W. R. Ballou, L. S. Baron, W. R. Majarian, R. N. Brey, W. T. Hockmeyer, J. F. Young, S. J. Cryz, J. Ou, G. H. Lowell, and J. D. Chulay. 1988. Oral Salmonella typhimurium vaccine expressing circumsporozoite protein protects against malaria. Science 240:336-338.
44. Sambrok, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
45. Sedegah, M., Y. Charoenvit, L. Minh, M. Belmonte, V. F. Majam, S. Abot, H. Ganeshan, S. Kumar, D. J. Bacon, A. Stowers, D. L. Narum, D. J. Carucci, and W. O. Rogers. 2004. Reduced immunogenicity of DNA vaccine plasmids in mixtures. Gene Ther. 11:448-456.
46. Sinnis, P., P. Clavijo, D. Fenyo, B. T. Chait, C. Cerami, and V. Nussenzweig. 1994. Structural and functional properties of region II-plus of the malaria circumsporozoite protein. J. Exp. Med. 180:297-306.
47. Sinnis, P., and E. Nardin. 2002. Sporozoite antigens: biology and immunology of the circumsporozoite protein and thrombospondin-related anonymous protein. Chem. Immunol. 80:70-96.
48. Smith, E. C., and A. W. Taylor-Robinson. 2003. Parasite-specific immunoglobulin isotypes during lethal and non-lethal murine malaria infections. Parasitol. Res. 89:26-33.
49. Stokes, M. G., R. W. Titball, B. N. Neeson, J. E. Galen, N. J. Walker, A. J. Stagg, D. C. Jenner, J. E. Thwaite, J. P. Nataro, L. W. Baillie, and H. S. Atkins. 2007. Oral administration of a Salmonella-based vaccine expressing Bacillus anthracis protective antigen confers protection against aerosolized B. anthracis. Infect. Immun. 75:1827-1834.
50. Stoute, J. A., W. R. Ballou, N. Kolodny, C. D. Deal, R. A. Wirtz, and L. E. Lindler. 1995. Induction of humoral immune response against Plasmodium falciparum sporozoites by immunization with a synthetic peptide mimotope whose sequence was derived from screening a filamentous phage epitope library. Infect. Immun. 63:934-939.
51. + T cells producing IFN-gamma. J. Immunol. 171:6961-6967.
52. Tacket, C. O., M. B. Sztein, G. A. Losonsky, S. S. Wasserman, J. P. Nataro, R. Edelman, D. Pickard, G. Dougan, S. N. Chatfield, and M. M. Levine. 1997. Safety of live oral Salmonella typhi vaccine strains with deletions in htrA and aroC aroD and immune response in humans. Infect. Immun. 65:452-456.
53. Taylor-Robinson, A. W. 1995. Regulation of immunity to malaria: valuable lessons learned from murine models. Parasitol. Today 11:334-342.
54. Taylor-Robinson, A. W. 2002. Exoerythrocytic malaria vaccine development: understanding host-parasite immunobiology underscores strategic success. Expert Rev. Vaccines 1:317-340.
55. Vindurampulle, C. J., L. F. Cuberos, E. M. Barry, M. F. Pasetti, and M. M. Levine. 2004. Recombinant Salmonella enterica serovar Typhi in a prime-boost strategy. Vaccine 22:3744-3750.
56. Wang, R., D. L. Doolan, T. P. Le, R. C. Hedstrom, K. M. Coonan, Y. Charoenvit, T. R. Jones, P. Hobart, M. Margalith, J. Ng, W. R. Weiss, M. Sedegah, C. de Taisne, J. A. Norman, and S. L. Hoffman. 1998. Induction of antigen-specific cytotoxic T lymphocytes in humans by a malaria DNA vaccine. Science 282:476-480.
57. + type 1 responses in humans by a malaria DNA vaccine. Proc. Natl. Acad. Sci. USA 98:10817-10822.
58. + T cell and antibody responses by sequential immunization with malaria DNA and recombinant protein. J. Immunol. 172:5561-5569.
59. Woodland, D. L. 2004. Jump-starting the immune system: prime-boosting comes of age. Trends Immunol. 25:98-104.
60. Zavala, F., A. Masuda, P. M. Graves, V. Nussenzweig, and R. S. Nussenzweig. 1985. Ubiquity of the repetitive epitope of the CS protein in different isolates of human malaria parasites. J. Immunol. 135:2790-2793.