Vaccines against Toxoplasma gondii: New developments and perspectives

Expert Review of Vaccines

Volumn 12, Issue 11, 2013, Pages 1287-1299

  Zhang, Nian Zhang ^a   Chen, Jia ^a   Wang, Meng ^a   Petersen, Eskild ^b   Zhu, Xing Quan ^a,c  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b AARHUS UNIVERSITY   (Denmark)

^c HEILONGJIANG BAYI AGRICULTURAL UNIVERSITY   (China)

Author keywords

cat; food animal; mice; Toxoplasma gondii; toxoplasmosis; vaccines

Indexed keywords

ADENOVIRUS VECTOR; BCG VACCINE; DNA VACCINE; EPITOPE; INACTIVATED VACCINE; INTERLEUKIN 15; INTERLEUKIN 18; INTERLEUKIN 2; INTERLEUKIN 21; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 7; LIVE VACCINE; PEPTIDE VACCINE; QUIL A; RECOMBINANT PROTEIN; RECOMBINANT VACCINE; SUBUNIT VACCINE; TOXOPLASMA GONDII VACCINE; VIRUS VECTOR;

ABORTION; ANIMAL PRODUCT; BRAIN CYST; CAT; CELLULAR IMMUNITY; EXPERIMENTAL STUDY; HOST; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOGENICITY; MEDICAL RESEARCH; NONHUMAN; PLASMID; PRIORITY JOURNAL; REVIEW; SHEEP; T LYMPHOCYTE; TOXOPLASMOSIS; VACCINATION;

ANIMALS; ANIMALS, DOMESTIC; CAT DISEASES; CATS; DRUG DISCOVERY; HUMANS; PROTOZOAN VACCINES; TOXOPLASMA; TOXOPLASMOSIS; TOXOPLASMOSIS, ANIMAL;

EID: 84887387971     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/14760584.2013.844652     Document Type: Review

References (113)

1. Petersen E, Kijlstra A, Stanford M. Epidemiology of ocular toxoplasmosis. Ocul. Immunol. Inflamm. 20(2), 68-75 (2012
2. Dubey JP. Toxoplasmosis of animals and humans. CRC Press, FL, USA (2010
3. Weiss LM, Kim K. Toxoplasma gondii. The model Apicomplexan: Perspective sand methods. Academic Press, London, UK (2007
4. Robert-Gangneux F, Darde ML. Epidemiology of and diagnostic strategies for toxoplasmosis. Clin. Microbiol. Rev. 25(2), 264-296 (2012
5. Jones JL, Hanson DL, Dworkin MS et al. Surveillance for AIDS-defining opportunistic illnesses, 1992-1997. MMWR Morb. Mortal. Wkly. Rep. 48(2), 1-22 (1999
6. Buxton D, Innes EA. A commercial vaccine for ovine toxoplasmosis. Parasitology 110, 11-16 (1995
7. Buxton D. Protozoan infections (Toxoplasma gondii, Neopora caninum and Sarcocystis spp.) in sheep and goat: Recent advances. Vet. Res. 29(3-4), 289-310 (1998
8. Coombs GH, Muller S. Recent advances in the search for new anti-coccidial drugs. Int. J. Parasitol. 32(5), 497-508 (2002
9. Innes EA. Vaccination against Toxoplasma gondii: An increasing priority for collaborative research? Expert Rev. Vaccines 9(10), 1117-1119 (2010
10. Vercruysse J, Knox DP, Schetters TP, Willadsen P. Veterinary parasitic vaccines: Pitfalls and future directions. Trends Parasitol. 20(10), 488-492 (2004
11. Kijlstra A, Jongert E. Control of the risk of human toxoplasmosis transmitted by meat. Int. J. Parasitol. 38(12), 1359-1370 (2008
12. Liu Q, Wei F, Gao S et al. Toxoplasma gondii infection in pregnant women in China. Trans. R. Soc. Trop. Med. Hyg. 103(2), 162-166 (2009
13. Dorny P, Praet N, Deckers N, Gabriel S. Emerging food-borne parasites. Vet. Parasitol. 163(3), 196-206 (2009
14. Tenter AM, Heckeroth AR, Weiss, LM. Toxoplasma gondii: From animals to humans. Int. J. Parasitol. 30(12-13), 1217-1258 (2000
15. Cook AJC, Gilbert RE, Buffolano W et al. Sources of Toxoplasma infection in pregnant women: European multicenter case-control study. BM J. 321(7254), 142-147 (2000
16. Cenci-Goga BT, Rossitto PV, Sechi P, McCrindle CM, Cullor JS. Toxoplasma in animals, food, and humans: An old parasite of new concern. Foodborne Pathog. Dis. 8(7), 751-762 (2011
17. Hill D, Dubey, JP. Toxoplasma gondii: Transmission, diagnosis and prevention. Clin. Microbiol. Infect. 8(10), 634-640 (2002
18. Zhou P, Chen ZG, Li HL et al. Toxoplasma gondii infection in humans in China. Parasit Vectors 4, 165 (2011
19. Dubey JP, Lago EG, Gennari SM, Su C, Jones JL. Toxoplasmosis in humans and animals in Brazil: High prevalence, high burden of disease, and epidemiology. Parasitology 139(11), 1375-1424 (2012
20. Innes EA, Vermeulen AN. Vaccination as a control strategy against the coccidial parasites Eimeria, Toxoplasma and Neospora. Parasitology 133, S145-S168 (2006
21. Kur J, Holec-Gasior L, ńiszczyska-Sawicka. Current status of toxoplasmosis vaccine development. Expert. Rev. Vaccines 8(6), 791-808 (2009
22. Innes EA, Bartley PM, Maley S, Katzer F, Buxton D. Veterinary vaccines against Toxoplasma gondii. Mem. Inst. Oswaldo. Cruz. 104(2), 246-251 (2009
23. Garcia JL. Vaccination concepts against Toxoplasma gondii. Expert. Rev. Vaccines 8(2), 215-225 (2009
24. Jongert E, Roberts CW, Gargano N, Förster-WaldI E, Petersen E. Vaccines against Toxoplasma gondii: Challenges and opportunities. Mem. Inst. Oswaldo. Cruz. 104(2), 252-266 (2009
25. 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
26. Freyre A, Choromanski L, Fishback JL, Popiel I. Immunization of cats with tissue cysts, bradyzoites, and tachyzoites of the T-263 strain of Toxoplasma gondii. J. Parasitol. 79(5), 716-719 (1993
27. Omata Y, Aihara Y, Kanda M, Saito A, Igarashi I, Suzuki N. Toxoplasma gondii: Experimental infection in cats vaccine with 60Co-irradiated tachyzoites. Vet. Parasitol. 65(3-4), 173-183 (1996
28. 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
29. Garcia JL, Navarro IT, Biazzono L et al. Protective activity against oocysts shedding in cats vaccinated with crude rhoptry proteins of the Toxoplasma gondii by the intranasal route. Vet. Parasitol. 145(3-4), 197-206 (2007
30. Zulpo DL, Headley SA, Biazzono L et al. Oocyst shedding in cats vaccinated by the nasal and rectal routes with crude rhoptry proteins of Toxoplasma gondii. Exp. Parasitol. 131(2), 223-230 (2012
31. Samra NA, McCrindle CM, Penzhorn BL, Cenci-Goga BT. Seroprevalence of toxoplasmosis in sheep in South Africa. J. S. Afr. Vet. Assoc. 78(3), 116-120 (2007
32. Dubey JP, Jones JL. Toxoplasma gondii infection in humans and animals in the United States. Int. J. Parasitol. 38(11), 1257-1278 (2008
33. Gao XJ, Zhao ZJ, He ZH et al. Toxoplasma gondii infection in pregnant women in China. Parasitology 139(2), 139-147 (2012
34. Roghmann MC, Faulkner CT, Lefkowitz A, Patton S, Zimmerman J, Morris JG. Decreased seroprevalence for Toxoplasma gondii in Seventh Day Adventists in Maryland. Am. J. Trop. Med. Hyg. 60(5), 790-792 (1999
35. Hiszczyńska-Sawicka E, Li H, Boyu Xu J et al. Induction of immune responses in sheep by vaccination with liposome-entrapped DNA complexes encoding Toxoplasma gondii MIC3 gene. Pol. J. Vet. Sci. 15(1), 3-9 (2012
36. Hiszczynska-Sawickaa E, Oledzka G, Holec-Gasiorc L et al. Evaluation of immune responses in sheep induced by DNA immunization with genes encoding GRA1, GRA4, GRA6 and GRA7 antigens of Toxoplasma gondii. Vet. Parasitol. 177(3-4), 281-289 (2011
37. Hiszczyńska-Sawickaa E, Xu JB, Oledzka G, Kur J, Bickerstaffe R, Stankiewicz M. Comparison of immune response in sheep immunized with DNA vaccine encoding Toxoplasma gondii GRA7 antigen in different adjuvant formulations. Exp. Parasitol. 124(4), 365-372 (2010
38. Hiszczyńska-Sawickaa E, Akhtar M, Kay GW et al. The immune responses of sheep after DNA immunization with, Toxoplasma gondii MAG1 antigen-with and without co-expression of ovine interleukin 6. Vet. Immunol. Immunop. 136(3-4), 324-329 (2010
39. Hiszczyńska-Sawickaa E, Li H, Xu JB et al. Modulation of immune response to Toxoplasma gondii in sheep by immunization with a DNA vaccine encoding ROP1 antigen as a fusion protein with ovine CD154. Vet. Parasitol. 183(1-2), 72-78 (2011
40. Li B, Oledzka G, Mcfarlane RG et al. Immunological response of sheep to injection of plasmids encoding Toxoplasma gondii SAG1 and ROP1 genes. Parasit. Immunol. 32(9-10), 671-683 (2010
41. Falcon J, Freyre A. Toxoplasma gondii: Prototype immunization of lambs against formation of muscle and brain cysts. Vet. Parasitol. 166(1-2), 15-20 (2009
42. 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
43. da Cunha IAL, Zulpo DL, Bogado ALG et al. Humoral and cellular immune responses in pigs immunized intranasally with crude rhoptry proteins of Toxoplasma gondii plus Quil-A. Vet. Parasitol. 186(3-4), 216-221 (2012
44. 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
45. Freire RL, Navarro IT, Bracarense APFRL, Gennari SM. Vaccination of pigs with Toxoplasma gondii antigens incorporated in immunostimulating complexes (ISCOM). Arq. Bras. Med. Vet. Zootec. 55(4), 388-396 (2003
46. Mevelec MN, Ducournau C, Ismael AB et al. Mic1-3 knockout Toxoplasma gondii is a good candidate for a vaccine against T. gondii-induced abortion in sheep. Vet. Res. 41(4), 49 (2010
47. Gazzinelli R, Xu Y, Hieny S, Cheever A, Sher A. Simultaneous depletion of CD4+ and CD8+ T lymphocytes is required to reactivate chronic infection with Toxoplasma gondii. J. Immunol. 149(1), 175-180 (1992
48. Wang Y, Wang M, Wang G et al. Increased survival time in mice vaccinated with a branched lysine multiple antigenic peptide containing B-And T-cell epitopes from T. gondii antigens. Vaccine 29(47), 8619-8623 (2011
49. Henriquez FL, Woods S, Cong H, McLeod R, Roberts CW. Immunogenetics of Toxoplasma gondii informs vaccine design. Trends Parasitol. 26(11), 550-555 (2010
50. Blanchard N, Gonzalez F, Schaeffer M et al. Immunodominant, protective response to the parasite Toxoplasma gondii requires antigen processing in the endoplasmic reticulum. Nat. Immunol. 9(8), 937-944 (2008
51. Tan TG, Mui E, Cong H et al. Identification of T. gondii epitopes, adjuvants, and host genetic factors that influence protection of mice and humans. Vaccine 28(23), 3977-3989 (2010
52. Cong H, Mui EJ, Witola WH et al Towards an immunosense vaccine to prevent toxoplasmosis: Protective Toxoplasma gondii eptopes restricted by HLA-A&z.ast;0201. Vaccine 29(4), 754-762 (2011
53. Cong H, Mui EJ, Witola WH et al. Toxoplasma gondii HLA-B&z.ast;0702- restricted GRA720-28 peptide with adjuvants and a universal helper T cell epitope elicits CD8+ T cells producing interferon-g and reduces parasite burden in HLA-B&z.ast;0702 mice. Hum. Immunol. 73(1), 1-10 (2012
54. Behnke MS, Fentress SJ, Mashayekhi M, Li LX, Taylor GA, Sibley LD. The polymorphic pseudokinase ROP5 controls virulence in Toxoplasma gondii by regulating the active kinase ROP18. PLoS Pathog. 8(11), e1002992 (2012
55. Fleckenstein MC, Reese ML, Könen-Waisman S, Boothroyd JC, Howard JC, Steinfeldt T. A Toxoplasma gondii pseudokinase inhibits host IRG resistance proteins. PLoS Biol. 10(7), e1001358 (2012
56. Niedelman W, Gold DA, Rosowski EE et al. The rhoptry proteins ROP18 and ROP5 mediate Toxoplasma gondii evasion of the murine, but not the human, interferon-gamma response. PLoS Pathog. 8(6), e1002784 (2012
57. Yuan ZG, Zhang XX, Lin RQ et al Protective effect against toxoplasmosis in mice induced by DNA immunization with gene encoding Toxoplasma gondii ROP18. Vaccine 29(38), 6614-6619 (2011
58. Jain S, O'Hagan DT, Singh M. The long-Term potential of biodegradable poly (lactide-co-glycolide) microparticles as the next-generation vaccine adjuvant. Expert. Rev. Vaccine 10(12), 1731-1742 (2011
59. Chuang SC, Ko, JC, Chen CP, Du JT, Yang CD. Induction of long-lasting protective immunity against Toxoplasma gondii in BALB/c mice by recombinant surface antigen 1 protein encapsulated in poly (lactide-co-glycolide) microparticles Parasit. Vectors 6, 34 (2013
60. Min J, Qu D, Li C et al. Enhancement of protective immune responses induced by Toxoplasma gondii dense granule antigen 7 (GRA7) against toxoplasmosis in mice using a prime-boost vaccination strategy. Vaccine 30(38), 5631-5636 (2012
61. Beghetto E, Nielsen HV, Porto PD 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
62. Jongert E, Lemiere A, Ginderachter JV, Craeye SD, Huygen K, D'Souza S. Functional characterization of in vivo effector CD4+ and CD8+ T cell responses in acute toxoplasmosis: An interplay of IFN-g and cytolytic T cells. Vaccine 28(13), 2556-2564 (2010
63. Hoseinian Khosroshahi K, Ghaffarifar F, D'Souza S, Sharifi Z, Dalimi A. Evaluation of the immune response induced by DNA vaccine cocktail expressing complete SAG1 and ROP2 genes against toxoplasmosis. Vaccine 29(4), 778-783 (2011
64. Fang R, Feng H, Hu M et al. Evaluation of immune responses induced by SAG1 and MIC3 vaccine cocktails against Toxoplasma gondii. Vet. Parasitol. 187(1-2), 140-146 (2012
65. Wang H, He S, Yao Y et al. Toxoplasma gondii: Protective effect of an intranasal SAG1 and MIC4 DNA vaccine in mice. Exp. Parasitol. 122(3), 226-232 (2009
66. Reyes-Sandoval A, Harty JT, Todryk SM. Viral vector vaccines make memory T cells against malaria. Immunology 121(2), 158-165 (2007
67. Mendes EA, Caetano BC, Penidoa MLO, Bruna-Romero O, Gazzinelli RT. MyD88-dependent protective immunity elicited by adenovirus 5 expressing the surface antigen 1 from Toxoplasma gondii is mediated by CD8+ T lymphocytes. Vaccine 29(27), 4476-4484 (2011
68. Machado AV, Caetano BC, Barbosa RP et al. Prime and boost immunization with influenza and adenovirus encoding the Toxoplasma gondii surface antigen 2 (SAG2) induces strong protective immunity. Vaccine 28(18), 3247-3256 (2010
69. Yu LZ, Yamagishi JY, Zhang SF et al. Protective effect of a prime-boost strategy with plasmid DNA followed by recombinant adenovirus expressing TgAMA1 as vaccines against Toxoplasma gondii infection in mice. Parasitol. Int. 61(3), 481-486 (2012
70. Nie H, Fang R, Xiong BQ et al. Immunogenicity and protective efficacy of two recombinant pseudorabies viruses expressing Toxoplasma gondii SAG1 and MIC3 proteins. Vet. Parasitol. 181(2-4), 215-221 (2011
71. Zhang G, Huang X, Boldbaatar D et al. Construction of Neospora caninum stably expressing TgSAG1 and evaluation of its protective effects against Toxoplasma gondii infection in mice. Vaccine 28(45), 7243-7247 (2010
72. Becher ML, Martin V, Kraemer M et al. Effect of codon optimization and subcellular targeting on Toxoplasma gondii antigen SAG1 expression in tobacco leaves to use in subcutaneous and oral immunization in mice. BMC. Biotechnol. 10, 52 (2010
73. Yacono ML, Farran I, Becher ML et al. A chloroplast-derived Toxoplasma gondii GRA4 antigen used as an oral vaccine protects against toxoplasmosis in mice. Plant Biotechnol. J. 10(9), 1136-1144 (2012
74. 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
75. Cui YL, He SY, Xue MF, Zhang J, Wang H, Yao Y. Protective effect of a multiantigenic DNA vaccine against Toxoplasma gondii with co-delivery of IL-12 in mice. Parasit. Immunol. 30(5), 309-313 (2008
76. Wei XQ, Leung BP, Niedbala W et al. Altered immune responses and susceptibility to Leishmania major and Staphylococcus aureus infection in IL-18-deficient mice. J. Immunol. 163(5), 2821-2828 (1999
77. Liu Q, Shang L, Jin H, Wei F, Zhu XQ, Gao H. The protective effect of a Toxoplasma gondii SAG1 plasmid DNA vaccine in mice is enhanced with IL-18. Res. Vet. Sci. 89(1), 93-97 (2010
78. Yan HK, Yuan ZG, Petersen E et al. Toxoplasma gondii: Protective immunity against experimental toxoplasmosis induced by a DNA vaccine encoding the perforin-like protein 1. Exp. Parasitol. 128(1), 38-43 (2011
79. Wang PY, Yuan ZG, Petersen E et al. Protective efficacy of a Toxoplasma gondii Rhoptry protein 13 plasmid DNA vaccine in mice. Clin. Vaccine Immunol. 19(12), 1916-1920 (2012
80. Grover HS, Blanchard N, Gonzalez F, Chan S, Robey EA, Shastri N. The Toxoplasma gondii peptide AS15 elicits CD4 T cells that can control parasite burden. Infect. Immun. 80(9), 3279-3288 (2012
81. Sanchez-Pla A, Reverter F, de Villa MCR, Comabella M. Transcriptomics: MRNA and alternative splicing. J. Neuroimmunol. 248(1-2), 23-31 (2012
82. Eissa MM, El-Azzouni MZ, Mady RF, Fathy FM, Baddour NM. Initial characterization of an autoclaved Toxoplasma vaccine in mice. Exp. Parasitol. 131(3), 310-316 (2012
83. Zorgi NE, Costa A, Junior AJG, do Nascimento N, Juniora HFA. Humoral responses and immune protection in mice immunized with irradiated T. gondii tachyzoites and challenged with three genetically distinct strains of T. gondii. Immunol. Lett. 138(2), 187-196 (2011
84. Gigley JP, Fox BA, Bzik DJ. Long-Term immunity to lethal acute or chronic Type II Toxoplasma gondii infection is effectively induced in genetically susceptible C57BL/6 mice by immunization with an attenuated Type I vaccine strain. Infect. Immun. 77(12), 5380-5388 (2009
85. Yang X, Huang S, Chen J et al. Evaluation of the adjuvant properties of Astragalus membranaceus and Scutellaria baicalensis GEORGI in the immune protection induced by UV-Attenuated Toxoplasma gondii in mouse models. Vaccine 28(3), 737-743 (2010
86. Cui X, Lei T, Yang D, Hao P, Li B, Liu Q. Toxoplasma gondii immune mapped protein-1 (TgIMP1) is a novel vaccine candidate against toxoplasmosis. Vaccine 30(13), 2282-2287 (2012
87. Li J, Han Q, Gong P et al. Toxoplasma gondii rhomboid protein 1 (TgROM1) is a potential vaccine candidate against toxoplasmosis. Vet. Parasitol. 184(2-4), 154-160 (2012
88. Li J, Huang X, Zhang G, Gong P, Zhang X, Wu L. Immune response and protective efficacy against homologous challenge in BALB/c mice vaccinated with DNA vaccine encoding Toxoplasma gondii actin depolymerizing factor gene. Vet. Parasitol. 179(1-3), 1-6 (2011
89. Makino M, Uemura N, Moroda M et al. Innate immunity in DNA vaccine with Toxoplasma gondii-heat shock protein 70 gene that induces DC activation and Th1 polarization. Vaccine 29(10), 1899-1905 (2011
90. Kikumura A, Fang H, Mun HS et al. Protective immunity against lethal anaphylactic reaction in Toxoplasma gondiiinfected mice by DNA vaccination with T. gondii-derived heat shock protein 70 gene. Parasitol. Int. 59(2), 105-111 (2010
91. Yuan ZG, Zhang XX, He XH et al. Protective immunity induced by Toxoplasma gondii Rhoptry protein 16 against toxoplasmosis in mice. Clin. Vaccine Immunol. 18(1), 119-124 (2011
92. Peng GH, Yuan ZG, Zhou DH et al. Toxoplasma gondii microneme protein 6 (MIC6) is a potential vaccine candidate against toxoplasmosis in mice. Vaccine 27(47), 6570-6574 (2009
93. Liu MM, Yuan ZG, Peng GH et al. Toxoplasma gondii microneme protein 8 (MIC8) is a potential vaccine candidate against toxoplasmosis. Parasitol. Res. 106(5), 1079-1084 (2010
94. Fang R, Nie H, Wang Z et al. Protective immune response in BALB/c mice induced by a suicidal DNA vaccine of the MIC3 gene of Toxoplasma gondii. Vet. Parasitol. 164(2-4), 134-140 (2009
95. Ismael AB, Hedhli D, Cérède O, Lebrun M, Dimier-Poisson I, Mévélec M. Further analysis of protection induced by the MIC3 DNA vaccine against T. gondii: CD4 and CD8 T cells are the major effectors of the MIC3 DNA vaccine-induced protection, both Lectin-like and EGF-like domains of MIC3 conferred protection. Vaccine 27(22), 2959-2966 (2009
96. Gong P, Huang X, Yu Q et al. The protective effect of a DNA vaccine encoding the Toxoplasma gondii cyclophilin gene in BALB/c mice. Parasit. Immunol. 35(3-4), 140-146 (2013
97. Sun XM, Zou J, Elashram SAA et al. DNA vaccination with a gene encoding Toxoplasma gondii GRA6 induces partial protection against toxoplasmosis in BALB/c mice. Parasit. Vectors 4, 213 (2011
98. Meng M, He S, Zhao G et al. Evaluation of protective immune responses induced by DNA vaccines encoding Toxoplasma gondii surface antigen 1 (SAG1) and 14-3-3 protein in BALB/c mice. Parasit. Vectors 5, 273 (2012
99. Wu XN, Lin J, Lin X, Chen J, Chen ZL, Lin JY. Multicomponent DNA vaccine-encoding Toxoplasma gondii GRA1 and SAG1 primes: Anti-Toxoplasma immune response in mice. Parasitol. Res. 111(5), 2001-2009 (2012
100. Zhou H, Min J, Zhao Q et al. Protective immune response against Toxoplasma gondii elicited by a recombinant DNA vaccine with a novel genetic adjuvant. Vaccine 30(10), 1800-1806 (2012
101. Rosenberg C, Craeye SD, Jongert E et al. Induction of partial protection against infection with Toxoplasma gondii genotype II by DNA vaccination with recombinant chimeric tachyzoite antigens. Vaccine 27(18), 2489-2498 (2009
102. Dziadek B, Gatkowska J, Brzostek A et al. Evaluation of three recombinant multi-Antigenic vaccines composed of surface and secretory antigens of Toxoplasma gondii in murine models of experimental toxoplasmosis. Vaccine 29(4), 821-830 (2011
103. Dziadek B, Gatkowska J, Grzybowski M, Dziadek J, Dzitko K, Dlugonsk H. Toxoplasma gondii: The vaccine potential of three trivalent antigen-cocktails composed of recombinant ROP2, ROP4, GRA4 and SAG1 proteins against chronic toxoplasmosis in BALB/c mice. Exp. Parasitol. 131(1), 133-138 (2012
104. Sanchez VR, Pitkowski MN, Cuppari AVF et al. Combination of CpG-oligodeoxynucleotides with recombinant ROP2 or GRA4 proteins induces protective immunity against Toxoplasma gondii infection. Exp. Parasitol. 128(4), 448-453 (2011
105. Yan HK, Yan H, Tao Y et al. Application and expression of Toxoplasma gondii surface antigen 2 (SAG2) and rhoptry protein 2 (ROP2) from recombinant Escherichia coli strain. Trans. Roy. Soc. Trop. Med. Hyg. 106(6), 356-362 (2012
106. Lau YL, Thiruvengadam G, Lee WW, Fong MY. Immunogenic characterization of the chimeric surface antigen 1 and 2 (SAG1/2) of Toxoplasma gondii expressed in the yeast Pichia pastoris. Parasitol. Res. 109(3), 871-878 (2011
107. Huang X, Li J, Zhang G, Gong P, Yang J, Zhang X. Toxoplasma gondii: Protective immunity against toxoplasmosis with recombinant actin depolymerizing factor protein in BALB/c mice. Exp. Parasitol. 130(3), 218-222 (2012
108. Qua DF, Yu HJ, Liu Z et al. Ginsenoside Rg1 enhances immune response induced by recombinant Toxoplasma gondii SAG1 antigen. Vet. Parasitol. 179(1-3), 28-34 (2011
109. Tan F, Hu X, Luo FJ, Pan CW, Chen XG Induction of protective Th1 immune responses in mice by vaccination with recombinant Toxoplasma gondii nucleoside triphosphate hydrolase-II. Vaccine 29(15), 2742-2748 (2011
110. Azzouz S, Maache M, Osuna A, Lawton P, Petavy AF. Toxoplasma gondii: Identification and immune response against a group of proteins involved in cellular invasion. Exp. Parasitol. 130(1), 63-68 (2012
111. Hedhli D, Dimier-Poisson I, Judge JW, Rosenberg B, Mévélec MN. Protective immunity against Toxoplasma challenge in mice by coadministration of T. gondii antigens and Eimeria profilin-like protein as an adjuvant. Vaccine 27(16), 2274-2281 (2009
112. Li WS, Chen QX, Ye JX et al. Comparative evaluation of immunization with recombinant protein and plasmid DNA vaccines of fusion antigen ROP2 and SAG1 from Toxoplasma gondii in mice: Cellular and humoral immune responses. Parasitol. Res. 109(3), 637-644 (2011
113. Shang L, Liu Q, Liu W et al. Protection in mice immunized with a heterologous prime-boost regime using DNA and recombinant pseudorabies expressing TgSAG1 against Toxoplasma gondii challenge. Vaccine 27(21), 2741-2745 (2009