{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T19:47:49Z","timestamp":1790624869048,"version":"4.1.0"},"reference-count":59,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2019,3,29]],"date-time":"2019-03-29T00:00:00Z","timestamp":1553817600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Immunol."],"DOI":"10.3389\/fimmu.2019.00592","type":"journal-article","created":{"date-parts":[[2019,3,29]],"date-time":"2019-03-29T00:26:01Z","timestamp":1553819161000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":37,"title":["Immunogenicity of a Virus-Like-Particle Vaccine Containing Multiple Antigenic Epitopes of Toxoplasma gondii Against Acute and Chronic Toxoplasmosis in Mice"],"prefix":"10.3389","volume":"10","author":[{"given":"Jingjing","family":"Guo","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aihua","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiahui","family":"Sun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenchao","family":"Sha","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kang","family":"Ai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ge","family":"Pan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chunxue","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huaiyu","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hua","family":"Cong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shenyi","family":"He","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2019,3,29]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"1625","DOI":"10.1086\/593019","article-title":"Parasite stage-specific recognition of endogenous Toxoplasma gondii-derived CD8+ T cell epitopes","volume":"198","author":"Frickel","year":"2008","journal-title":"J Infect Dis."},{"key":"B2","doi-asserted-by":"publisher","first-page":"3243","DOI":"10.1016\/j.vaccine.2014.03.092","article-title":"Effectiveness of a novel immunogenic nanoparticle platform for Toxoplasma peptide vaccine in HLA transgenic mice","volume":"32","author":"El","year":"2014","journal-title":"Vaccine"},{"key":"B3","doi-asserted-by":"publisher","first-page":"1117","DOI":"10.1586\/erv.10.113","article-title":"Vaccination against Toxoplasma gondii: an increasing priority for collaborative research","volume":"9","author":"Innes","year":"2010","journal-title":"Expert Rev Vaccines"},{"key":"B4","doi-asserted-by":"publisher","first-page":"592","DOI":"10.1038\/nri3488","article-title":"Applications of nanotechnology for immunology","volume":"13","author":"Smith","year":"2013","journal-title":"Nat Rev Immunol."},{"key":"B5","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1016\/j.copbio.2015.03.014","article-title":"Nanoparticles as synthetic vaccines","volume":"34","author":"Smith","year":"2015","journal-title":"Curr Opin Biotechnol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"1089","DOI":"10.1016\/j.copbio.2013.02.008","article-title":"Virus-like particles: the future of microbial factories and cell-free systems as platforms for vaccine development","volume":"24","author":"Rodr\u00edguez-Limas","year":"2013","journal-title":"Curr Opin Biotechnol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"58","DOI":"10.1016\/j.vaccine.2012.10.083","article-title":"Virus-like particles as a highly efficient vaccine platform: diversity of targets and production systems and advances in clinical development","volume":"31","author":"Kushnir","year":"2012","journal-title":"Vaccine"},{"key":"B8","doi-asserted-by":"publisher","first-page":"143","DOI":"10.1586\/erv.13.10","article-title":"Virus-like particle-based vaccines against hepatitis C virus infection","volume":"12","author":"Bellier","year":"2013","journal-title":"Expert Rev Vaccines"},{"key":"B9","doi-asserted-by":"publisher","first-page":"108","DOI":"10.1016\/j.virol.2004.02.022","article-title":"An amino-terminal segment of hantavirus nucleocapsid protein presented on hepatitis B virus core particles induces a strong and highly cross-reactive antibody response in mice","volume":"323","author":"Geldmacher","year":"2004","journal-title":"Virology"},{"key":"B10","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1586\/erv.12.150","article-title":"Hepatitis B core-based virus-like particles to present heterologous epitopes","volume":"12","author":"Roose","year":"2013","journal-title":"Expert Rev Vaccines"},{"key":"B11","doi-asserted-by":"publisher","first-page":"3977","DOI":"10.1016\/j.vaccine.2010.03.028","article-title":"Identification of T. gondii epitopes, adjuvants, and host genetic factors that influence protection of mice and humans","volume":"28","author":"Tan","year":"2010","journal-title":"Vaccine"},{"key":"B12","first-page":"419","article-title":"Definitive identification of a gene that confers resistance against Toxoplasma cyst burden and encephalitis","volume":"85","author":"Brown","year":"1995","journal-title":"Immunology"},{"key":"B13","doi-asserted-by":"publisher","first-page":"550","DOI":"10.1016\/j.pt.2010.06.004","article-title":"Immunogenetics of Toxoplasma gondii informs vaccine design","volume":"26","author":"Henriquez","year":"2010","journal-title":"Trends Parasitol."},{"key":"B14","doi-asserted-by":"publisher","first-page":"937","DOI":"10.1038\/ni.1629","article-title":"Immunodominant, protective response to the parasite Toxoplasma gondii requires antigen processing in the endoplasmic reticulum","volume":"9","author":"Blanchard","year":"2008","journal-title":"Nat Immunol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"225","DOI":"10.1017\/S0031182001008460","article-title":"Anti-SAG1 peptide antibodies inhibit the penetration of Toxoplasma gondii tachyzoites into enterocyte cell lines","volume":"123","author":"Velge-Roussel","year":"2001","journal-title":"Parasitology"},{"key":"B16","doi-asserted-by":"crossref","first-page":"1353","DOI":"10.1016\/0161-5890(94)90054-X","article-title":"Antigenicity and immunogenicity of P30-derived peptides in experimental models of toxoplasmosis","volume":"31","author":"Godard","year":"1994","journal-title":"Mol Immunol."},{"key":"B17","doi-asserted-by":"publisher","first-page":"447","DOI":"10.1016\/j.jmb.2005.09.028","article-title":"Crystal structure of the complex between the monomeric form of Toxoplasma gondii surface antigen 1 (SAG1) and a monoclonal antibody that mimics the human immune response","volume":"354","author":"Graille","year":"2005","journal-title":"J Mol Biol"},{"key":"B18","doi-asserted-by":"publisher","first-page":"62","DOI":"10.1016\/j.exppara.2006.02.005","article-title":"Toxoplasma gondii: immunogenicity and protection by P30 peptides in a murine model","volume":"114","author":"Siachoque","year":"2006","journal-title":"Exp Parasitol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1016\/j.exppara.2009.06.017","article-title":"Toxoplasma gondii: P30 peptides recognition pattern in human toxoplasmosis","volume":"123","author":"Cardona","year":"2009","journal-title":"Exp. Parasitol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"3279","DOI":"10.1128\/IAI.00425-12","article-title":"The Toxoplasma gondii peptide AS15 elicits CD4 T cells that can control parasite burden","volume":"80","author":"Grover","year":"2012","journal-title":"Infect Immun."},{"key":"B21","doi-asserted-by":"crossref","first-page":"1561","DOI":"10.1093\/infdis\/172.6.1561","article-title":"Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease","volume":"172","author":"Howe","year":"1995","journal-title":"J Infect Dis."},{"key":"B22","doi-asserted-by":"publisher","first-page":"487","DOI":"10.1016\/j.pt.2011.08.001","article-title":"Toxoplasma gondii effectors are master regulators of the inflammatory response","volume":"27","author":"Melo","year":"2011","journal-title":"Trends Parasitol."},{"key":"B23","doi-asserted-by":"crossref","first-page":"3567","DOI":"10.1073\/pnas.1315156111","article-title":"Toxoplasma aldolase is required for metabolism but dispensable for host-cell invasion","volume":"111","author":"Shen","year":"2014","journal-title":"Proc Natl Acad Sci U S A."},{"key":"B24","doi-asserted-by":"publisher","first-page":"19557","DOI":"10.1038\/srep19557","article-title":"Metabolomic profiling of mice serum during toxoplasmosis progression using liquid chromatography-mass spectrometry","volume":"6","author":"Zhou","year":"2016","journal-title":"Sci Rep"},{"key":"B25","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1016\/j.pep.2012.11.002","article-title":"Periplasmic production via the pET expression system of soluble, bioactive human growth hormone","volume":"87","author":"Sockolosky","year":"2013","journal-title":"Protein Expr Purif."},{"key":"B26","doi-asserted-by":"publisher","first-page":"190","DOI":"10.1016\/j.molimm.2012.05.015","article-title":"C\u03b5mX peptide-carrying HBcAg virus-like particles induced antibodies that down-regulate mIgE-B lymphocytes","volume":"52","author":"Lin","year":"2012","journal-title":"Mol Immunol."},{"key":"B27","doi-asserted-by":"publisher","first-page":"43160","DOI":"10.1038\/srep43160","article-title":"Yield optimisation of Hepatitis B virus core particles in E. coli expression system for drug delivery applications","volume":"7","author":"Bin","year":"2017","journal-title":"Sci Rep"},{"key":"B28","doi-asserted-by":"publisher","first-page":"223","DOI":"10.5114\/ceji.2017.70962","article-title":"Immune complex negatively regulates toll-like receptor 3-triggered tumour necrosis factor \u03b1 production in B cells","volume":"42","author":"Qian","year":"2017","journal-title":"Cent Eur J Immunol"},{"key":"B29","doi-asserted-by":"publisher","first-page":"12950","DOI":"10.1128\/JVI.77.24.12950-12960.2003","article-title":"Stability and morphology comparisons of self-assembled virus-like particles from wild-type and mutant human hepatitis B virus capsid proteins","volume":"77","author":"Newman","year":"2003","journal-title":"J Virol."},{"key":"B30","doi-asserted-by":"publisher","first-page":"1972","DOI":"10.1016\/j.vaccine.2008.02.030","article-title":"High immunogenicity of a hydrophilic component of the hepatitis B virus preS1 sequence exposed on the surface of three virus-like particle carriers","volume":"26","author":"Skrastina","year":"2008","journal-title":"Vaccine"},{"key":"B31","doi-asserted-by":"publisher","first-page":"164","DOI":"10.1016\/j.biomaterials.2015.01.056","article-title":"Porous nanoparticles as delivery system of complex antigens for an effective vaccine against acute and chronic Toxoplasma gondii infection","volume":"50","author":"Dimier-Poisson","year":"2015","journal-title":"Biomaterials"},{"key":"B32","doi-asserted-by":"publisher","first-page":"163","DOI":"10.3389\/fcimb.2018.00163","article-title":"Chitosan microsphere used as an effective system to deliver a linked antigenic peptides vaccine protect mice against acute and chronic toxoplasmosis","volume":"8","author":"Guo","year":"2018","journal-title":"Front Cell Infect Microbiol"},{"key":"B33","doi-asserted-by":"publisher","first-page":"2282","DOI":"10.1016\/j.vaccine.2012.01.073","article-title":"Toxoplasma gondii immune mapped protein-1 (TgIMP1) is a novel vaccine candidate against toxoplasmosis","volume":"30","author":"Cui","year":"2012","journal-title":"Vaccine"},{"key":"B34","doi-asserted-by":"publisher","first-page":"4578","DOI":"10.1016\/j.vaccine.2013.07.058","article-title":"The virulence-related rhoptry protein 5 (ROP5) of Toxoplasma gondii is a novel vaccine candidate against toxoplasmosis in mice","volume":"31","author":"Zheng","year":"2013","journal-title":"Vaccine"},{"key":"B35","doi-asserted-by":"publisher","first-page":"7412","DOI":"10.1021\/bi9604800","article-title":"Dimorphism of hepatitis B virus capsids is strongly influenced by the C-terminus of the capsid protein","volume":"35","author":"Zlotnick","year":"1996","journal-title":"Biochemistry"},{"key":"B36","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1128\/mmbr.64.1.51-68.2000","article-title":"Hepatitis B virus biology","volume":"64","author":"Seeger","year":"2000","journal-title":"Microbiol Mol Biol Rev."},{"key":"B37","doi-asserted-by":"publisher","first-page":"1565","DOI":"10.1586\/erv.09.121","article-title":"Use of hepadnavirus core proteins as vaccine platforms","volume":"8","author":"Whitacre","year":"2009","journal-title":"Expert Rev Vaccines"},{"key":"B38","doi-asserted-by":"publisher","first-page":"843","DOI":"10.1016\/j.molcel.2006.04.025","article-title":"Native hepatitis B virions and capsids visualized by electron cryomicroscopy","volume":"22","author":"Dryden","year":"2006","journal-title":"Mol Cell"},{"key":"B39","doi-asserted-by":"publisher","first-page":"3392","DOI":"10.1016\/j.vaccine.2015.04.066","article-title":"Development of a candidate influenza vaccine based on virus-like particles displaying influenza M2e peptide into the immunodominant loop region of hepatitis B core antigen: Insertion of multiple copies of M2e increases immunogenicity and protective efficiency","volume":"33","author":"Ravin","year":"2015","journal-title":"Vaccine"},{"key":"B40","doi-asserted-by":"publisher","first-page":"e0120751","DOI":"10.1371\/journal.pone.0120751","article-title":"Tandem fusion of hepatitis B core antigen allows assembly of virus-like particles in bacteria and plants with enhanced capacity to accommodate foreign proteins","volume":"10","author":"Peyret","year":"2015","journal-title":"PLoS ONE"},{"key":"B41","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1016\/j.imbio.2013.08.008","article-title":"Deletion modification enhances anthrax specific immunity and protective efficacy of a hepatitis B core particle-based anthrax epitope vaccine","volume":"219","author":"Yin","year":"2014","journal-title":"Immunobiology"},{"key":"B42","doi-asserted-by":"publisher","first-page":"842","DOI":"10.1039\/c5sc03892h","article-title":"Peptide-based synthetic vaccines","volume":"7","author":"Skwarczynski","year":"2016","journal-title":"Chem Sci"},{"key":"B43","doi-asserted-by":"publisher","first-page":"651","DOI":"10.1111\/j.1365-3024.2007.00982.x","article-title":"Congenital and acquired toxoplasmosis: diversity and role of antibodies in different compartments of the host","volume":"29","author":"Correa","year":"2007","journal-title":"Parasite Immunol."},{"key":"B44","doi-asserted-by":"publisher","first-page":"1026","DOI":"10.1128\/IAI.68.3.1026-1033.2000","article-title":"B cells are essential for vaccination-induced resistance to virulent Toxoplasma gondii","volume":"68","author":"Sayles","year":"2000","journal-title":"Infect Immun."},{"key":"B45","doi-asserted-by":"publisher","first-page":"216","DOI":"10.3389\/fmicb.2017.00216","article-title":"Immuno-Efficacy of a T. gondii secreted protein with an altered thrombospondin repeat (TgSPATR) As a Novel DNA Vaccine Candidate against Acute Toxoplasmosis in BALB\/c Mice","volume":"8","author":"Zheng","year":"2017","journal-title":"Front Microbiol"},{"key":"B46","doi-asserted-by":"publisher","first-page":"185","DOI":"10.1007\/978-1-4939-1115-8","article-title":"Prediction of conformational B-cell epitopes","volume":"1184","author":"Zhang","year":"2014","journal-title":"Methods Mol Biol."},{"key":"B47","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1128\/CMR.11.4.569","article-title":"Regulation and function of T-cell-mediated immunity during Toxoplasma gondii infection","volume":"11","author":"Denkers","year":"1998","journal-title":"Clin Microbiol Rev."},{"key":"B48","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1093\/intimm\/dxy004","article-title":"Immune response to Toxoplasma gondii","volume":"40","author":"Filisetti","year":"2004","journal-title":"Ann Ist Super Sanita"},{"key":"B49","doi-asserted-by":"publisher","first-page":"609","DOI":"10.3389\/fmicb.2016.00609","article-title":"Evaluation of immunoprotection conferred by the subunit vaccines of GRA2 and GRA5 against acute toxoplasmosis in BALB\/c Mice","volume":"7","author":"Ching","year":"2016","journal-title":"Front Microbiol"},{"key":"B50","doi-asserted-by":"publisher","first-page":"808","DOI":"10.3389\/fmicb.2016.00808","article-title":"Induction of protective immunity against toxoplasmosis in BALB\/c mice vaccinated with Toxoplasma gondii Rhoptry-1","volume":"7","author":"Sonaimuthu","year":"2016","journal-title":"Front Microbiol"},{"key":"B51","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1016\/0166-6851(95)00010-X","article-title":"Characterization of a dense granule antigen of Toxoplasma gondii (GRA6) associated to the network of the parasitophorous vacuole","volume":"70","author":"Lecordier","year":"1995","journal-title":"Mol Biochem Parasitol."},{"key":"B52","doi-asserted-by":"publisher","first-page":"98","DOI":"10.1016\/j.molbiopara.2005.10.011","article-title":"Characterization, biosynthesis and fate of ROP7, a ROP2 related rhoptry protein of Toxoplasma gondii","volume":"146","author":"Hajj","year":"2006","journal-title":"Mol Biochem Parasitol."},{"key":"B53","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1006\/expr.1994.1039","article-title":"Experimental induction of bradyzoite-specific antigen expression and cyst formation by the RH strain of Toxoplasma gondii in vitro","volume":"78","author":"So\u00eate","year":"1994","journal-title":"Exp Parasitol."},{"key":"B54","doi-asserted-by":"publisher","first-page":"605","DOI":"10.3389\/fmicb.2017.00605","article-title":"Induction of Protective Immunity against Toxoplasma gondii in mice by nucleoside triphosphate hydrolase-II (NTPase-II) Self-amplifying RNA vaccine encapsulated in lipid nanoparticle (LNP)","volume":"8","author":"Luo","year":"2017","journal-title":"Front Microbiol"},{"key":"B55","doi-asserted-by":"crossref","first-page":"798","DOI":"10.4049\/jimmunol.157.2.798","article-title":"In the absence of endogenous IL-10, mice acutely infected with Toxoplasma gondii succumb to a lethal immune response dependent on CD4+ T cells and accompanied by overproduction of IL-12, IFN-gamma and TNF-alpha","volume":"157","author":"Gazzinelli","year":"1996","journal-title":"J Immunol."},{"key":"B56","doi-asserted-by":"publisher","first-page":"2512","DOI":"10.1016\/s0264-410x(00)00035-9","article-title":"Induction of protective immunity against toxoplasmosis in mice by DNA immunization with a plasmid encoding Toxoplasma gondii GRA4 gene","volume":"18","author":"Desolme","year":"2000","journal-title":"Vaccine"},{"key":"B57","doi-asserted-by":"publisher","first-page":"487","DOI":"10.1186\/1471-2334-14-487","article-title":"Protective efficacy of Toxoplasma gondii calcium-dependent protein kinase 1 (TgCDPK1) adjuvated with recombinant IL-15 and IL-21 against experimental toxoplasmosis in mice","volume":"14","author":"Chen","year":"2014","journal-title":"BMC Infect Dis."},{"key":"B58","doi-asserted-by":"publisher","first-page":"730","DOI":"10.3389\/fimmu.2017.00730","article-title":"Immunization with Toxoplasma gondii GRA17 deletion mutant induces partial protection and survival in challenged mice","volume":"8","author":"Wang","year":"2017","journal-title":"Front Immunol"},{"key":"B59","doi-asserted-by":"publisher","first-page":"508","DOI":"10.1089\/vim.2016.0135","article-title":"Major immunodominant region of Hepatitis B virus core antigen as a delivery vector to improve the immunogenicity of the fusion antigen ROP2-SAG1 multiepitope from Toxoplasma gondii in Mice","volume":"30","author":"Wang","year":"2017","journal-title":"Viral Immunol."}],"container-title":["Frontiers in Immunology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fimmu.2019.00592\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,9,14]],"date-time":"2023-09-14T20:31:28Z","timestamp":1694723488000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fimmu.2019.00592\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,3,29]]},"references-count":59,"alternative-id":["10.3389\/fimmu.2019.00592"],"URL":"https:\/\/doi.org\/10.3389\/fimmu.2019.00592","relation":{},"ISSN":["1664-3224"],"issn-type":[{"value":"1664-3224","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,3,29]]},"article-number":"592"}}