{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T12:53:45Z","timestamp":1789044825178,"version":"build-2803163510"},"reference-count":66,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,1,13]],"date-time":"2022-01-13T00:00:00Z","timestamp":1642032000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100008732","name":"Uehara Memorial Foundation","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100008732","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100015103","name":"Japan Racing Association","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100015103","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001700","name":"Ministry of Education, Culture, Sports, Science and Technology","doi-asserted-by":"publisher","award":["Young Scientists (B) (17K15677), Young Scientists (19K16628)"],"award-info":[{"award-number":["Young Scientists (B) (17K15677), Young Scientists (19K16628)"]}],"id":[{"id":"10.13039\/501100001700","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Infect. Microbiol."],"abstract":"<jats:p><jats:italic>Toxoplasma gondii<\/jats:italic>chronically infects the brain as latent cysts containing bradyzoites and causes various effects in the host. Recently, the molecular mechanisms of cyst formation in the mouse brain have been elucidated, but those in the human brain remain largely unknown. Here, we show that abnormal glutamine metabolism caused by both interferon-\u03b3 (IFN-\u03b3) stimulation and<jats:italic>T. gondii<\/jats:italic>infection induce cyst formation in human neuroblastoma cells regardless of the anti-<jats:italic>T. gondii<\/jats:italic>host factor nitric oxide (NO) level or Indoleamine 2,3-dioxygenase-1 (IDO1) expression. IFN-\u03b3 stimulation promoted intracellular glutamine degradation in human neuronal cells. Additionally,<jats:italic>T. gondii<\/jats:italic>infection inhibited the mRNA expression of the host glutamine transporters SLC38A1 and SLC38A2. These dual effects led to glutamine starvation and triggered<jats:italic>T. gondii<\/jats:italic>stage conversion in human neuronal cells. Furthermore, these mechanisms are conserved in human iPSC-derived glutamatergic neurons. Taken together, our data suggest that glutamine starvation in host cells is an important trigger of<jats:italic>T. gondii<\/jats:italic>stage conversion in human neurons.<\/jats:p>","DOI":"10.3389\/fcimb.2021.788303","type":"journal-article","created":{"date-parts":[[2022,1,13]],"date-time":"2022-01-13T06:46:11Z","timestamp":1642056371000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":12,"title":["Depletion of Intracellular Glutamine Pools Triggers Toxoplasma gondii Stage Conversion in Human Glutamatergic Neurons"],"prefix":"10.3389","volume":"11","author":[{"given":"Hironori","family":"Bando","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yasuhiro","family":"Fukuda","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nina","family":"Watanabe","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeje Temitope","family":"Olawale","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kentaro","family":"Kato","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,1,13]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"273","DOI":"10.2147\/dddt.S60973","article-title":"Drugs in Development for Toxoplasmosis: Advances, Challenges, and Current Status","volume":"11","author":"Alday","year":"2017","journal-title":"Drug Des. Devel. Ther."},{"key":"B2","doi-asserted-by":"publisher","first-page":"641","DOI":"10.1111\/j.1471-4159.2006.03913.x","article-title":"The Glutamate\/GABA-Glutamine Cycle: Aspects of Transport, Neurotransmitter Homeostasis and Ammonia Transfer","volume":"98","author":"Bak","year":"2006","journal-title":"J. Neurochem."},{"key":"B3","doi-asserted-by":"publisher","DOI":"10.1128\/mBio.01738-18","article-title":"Inducible Nitric Oxide Synthase Is a Key Host Factor for Toxoplasma GRA15-Dependent Disruption of the Gamma Interferon-Induced Antiparasitic Human Response","volume":"9","author":"Bando","year":"2018","journal-title":"MBio"},{"key":"B4","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2019.00140","article-title":"Toxoplasma Effector GRA15-Dependent Suppression of IFN-\u03b3-Induced Antiparasitic Response in Human Neurons","volume":"9","author":"Bando","year":"2019","journal-title":"Front. Cell Infect. Microbiol."},{"key":"B5","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2018.02073","article-title":"Toxoplasma Effector TgIST Targets Host IDO1 to Antagonize the IFN-Gamma-Induced Anti-Parasitic Response in Human Cells","volume":"9","author":"Bando","year":"2018","journal-title":"Front. Immunol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1016\/j.jchemneu.2009.03.004","article-title":"Glutamatergic Neurotransmission in the Nucleus Tractus Solitarii: Structural and Functional Characteristics","volume":"38","author":"Baude","year":"2009","journal-title":"J. Chem. Neuroanat."},{"key":"B7","doi-asserted-by":"publisher","first-page":"8485","DOI":"10.4049\/jimmunol.181.12.8485","article-title":"Dendritic Cells Expressing Plasmacytoid Marker PDCA-1 are Trojan Horses During Toxoplasma Gondii Infection","volume":"181","author":"Bierly","year":"2008","journal-title":"J. Immunol."},{"key":"B8","doi-asserted-by":"publisher","first-page":"12998","DOI":"10.1073\/pnas.0903831106","article-title":"Host-Derived Glucose and its Transporter in the Obligate Intracellular Pathogen Toxoplasma Gondii are Dispensable by Glutaminolysis","volume":"106","author":"Blume","year":"2009","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B9","doi-asserted-by":"publisher","first-page":"1141","DOI":"10.1128\/iai.61.3.1141-1145.1993","article-title":"Induction of Bradyzoite-Specific Toxoplasma Gondii Antigens in Gamma Interferon-Treated Mouse Macrophages","volume":"61","author":"Bohne","year":"1993","journal-title":"Infect. Immun."},{"key":"B10","doi-asserted-by":"publisher","first-page":"1761","DOI":"10.1128\/iai.62.5.1761-1767.1994","article-title":"Reduced Replication of Toxoplasma Gondii is Necessary for Induction of Bradyzoite-Specific Antigens: A Possible Role for Nitric Oxide in Triggering Stage Conversion","volume":"62","author":"Bohne","year":"1994","journal-title":"Infect. Immun."},{"key":"B11","doi-asserted-by":"publisher","first-page":"935","DOI":"10.1016\/j.ijpara.2009.02.003","article-title":"Toxoplasma Gondii: 25 Years and 25 Major Advances for the Field","volume":"39","author":"Boothroyd","year":"2009","journal-title":"Int. J. Parasitol."},{"key":"B12","doi-asserted-by":"publisher","first-page":"595","DOI":"10.1007\/s10545-012-9546-2","article-title":"Ammonia Toxicity to the Brain","volume":"36","author":"Braissant","year":"2013","journal-title":"J. Inherit. Metab. Dis."},{"key":"B13","doi-asserted-by":"publisher","first-page":"2375","DOI":"10.1182\/blood-2005-03-0979","article-title":"A Two-Step Induction of Indoleamine 2,3 Dioxygenase (IDO) Activity During Dendritic-Cell Maturation","volume":"106","author":"Braun","year":"2005","journal-title":"Blood"},{"key":"B14","doi-asserted-by":"publisher","first-page":"e01428","DOI":"10.1128\/mBio.01428-15","article-title":"Toxoplasma Gondii Infections Alter GABAergic Synapses and Signaling in the Central Nervous System","volume":"6","author":"Brooks","year":"2015","journal-title":"mBio"},{"key":"B15","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1005447","article-title":"Neurons are the Primary Target Cell for the Brain-Tropic Intracellular Parasite Toxoplasma Gondii","volume":"12","author":"Cabral","year":"2016","journal-title":"PloS Pathog."},{"key":"B16","doi-asserted-by":"publisher","DOI":"10.1016\/j.intimp.2020.106302","article-title":"Arctigenin Ameliorates Depression-Like Behaviors in Toxoplasma Gondii-Infected Intermediate Hosts via the TLR4\/NF-\u03baB and TNFR1\/NF-\u03baB Signaling Pathways","volume":"82","author":"Cheng","year":"2020","journal-title":"Int. Immunopharmacol."},{"key":"B17","doi-asserted-by":"publisher","first-page":"E1913","DOI":"10.1073\/pnas.1220272110","article-title":"Motile Invaded Neutrophils in the Small Intestine of Toxoplasma Gondii-Infected Mice Reveal a Potential Mechanism for Parasite Spread","volume":"110","author":"Coombes","year":"2013","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B18","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1005643","article-title":"GLT-1-Dependent Disruption of CNS Glutamate Homeostasis and Neuronal Function by the Protozoan Parasite Toxoplasma Gondii","volume":"12","author":"David","year":"2016","journal-title":"PloS Pathog."},{"key":"B19","doi-asserted-by":"publisher","first-page":"877","DOI":"10.1016\/j.ijpara.2009.01.005","article-title":"History of the Discovery of the Life Cycle of Toxoplasma Gondii","volume":"39","author":"Dubey","year":"2009","journal-title":"Int. J. Parasitol."},{"key":"B20","volume-title":"Toxoplasmosis of Animals and Humans","author":"Dubey","year":"2010"},{"key":"B21","doi-asserted-by":"publisher","first-page":"204","DOI":"10.1038\/nrn2969","article-title":"From Glutamate Co-Release to Vesicular Synergy: Vesicular Glutamate Transporters","volume":"12","author":"El Mestikawy","year":"2011","journal-title":"Nat. Rev. Neurosci."},{"key":"B22","first-page":"48","article-title":"Toxoplasma and Toxoplasmosis","volume":"142","author":"El-On","year":"2003","journal-title":"Harefuah"},{"key":"B23","doi-asserted-by":"publisher","first-page":"245","DOI":"10.1016\/0301-0082(90)90013-7","article-title":"Metabolism and Role of Glutamate in Mammalian Brain","volume":"35","author":"Ereci\u0144ska","year":"1990","journal-title":"Prog. Neurobiol."},{"key":"B24","first-page":"111","article-title":"An Ultrastructural Study of the Effect of Treatment With Atovaquone in Brains of Mice Chronically Infected With the ME49 Strain of Toxoplasma Gondii","volume":"75","author":"Ferguson","year":"1994","journal-title":"Int. J. Exp. Pathol."},{"key":"B25","doi-asserted-by":"publisher","first-page":"516","DOI":"10.1002\/jnr.490320407","article-title":"Expression of the Class III Beta-Tubulin Isotype in Developing Neurons in Culture","volume":"32","author":"Ferreira","year":"1992","journal-title":"J. Neurosci. Res."},{"key":"B26","doi-asserted-by":"publisher","first-page":"381","DOI":"10.1016\/j.ijmm.2008.10.002","article-title":"Primary Skeletal Muscle Cells Trigger Spontaneous Toxoplasma Gondii Tachyzoite-to-Bradyzoite Conversion at Higher Rates Than Fibroblasts","volume":"299","author":"Ferreira-Da-Silva Mda","year":"2009","journal-title":"Int. J. Med. Microbiol."},{"key":"B27","doi-asserted-by":"publisher","first-page":"323","DOI":"10.1016\/j.ijpara.2003.12.001","article-title":"Toxoplasma Gondii Lacks the Enzymes Required for De Novo Arginine Biosynthesis and Arginine Starvation Triggers Cyst Formation","volume":"34","author":"Fox","year":"2004","journal-title":"Int. J. Parasitol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"178","DOI":"10.1056\/NEJM198001173020316","article-title":"Hepatitis in Toxoplasmosis","volume":"302","author":"Frenkel","year":"1980","journal-title":"N. Engl. J. Med."},{"key":"B29","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1016\/S0169-4758(99)01614-2","article-title":"No NO Production During Human Toxoplasma Infection","volume":"16","author":"Gomez-Marin","year":"2000","journal-title":"Parasitol. Today"},{"key":"B30","doi-asserted-by":"publisher","first-page":"61","DOI":"10.1016\/j.neuroscience.2004.09.023","article-title":"Immunohistochemical Localization of the Amino Acid Transporter SNAT2 in the Rat Brain","volume":"130","author":"Gonz\u00e1lez-Gonz\u00e1lez","year":"2005","journal-title":"Neuroscience"},{"key":"B31","first-page":"1171","article-title":"Effects of Drug Therapy on Toxoplasma Cysts in an Animal Model of Acute and Chronic Disease","volume":"39","author":"Gormley","year":"1998","journal-title":"Invest. Ophthalmol. Vis. Sci."},{"key":"B32","doi-asserted-by":"publisher","first-page":"1150","DOI":"10.1097\/00005072-199611000-00006","article-title":"Growth and Development of Toxoplasma Gondii in Human Neurons and Astrocytes","volume":"55","author":"Halonen","year":"1996","journal-title":"J. Neuropathol. Exp. Neurol."},{"key":"B33","doi-asserted-by":"publisher","first-page":"668","DOI":"10.1128\/iai.57.3.668-672.1989","article-title":"Identification of Stage-Specific Antigens of Toxoplasma Gondii","volume":"57","author":"Kasper","year":"1989","journal-title":"Infect. Immun."},{"key":"B34","doi-asserted-by":"publisher","first-page":"152","DOI":"10.1016\/j.brainres.2018.08.019","article-title":"Distributions of GABAergic and Glutamatergic Neurons in the Brains of a Diurnal and Nocturnal Rodent","volume":"1700","author":"Langel","year":"2018","journal-title":"Brain Res."},{"key":"B35","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0109803","article-title":"Toxoplasma Gondii is Dependent on Glutamine and Alters Migratory Profile of Infected Host Bone Marrow Derived Immune Cells Through SNAT2 and CXCR4 Pathways","volume":"9","author":"Lee","year":"2014","journal-title":"PloS One"},{"key":"B36","doi-asserted-by":"publisher","DOI":"10.1128\/iai.00139-19","article-title":"Persistent Toxoplasma Infection of the Brain Induced Neurodegeneration Associated With Activation of Complement and Microglia","volume":"87","author":"Li","year":"2019","journal-title":"Infect. Immun."},{"key":"B37","doi-asserted-by":"publisher","first-page":"203","DOI":"10.15698\/mic2017.07.579","article-title":"Impact of the Host on Toxoplasma Stage Differentiation","volume":"4","author":"L\u00fcder","year":"2017","journal-title":"Microb. Cell"},{"key":"B38","doi-asserted-by":"publisher","first-page":"198","DOI":"10.1016\/s1471-4922(02)02248-1","article-title":"Toxoplasma Gondii Tachyzoite-Bradyzoite Interconversion","volume":"18","author":"Lyons","year":"2002","journal-title":"Trends Parasitol."},{"key":"B39","doi-asserted-by":"publisher","first-page":"2013","DOI":"10.1084\/jem.20131272","article-title":"Selective and Strain-Specific NFAT4 Activation by the Toxoplasma Gondii Polymorphic Dense Granule Protein GRA6","volume":"211","author":"Ma","year":"2014","journal-title":"J. Exp. Med."},{"key":"B40","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1007\/978-1-4939-9857-9_15","article-title":"Toxoplasma Gondii: Bradyzoite Differentiation In Vitro and In Vivo","volume":"2071","author":"Mayoral","year":"2020","journal-title":"Methods Mol. Biol."},{"key":"B41","doi-asserted-by":"publisher","first-page":"554","DOI":"10.1086\/590149","article-title":"Management of Toxoplasma Gondii Infection During Pregnancy","volume":"47","author":"Montoya","year":"2008","journal-title":"Clin. Infect. Dis."},{"key":"B42","doi-asserted-by":"publisher","first-page":"3328","DOI":"10.4049\/jimmunol.1302822","article-title":"Role of Mouse and Human Autophagy Proteins in IFN-Gamma-Induced Cell-Autonomous Responses Against Toxoplasma Gondii","volume":"192","author":"Ohshima","year":"2014","journal-title":"J. Immunol."},{"key":"B43","doi-asserted-by":"publisher","first-page":"153","DOI":"10.1016\/j.micinf.2015.09.023","article-title":"Infection and Characterization of Toxoplasma Gondii in Human Induced Neurons From Patients With Brain Disorders and Healthy Controls","volume":"18","author":"Passeri","year":"2016","journal-title":"Microbes Infect."},{"key":"B44","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1089\/jir.1986.6.267","article-title":"Characterization of an Indoleamine 2,3-Dioxygenase Induced by Gamma-Interferon in Cultured Human Fibroblasts","volume":"6","author":"Pfefferkorn","year":"1986","journal-title":"J. Interferon Res."},{"key":"B45","doi-asserted-by":"publisher","first-page":"e105","DOI":"10.1371\/journal.ppat.0020105","article-title":"Changes in the Expression of Human Cell Division Autoantigen-1 Influence Toxoplasma Gondii Growth and Development","volume":"2","author":"Radke","year":"2006","journal-title":"PloS Pathog."},{"key":"B46","doi-asserted-by":"publisher","first-page":"6871","DOI":"10.1073\/pnas.1300059110","article-title":"ApiAP2 Transcription Factor Restricts Development of the Toxoplasma Tissue Cyst","volume":"110","author":"Radke","year":"2013","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B47","doi-asserted-by":"publisher","first-page":"264","DOI":"10.1128\/cmr.05013-11","article-title":"Epidemiology of and Diagnostic Strategies for Toxoplasmosis","volume":"25","author":"Robert-Gangneux","year":"2012","journal-title":"Clin. Microbiol. Rev."},{"key":"B48","doi-asserted-by":"publisher","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":"B49","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1111\/acps.12423","article-title":"Beyond the Association. Toxoplasma Gondii in Schizophrenia, Bipolar Disorder, and Addiction: Systematic Review and Meta-Analysis","volume":"132","author":"Sutterland","year":"2015","journal-title":"Acta Psychiatr. Scand."},{"key":"B50","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1111\/cmi.12342","article-title":"Withdrawal of Skeletal Muscle Cells From Cell Cycle Progression Triggers Differentiation of Toxoplasma Gondii Towards the Bradyzoite Stage","volume":"17","author":"Swierzy","year":"2015","journal-title":"Cell Microbiol."},{"key":"B51","doi-asserted-by":"publisher","first-page":"496","DOI":"10.1016\/j.micinf.2016.03.012","article-title":"Use of Human Induced Pluripotent Stem Cell-Derived Neurons as a Model for Cerebral Toxoplasmosis","volume":"18","author":"Tanaka","year":"2016","journal-title":"Microbes Infect."},{"key":"B52","doi-asserted-by":"publisher","first-page":"2091","DOI":"10.3791\/2091","article-title":"Toxoplasma Gondii Cyst Wall Formation in Activated Bone Marrow-Derived Macrophages and Bradyzoite Conditions","volume":"42","author":"Tobin","year":"2010","journal-title":"J. Vis. Exp."},{"key":"B53","doi-asserted-by":"publisher","first-page":"3750","DOI":"10.1128\/iai.59.10.3750-3753.1991","article-title":"Characterization of Bradyzoite-Specific Antigens of Toxoplasma Gondii","volume":"59","author":"Tomavo","year":"1991","journal-title":"Infect. Immun."},{"key":"B54","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1003823","article-title":"The Toxoplasma Gondii Cyst Wall Protein CST1 is Critical for Cyst Wall Integrity and Promotes Bradyzoite Persistence","volume":"9","author":"Tomita","year":"2013","journal-title":"PloS Pathog."},{"key":"B55","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1007\/s11010-009-0219-x","article-title":"Nitric Oxide and Nitric Oxide Synthase Isoforms in the Normal, Hypertrophic, and Failing Heart","volume":"333","author":"Umar","year":"2010","journal-title":"Mol. Cell Biochem."},{"key":"B56","doi-asserted-by":"publisher","first-page":"515","DOI":"10.1016\/j.parint.2008.06.004","article-title":"Dissemination of Extracellular and Intracellular Toxoplasma Gondii Tachyzoites in the Blood Flow","volume":"57","author":"Unno","year":"2008","journal-title":"Parasitol. Int."},{"key":"B57","doi-asserted-by":"publisher","first-page":"4049","DOI":"10.1074\/jbc.275.6.4049","article-title":"Cloning and Functional Identification of a Neuronal Glutamine Transporter","volume":"275","author":"Varoqui","year":"2000","journal-title":"J. Biol. Chem."},{"key":"B58","doi-asserted-by":"publisher","first-page":"359","DOI":"10.1016\/j.cell.2019.12.013","article-title":"Identification of a Master Regulator of Differentiation in Toxoplasma","volume":"180","author":"Waldman","year":"2020","journal-title":"Cell"},{"key":"B59","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1093\/mutage\/gey023","article-title":"Effects of Ammonia on Apoptosis and Oxidative Stress in Bovine Mammary Epithelial Cells","volume":"33","author":"Wang","year":"2018","journal-title":"Mutagenesis"},{"key":"B60","doi-asserted-by":"publisher","first-page":"e01155","DOI":"10.1128\/mBio.01155-15","article-title":"Novel Approaches Reveal That Toxoplasma Gondii Bradyzoites Within Tissue Cysts Are Dynamic and Replicating Entities In Vivo","volume":"6","author":"Watts","year":"2015","journal-title":"mBio"},{"key":"B61","doi-asserted-by":"publisher","first-page":"150","DOI":"10.1111\/j.1550-7408.1995.tb01556.x","article-title":"A Cell Culture System for Study of the Development of Toxoplasma Gondii Bradyzoites","volume":"42","author":"Weiss","year":"1995","journal-title":"J. Eukaryot. Microbiol."},{"key":"B62","doi-asserted-by":"publisher","first-page":"1096","DOI":"10.1021\/acs.jmedchem.8b00961","article-title":"Overview of the Development of Glutaminase Inhibitors: Achievements and Future Directions","volume":"62","author":"Xu","year":"2019","journal-title":"J. Med. Chem."},{"key":"B63","doi-asserted-by":"publisher","first-page":"302","DOI":"10.1016\/j.immuni.2012.06.009","article-title":"A Cluster of Interferon-Gamma-Inducible P65 GTPases Plays a Critical Role in Host Defense Against Toxoplasma Gondii","volume":"37","author":"Yamamoto","year":"2012","journal-title":"Immunity"},{"key":"B64","doi-asserted-by":"crossref","first-page":"1340","DOI":"10.4049\/jimmunol.160.3.1340","article-title":"Decreased Resistance of TNF Receptor P55- and P75-Deficient Mice to Chronic Toxoplasmosis Despite Normal Activation of Inducible Nitric Oxide Synthase In Vivo","volume":"160","author":"Yap","year":"1998","journal-title":"J. Immunol."},{"key":"B65","doi-asserted-by":"publisher","first-page":"530","DOI":"10.1038\/nrn.2017.85","article-title":"Neuronal Cell-Type Classification: Challenges, Opportunities and the Path Forward","volume":"18","author":"Zeng","year":"2017","journal-title":"Nat. Rev. Neurosci."},{"key":"B66","doi-asserted-by":"publisher","first-page":"228","DOI":"10.1006\/expr.1995.1028","article-title":"Toxoplasma Gondii: Identification and Characterization of a Cyst Molecule","volume":"80","author":"Zhang","year":"1995","journal-title":"Exp. Parasitol."}],"container-title":["Frontiers in Cellular and Infection Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2021.788303\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,22]],"date-time":"2023-01-22T20:23:48Z","timestamp":1674419028000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2021.788303\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,1,13]]},"references-count":66,"alternative-id":["10.3389\/fcimb.2021.788303"],"URL":"https:\/\/doi.org\/10.3389\/fcimb.2021.788303","relation":{},"ISSN":["2235-2988"],"issn-type":[{"value":"2235-2988","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,1,13]]},"article-number":"788303"}}