{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,26]],"date-time":"2026-08-26T09:41:34Z","timestamp":1787737294900,"version":"build-2784847793"},"reference-count":47,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2023,9,1]],"date-time":"2023-09-01T00:00:00Z","timestamp":1693526400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2023,9,1]],"date-time":"2023-09-01T00:00:00Z","timestamp":1693526400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2023,9,1]],"date-time":"2023-09-01T00:00:00Z","timestamp":1693526400000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-017"},{"start":{"date-parts":[[2023,9,1]],"date-time":"2023-09-01T00:00:00Z","timestamp":1693526400000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-037"},{"start":{"date-parts":[[2023,9,1]],"date-time":"2023-09-01T00:00:00Z","timestamp":1693526400000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-012"},{"start":{"date-parts":[[2023,9,1]],"date-time":"2023-09-01T00:00:00Z","timestamp":1693526400000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-029"},{"start":{"date-parts":[[2023,9,1]],"date-time":"2023-09-01T00:00:00Z","timestamp":1693526400000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-004"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32060801"],"award-info":[{"award-number":["32060801"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32260888"],"award-info":[{"award-number":["32260888"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["2017YFD0501200"],"award-info":[{"award-number":["2017YFD0501200"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Acta Tropica"],"published-print":{"date-parts":[[2023,9]]},"DOI":"10.1016\/j.actatropica.2023.106977","type":"journal-article","created":{"date-parts":[[2023,7,1]],"date-time":"2023-07-01T10:57:28Z","timestamp":1688209048000},"page":"106977","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":5,"special_numbering":"C","title":["The regulatory roles of Fasciola hepatica GSTO1 protein in inflammatory cytokine expression and apoptosis in murine macrophages"],"prefix":"10.1016","volume":"245","author":[{"given":"Wang","family":"Xifeng","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhang","family":"Jiahua","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li","family":"Ningxing","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhang","family":"Guowu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shang","family":"Yunxia","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cai","family":"Xuepeng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qiao","family":"Jun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xia","family":"Xianzhu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Meng","family":"Qingling","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.actatropica.2023.106977_bib0001","doi-asserted-by":"crossref","first-page":"2275","DOI":"10.1038\/s41598-018-37652-x","article-title":"Fasciola hepatica GST downregulates NF-\u03baB pathway effectors and inflammatory cytokines while promoting survival in a mouse septic shock model","volume":"9","author":"Aguayo","year":"2019","journal-title":"Sci. Rep."},{"key":"10.1016\/j.actatropica.2023.106977_bib0002","doi-asserted-by":"crossref","DOI":"10.3389\/fimmu.2021.716469","article-title":"NF-\u03baB: at the borders of autoimmunity and inflammation","volume":"12","author":"Barnabei","year":"2021","journal-title":"Front. Immunol."},{"key":"10.1016\/j.actatropica.2023.106977_bib0003","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1096\/fj.06-7426com","article-title":"Oxidative stress in Caenorhabditis elegans: protective effects of the Omega class glutathione transferase (GSTO-1)","volume":"22","author":"Burmeister","year":"2008","journal-title":"FASEB. J."},{"key":"10.1016\/j.actatropica.2023.106977_bib0004","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1016\/0167-5699(94)90150-3","article-title":"Macrophage activation revisited","volume":"15","author":"Celada","year":"1994","journal-title":"Immunol. Today."},{"key":"10.1016\/j.actatropica.2023.106977_bib0005","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1111\/j.1574-6976.2000.tb00532.x","article-title":"Heterologous protein expression in the methylotrophic yeast Pichia pastoris","volume":"24","author":"Cereghino","year":"2000","journal-title":"FEMS. Microbiol. Rev."},{"key":"10.1016\/j.actatropica.2023.106977_bib0006","doi-asserted-by":"crossref","first-page":"273","DOI":"10.3892\/mmr.2021.11912","article-title":"Schistosoma japonicum cystatin suppresses osteoclastogenesis via manipulating the NF-\u03baB signaling pathway","volume":"23","author":"Chen","year":"2021","journal-title":"Mol. Med. Rep."},{"key":"10.1016\/j.actatropica.2023.106977_bib0007","article-title":"Quantitation of apoptosis and necrosis by annexin V binding, propidium iodide uptake, and flow cytometry","volume":"10","author":"Crowley","year":"2016","journal-title":"Cold. Spring. Harb. Protoc."},{"key":"10.1016\/j.actatropica.2023.106977_bib0008","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/S0304-4165(98)00132-9","article-title":"Asparagine-linked glycosylation in the yeast Golgi","volume":"1426","author":"Dean","year":"1999","journal-title":"Biochim. Biophys. Acta."},{"key":"10.1016\/j.actatropica.2023.106977_bib0009","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pntd.0007087","article-title":"Surface molecules of extracellular vesicles secreted by the helminth pathogen Fasciola hepatica direct their internalisation by host cells","volume":"13","author":"De la Torre-Escudero","year":"2019","journal-title":"PLoS. Negl. Trop. Dis."},{"key":"10.1016\/j.actatropica.2023.106977_bib0010","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1128\/IAI.73.1.166-173.2005","article-title":"Thioredoxin peroxidase secreted by Fasciola hepatica induces the alternative activation of macrophages","volume":"73","author":"Donnelly","year":"2005","journal-title":"Infect. Immun."},{"key":"10.1016\/j.actatropica.2023.106977_bib0011","doi-asserted-by":"crossref","first-page":"4022","DOI":"10.1096\/fj.08-106278","article-title":"Helminth 2-Cys peroxiredoxin drives Th2 responses through a mechanism involving alternatively activated macrophages","volume":"22","author":"Donnelly","year":"2008","journal-title":"FASEB. J."},{"key":"10.1016\/j.actatropica.2023.106977_bib0012","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/j.vetpar.2017.03.015","article-title":"Apoptosis of peritoneal leucocytes during early stages of Fasciola hepatica infections in sheep","volume":"238","author":"Escamilla","year":"2017","journal-title":"Vet. Parasitol."},{"key":"10.1016\/j.actatropica.2023.106977_bib0013","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1007\/978-1-0716-0475-5_11","article-title":"Purification of native Fasciola hepatica fatty acid-binding protein and induction of alternative activation of human macrophages","volume":"2137","author":"Figueroa-Santiago","year":"2020","journal-title":"Methods. Mol. Biol."},{"key":"10.1016\/j.actatropica.2023.106977_bib0014","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1128\/IAI.00732-07","article-title":"Possible role for Toll-like receptors in interaction of Fasciola hepatica excretory\/secretory products with bovine macrophages","volume":"76","author":"Flynn","year":"2008","journal-title":"Infect. Immun."},{"key":"10.1016\/j.actatropica.2023.106977_bib0015","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/S0039-9140(03)00238-8","article-title":"Study of interactions between DNA-ethidium bromide (EB) and DNA-acridine orange (AO), in solution, using hanging mercury drop electrode (HMDE)","volume":"61","author":"Gherghi","year":"2003","journal-title":"Talanta"},{"key":"10.1016\/j.actatropica.2023.106977_bib0016","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1111\/j.1600-065X.1991.tb00822.x","article-title":"Cell death mechanisms and the immune system","volume":"121","author":"Golstein","year":"1991","journal-title":"Immunol. Rev."},{"key":"10.1016\/j.actatropica.2023.106977_bib0017","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1016\/j.vetimm.2012.06.022","article-title":"Fasciola hepatica products induce apoptosis of peritoneal macrophages","volume":"148","author":"Guasconi","year":"2012","journal-title":"Vet. Immunol. Immunopathol."},{"key":"10.1016\/j.actatropica.2023.106977_bib0018","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1007\/978-1-0716-0475-5_9","article-title":"Immunomodula -tory effect of Fasciola hepatica excretory-secretory products on macrophages","volume":"2137","author":"Guasconi","year":"2020","journal-title":"Methods. Mol. Biol."},{"key":"10.1016\/j.actatropica.2023.106977_bib0019","doi-asserted-by":"crossref","first-page":"987","DOI":"10.1038\/ni1112","article-title":"Toll-like receptor control of the adaptive immune responses","volume":"5","author":"Iwasaki","year":"2004","journal-title":"Nat. Immunol."},{"key":"10.1016\/j.actatropica.2023.106977_bib0020","doi-asserted-by":"crossref","first-page":"7454","DOI":"10.4049\/jimmunol.173.12.7454","article-title":"Helminth antigens modulate TLR-initiated dendritic cell activation","volume":"173","author":"Kane","year":"2004","journal-title":"J. Immunol."},{"key":"10.1016\/j.actatropica.2023.106977_bib0021","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1186\/s13071-016-1622-2","article-title":"Clonorchis sinensis omega-class glutathione transferases play major roles in the protection of the reproductive system during maturation and the response to oxidative stress","volume":"9","author":"Kim","year":"2016","journal-title":"Parasit. Vectors."},{"key":"10.1016\/j.actatropica.2023.106977_bib0022","doi-asserted-by":"crossref","first-page":"448","DOI":"10.1016\/j.coi.2007.07.002","article-title":"Alternatively activated macrophages in helminth infections","volume":"19","author":"Kreider","year":"2007","journal-title":"Curr. Opin. Immunol."},{"issue":"5","key":"10.1016\/j.actatropica.2023.106977_bib0023","doi-asserted-by":"crossref","first-page":"e1666","DOI":"10.1371\/journal.pntd.0001666","article-title":"The Sigma class glutathione transferase from the liver fluke Fasciola hepatica","volume":"6","author":"LaCourse","year":"2012","journal-title":"PLoS. Negl. Trop. Dis."},{"key":"10.1016\/j.actatropica.2023.106977_bib0024","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1006\/bbrc.1993.1410","article-title":"Removals of hydrogen peroxide and hydroxyl radical by thiol-specific antioxidant protein as a possible role in vivo","volume":"192","author":"Lim","year":"1993","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"10.1016\/j.actatropica.2023.106977_bib0025","doi-asserted-by":"crossref","first-page":"793","DOI":"10.1016\/j.vaccine.2020.10.061","article-title":"Recombinant H7 hemagglutinin expressed in glycoengineered Pichia pastoris forms nanoparticles that protect mice from challenge with H7N9 influenza virus","volume":"38","author":"Liu","year":"2020","journal-title":"Vaccine"},{"key":"10.1016\/j.actatropica.2023.106977_bib0026","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/j.cyto.2008.01.006","article-title":"LPS\/TLR4 signal transduction pathway","volume":"42","author":"Lu","year":"2008","journal-title":"Cytokine"},{"key":"10.1016\/j.actatropica.2023.106977_bib0027","doi-asserted-by":"crossref","first-page":"3924","DOI":"10.4049\/jimmunol.1401182","article-title":"Fasciola hepatica fatty acid binding protein inhibits TLR4 activation and suppresses the inflammatory cytokines induced by lipopolysaccharide in vitro and in vivo","volume":"194","author":"Martin","year":"2015","journal-title":"J. Immunol."},{"key":"10.1016\/j.actatropica.2023.106977_bib0028","doi-asserted-by":"crossref","DOI":"10.1101\/cshperspect.a026716","article-title":"Caspase functions in cell death and disease","volume":"7","author":"McIlwain","year":"2015","journal-title":"Cold. Spring. Harb. Perspect. Biol."},{"key":"10.1016\/j.actatropica.2023.106977_bib0029","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.meegid.2007.10.001","article-title":"First phenotypic description of Fasciola hepatica\/Fasciola gigantica intermediate forms from the human endemic area of the Nile Delta","volume":"8","author":"Periago","year":"2008","journal-title":"Egypt. Infect. Genet. Evol."},{"key":"10.1016\/j.actatropica.2023.106977_bib0030","doi-asserted-by":"crossref","first-page":"e45","DOI":"10.1093\/nar\/29.9.e45","article-title":"A new mathematical model for relative quantification in real-time RT-PCR","volume":"29","author":"Pfaffl","year":"2001","journal-title":"Nucleic. Acids. Research."},{"key":"10.1016\/j.actatropica.2023.106977_bib0031","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1016\/j.bbamcr.2010.10.010","article-title":"Anti- apoptosis and cell survival: a review","volume":"1813","author":"Portt","year":"2011","journal-title":"Biochim. Biophys. Acta."},{"key":"10.1016\/j.actatropica.2023.106977_bib0032","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/bs.apcsb.2021.01.001","article-title":"Apoptosis in infectious diseases as a mechanism of immune evasion and survival","volume":"125","author":"Quarleri","year":"2021","journal-title":"Adv. Protein. Chem. Struct. Biol."},{"key":"10.1016\/j.actatropica.2023.106977_bib0033","doi-asserted-by":"crossref","first-page":"3100","DOI":"10.1038\/sj.onc.1210392","article-title":"Differential regulation and properties of MAPKs","volume":"26","author":"Raman","year":"2007","journal-title":"Oncogene"},{"key":"10.1016\/j.actatropica.2023.106977_bib0034","doi-asserted-by":"crossref","first-page":"2182","DOI":"10.3389\/fimmu.2020.02182","article-title":"Fasciola hepatica -derived molecules as regulators of the host immune response","volume":"11","author":"Ryan","year":"2020","journal-title":"Front. Immunol."},{"key":"10.1016\/j.actatropica.2023.106977_bib0035","doi-asserted-by":"crossref","first-page":"1290","DOI":"10.1182\/blood-2008-04-149856","article-title":"Inhibition of TLR3 and TLR4 function and expression in human dendritic cells by helminth parasites","volume":"112","author":"Semnani","year":"2008","journal-title":"Blood"},{"key":"10.1016\/j.actatropica.2023.106977_bib0036","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/j.vetimm.2007.03.007","article-title":"Excretory-secretory products from Fasciola hepatica induce eosinophil apoptosis by a caspase-dependent mechanism","volume":"117","author":"Serradell","year":"2007","journal-title":"Vet. Immunol. Immunopathol."},{"key":"10.1016\/j.actatropica.2023.106977_bib0037","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.molbiopara.2008.10.005","article-title":"Involvement of a mitochondrial pathway and key role of hydrogen peroxide during eosinophil apoptosis induced by excretory-secretory products from Fasciola hepatica","volume":"163","author":"Serradell","year":"2009","journal-title":"Mol. Biochem. Parasitol."},{"key":"10.1016\/j.actatropica.2023.106977_bib0038","doi-asserted-by":"crossref","first-page":"6642","DOI":"10.3390\/ijms21186642","article-title":"Toxoplasma GRA16 inhibits NF-\u03baB activation through PP2A-B55 upregulation in non-small-cell lung carcinoma cells","volume":"21","author":"Seo","year":"2020","journal-title":"Int. J. Mol. Sci."},{"key":"10.1016\/j.actatropica.2023.106977_bib0039","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1111\/pim.12192","article-title":"Identifying the immunomodulatory components of helminths","volume":"37","author":"Shepherd","year":"2015","journal-title":"Parasite. Immunol."},{"key":"10.1016\/j.actatropica.2023.106977_bib0040","first-page":"73","article-title":"Glutathione S-transferase in helminth parasites","volume":"40","author":"Vibanco-P\u00e9rez","year":"1998","journal-title":"Rev. Latinoam. Microbiol."},{"key":"10.1016\/j.actatropica.2023.106977_bib0041","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1111\/pim.12033","article-title":"Fasciola hepatica tegumental coat antigen suppresses MAPK signalling in dendritic cells and up-regulates the expression of SOCS3","volume":"35","author":"Vukman","year":"2013","journal-title":"Parasite. Immunol."},{"key":"10.1016\/j.actatropica.2023.106977_bib0042","doi-asserted-by":"crossref","first-page":"45006","DOI":"10.1038\/srep45006","article-title":"Resveratrol mitigates lipopolysaccharide-mediated acute inflammation in rats by inhibiting the TLR4\/NF-\u03baBp65\/MAPKs signaling cascade","volume":"7","author":"Wang","year":"2017","journal-title":"Sci. Rep."},{"key":"10.1016\/j.actatropica.2023.106977_bib0043","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/j.exppara.2013.01.013","article-title":"Microarray analysis of rat immune responses to liver fluke infection following vaccination with Fasciola hepatica phosphoglycerate kinase","volume":"134","author":"Weso\u0142owska","year":"2013","journal-title":"Exp. Parasitol."},{"key":"10.1016\/j.actatropica.2023.106977_bib0044","doi-asserted-by":"crossref","first-page":"3823","DOI":"10.1182\/blood.V95.12.3823.012k07_3823_3831","article-title":"LPS induces apoptosis in macrophages mostly through the autocrine production of TNF-alpha","volume":"95","author":"Xaus","year":"2000","journal-title":"Blood"},{"key":"10.1016\/j.actatropica.2023.106977_bib0045","doi-asserted-by":"crossref","first-page":"199","DOI":"10.2478\/jvetres-2022-0018","article-title":"Molecular characteristics and genetic diversity of Fasciola hepatica from sheep in Xinjiang","volume":"66","author":"Xifeng","year":"2022","journal-title":"China. J. Vet. Res."},{"key":"10.1016\/j.actatropica.2023.106977_bib0046","doi-asserted-by":"crossref","first-page":"737","DOI":"10.1007\/s13238-014-0089-1","article-title":"Mitochondria-mediated apoptosis in mammals","volume":"5","author":"Xiong","year":"2014","journal-title":"Protein. Cell."},{"key":"10.1016\/j.actatropica.2023.106977_bib0047","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1007\/s12192-013-0406-2","article-title":"A novel Omega-class glutathione S-transferase gene in Apis cerana cerana: molecular characterisation of GSTO2 and its protective effects in oxidative stress","volume":"18","author":"Zhang","year":"2013","journal-title":"Cell. Stress. Chaperones."}],"container-title":["Acta Tropica"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0001706X2300164X?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0001706X2300164X?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,9,11]],"date-time":"2025-09-11T00:42:56Z","timestamp":1757551376000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0001706X2300164X"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,9]]},"references-count":47,"alternative-id":["S0001706X2300164X"],"URL":"https:\/\/doi.org\/10.1016\/j.actatropica.2023.106977","relation":{},"ISSN":["0001-706X"],"issn-type":[{"value":"0001-706X","type":"print"}],"subject":[],"published":{"date-parts":[[2023,9]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"The regulatory roles of Fasciola hepatica GSTO1 protein in inflammatory cytokine expression and apoptosis in murine macrophages","name":"articletitle","label":"Article Title"},{"value":"Acta Tropica","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.actatropica.2023.106977","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2023 Elsevier B.V. All rights reserved.","name":"copyright","label":"Copyright"}],"article-number":"106977"}}