Protective efficacy induced by DNA prime and recombinant protein boost vaccination with Toxoplasma gondii GRA14 in mice

Lindsay, 2011, Toxoplasma gondii: the changing paradigm of congenital toxoplasmosis, Parasitology, 138, 1829, 10.1017/S0031182011001478 J. Flegr, 2014, Toxoplasmosis-a global threat. Correlation of latent toxoplasmosis with specific disease burden in a set of 88 countries, PLoS One, 9, 10.1371/journal.pone.0090203 Dubey, 1998, Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts, Clin. Microbiol. Rev., 11, 267, 10.1128/CMR.11.2.267 Contini, 2008, Clinical and diagnostic management of toxoplasmosis in the immunocompromised patient, Parassitologia, 50, 45 Dubey, 2012, Toxoplasmosis in humans and animals in Brazil: high prevalence, high burden of disease, and epidemiology, Parasitology, 139, 1375, 10.1017/S0031182012000765 Sharif, 2016, The efficacy of herbal medicines against Toxoplasma gondii during the last 3 decades: a systematic review, Can. J. Physiol. Pharmacol., 94, 1237, 10.1139/cjpp-2016-0039 Buxton, 1991, Vaccination of sheep with a live incomplete strain (S48) of Toxoplasma gondii and their immunity to challenge when pregnant, Vet. Rec., 129, 89, 10.1136/vr.129.5.89 Rezaei, 2019, A systematic review of Toxoplasma gondii antigens to find the best vaccine candidates for immunization, Microb. Pathog., 126, 172, 10.1016/j.micpath.2018.11.003 Fang, 2012, Evaluation of immune responses induced by SAG1 and MIC3 vaccine cocktails against Toxoplasma gondii, Vet. Parasitol., 187, 140, 10.1016/j.vetpar.2011.12.007 Zhang, 2015, Protective efficacy of two novel DNA vaccines expressing Toxoplasma gondii rhomboid 4 and rhomboid 5 proteins against acute and chronic toxoplasmosis in mice, Expert Rev. Vaccines, 14, 1289, 10.1586/14760584.2015.1061938 Allahyari, 2016, Synergistic effect of rSAG1 and rGRA2 antigens formulated in PLGA microspheres in eliciting immune protection against Toxoplasama gondii, Exp. Parasitol., 170, 236, 10.1016/j.exppara.2016.09.008 Nam, 2009, GRA proteins of Toxoplasma gondii: maintenance of host-parasite interactions across the parasitophorous vacuolar membrane, Korean J. Parasitol., 47, S29, 10.3347/kjp.2009.47.S.S29 Ahmadpour, 2017, Enhancing immune responses to a DNA vaccine encoding Toxoplasma gondii GRA14 by calcium phosphate nanoparticles as an adjuvant, Immunol. Lett., 185, 40, 10.1016/j.imlet.2017.03.006 Rome, 2008, Intervacuolar transport and unique topology of GRA14, a novel dense granule protein in Toxoplasma gondii, Infect. Immun., 76, 4865, 10.1128/IAI.00782-08 Jongert, 2009, Vaccines against Toxoplasma gondii: challenges and opportunities, Mem. Inst. Oswaldo Cruz, 104, 252, 10.1590/S0074-02762009000200019 Meng, 2013, DNA prime and peptide boost immunization protocol encoding the Toxoplasma gondii GRA4 induces strong protective immunity in BALB/c mice, BMC Infect. Dis., 13, 494, 10.1186/1471-2334-13-494 Kang, 2000, Decreased resistance of B cell-deficient mice to infection with Toxoplasma gondii despite unimpaired expression of IFN-γ, TNF-α, and inducible nitric oxide synthase, J. Immunol., 164, 2629, 10.4049/jimmunol.164.5.2629 Grim, 2004, Preliminary results of an anticircumsporozoite DNA vaccine trial for protection against avian malaria in captive African black-footed penguins (Spheniscus demersus), J. Zoo Wildl. Med., 35, 154, 10.1638/03-060 de Alencar, 2009, Perforin and gamma interferon expression are required for CD4+ and CD8+ T-cell-dependent protective immunity against a human parasite, Trypanosoma cruzi, elicited by heterologous plasmid DNA prime-recombinant adenovirus 5 boost vaccination, Infect. Immun., 77, 4383, 10.1128/IAI.01459-08 Gilbert, 2002, Enhanced CD8 T cell immunogenicity and protective efficacy in a mouse malaria model using a recombinant adenoviral vaccine in heterologous prime–boost immunisation regimes, Vaccine, 20, 1039, 10.1016/S0264-410X(01)00450-9 EL-Malky, 2014, Vaccination with Toxoplasma lysate antigen and CpG oligodeoxynucleotides: comparison of immune responses in intranasal versus intramuscular administrations, Parasitol. Res., 113, 2277, 10.1007/s00436-014-3882-0 Abkar, 2017, Oral immunization of mice with Omp31-loaded N-trimethyl chitosan nanoparticles induces high protection against Brucella melitensis infection, Int. J. Nanomed., 12, 8769, 10.2147/IJN.S149774 Amini, 2017, Aluminum hydroxide nanoparticles show strong activity to stimulate Th-1 immune response against tuberculosis, Artif. Cells, Nanomed. Biotechnol., 45, 1331 Nie, 2011, Immunogenicity and protective efficacy of two recombinant pseudorabies viruses expressing Toxoplasma gondii SAG1 and MIC3 proteins, Vet. Parasitol., 181, 215, 10.1016/j.vetpar.2011.04.039 Fang, 2010, Construction and immunogenicity of pseudotype baculovirus expressing Toxoplasma gondii SAG1 protein in BALB/c mice model, Vaccine, 28, 1803, 10.1016/j.vaccine.2009.12.005 Khosroshahi, 2011, Evaluation of the immune response induced by DNA vaccine cocktail expressing complete SAG1 and ROP2 genes against toxoplasmosis, Vaccine, 29, 778, 10.1016/j.vaccine.2010.11.012 Lakhrif, 2018, Targeted delivery of Toxoplasma gondii antigens to dendritic cells promote immunogenicity and protective effciency against toxoplasmosis, Front. Immunol., 9 Zhang, 2010, Construction of Neospora caninum stably expressing TgSAG1 and evaluation of its protective effects against Toxoplasma gondii infection in mice, Vaccine, 28, 7243, 10.1016/j.vaccine.2010.08.096 Ahmadpour, 2017, Evaluation of the immune response in BALB/c mice induced by a novel DNA vaccine expressing GRA 14 against Toxoplasma gondii, Parasite Immunol., 39, 10.1111/pim.12419 Fachado, 2003, Protective effect of a naked DNA vaccine cocktail against lethal toxoplasmosis in mice, Vaccine, 21, 1327, 10.1016/S0264-410X(02)00692-8 Liu, 2014, Toxoplasma gondii: immune response and protective efficacy induced by ROP16/GRA7 multicomponent DNA vaccine with a genetic adjuvant B7-2, Hum. Vaccines Immunother., 10, 184, 10.4161/hv.26703 Foulds, 2006, Th1 memory: implications for vaccine development, Immunol. Rev., 211, 58, 10.1111/j.0105-2896.2006.00400.x Yarovinsky, 2014, Innate immunity to Toxoplasma gondii infection, Nat. Rev. Immunol., 14, 109, 10.1038/nri3598 Kendall, 2000, Antibody and cytokine responses to the cilium-associated respiratory bacillus in BALB/c and C57BL/6 mice, Infect. Immun., 68, 4961, 10.1128/IAI.68.9.4961-4967.2000 Reed, 2013, Key roles of adjuvants in modern vaccines, Nat. Med., 19, 1597, 10.1038/nm.3409 Lin, 2017, Calcium phosphate nanoparticles as a new generation vaccine adjuvant, Expert Rev. Vaccines, 16, 895, 10.1080/14760584.2017.1355733 He, 2015, Advances in aluminum hydroxide-based adjuvant research and its mechanism, Hum. Vaccines Immunother., 11, 477, 10.1080/21645515.2014.1004026 Rahimi, 2017, Immunological evaluation of a DNA cocktail vaccine with co-delivery of calcium phosphate nanoparticles (CaPNs) against the Toxoplasma gondii RH strain in BALB/c mice, Parasitol. Res., 116, 609, 10.1007/s00436-016-5325-6 Flach, 2011, Alum interaction with dendritic cell membrane lipids is essential for its adjuvanticity, Nat. Med., 17, 479, 10.1038/nm.2306 Roozbehani, 2018, Characterization of a multi-epitope peptide with selective MHC-binding capabilities encapsulated in PLGA nanoparticles as a novel vaccine candidate against Toxoplasma gondii infection, Vaccine, 36, 6124, 10.1016/j.vaccine.2018.08.068 Kordbacheh, 2019, Recombinant HcpA-EspA-Tir-Stx2B chimeric protein induces immunity against attachment and toxicity of Escherichia coli O157: H7, Microb. Pathog., 129, 176, 10.1016/j.micpath.2019.02.004 Johnson, 2004, Vaccination protects B cell-deficient mice against an oral challenge with mildly virulent Toxoplasma gondii, Vaccine, 22, 4054, 10.1016/j.vaccine.2004.03.056 Li, 2011, 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, 637, 10.1007/s00436-011-2296-5 Yu, 2012, 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, 481, 10.1016/j.parint.2012.04.001 Dadimoghaddam, 2014, Tissue tropism and parasite burden of Toxoplasma gondii RH strain in experimentally infected mice, Asian. Pac. J. Trop. Med., 7, 521, 10.1016/S1995-7645(14)60087-0