Current status of toxoplasmosis vaccine development

Expert Review of Vaccines

Volumn 8, Issue 6, 2009, Pages 791-808

  Kur, Józef ^a   Holec Ga̧sior, Lucyna ^a   Hiszczyńska Sawicka, Elzbieta ^a  

^a GDANSK UNIVERSITY OF TECHNOLOGY   (Poland)

Author keywords

Adjuvant; Bradyzoite; Cellular Th1 response; DNA vaccine; Humoral response; Recombinant antigen; Tachyzoite; Toxoplasmosis

Indexed keywords

TOXOPLASMA GONDII VACCINE;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ENCEPHALITIS; HUMORAL IMMUNITY; IMMUNE RESPONSE; PRIORITY JOURNAL; REVIEW; TH1 CELL; TOXOPLASMA GONDII; TOXOPLASMOSIS;

ANIMALS; BIOMEDICAL RESEARCH; HUMANS; PROTOZOAN VACCINES; TOXOPLASMA; TOXOPLASMOSIS;

EID: 67049167220     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/erv.09.27     Document Type: Review

References (124)

1. Lautenslager JP. Toxoplasmosis as a significant disease in man and animals with special reference to preventive measures by the farm community. Can. Vet. J. 28(5), 261-264 (1987).
2. Montoya JG, Liesenfeld O. Toxoplasmosis. Lancet 363(9425), 1965-1976 (2004).
3. Dubey JP, Jones JL. Toxoplasma gondii infection in humans and animals in the United States. Int. J. Parasitol. 38(11), 1257-1278 (2008).
4. Buxton D, Innes EA. A commercial vaccine for ovine toxoplasmosis. Parasitology 110, 11-16 (1995).
5. Buxton D. Protozoan infections (Toxoplasma gondii, Neospora caninum and Sarcocystis spp.) in sheep and goats: recent advances. Vet. Res. 29(3-4), 289-310 (1998). (Pubitemid 28293469)
6. Vercruysse J, Knox DP, Schetters TP, Willadsen P. Veterinary parasitic vaccines: pitfalls and future directions. Trends Parasitol. 20(10), 488-492 (2004). (Pubitemid 39195059)
7. Innes EA, Vermeulen AN. Vaccination as a control strategy against the coccidial parasites Eimeria, Toxoplasma and Neospora. Parasitology 133, 145-168 (2006). • Describes vaccination strategies against coccidial parasites Eimeria, Toxoplasma and Neospora, which are significant causes of disease in food-producing animals. The paper discusses current vaccination strategies and recent research looking towards developing new vaccine targets and approaches. (Pubitemid 46208035)
8. Araujo FG. Immunization against Toxoplasma gondii. Parasitol. Today 10(9), 358-360 (1994). (Pubitemid 24263764)
9. O'Connell E, Wilkins MF, Te Punga WA. Toxoplasmosis in sheep. II. The ability of a live vaccine to prevent lamb losses after an intravenous challenge with Toxoplasma gondii. NZ Vet. J. 36(1), 1-4 (1988).
10. Wilkins MF, O'Connell E, Te Punga WA. Toxoplasmosis in sheep III. Further evaluation of the ability of a live Toxoplasma gondii vaccine to prevent lamb losses and reduce congenital infection following experimental oral challenge. NZ Vet. J. 36(2), 86-89 (1988).
11. Buxton D, Thomson KM, Maley S, Wright S, Bos HJ. Experimental challenge of sheep 18 months after vaccination with a live (S48) Toxoplasma gondii vaccine. Vet. Rec. 133(13), 310-312 (1993). (Pubitemid 23288466)
12. Tenter AM, Heckeroth AR, Weiss LM. Toxoplasma gondii: from animals to humans. Int. J. Parasitol. 30(12-13), 1217-1258 (2000).
13. Gazzinelli RT, Amichay D, Sharton-Kersten T, Grunwald E, Farber JM, Sher A. Role of macrophage derived cytokines in the induction and regulation of cell mediated immunity to Toxoplasma gondii. Curr. Top. Microbiol. Immunol. 219, 127-140 (1996). (Pubitemid 26272951)
14. Sher A, Reis e Sousa C. Ignition of the type 1 response to intracellular infection by dendric cell derived IL-12. Eur. Cytokine Netw. 9(3), 65-68 (1998). (Pubitemid 28508765)
15. Sibley LD, Adam SL, Fukutomi Y. Tumor necrosis factor-α triggers antitoxoplasmal activity of IFN-γ primed macrophages. J. Immunol. 147(7), 2340-2345 (1991).
16. Sher A, Oswald IP, Hieny S, Gazzinelli RT. Toxoplasma gondii induces a T independent IFN-γ response in natural killer cells that requires both adherant accessory cells and tumor necrosis factor-α. J. Immunol. 150(9), 3982-3989 (1993). (Pubitemid 23129780)
17. Langermans JAM, Van Der Hulst MEB, Nibbering PH, Hiemstra OPS, Fransen L, Van Furth R. INF-γ induced L-arginine dependent toxoplasmastatic activity in murine peritoneal macrophages is mediated by endogenous tumor necrosis factor-α. J. Immunol. 148(2), 568-574 (1992).
18. Sher A, Collazzo C, Scanga C, Jankovic D, Yap G, Aliberti J. Induction and regulation of IL-12-dependent host resistance to Toxoplasma gondii. Immunol Res. 27(2-3), 521-528 (2003). (Pubitemid 36995032)
19. Luft BJ, Remington JS. Toxoplasmatic encephalitis in AIDS. Clin. Infect. Dis. 15, 211-222 (1992).
20. Suzuki Y, Orellana MA, Schreiber RD, Remington JS. Interferon-γ: the major mediator of resistance against Toxoplasma gondii. Science 240(4851), 516-518 (1988).
21. Sayles PC, Gibson GW, Johnson LL. B cells are essential for vaccination-induced resistance to virulent Toxoplasma gondii. Infect. Immun. 68(3), 1026-1033 (2000). (Pubitemid 30108487)
22. Johnson LL, Sayles PC. Deficient humoral responses underlie susceptibility to Toxoplasma gondii in CD4-deficient mice. Infect. Immun. 70(1), 185-191 (2002). (Pubitemid 34028616)
23. Buxton D. Toxoplasmosis: the first commercial vaccine. Parasitol. Today 9(9), 335-337 (1993).
24. Frenkel JK, Pfefferkorn ER, Smith DD, Fishback JL. Prospective vaccine prepared from a new mutant of Toxoplasma gondii for use in cats. Am. J. Vet. Res. 52(5), 759-763 (1991).
25. Lindsay DS. Blagburn BL, Dubey JP. Safety and results of challenge of weaned pigs given a temperature sensitive mutant of Toxoplasma gondii. J. Parasitol. 79(1), 71-76 (1993).
26. Gatkowska J, Ga̧sior A, Kur J, Długońska H. Toxoplasma gondii: chimeric Dr fimbriae as a recombinant vaccine against toxoplasmosis. Exp. Parasitol. 118(2), 266-270 (2008). (Pubitemid 350309297)
27. Couper KN, Nielsen HV, Petersen E, Roberts F, Roberts CW, Alexander J. DNA vaccination with the immunodominant tachyzoite surface antigen (SAG-1) protects against adult acquired Toxoplasma gondii infection but does not prevent maternofoetal transmission. Vaccine 21(21-22), 2813-2820 (2003). (Pubitemid 36703192)
28. Dimier-Poisson I, Aline F, Bout D, Mévélec MN. Induction of protective immunity against toxoplasmosis in mice by immunization with Toxoplasma gondii RNA. Vaccine 24(10), 1705-1709 (2006). •• Suggests that RNA vaccination by a mucosal route produces a protective immune response against Toxoplasma gondii. These are important findings in the context that T. gondii enters the mucosal surfaces of the host and so immunity at these sites is of major interest. (Pubitemid 43238248)
29. Cong H, Gu QM, Jiang Y et al. Oral immunization with a live recombinant attenuated Salmonella typhimurium protects mice against Toxoplasma gondii. Parasite Immunol. 27(1-2), 29-35 (2005). •• First report of protection against T. gondii afforded by oral immunization with Salmonella expressing a multi-antigenic gene linked to a cholera toxin genetic adjuvant. The results from this study should contribute to the development of a highly protective orally delivered DNA vaccine against T. gondii.
30. Siachoque H, Guzman F, Burgos J, Patarroyo ME, Gomez-Marin JE. Toxoplasma gondii: immunogenicity and protection by P30 peptides in a murine model. Exp. Parasitol. 114(1), 62-65 (2006). (Pubitemid 44188651)
31. Fox BA, Bzik DJ. De novo pyrimidine biosynthesis is required for virulence of Toxoplasma gondii. Nature 415, 925-929 (2002). (Pubitemid 34174756)
32. Spencer JA, Smith BF, Guarino AJ, Blagburn BL, Baker HJ. The use of CpG as an adjuvant to Toxoplasma gondii vaccination. Parasitol. Res. 92(4), 313-316 (2004). (Pubitemid 38339987)
33. Denkers EY, Gazzinelli RT. Regulation and function of T-cell-mediated immunity during Toxoplasma gondii infection. Clin. Microbiol. Rev. 11(4), 569-588 (1998). (Pubitemid 28497562)
34. Boothroyd JC, Hehl A, Knoll LJ, Manger ID. The surface of Toxoplasma: more or less. Int. J. Parasitol. 28(1), 3-9 (1997). (Pubitemid 28082055)
35. Jung C, Lee CY, Grigg ME. The SRS superfamily of Toxoplasma surface proteins. Int. J. Parasitol. 34(3), 285-296 (2004). (Pubitemid 38299179)
36. Lekutis C, Ferguson DJ, Grigg ME, Camps M, Boothroyd JC. Surface antigens of Toxoplasma gondii: variations on a theme. Int. J. Parasitol. 31(12), 1285-1292 (2001). (Pubitemid 32868708)
37. Grimwood J, Smith JE. Toxoplasma gondii: the role of parasite surface and secreted proteins in host cell invasion. Int. J. Parasitol. 26(2), 169-173 (1996). (Pubitemid 26072798)
38. Mineo JR, Kasper LH. Attachment of Toxoplasma gondii to host cells involves major surface protein, SAG-1 (P30). Exp. Parasitol. 79(1), 11-20 (1994). (Pubitemid 124011147)
39. Debard N, Buzoni-Gatel D, Bout D. Intranasal immunization with SAG1 protein of Toxoplasma gondii in association with cholera toxin dramatically reduces development of cerebral cysts after oral infection. Infect. Immun. 64(6), 2158-2166 (1996). (Pubitemid 26167229)
40. Bulow R, Boothroyd JC. Protection of mice from fatal Toxoplasma gondii infection by immunization with p30 antigen in liposomes. J. Immunol. 147(10), 3496-3500 (1991).
41. Petersen E, Nielsen HV, Christiansen L, Spenter J. Immunization with E. coli produced recombinant T. gondii SAG1 with alum as adjuvant protect mice against lethal infection with Toxoplasma gondii. Vaccine 16(13), 1283-1289 (1998). (Pubitemid 28308409)
42. Letscher-Bru V, Villard O, Risse B, Zauke M, Klein JP, Kien TT. Protective effect of vaccination with a combination of recombinant surface antigen 1 and IL 12 against toxoplasmosis in mice. Infect. Immun. 66(9), 4503-4506 (1998). (Pubitemid 28402732)
43. Biemans R, Grégoire D, Haumont M et al. The conformation of purified Toxoplasma gondii SAG1 antigen, secreted from engineered Pichia pastoris, is adequate for serorecognition and cell proliferation. J. Biotech. 66(2-3), 137-146 (1998). (Pubitemid 28544955)
44. Haumont M, Delhaye L, Garcia L et al. Protective immunity against congenital toxoplasmosis with recombinant SAG1 protein in a guinea pig model. Infect. Immun. 68(9), 4948-4953 (2000).
45. Chen XG, Fung MC, Ma X, Peng HJ, Shen SM, Liu GZ. Baculovirus expression of the major surface antigen of Toxoplasma gondii mice injected with the recombinant and the immune response of P30. Southeast Asian J. Trop. Med. Public Health 30(1), 42-46 (1999).
46. Darcy F, Maes P, Gras-Masse H. Protection of mice and nude rats against toxoplasmosis by a multiple antigenic peptide construction derived from Toxoplasma gondii P30 antigen. J. Immunol. 149(11), 3636-3641 (1992).
47. Godard I, Estaquier J, Zenner L et al. Antigenicity and immunogenicity of P30-derived peptides in experimental models of toxoplasmosis. Mol. Immunol. 31(17), 1353-1363 (1994). (Pubitemid 24355148)
48. Velge-Roussel F, Moretto M, Buzoni-Gatel D. Differences in immunological response to a T. gondii protein (SAG1) derived peptide between two strains of mice: eVect on protection in T. gondii infection. Mol. Immunol. 34(15), 1045-1053 (1997). (Pubitemid 28080601)
49. Caetano BC, Bruña-Romero O, Fux B, Mendes EA, Penido ML, Gazzinelli RT. Vaccination with replication-deficient recombinant adenoviruses encoding the main surface antigens of Toxoplasma gondii induces immune response and protection against infection in mice. Hum Gene Ther. 17(4), 415-426 (2006).
50. Lau YL, Fong MY. Toxoplasma gondii: serological characterization and immunogenicity of recombinant surface antigen 2 (SAG2) expressed in the yeast Pichia pastoris. Exp Parasitol. 119(3), 373-378 (2008).
51. Nielsen HV, Lauemoller SL, Christiansen L, Buus S, Fomsgaard A, Petersen E. Complete protection against lethal Toxoplasma gondii infection in mice immunized with a plasmid encoding the SAG1 gene. Infect. Immun. 67(12), 6358-6363 (1999).
52. Angus CW, Klivington-Evans D, Dubey JP, Kovacs JA. Immunization with a DNA plasmid encoding the SAG1 (P30) protein of Toxoplasma gondii is immunogenic and protective in rodents. J. Infec. Dis. 181(1), 317-324 (2000). (Pubitemid 30049063)
53. Letscher-Bru V, Pfaff AW, Abou-Bacar A et al. Vaccination with Toxoplasma gondii SAG-1 protein is protective against congenital toxoplasmosis in BALB/c mice but not in CBA/J mice. Infect. Immun. 71(11), 6615-6619 (2003). • Describes vaccination strategies with surfacen antigen 1 and indicates that the effect of vaccination with SAG1 is controlled by the genetic background of the mouse. (Pubitemid 37337722)
54. Kim JJ, Ayyavoo V, Bagarazzi ML et al. In vivo engineering of a cellular immune response by coadministration of IL-12 expression vector with a DNA immunogen. J. Immunol. 158(2), 816-826 (1997). (Pubitemid 127492659)
55. Chow YH, Chiang BL, Lee YL et al. Development of Th1 and Th2 populations and the nature of immune responses to hepatitis B virus DNA vaccines can be modulated by co-delivery of various cytokine genes. J. Immunol. 160(3), 1320-1329 (1998).
56. +T cell-mediated protective immunity against herpes simplex virus-2 challenge. J. Immunol. 162(5), 2912-2921 (1999).
57. Fachado A, Rodriguez A, Angel SO et al. Protective effect of a naked DNA vaccine cocktail against lethal toxoplasmosis in mice. Vaccine 21(13-14), 1327-1335 (2003). (Pubitemid 36266690)
58. Mévélec MN, Bout D, Desolme B et al. Evaluation of protective effect of DNA vaccination with genes encoding antigens GRA4 and SAG1 associated with GM-CSF plasmid, against acute, chronical and congenital toxoplasmosis in mice. Vaccine 23(36), 4489-4499 (2005). (Pubitemid 40967977)
59. Beghetto E, Nielsen HV, Del Porto P et al. A combination of antigenic regions of Toxoplasma gondii microneme proteins induces protective immunity against oral infection with parasite cysts. J. Infect. Dis. 191(4), 637-645 (2005). (Pubitemid 40216681)
60. Zhang J, He S, Jiang H et al. Evaluation of the immune response induced by multiantigenic DNA vaccine encoding SAG1 and ROP2 of Toxoplasma gondii and the adjuvant properties of murine IL-12 plasmid in BALB/c mice. Parasitol. Res. 101(2), 331-338 (2007). (Pubitemid 46980516)
61. Cui YL, He SY, Xue MF, Zhang J, Wang HX, Yao Y. Protective effect of a multiantigenic DNA vaccine against Toxoplasma gondii with co-delivery of IL-12 in mice. Parasite Immunol. 30(5), 309-313 (2008).
62. Xue M, He S, Zhang J, Cui Y, Yao Y, Wang H. Comparison of cholera toxin A2/B and murine IL-12 as adjuvants of Toxoplasma multi-antigenic SAG1-ROP2 DNA vaccine. Exp. Parasitol. 119(3), 352-357 (2008).
63. Xue M, He S, Cui Y, Yao Y, Wang H. Evaluation of the immune response elicited by multi-antigenic DNA vaccine expressing SAG1, ROP2 and GRA2 against Toxoplasma gondii. Parasitol. Int. 57(4), 424-429 (2008).
64. Jongert E, Verhelst D, Abady M, Petersen E, Gargano N. Protective Th1 immune responses against chronic toxoplasmosis induced by a protein-protein vaccine combination but not by its DNA-protein counterpart. Vaccine 26(41), 5289-5295 (2008). •• First report to investigate whether combined heterologous protein-DNA vaccine mixture could provide protective activity against T. gondii. It was shown that this vaccine can induce humoral and cellular immune responses to both vaccine components, and that the cellular Th1 immune response contributes to protection against toxoplasmosis.
65. Qu D, Wang S, Cai W, Du A. Protective effect of a DNA vaccine delivered in attenuated Salmonella typhimurium against Toxoplasma gondii infection in mice. Vaccine 26(35), 4541-4548 (2008).
66. Carruthers VB, Sibley LD. Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur. J. Cell. Biol. 73, 114-123 (1997). (Pubitemid 27267908)
67. Garcia JL, Gennari SM, Navarro IT et al. Partial protection against tissue cysts formation in pigs vaccinated with crude rhoptry proteins of Toxoplasma gondii. Vet. Parasitol. 129(3-4), 209-217 (2005). (Pubitemid 40544615)
68. Garcia JL, Navarro IT, Biazzono L et al. Protective activity against oocyst shedding in cats vaccinated with crude rhoptry proteins of the Toxoplasma gondii by the intranasal route. Vet. Parasitol. 145(3-4), 197-206 (2007). (Pubitemid 46436364)
69. Vercammen M, Scorza T, Huygen K et al. DNA vaccination with genes encoding Toxoplasma gondii antigens GRA1, GRA7, and ROP2 induces partially protective immunity against lethal challenge in mice. Infect. Immun. 68(1), 38-45 (2000). (Pubitemid 30016675)
70. Leyva R, Hérion P, Saavedra R. Genetic immunization with plasmid DNA coding for the ROP2 protein of Toxoplasma gondii. Parasitol. Res. 87(1), 70-79 (2001).
71. Wei QK, Li J, Fu TX et al. Studies on the immunoprotection of ROP2 nuclei acid vaccine in Toxoplasma gondii infection. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 24(5), 337-341 (2006).
72. Roque-ReséNdiz JL, Rosales R, Herion P. MVA ROP2 vaccinia virus recombinant as a vaccine candidate for toxoplasmosis. Parasitology 128(4), 397-405 (2004). (Pubitemid 38621699)
73. Mishima M, Xuan X, Yokoyama N et al. Recombinant feline herpesvirus type 1 expressing Toxoplasma gondii ROP2 antigen inducible protective immunity in cats. Parasitol. Res. 88(2), 144-149 (2002). (Pubitemid 34151142)
74. Wang H, Liu Q, Liu K et al. Immune response induced by recombinant Mycobacterium bovis BCG expressing ROP2 gene of Toxoplasma gondii. Parasitol. Int. 56(4), 263-268 (2007). (Pubitemid 47391413)
75. Martin V, Supanitsky A, Echeverria PC et al. Recombinant GRA4 or ROP2 protein combined with alum or the gra4 gene provides partial protection in chronic murine models of toxoplasmosis. Clin. Diagn. Lab. Immunol. 11(4), 704-710 (2004). (Pubitemid 38943993)
76. Echeverria PC, de Miguel N, Costas M, Angel SO. Potent antigen-specific immunity to Toxoplasma gondii in adjuvant-free vaccination system using Rop2-Leishmania infantum Hsp83 fusion protein. Vaccine 24(19), 4102-4110 (2006).
77. Soldati D, Dubremetz JF, Lebrun M. Microneme proteins: structural and functional requirements to promote adhesion and invasion by the apicomplexan parasite Toxoplasma gondii. Int. J. Parasitol. 31(12), 1293-1302 (2001). (Pubitemid 32868709)
78. Tomley FM, Soldati DS. Mix and match modules: structure and function of microneme proteins in apicomplexan parasites. Trends Parasitol. 17(2), 81-88 (2001). (Pubitemid 32416554)
79. Meissner M, Reiss M, Viebig N et al. A family of transmembrane microneme proteins of Toxoplasma gondii contain EGF-like domains and function as escorters. J. Cell Sci. 115(3), 563-574 (2002). (Pubitemid 34182983)
80. Reiss M, Viebig N, Brecht S et al. Identification and characterization of an escorter for two secretory adhesins in Toxoplasma gondii. J. Cell Biol. 152(3), 563-578 (2001). (Pubitemid 34280239)
81. Lourenço EV, Bernardes ES, Silva NM, Mineo JR, Panunto-Castelo A, Roque-Barreira MC. Immunization with MIC1 and MIC4 induces protective immunity against Toxoplasma gondii. Microbes Infect. 8(5), 1244-1251 (2006) (Pubitemid 43831688)
82. Ismael AB, Sekkai D, Collin C, Bout D, Mevelec MN. The MIC3 gene of Toxoplasma gondii is a novel potent vaccine candidate against toxoplasmosis. Infect. Immun. 71(11), 6222-6228 (2003). (Pubitemid 37337678)
83. Dautu G, Munyaka B, Carmen G et al. Toxoplasma gondii: DNA vaccination with genes encoding antigens MIC2, M2AP, AMA1 and BAG1 and evaluation of their immunogenic potential. Exp. Parasitol. 116(3), 273-282 (2007). (Pubitemid 46709897)
84. Capron A, Dessaint JP. Vaccination against parasitic diseases, some alternative concepts for the definition of protective antigens. Ann. Inst. Pasteur Immunol. 139(1), 109-117 (1988). (Pubitemid 18076350)
85. Cesbron MF, Capron A. Excreted-secreted antigens of Toxoplasma gondii: their origin and role in the host parasite interaction. Res. Immunol. 144(1), 41-44 (1993). (Pubitemid 23064900)
86. Cesbron-Delauw MF. Dense granule organelles of Toxoplasma gondii: their role in the host parasite relationship. Parasitol. Today 10(8), 293-296 (1994). (Pubitemid 2111946)
87. Hughes HP, van Knapen F. Characterisation of a secretory antigen from Toxoplasma gondii and its role in circulating antigen production. Int. J. Parasitol. 12(5), 433-437 (1982). (Pubitemid 13239478)
88. Asai T, Kim TJ, Kobayashi M, Kojima S. Detection of nucleoside triphosphate hydrolase as a circulating antigen in sera of mice infected with Toxoplasma gondii. Infect. Immun. 55(5), 1332-1335 (1987). (Pubitemid 17065694)
89. Hassl A, Aspock H. Detection and characterization of circulating antigens in acute experimental infections of mice with four different strains of Toxoplasma gondii. Zentralbl Bakteriol. 272(4), 526-534 (1990). (Pubitemid 20237670)
90. Mercier C, Adjogble KD, Daubener W, Cesbron-Delauw MF. Dense granules: are they key organelles to help understand the parasitophorous vacuole of all apicomplexa parasites? Int. J. Parasitol. 35(8), 829-849 (2005). (Pubitemid 40905201)
91. Murray A, Mercier C, Decoster A, Lecordier L, Capron A, Cesbron-Delauw MF. Multiple B-cell epitopes in a recombinant GRA2 secreted antigen of Toxoplasma gondii. Appl. Parasitol. 34(4), 235-244 (1993).
92. Golkar M, Rafati S, Taslimi Y, Taheri T, Doustdari F, Assmar M. High level expression and evaluation of the antigenicity of a recombinant Toxoplasma gondii GRA2 protein. Iranian J. Biotech. 2, 170-176 (2004).
93. Prigione I, Facchetti P, Lecordier L et al. T cell clones raised from chronically infected healthy humans by stimulation with Toxoplasma gondii excretory-secretory antigens cross-react with live tachyzoites: characterization of the fine antigenic specificity of the clones and implications for vaccine development. J. Immunol. 164(7), 3741-3748 (2000). (Pubitemid 30169830)
94. Cesbron-Delauw MF, Lecordier L, Mercier C. Role of secretory dense granule organelles in the pathogenesis of toxoplasmosis. Curr. Top. Microbiol. Immunol. 219, 59-65 (1996). (Pubitemid 26272945)
95. Zenner L, Estaquier J, Darcy F, Maes P, Capron A, Cesbron-Delauw MF. Protective immunity in the rat model of congenital toxoplasmosis and the potential of excreted-secreted antigens as vaccine components. Parasite Immunol. 21(5), 261-272 (1999). (Pubitemid 29199815)
96. Zhou H, Gu Q, Zhao Q et al. Toxoplasma gondii: expression and characterization of a recombinant protein containing SAG1 and GRA2 in Pichia pastoris. Parasitol. Res. 100(4), 829-835 (2007). (Pubitemid 46175250)
97. Ferrandiz J, Mercier C, Wallon M, Picot S, Cesbron-Delauw MF, Peyron F. Limited value of assays using detection of immunoglobulin G antibodies to the two recombinant dense granule antigens, GRA1 and GRA6 Nt of Toxoplasma gondii, for distinguishing between acute and chronic infections in pregnant women. Clin. Diagn. Lab. Immunol. 11(6), 1016-1021 (2004). (Pubitemid 39540837)
98. Peyron F, Lobry JR, Musset K et al. Serotyping of Toxoplasma gondii in chronically infected pregnant women: predominance of type II in Europe and types I and III in Colombia (South America). Microbes Infect. 8 (9-10), 2333-2340 (2006). (Pubitemid 44499053)
99. Gatkowska J, Hiszczynska-Sawicka E, Kur J, Holec L, Dlugonska H. Toxoplasma gondii: an evaluation of diagnostic value of recombinant antigens in a murine model. Exp. Parasitol. 114(3), 220-227 (2006). (Pubitemid 44547930)
100. Golkar M, Shokrgozar MA, Rafati S et al. Evaluation of protective effect of recombinant dense granule antigens GRA2 and GRA6 formulated in monophosphoryl lipid A (MPL) adjuvant against Toxoplasma chronic infection in mice. Vaccine 25(21), 4301-4311 (2007). (Pubitemid 46646961)
101. Zhang G, Huong VT, Battur B et al. A heterologous prime-boost vaccination regime using DNA and a vaccinia virus, both expressing GRA4, induced protective immunity against Toxoplasma gondii infection in mice. Parasitology 134(10), 1339-1346 (2007). (Pubitemid 47236810)
102. Di Cristina M, Del Porto P, Buffolano W et al. The Toxoplasma gondii bradyzoite antigens BAG1 and MAG1 induce early humoral and cell-mediated immune responses upon human infection. Microbes Infect. 6(2), 164-171 (2004). (Pubitemid 38293293)
103. Bohne W, Gross U, Ferguson DJ, Heesemann J. Cloning and characterization of a bradyzoite-specifically expressed gene (hsp30/bag1) of Toxoplasma gondii, related to genes encoding small heat-shock proteins of plants. Mol. Microbiol. 16(6), 1221-1230 (1995).
104. Parmley SF, Weiss LM, Yang S. Cloning of a bradyzoite-speciffic gene of Toxoplasma gondii encoding a cytoplasmic antigen. Mol. Biochem. Parasitol. 73 (1-2), 253-257 (1995).
105. Parmley SF, Yang S, Harth G, Sibley LD, Sucharczuk A, Remington JS. Molecular characterization of a 65-kilodalton Toxoplasma gondii antigen expressed abundantly in the matrix of tissue cysts. Mol. Biochem. Parasitol. 66(2), 283-296 (1994). (Pubitemid 24272075)
106. Mun HS, Aosai F, Yano A. Role of Toxoplasma gondii HSP70 and Toxoplasma gondii HSP30/bag1 in antibody formation and prophylactic immunity in mice experimentally infected with Toxoplasma gondii. Microbiol. Immunol. 43(5), 471-479 (1999). (Pubitemid 29250005)
107. Parmley SF, Slifer T, Araujo F. Protective effects of immunization with a recombinant cyst antigen in mouse models of infection with Toxoplasma gondii tissue cysts. J. Infect. Dis. 185(l), 90-95 (2002). (Pubitemid 34142834)
108. Nielsen HV, Di Cristina M, Beghetto E, Spadoni A, Petersen E, Gargano N. Toxoplasma gondii: DNA vaccination with bradyzoite antigens induces protective immunity in mice against oral infection with parasite cysts. Exp. Parasitol. 112, 274-279 (2006).
109. Lundén A, Lövgren K, Uggla A, Araujo FG. Immune responses and resistance to Toxoplasma gondii in mice immunized with antigens of the parasite incorporated into immunostimulating complexes. Infect. Immun. 61(6), 2639-2643 (1993). (Pubitemid 23159261)
110. Stanley AC, Buxton D, Innes EA, Huntley JF. Intranasal immunisation with Toxoplasma gondii tachyzoite antigen encapsulated into PLG microspheres induces humoral and cell-mediated immunity in sheep. Vaccine 22(29-30), 3929-3941 (2004). (Pubitemid 39208755)
111. Costa-Silva TA, Meira CS, Ferreira IM, Hiramoto RM, Pereira-Chioccola VL. Evaluation of immunization with tachyzoite excreted-secreted proteins in a novel susceptible mouse model (A/Sn) for Toxoplasma gondii. Exp. Parasitol. 120(3), 227-234 (2008).
112. Chen G, Chen H, Guo H, Zheng H. Protective effect of DNA-mediated immunization with a combination of SAG1 and IL-2 gene adjuvant against infection of Toxoplasma gondii in mice. Chin. Med. J. (Engl.) 115(10), 1448-1452 (2002). (Pubitemid 35282898)
113. Lundén A, Parmley SF, Bengtsson KL, Araujo FG. Use of a recombinant antigen, SAG2, expressed as a glutathione-S-transferase fusion protein to immunize mice against Toxoplasma gondii. Parasitol. Res. 83(1), 6-9 (1997). (Pubitemid 26396341)
114. Yang CD, Chang GN, Chao D. Protective immunity against Toxoplasma gondii in mice induced by a chimeric protein rSAG1/2. Parasitol Res. 92(1), 58-64 (2004). (Pubitemid 38167940)
115. Lee YH, Shin DW, Lee JH, Nam HW, Ahn MH. Vaccination against murine toxoplasmosis using recombinant Toxoplasma gondii SAG3 antigen alone or in combination with Quil A. Yonsei Med. J. 48(3), 396-404 (2007).
116. Chen H, Chen G, Zheng H, Guo H. Induction of immune responses in mice by vaccination with liposome-entrapped DNA complexes encoding Toxoplasma gondii SAG1 and ROP1 genes. Chin. Med. J. (Engl.) 116(10), 1561-1566 (2003). (Pubitemid 37461680)
117. Jongert E, Melkebeek V, De Craeye S, Dewit J, Verhelst D, Cox E. An enhanced GRA1-GRA7 cocktail DNA vaccine primes anti-Toxoplasma immune responses in pigs. Vaccine 26(8), 1025-1031 (2008). • Describes DNA vaccination against T. gondii in pigs. The results indicate that pigs can be efficiently primed against T. gondii infection by means of a DNA vaccine. It was demonstrated that administration of a cocktail DNA vaccine is able to elicit humoral and cellular immune responses against T. gondii in pigs. It is therefore possible that the enhanced type 1 responses observed in these animals could protect against the acute phase of infection.
118. Jongert E, de Craeye S, Dewit J, Huygen K. GRA7 provides protective immunity in cocktail DNA vaccines against Toxoplasma gondii. Parasite Immunol. 29(9), 445-453 (2007). (Pubitemid 47313228)
119. Igarashi M, Kano F, Tamekuni K. Toxoplasma gondii: cloning, sequencing, expression, and antigenic characterization of ROP2, GRA5 and GRA7. Genet. Mol. Res. 7(2), 305-313 (2008).
120. Guo H, Chen G, Lu F, Chen H, Zheng H. Immunity induced by DNA vaccine of plasmid encoding the rhoptry protein 1 gene combined with the genetic adjuvant of pcIFN-g against Toxoplasma gondii in mice. Chin. Med. J. (Engl.) 114(3), 317-320 (2001). (Pubitemid 32231950)
121. Chen G, Guo H, Lu F, Zheng H. Construction of a recombinant plasmid harbouring the rhoptry protein 1 gene of Toxoplasma gondii and preliminary observations on DNA immunity. Chin. Med. J. (Engl.) 114(8), 837-840 (2001). (Pubitemid 32834942)
122. + T cells to control acute Toxoplasma gondii infection. Infect. Immun. 71(1), 309-316 (2003).
123. Bivas-Benita M, Laloup M, Versteyhe S et al. Generation of Toxoplasma gondii GRA1 protein and DNA vaccine loaded chitosan particles: preparation, characterization, and preliminary in vivo studies. Int. J. Pharm. 266(1-2), 17-27 (2003). (Pubitemid 37249304)
124. Desolme B, Mévélec MN, Buzoni-Gatel D, Bout D. Induction of protective immunity against toxoplasmosis in mice by DNA immunization with a plasmid encoding Toxoplasma gondii GRA4 gene. Vaccine 18(23), 2512-2521 (2000). (Pubitemid 30207036)