Abstract
Toxoplasmosis is a worldwide-distributed infection caused by Toxoplasma gondii, which causes a wide range of clinical syndromes in humans, mammals and birds. T. gondii is considered a parasite of veterinary and medical importance, because it may cause abortion or congenital disease in its intermediate hosts. Despite the economic losses associated with T. gondii infection in farm animals and the socio-economic impact caused by this zoonotic disease in the human population, there is no effective treatment available for humans or animals able to eliminate the parasite from the host once the chronic infection has been established. The only commercial vaccine is the S48 strain of attenuated tachyzoites for use in sheep. However, this vaccine causes side effects, has a short life time and induces a short-term immunity. So far, no acellular vaccine against toxoplasmosis has been commercialized. In fact, future challenges include the development of an effective vaccine to prevent toxoplasmosis. Most parasitologists and vaccinologists agree that future efforts should be concentrated on developing multi-antigen vaccines and more efficient delivery systems able to express heterologous proteins abundantly as well as on searching for immunization schedules and adequate adjuvants to enhance the protective responses. To achieve this, platforms for the production of acellular vaccines based on the use of plants can have an important role.
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References
Ahmad P, Ashraf M, Younis M et al (2012) Role of transgenic plants in agriculture and biopharming. Biotechnol Adv 30(3):524–540. https://doi.org/10.1016/j.biotechadv.2011.09.006
Albarracín RM, Becher ML, Farran I et al (2015) The fusion of Toxoplasma gondii SAG1 vaccine candidate to Leishmania infantum heat shock protein 83-kDa improves expression levels in tobacco chloroplasts. Biotechnol J 10(5):748–759. https://doi.org/10.1002/biot.201400742
Altcheh J, Diaz NS, Pepe CM et al (2006) Kinetic analysis of the humoral immune response against 3 Toxoplasma gondii-recombinant proteins in infants with suspected congenital toxoplasmosis. Diagn Microbiol Infect Dis 56(2):161–165
Alves CM, Silva DA, Azzolini AE et al (2013) Galectin-3 is essential for reactive oxygen species production by peritoneal neutrophils from mice infected with a virulent strain of Toxoplasma gondii. Parasitology 140(2):210–219. https://doi.org/10.1017/S0031182012001473
Ayaz E, Türkoğlu ŞA, Orallar H (2016) Toxoplasma gondii and Epilepsy. Turkiye Parazitol Derg 40(2):90–96. https://doi.org/10.5152/tpd.2016.4708
Azevedo KM, Setúbal S, Lopes VG et al (2010) Congenital toxoplasmosis transmitted by human immunodeficiency-virus infected women. Braz J Infect Dis 14(2):186–189
Basavaraju A (2016) Toxoplasmosis in HIV infection: an overview. Trop Parasitol 6(2):129–135
Barragan A, Sibley LD (2002) Transepithelial migration of Toxoplasma gondii is linked to parasite motility and virulence. J Exp Med 195(12):1625–1633
Belluco S, Mancin M, Conficoni D et al (2016) Investigating the determinants of Toxoplasma gondii prevalence in meat: a systematic review and meta-regression. PLoS ONE 11(4):e0153856. https://doi.org/10.1371/journal.pone.0153856
Bereswill S, Kühl AA, Alutis M et al (2014) The impact of Toll-like-receptor-9 on intestinal microbiota composition and extra-intestinal sequelae in experimental Toxoplasma gondii induced ileitis. Gut Pathog 6:19. https://doi.org/10.1186/1757-4749-6-19
Berinstein A, Vazquez-Rovere C, Asurmendi S et al (2005) Mucosal and systemic immunization elicited by Newcastle disease virus (NDV) transgenic plants as antigens. Vaccine 23(48–49):5583–5589
Bertranpetit E, Jombart T, Paradis E et al (2017) Phylogeography of Toxoplasma gondii points to a South American origin. Infect Genet Evol 48:150–155. https://doi.org/10.1016/j.meegid.2016.12.020
Bierly AL, Shufesky WJ, Sukhumavasi W et al (2008) Dendritic cells expressing plasmacytoid marker PDCA-1 are Trojan horses during Toxoplasma gondii infection. J Immunol 181(12):8485–8491
Blader IJ, Coleman BI, Chen CT et al (2015) Lytic cycle of Toxoplasma gondii: 15 years later. Annu Rev Microbiol 69:463–485. https://doi.org/10.1146/annurev-micro-091014-104100
Bliss SK, Gavrilescu LC, Alcaraz A et al (2001) Neutrophil depletion during Toxoplasma gondii infection leads to impaired immunity and lethal systemic pathology. Infect Immun 69(8):4898–4905
Bourguin I, Chardès T, Bout D (1993) Oral immunization with Toxoplasma gondii antigens in association with cholera toxin induces enhanced protective and cell-mediated immunity in C57BL/6 mice. Infect Immun 61(5):2082–2088
Bowie WR, King AS, Werker DH et al (1997) Outbreak of toxoplasmosis associated with municipal drinking water. The BC Toxoplasma Investigation Team. Lancet 350(9072):173–177
Bresciani KDS, Costa AJ, Toniollo GH et al (1999) Experimental toxoplasmosis in pregnant bitches. Vet Parasitol 86:143–145
Bresciani KDS, Toniollo GH, Costa AJ et al (2001) Clinical, parasitological and obstetric observations in pregnant bitches with experimental toxoplasmosis. Ciênc Rur 31:1039–1043
Bresciani KD, Costa AJ, Toniollo GH et al (2009) Transplacental transmission of Toxoplasma gondii in reinfected pregnant female canines. Parasitol Res 104(5):1213–1217. https://doi.org/10.1007/s00436-008-1317-5
Burg JL, Perelman D, Kasper LH et al (1988) Molecular analysis of the gene encoding the major surface antigen of Toxoplasma gondii. J Immunol 141(10):3584–3591
Buriani G, Mancini C, Benvenuto E et al (2011) Plant heat shock protein 70 as carrier for immunization against a plant-expressed reporter antigen. Transgenic Res 20(2):331–344. https://doi.org/10.1007/s11248-010-9418-1
Buriani G, Mancini C, Benvenuto E et al (2012) Heat-shock protein 70 from plant biofactories of recombinant antigens activate multiepitope-targeted immune responses. Plant Biotechnol J 10(3):363–371. https://doi.org/10.1111/j.1467-7652.2011.00673.x
Butcher BA, Kim L, Johnson PF et al (2001) Toxoplasma gondii tachyzoites inhibit proinflammatory cytokine induction in infected macrophages by preventing nuclear translocation of the transcription factor NF-kappa B. J Immunol 167(4):2193–2201
Buxton D, Thomson K, Maley S (1991) Vaccination of sheep with a live incomplete strain (S48) of Toxoplasma gondii and their immunity to challenge when pregnant. Vet Rec 129(5):89–93
Buxton D, Maley SW, Wright SE et al (2007) Toxoplasma gondii and ovine toxoplasmosis: new aspects of an old story. Vet Parasitol 149(1–2):25–28
Cañedo-Solares I, Calzada-Ruiz M, Ortiz-Alegría LB et al (2013) Endothelial cell invasion by Toxoplasma gondii: differences between cell types and parasite strains. Parasitol Res 112(8):3029–3033. https://doi.org/10.1007/s00436-013-3476-2
Cardona N, de-la-Torre A, Siachoque H (2009) Toxoplasma gondii: P30 peptides recognition pattern in human toxoplasmosis. Exp Parasitol 123(2):199–202. https://doi.org/10.1016/j.exppara.2009.06.017
Chebolu S, Daniell H (2007) Stable expression of Gal/GalNAc lectin of Entamoeba histolytica in transgenic chloroplasts and immunogenicity in mice towards vaccine development for amoebiasis. Plant Biotechnol J 5(2):230–239
Chen R, Lu SH, Tong QB, Lou D, Shi DY, Jia BB, Huang GP, Wang JF (2009) Protective effect of DNA-mediated immunization with liposome-encapsulated GRA4 against infection of Toxoplasma gondii. J Zhejiang Univ Sci B 10(7):512–521
Clemente M, Curilovic R, Sassone A et al (2005) Production of the main surface antigen of Toxoplasma gondii in tobacco leaves and analysis of its antigenicity and immunogenicity. Mol Biotechnol 30:41–50
Clemente M (2014) Overview of plant-made vaccine antigens against toxoplasmosis. In: Rosales-Mendoza S (ed) Genetically engineered plants as a source of vaccines against wide spread diseases. Springer, New York, pp 215–241. https://doi.org/10.1007/978-1-4939-0850-9_11
Clemente M, Corigliano MG (2012) Overview of plant-made vaccine antigens against malaria. J Biomed Biotechnol 2012:206918. https://doi.org/10.1155/2012/206918
Cohen SB, Denkers EY (2014) Border maneuvers: deployment of mucosal immune defenses against Toxoplasma gondii. Mucosal Immunol 7(4):744–752. https://doi.org/10.1038/mi.2014.25
Cook AJC, Gilbert RE, Buffolano W et al (2000) Sources of toxoplasma infection in pregnant women: European multicentre case-control study. BMJ 321:142–147
Corigliano MG, Maglioco A, Becher ML, Goldman A, Martín V, Angel SO, Clemente M, Kanellopoulos J (2011) Plant Hsp90 proteins interact with B-Cells and stimulate their proliferation. PLoS ONE 6(6):e21231
Corigliano MG, Fenoy I, Sander V et al (2013) Plant heat shock protein 90 as carrier-adjuvant for immunization against a reporter antigen. Vaccine 31(49):5872–5878. https://doi.org/10.1016/j.vaccine.2013.09.047
Coster LO (2013) Parasitic infections in solid organ transplant recipients. Infect Dis Clin North Am 27(2):395–427. https://doi.org/10.1016/j.idc.2013.02.008
Dabritz HA, Miller MA, Atwill ER et al (2007) Detection of Toxoplasma gondii-like oocysts in cat feces and estimates of the environmental oocyst burden. J Am Vet Med Assoc 231(11):1676–1684
Debierre-Grockiego F, Campos MA, Azzouz N et al (2007) Activation of TLR2 and TLR4 by glycosylphosphatidylinositols derived from Toxoplasma gondii. J Immunol 179(2):1129–1137
Del Grande C, Galli L, Schiavi E (2017) Is Toxoplasma gondii a trigger of bipolar disorder? Pathogens 10;6(1): pii E3. https://doi.org/10.3390/pathogens6010003
Del Rio L, Bennouna S, Salinas J et al (2001) CXCR2 deficiency confers impaired neutrophil recruitment and increased susceptibility during Toxoplasma gondii infection. J Immunol 167(11):6503–6509
Del Yácono LM, Farran I, Becher ML et al (2012) Chloroplast-derived Toxoplasma gondii GRA4 antigen used as an oral vaccine protects against toxoplasmosis in mice. Plant Biotechnol J 10(9):1136–1144. https://doi.org/10.1111/pbi.12001
Delhaes L, Ajzenberg D, Sicot B et al (2010) Severe congenital toxoplasmosis due to a Toxoplasma gondii strain with an atypical genotype: case report and review. Prenat Diagn 30(9):902–905. https://doi.org/10.1002/pd.2563
Denkers EY, Scharton-Kersten T, Barbieri S et al (1996) A role for CD4+ NK1.1+ T lymphocytes as major histocompatibility complex class II independent helper cells in the generation of CD8+ effector function against intracellular infection. J Exp Med 184(1):131–139
Denkers EY, Schneider AG, Cohen SB, Butcher BA (2012) Phagocyte responses to protozoan infection and how Toxoplasma gondii meets the challenge. Publ Libr Sci Pathog 8:e1002794
Derouin F, Santillana-Hayat M (2000) Anti-toxoplasma activities of antiretroviral drugs and interactions with pyrimethamine and sulfadiazine in vitro. Antimicrob Agents Chemother 44(9):2575–2577
Desolme B, Mévélec MN, Buzoni-Gatel D et al (2000) Induction of protective immunity against toxoplasmosis in mice by DNA immunization with a plasmid encoding Toxoplasma gondii GRA4 gene. Vaccine 18(23):2512–2521
Dhama K, Rajagunalan S, Chakraborty S et al (2013) Food-borne pathogens of animal origin-diagnosis, prevention, control and their zoonotic significance: a review. Pak J Biol Sci 16(20):1076–1085
Dickerson FB, Stallings CR, Boronow JJ et al (2009) A double-blind trial of adjunctive azithromycin in individuals with schizophrenia who are seropositive for Toxoplasma gondii. Schizophr Res 112(1–3):198–199. https://doi.org/10.1016/j.schres.2009.05.005
Długonska H (2014) Toxoplasma gondii and the host cells. Ann Parasitol 60(2):83–88
Du J, An R, Chen L et al (2014) Toxoplasma gondii virulence factor ROP18 inhibits the host NF-κB pathway by promoting p65 degradation. J Biol Chem 289(18):12578–12592. https://doi.org/10.1074/jbc.M113.544718
Dubey JP (1982) Repeat transplacental transfer of Toxoplasma gondii in dairy goats. J Am Vet Med Assoc 180(10):1220–1221
Dubey JP, Brown CA, Carpenter JL et al (1992) Fatal toxoplasmosis in domestic rabbits in the USA. Vet Parasitol 44(3–4):305–309
Dubey JP (1996) Infectivity and pathogenicity of Toxoplasma gondii oocysts for cats. J Parasitol 82(6):957–961
Dubey JP (2007) The history and life cycle of Toxoplasma gondii. In: Weiss LM, Kim K (ed) Toxoplasma gondii. The model apicomplexan: perspectives and methods. Academic Press, New York, pp 1–1
Dubey JP (2008) The history of Toxoplasma gondii-the first 100 years. J Eukaryot Microbiol 55(6):467–475. https://doi.org/10.1111/j.1550-7408.2008.00345.x
Dubey JP (2009) Toxoplasmosis in pigs–the last 20 years. Vet Parasitol 164(2–4):89–103. https://doi.org/10.1016/j.vetpar.2009.05.018
Dubey JP, Lindsay DS, Lappin MR (2009) Toxoplasmosis and other intestinal coccidial infections in cats and dogs. Vet Clin North Am Small Anim Pract 39(6):1009–1034. https://doi.org/10.1016/j.cvsm.2009.08.001
Dubey JP, Passos LM, Rajendran C et al (2011) Isolation of viable Toxoplasma gondii from feral guinea fowl (Numida meleagris) and domestic rabbits (Oryctolagus cuniculus) from Brazil. J Parasitol 97(5):842–845. https://doi.org/10.1645/GE-2728.1
Dubey JP, Verma SK, Villena I et al (2016) Toxoplasmosis in the Caribbean islands: literature review, seroprevalence in pregnant women in ten countries, isolation of viable Toxoplasma gondii from dogs from St. Kitts, West Indies with report of new T. gondii genetic types. Parasitol Res 115(4):1627–1634. https://doi.org/10.1007/s00436-015-4900-6
Dunn D, Wallon M, Peyron F, Petersen E, Peckham C, Gilbert R (1999) Mother-to-child transmission of toxoplasmosis: risk estimates for clinical counselling. Lancet 353(9167):1829–1833
Dupont CD, Christian DA, Hunter CA (2012) Immune response and immunopathology during toxoplasmosis. Semin Immunopathol 34(6):793–813. https://doi.org/10.1007/s00281-012-0339-3
Elsheikha HM, Büsselberg D, Zhu XQ (2016) The known and missing links between Toxoplasma gondii and schizophrenia. Metab Brain Dis 31(4):749–759. https://doi.org/10.1007/s11011-016-9822-1
Esch KJ1, Petersen CA (2013) Transmission and epidemiology of zoonotic protozoal diseases of companion animals. Clin Microbiol Rev 26(1):58–85. https://doi.org/10.1128/cmr.00067-12
Elbez-Rubinstein A, Ajzenberg D, Dardé ML et al (2009) Congenital toxoplasmosis and reinfection during pregnancy: case report, strain characterization, experimental model of reinfection, and review. J Infect Dis 199(2):280–285
Emery S, Kelleher AD, Workman C et al (2007) Influence of IFNgamma co-expression on the safety and antiviral efficacy of recombinant fowlpox virus HIV therapeutic vaccines following interruption of antiretroviral therapy. Hum Vaccin 3(6):260–267
Ferguson DJ, Hutchison WM (1987) An ultrastructural study of the early development and tissue cyst formation of Toxoplasma gondii in the brains of mice. Parasitol Res 73(6):483–491
Ferraro G, Laguía Becher M, Angel SO et al (2008) Efficient expression of a Toxoplasma gondii dense granule Gra4 antigen in tobacco leaves. Exp Parasitol 120:118–122. https://doi.org/10.1016/j.exppara.2008.06.002
Feustel SM, Meissner M, Liesenfeld O (2012) Toxoplasma gondii and the blood-brain barrier. Virulence 3(2):182–192. https://doi.org/10.4161/viru.19004
Frenkel JK, Dubey JP, Miller NL (1970) Toxoplasma gondii in cats: fecal stages identified as coccidian oocysts. Science 167:893–896
Fricker-Hidalgo H, Cimon B, Chemla C et al (2013) Toxoplasma seroconversion with negative or transient immunoglobulin M in pregnant women: myth or reality? A French multicenter retrospective study. J Clin Microbiol 51(7):2103–2111. https://doi.org/10.1128/JCM.00169-13
Ganapathy M1, Perumal A, Mohan C et al (2014) Immunogenicity of Brugia malayi Abundant Larval Transcript-2, a potential filarial vaccine candidate expressed in tobacco. Plant Cell Rep 33(1):179–188. https://doi.org/10.1007/s00299-013-1521-3
Garcia JL, Innes EA, Katzer F (2014) Current progress toward vaccines against Toxoplasma gondii. Vaccine: Develop Ther 4:23–37
Gazzinelli RT, Eltoum I, Wynn TA et al (1993) Acute cerebral toxoplasmosis is induced by in vivo neutralization of TNF-alpha and correlates with the down-regulated expression of inducible nitric oxide synthase and other markers of macrophage activation. J Immunol 151(7):3672–3681
Gilbert R, Gras L (2003) European multicentre study on congenital toxoplasmosis. Effect of timing and type of treatment on the risk of mother to child transmission of Toxoplasma gondii. BJOG 110(2):112–120
Glasner PD, Silveira C, Kruszon-Moran D et al (1992) An unusually high prevalence of ocular toxoplasmosis in southern Brazil. Am J Ophthalmol 114(2):136–144
Gómez E, Chimeno Zoth S, Carrillo E et al (2008) Mucosal immunity induced by orally administered transgenic plants. Immunobiology 213(8):671–675. https://doi.org/10.1016/j.imbio.2008.02.002
Gonzalez-Rabade N, McGowan EG, Zhou F et al (2011) Immunogenicity of chloroplast-derived HIV-1 p24 and a p24-Nef fusion protein following subcutaneous and oral administration in mice. Plant Biotechnol J 9(6):629–638. https://doi.org/10.1111/j.1467-7652.2011.00609.x
Granell A, Fernández del-Carmen A, Orzáez D (2010) In planta production of plant-derived and non-plant-derived adjuvants. Expert Rev Vaccines 9(8):843–858. https://doi.org/10.1586/erv.10.80
Gras L, Wallon M, Pollak A et al (2005) Association between prenatal treatment and clinical manifestations of congenital toxoplasmosis in infancy: a cohort study in 13 European centres. Acta Paediatr 94(12):1721–1731
Guo M, Dubey JP, Hill D et al (2015) Prevalence and risk factors for Toxoplasma gondii infection in meat animals and meat products destined for human consumption. J Food Prot 78(2):457–476. https://doi.org/10.4315/0362-028X.JFP-14-328
Halonen SK1, Weiss LM (2013) Toxoplasmosis. Handb Clin Neurol 114:125–145. https://doi.org/10.1016/b978-0-444-53490-3.00008-x
Harning D, Spenter J, Metsis A et al (1996) Recombinant Toxoplasma gondii surface antigen 1 (P30) expressed in Escherichia coli is recognized by human Toxoplasma-specific immunoglobulin M (IgM) and IgG antibodies. Clin Diagn Lab Immunol 3(3):355–357
Harker KS, Ueno N, Lodoen MB (2015) Toxoplasma gondii dissemination: a parasite’s journey through the infected host. Parasite Immunol 37(3):141–149. https://doi.org/10.1111/pim.12163
Hayden CA, Egelkrout EM, Moscoso AM et al (2012) Production of highly concentrated, heat-stable hepatitis B surface antigen in maize. Plant Biotechnol J 10(8):979–984. https://doi.org/10.1111/j.1467-7652.2012.00727.x
Hennequin C, Dureau P, N’Guyen L et al (1997) Congenital toxoplasmosis acquired from an immune woman. Pediatr Infect Dis J 16(1):75–77
Hernandez M, Rosas G, Cervantes J et al (2014) Transgenic plants: a 5-year update on oral antipathogen vaccine development. Expert Rev Vaccines 13(12):1523–1536. https://doi.org/10.1586/14760584.2014.953064
Hiszczynska-Sawicka E, Gatkowska JM, Grzybowski MM et al (2014) Veterinary vaccines against toxoplasmosis. Parasitology 141(11):1365–1378. https://doi.org/10.1017/S0031182014000481
Holland GN (2003) Ocular toxoplasmosis: a global reassessment. Part I: epidemiology and course of disease. Am J Ophthalmol 136(6):973–988
Hu K, Johnson J, Florens L et al (2006) Cytoskeletal components of an invasion machine-the apical complex of Toxoplasma gondii. PLoS Pathog 2(2):e13. https://doi.org/10.1371/journal.ppat.0020013
Innes EA, Vermeulen AN (2006) Vaccination as a control strategy against the coccidial parasites Eimeria Toxoplasma and Neospora. Parasitology 133(Suppl):S145–S168
Innes EA (2010) Vaccination against Toxoplasma gondii: an increasing priority for collaborative research? Expert Rev Vaccines 9(10):1117–1119. https://doi.org/10.1586/erv.10.113
Israelski DM, Remington JS (1993) Toxoplasmosis in the non-AIDS immunocompromised host. Curr Clin Top Infect Dis 13:322–356
Jacob SS, Cherian S, Sumithra TG et al (2013) Edible vaccines against veterinary parasitic diseases—current status and future prospects. Vaccine 31(15):1879–1885. https://doi.org/10.1016/j.vaccine.2013.02.022
Jasper S, Vedula SS, John SS et al (2017) Corticosteroids as adjuvant therapy for ocular toxoplasmosis. Cochrane Database Syst Rev 1:CD007417. https://doi.org/10.1002/14651858.cd007417
Jiang HH, Li MW, Xu MJ et al (2015) Prevalence of Toxoplasma gondii in dogs in Zhanjiang, Southern China. Korean J Parasitol 53(4):493–496. https://doi.org/10.3347/kjp.2015.53.4.493
Jones JL, Dargelas V, Roberts J et al (2009) Risk factors for Toxoplasma gondii infection in the United States. Clin Infect Dis 49(6):878–884. https://doi.org/10.1086/605433
Jongert E, Roberts CW, Gargano N (2009) Vaccines against Toxoplasma gondii: challenges and opportunities. Mem Inst Oswaldo Cruz 104(2):252–266. Erratum in: Mem Inst Oswaldo Cruz. 2010 Feb; 105
Kapusta J, Pniewski T, Wojciechowicz J et al (2010) Nanogram doses of alum-adjuvanted HBs antigen induce humoral immune response in mice when orally administered. Arch Immunol Ther Exp (Warsz) 58(2):143–151. https://doi.org/10.1007/s00005-010-0065-2
Katzer F, Brülisauer F, Collantes-Fernández E et al (2011) Increased Toxoplasma gondii positivity relative to age in 125 Scottish sheep flocks; evidence of frequent acquired infection. Vet Res 42:121. https://doi.org/10.1186/1297-9716-42-121
Kesik-Brodacka M, Lipiec A, Kozak Ljunggren M et al (2017) Immune response of rats vaccinated orally with various plant-expressed recombinant cysteine proteinase constructs when challenged with Fasciola hepatica metacercariae. PLoS Negl Trop Dis 11(3):e0005451. https://doi.org/10.1371/journal.pntd.0005451
Khan IA, Smith KA, Kasper LH (1988) Induction of antigen-specific parasiticidal cytotoxic T cell splenocytes by a major membrane protein (P30) of Toxoplasma gondii. J Immunol 141(10):3600–3605
Khan IA, Murphy PM, Casciotti L et al (2001) Mice lacking the chemokine receptor CCR1 show increased susceptibility to Toxoplasma gondii infection. J Immunol 166(3):1930–1937
Khurana S, Batra N (2016) Toxoplasmosis in organ transplant recipients: evaluation, implication, and prevention. Trop Parasitol 6(2):123–128
Kieffer F, Wallon M (2013) Congenital toxoplasmosis. Handb Clin Neurol 112:1099–1101. https://doi.org/10.1016/B978-0-444-52910-7.00028-3
Kim JY, Ahn MH, Jun HS et al (2006) Toxoplasma gondii inhibits apoptosis in infected cells by caspase inactivation and NF-kappaB activation. Yonsei Med J 47(6):862–869
Kim SK, Fouts AE, Boothroyd JC (2007) Toxoplasma gondii dysregulates IFN-gamma-inducible gene expression in human fibroblasts: insights from a genome-wide transcriptional profiling. J Immunol 178(8):5154–5165
Kim JH, Kang KI, Kang WC et al (2009) Porcine abortion outbreak associated with Toxoplasma gondii in Jeju Island. Korea J Vet Sci 10:147–151
Kong Q, Richter L, Yang YF (2001) Oral immunization with hepatitis B surface antigen expressed in transgenic plants. Proc Natl Acad Sci U S A 98(20):11539115–11539144
Kostrzak A, Cervantes Gonzalez M, Guetard D et al (2009) Oral administration of low doses of plant-based HBsAg induced antigen-specific IgAs and IgGs in mice, without increasing levels of regulatory T cells. Vaccine 27(35):4798–47807. https://doi.org/10.1016/j.vaccine.2009.05.092
Labruyere E, Lingnau M, Mercier C et al (1999) Differential membrane targeting of the secretory proteins GRA4 and GRA6 within the parasitophorous vacuole formed by Toxoplasma gondii. Mol Biochem Parasitol 20;102(2):311–324
Laguía-Becher M, Martín V, Kraemer M et al (2010) 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. https://doi.org/10.1186/1472-6750-10-52
Langermans JA, van der Hulst ME, Nibbering PH et al (1992) Endogenous tumor necrosis factor alpha is required for enhanced antimicrobial activity against Toxoplasma gondii and Listeria monocytogenes in recombinant gamma interferon-treated mice. Infect Immun 60(12):5107–5112
Licciardi PV, Underwood JR (2011) Plant-derived medicines: a novel class of immunological adjuvants. Int Immunopharmacol 11(3):390–398. https://doi.org/10.1016/j.intimp.2010.10.014
Limaye A, Koya V, Samsam M et al (2006) Receptor-mediated oral delivery of a bioencapsulated green fluorescent protein expressed in transgenic chloroplasts into the mouse circulatory system. FASEB J 20(7):959–961
Lim SS, Othman RY (2014) Recent advances in Toxoplasma gondii immunotherapeutics. Korean J Parasitol 52(6):581–593. https://doi.org/10.3347/kjp.2014.52.6.581
Lindsay DS, Dubey JP (2011) Toxoplasma gondii: the changing paradigm of congenital toxoplasmosis. Parasitology 138(14):1829–1831. https://doi.org/10.1017/S0031182011001478
Machacova T, Bartova E, Sedlak K (2016) Seroprevalence and risk factors of infections with Neospora caninum and Toxoplasma gondii in hunting dogs from Campania region, southern Italy. Folia Parasitol (Praha) 6;63. pii:2016.012. https://doi.org/10.14411/fp.2016.012
Magalhães FJ, Ribeiro-Andrade M, Souza FM et al (2017) Seroprevalence and spatial distribution of Toxoplasma gondii infection in cats, dogs, pigs and equines of the Fernando de Noronha Island. Brazil Parasitol Int 66(2):43–46. https://doi.org/10.1016/j.parint.2016.11.014
Makioka A, Kobayashi A (1991) Toxoplasmacidal activity of macrophages activated by recombinant major surface antigen (P30) of Toxoplasma gondii. Infect Immun 59(8):2851–2852
Marchioro AA, Tiyo BT, Colli CM et al (2016) First Detection of Toxoplasma gondii DNA in the fresh leafs of vegetables in South America. Vector Borne Zoonotic Dis 16(9):624–626. https://doi.org/10.1089/vbz.2015.1937
Martin V, Supanitsky A, Echeverria P et al (2004) Recombinant GRA4 or ROP2 protein combined with alum or the gra4 gene provides partial protection in chronic murine models of toxoplasmosis. Clin Lab Immunol 11:704–710
Mason HS, Herbst-Kralovetz MM (2012) Plant-derived antigens as mucosal vaccines. Curr Top Microbiol Immunol 354:101–120. https://doi.org/10.1007/82_2011_158
Mastropaolo JP, Moskowitz KH, Dacanay RJ et al (1989) Conditioned taste aversions as a behavioral baseline for drug discrimination learning: an assessment with phencyclidine. Pharmacol Biochem Behav 32(1):1–8
Matias M, Gomes A, Marques T, Fonseca AC (2014) Ocular toxoplasmosis: a very rare presentation in an immunocompetent patient. BMJ Case Rep. https://doi.org/10.1136/bcr-2014-205846
Matsumoto Y, Suzuki S, Nozoye T et al (2009) Oral immunogenicity and protective efficacy in mice of transgenic rice plants producing a vaccine candidate antigen (As16) of Ascaris suum fused with cholera toxin B subunit. Transgenic Res 18(2):185–192. https://doi.org/10.1007/s11248-008-9205-4
McGettigan BD, Hew M, Phillips E et al (2012) Sulphadiazine-induced renal stones in a 63-year-old HIV-infected man treated for toxoplasmosis. BMJ Case Rep pii:bcr2012006638. https://doi.org/10.1136/bcr-2012-006638
Melzer T, Duffy A, Weiss LM et al (2008) The gamma interferon (IFN-gamma)-inducible GTP-binding protein IGTP is necessary for toxoplasma vacuolar disruption and induces parasite egression in IFN-gamma-stimulated astrocytes. Infect Immun 76(11):4883–4894. https://doi.org/10.1128/iai.01288-07
Mennechet FJ, Kasper LH, Rachinel N et al (2004) Intestinal intraepithelial lymphocytes prevent pathogen-driven inflammation and regulate the Smad/T-bet pathway of lamina propria CD4+ T cells. Eur J Immunol 34(4):1059–1067
Menzies FM, Henriquez FL, Roberts CW (2008) Immunological control of congenital toxoplasmosis in the murine model. Immunol Lett 115(2):83–89
Mévélec MN, Mercereau-Puijalon O, Buzoni-Gatel D et al (1998) Mapping of B epitopes in GRA4, a dense granule antigen of Toxoplasma gondii and protection studies using recombinant proteins administered by the oral route. Parasite Immunol 20(4):183–195
Mévélec MN, Bout D, Desolme B et al (2005) 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 23:4489–4499
Miller CM, Boulter NR, Ikin RJ, Smith NC (2009) The immunobiology of the innate response to Toxoplasma gondii. Int J Parasitol 39(1):23–39. https://doi.org/10.1016/j.ijpara.2008.08.002
Molestina RE, Payne TM, Coppens I et al (2003) Activation of NF-kappaB by Toxoplasma gondii correlates with increased expression of antiapoptotic genes and localization of phosphorylated IkappaB to the parasitophorous vacuole membrane. J Cell Sci 116(Pt 21):4359–4371
Moncada PA, Montoya JG (2012) Toxoplasmosis in the fetus and newborn: an update on prevalence, diagnosis and treatment. Expert Rev Anti Infect Ther 10(7):815–828. https://doi.org/10.1586/eri.12.58
Monreal-Escalante E, Govea-Alonso DO, Hernández M et al (2016) Towards the development of an oral vaccine against porcine cysticercosis: expression of the protective HP6/TSOL18 antigen in transgenic carrots cells. Planta 243(3):675–685. https://doi.org/10.1007/s00425-015-2431-0
Montazeri M, Sharif M, Sarvi S et al (2017) A systematic review of in vitro and in vivo activities of anti-Toxoplasma drugs and compounds (2006-2016). Front Microbio 8:25. https://doi.org/10.3389/fmicb.2017.00025
Montoya JG, Liesenfeld O (2004) Toxoplasmosis. Lancet 363(9425):1965–1976
Muñoz M, Liesenfeld O, Heimesaat MM (2011) Immunology of Toxoplasma gondii. Immunol Rev 240(1):269–285. https://doi.org/10.1111/j.1600-065X.2010.00992.x
Nicolle C, Manceaux L (1908) Sur une infection à corps de Leishman (ou organismes voisins) du gondi. C R Hebd Seances Acad Sci 147:763–766
Nigro M, Gutierrez A, Hoffer AM et al (2003) Evaluation of Toxoplasma gondii recombinant proteins for the diagnosis of recently acquired toxoplasmosis by an immunoglobulin G analysis. Diagn Microbiol Infect Dis 47:609–613
Okamoto N, Keeling PJ (2014) The 3D structure of the apical complex and association with the flagellar apparatus revealed by serial TEM tomography in Psammosa pacifica, a distant relative of the Apicomplexa. PLoS ONE 9(1):e84653. https://doi.org/10.1371/journal.pone.0084653
Paul M, Ma JK (2010) Plant-made immunogens and effective delivery strategies. Expert Rev Vaccines 9(8):821–833. https://doi.org/10.1586/erv.10.88
Peng HJ, Chen XG, Lindsay DS (2011) A review: competence, compromise, and concomitance-reaction of the host cell to Toxoplasma gondii infection and development. J Parasitol 97(4):620–628. https://doi.org/10.1645/GE-2712.1
Perkins ES (1973) Ocular toxoplasmosis. Br J Ophthalmol 57(1):1–17
Pleyer U, Schlüter D, Mänz M (2014) Ocular toxoplasmosis: recent aspects of pathophysiology and clinical implications. Ophthalmic Res 52(3):116–123. https://doi.org/10.1159/000363141
Pollard AM, Onatolu KN, Hiller L et al (2008) Highly polymorphic family of glycosylphosphatidylinositol-anchored surface antigens with evidence of developmental regulation in Toxoplasma gondii. Infect Immun 76(1):103–110
Raeghi S, Akaberi A, Sedeghi S (2011) Seroprevalence of Toxoplasma gondii in sheep, cattle and horses in Urmia North-West of Iran. Iran J Parasitol 6(4):90–94
Rajapakse R, Uring-Lambert B, Andarawewa KL (2007) 1,25(OH)2D3 inhibits in vitro and in vivo intracellular growth of apicomplexan parasite Toxoplasma gondii. J Steroid Biochem Mol Biol 103(3–5):811–814
Reichmann G, Walker W, Villegas EN (2000) The CD40/CD40 ligand interaction is required for resistance to toxoplasmic encephalitis. Infect Immun 68(3):1312–1318
Rodriguez JB, Szajnman SH (2012) New antibacterials for the treatment of toxoplasmosis; a patent review. Expert Opin Ther Pat 22(3):311–333. https://doi.org/10.1517/13543776.2012.668886
Robert-Gangneux F, Dardé ML (2012) Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev 25(2):264–96. doi:0.1128/CMR.05013-11. Erratum in: Clin Microbiol Rev 2012 25(3):583
Rosales-Mendoza S, Salazar-González JA (2014) Immunological aspects of using plant cells as delivery vehicles for oral vaccines. Expert Rev Vaccines 13(6):737–749. https://doi.org/10.1586/14760584.2014.913483
Rosso F, Les JT, Agudelo A et al (2008) Prevalence of infection with Toxoplasma gondii among pregnant women in Cali, Colombia, South America. Am J Trop Med Hyg 78(3):504–508
Rostami A, Seyyedtabaei SJ, Aghamolaie S et al (2016) Seroprevalence and risk factors associated with Toxoplasma gondii infection among rural communities in northern Iran. Rev Inst Med Trop Sao Paulo 22(58):70. https://doi.org/10.1590/S1678-9946201658070
Sathish K, Sriraman R, Subramanian BM et al (2012) Plant expressed coccidial antigens as potential vaccine candidates in protecting chicken against coccidiosis. Vaccine 30(30):4460–4464. https://doi.org/10.1016/j.vaccine.2012.04.076
Saeij JP, Coller S, Boyle JP et al (2007) Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue. Nature 445(7125):324–327
Sánchez VR, Pitkowski MN, Fernández Cuppari AV, Rodríguez FM, Fenoy IM, Frank FM, Goldman A, Corral RS, Martin V (2011) Combination of CpG-oligodeoxynucleotides with recombinant ROP2 or GRA4 proteins induces protective immunity against Toxoplasma gondii infection. Exp Parasitol 128(4):448–453. https://doi.org/10.1016/j.exppara.2011.04.004
Sanecka A, Frickel EM (2012) Use and abuse of dendritic cells by Toxoplasma gondii. Virulence 3(7):678–689. https://doi.org/10.4161/viru.22833
Santi L, Batchelor L, Huang Z et al (2008) An efficient plant viral expression system generating orally immunogenic Norwalk virus-like particles. Vaccine 26(15):1846–1854. https://doi.org/10.1016/j.vaccine.2008.01.053
Scallan E, Hoekstra RM, Angulo FJ et al (2011) Foodborne illness acquired in the United States-major pathogens. Emerg Infect Dis 17:7–15
Shaapan RM (2016) The common zoonotic protozoal diseases causing abortion. J Parasit Dis 40(4):1116–1129
Shapira S, Harb OS, Margarit J et al (2005) Initiation and termination of NF-kappaB signaling by the intracellular protozoan parasite Toxoplasma gondii. J Cell Sci 118(Pt 15):3501–3508
Shibre T, Alem A, Abdulahi A et al (2010) Trimethoprim as adjuvant treatment in schizophrenia: a double-blind, randomized, placebo-controlled clinical trial. Schizophr Bull 36(4):846–851. https://doi.org/10.1093/schbul/sbn191
Siachoque H, Guzman F, Burgos J et al (2006) Toxoplasma gondii: immunogenicity and protection by P30 peptides in a murine model. Exp Parasitol 114(1):62–65
Sibley LD, Adams LB, Fukutomi Y et al (1991) Tumor necrosis factor-alpha triggers antitoxoplasmal activity of IFN-gamma primed macrophages. J Immunol 147(7):2340–2345
Sibley LD (2011) Invasion and intracellular survival by protozoan parasites. Immunol Rev 240(1):72–91. https://doi.org/10.1111/j.1600-065X.2010.00990.x
Skariah S, McIntyre MK, Mordue DG (2010) Toxoplasma gondii: determinants of tachyzoite to bradyzoite conversion. Parasitol Res 107(2):253–260. https://doi.org/10.1007/s00436-010-1899-6
Sturge CR, Yarovinsky F (2014) Complex immune cell interplay in the gamma interferon response during Toxoplasma gondii infection. Infect Immun 82(8):3090–3097. https://doi.org/10.1128/IAI.01722-14
Suzuki Y, Conley FK, Remington JS (1989) Importance of endogenous IFN-gamma for prevention of toxoplasmic encephalitis in mice. J Immunol 143(6):2045–2050
Suzuki Y, Remington JS (1993) Toxoplasmic encephalitis in AIDS patients and experimental models for study of the disease and its treatment. Res Immunol 144(1):66–67
Tenter AM, Heckeroth AR, Weiss LM (2000) Toxoplasma gondii: from animals to humans. Int J Parasitol 30(12–13):1217–1258. Erratum in: Int J Parasitol 2001 31(2):217–220
Thiébaut R, Leproust S, Chêne G et al (2007) Effectiveness of prenatal treatment for congenital toxoplasmosis: a meta-analysis of individual patients’ data. Lancet 369(9556):115–122
Torgerson PR, Mastroiacovo P (2013) The global burden of congenital toxoplasmosis: a systematic review. Bull World Health Organ 91(7):501–508. https://doi.org/10.2471/BLT.12.111732
Torrey EF, Yolken RH (2003) Toxoplasma gondii and schizophrenia. Emerg Infect Dis 9(11):1375–1380
Vajdy M (2011) Immunomodulatory properties of vitamins, flavonoids and plant oils and their potential as vaccine adjuvants and delivery systems. Expert Opin Biol Ther 11(11):1501–1513. https://doi.org/10.1517/14712598.2011.623695
Vaudaux JD, Muccioli C, James ER et al (2010) Identification of an atypical strain of Toxoplasma gondii as the cause of a waterborne outbreak of toxoplasmosis in Santa Isabel do Ivai, Brazil. J Infect Dis 202(8):1226–1233
Wang Y, Wang G, Zhang D et al (2013) Screening and identification of novel B cell epitopes of Toxoplasma gondii SAG1. Parasit Vectors 6:125. https://doi.org/10.1186/1756-3305-6-125
Wang Y, Yin H (2014) Research progress on surface antigen 1 (SAG1) of Toxoplasma gondii. Parasit Vectors 7:180. https://doi.org/10.1186/1756-3305-7-180
Wiengcharoen J, Thompson RC, Nakthong C et al (2011) Transplacental transmission in cattle: is Toxoplasma gondii less potent than Neospora caninum? Parasitol Res 108(5):1235–1241. https://doi.org/10.1007/s00436-010-2172-8
Wilbers RH, Westerhof LB, van Noort K et al (2017) Production and glyco-engineering of immunomodulatory helminth glycoproteins in plants. Sci Rep 7:45910. https://doi.org/10.1038/srep45910
Wilson CB, Remington JS, Stagno S et al (1980) Development of adverse sequelae in children born with subclinical congenital Toxoplasma infection. Pediatrics 66(5):767–774
Xiao J, Yolken RH (2015) Strain hypothesis of Toxoplasma gondii infection on the outcome of human diseases. Acta Physiol (Oxf) 213(4):828–845. https://doi.org/10.1111/apha.12458
Yarovinsky F, Hieny S, Sher A (2008) Recognition of Toxoplasma gondii by TLR11 prevents parasite-induced immunopathology. J Immunol 181(12):8478–8484
Yusibov V, Rabindran S (2008) Recent progress in the development of plant derived vaccines. Expert Rev Vaccines 7(8):1173–1183. https://doi.org/10.1586/14760584.7.8.1173
Yusibov V, Streatfield SJ, Kushnir N (2011) Clinical development of plant-produced recombinant pharmaceuticals: vaccines, antibodies and beyond. Hum Vaccin 7(3):313–321
Zhang H, Liu M, Li Y et al (2010) Oral immunogenicity and protective efficacy in mice of a carrot-derived vaccine candidate expressing UreB subunit against Helicobacter pylori. Protein Expr Purif 69(2):127–131. https://doi.org/10.1016/j.pep.2009.07.016
Zhang NZ, Chen J, Wang M (2013) Vaccines against Toxoplasma gondii: new developments and perspectives. Expert Rev Vaccines 12(11):1287–1299. https://doi.org/10.1586/14760584.2013.844652
Zhang NZ, Wang M, Xu Y (2015) Recent advances in developing vaccines against Toxoplasma gondii: an update. Expert Rev Vaccines 14(12):1609–1621. https://doi.org/10.1586/14760584.2015.1098539
Zhu S (2009) Psychosis may be associated with toxoplasmosis. Med Hypotheses 3(5):799–801. https://doi.org/10.1016/j.mehy.2009.04.013
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Sander, V., Angel, S.O., Clemente, M. (2018). A Comprehensive Review of Toxoplasma Gondii Biology and Host-Cell Interaction: Challenges for a Plant-Based Vaccine. In: MacDonald, J. (eds) Prospects of Plant-Based Vaccines in Veterinary Medicine. Springer, Cham. https://doi.org/10.1007/978-3-319-90137-4_4
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