{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,16]],"date-time":"2026-10-16T10:38:43Z","timestamp":1792147123652,"version":"4.4.0"},"reference-count":69,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2025,1,22]],"date-time":"2025-01-22T00:00:00Z","timestamp":1737504000000},"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. Genet."],"abstract":"<jats:sec><jats:title>Introduction<\/jats:title><jats:p>Fasciolopsiasis, a food-borne intestinal disease is most common in Asia and the Indian subcontinent. Pigs are the reservoir host, and fasciolopsiasis is most widespread in locations where pigs are reared and aquatic plants are widely consumed. Human infection has been most commonly documented in China, Bangladesh, Southeast Asia, and parts of India. It predominates in school-age children, and significant worm burdens are not uncommon. The causal organism is <jats:italic>Fasciolopsis buski<\/jats:italic>, a giant intestinal fluke that infects humans and causes diarrhoea, fever, ascites, and intestinal blockage. The increasing prevalence of medication resistance and the necessity for an effective vaccination make controlling these diseases challenging.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>Over the last decade, we have achieved major advances in our understanding of intestinal fluke biology by in-depth interrogation and analysis of evolving <jats:italic>F. buski<\/jats:italic> omics datasets. The creation of large omics datasets for <jats:italic>F. buski<\/jats:italic> by our group has accelerated the discovery of key molecules involved in intestinal fluke biology, toxicity, and virulence that can be targeted for vaccine development. Finding successful vaccination antigen combinations from these huge number of genes\/proteins in the available omics datasets is the key in combating these neglected tropical diseases. In the present study, we developed an <jats:italic>in silico<\/jats:italic> workflow to select antigens for composing a chimeric vaccine, which could be a significant technique for developing a fasciolopsiasis vaccine that prevents the parasite from causing serious harm.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results and discussion<\/jats:title><jats:p>This chimeric vaccine can now be tested experimentally and compared to other vaccine candidates to determine its potential influence on human health. Although the results are encouraging, additional validation is needed both <jats:italic>in vivo<\/jats:italic> and <jats:italic>in vitro<\/jats:italic>. Considering the extensive genetic data available for intestinal flukes that has expanded with technological advancements, we may need to reassess our methods and suggest a more sophisticated technique in the future for identifying vaccine molecules.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fgene.2024.1451853","type":"journal-article","created":{"date-parts":[[2025,1,22]],"date-time":"2025-01-22T07:11:40Z","timestamp":1737529900000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":3,"title":["In silico design of an epitope-based vaccine ensemble for fasliolopsiasis"],"prefix":"10.3389","volume":"15","author":[{"given":"Ruchishree","family":"Konhar","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kanhu Charan","family":"Das","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aiboklang","family":"Nongrum","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rohan Raj","family":"Samal","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shailesh Kumar","family":"Sarangi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Devendra Kumar","family":"Biswal","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2025,1,22]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1016\/j.softx.2015.06.001","article-title":"Gromacs: high performance molecular simulations through multi-level parallelism from laptops to supercomputers","author":"Abraham","year":"2015","journal-title":"SoftwareX"},{"key":"B3","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1016\/S0022-2836(05)80360-2","article-title":"Basic local alignment search tool","volume":"215","author":"Altschul","year":"1990","journal-title":"J. Mol. Biol."},{"key":"B4","doi-asserted-by":"publisher","first-page":"2963","DOI":"10.1080\/07391102.2020.1850357","article-title":"Design of a multi-epitope-based vaccine targeting M-protein of SARS-CoV2: an immunoinformatics approach","volume":"40","author":"Ayyagari","year":"2022","journal-title":"J. Biomol. Struct. Dyn."},{"key":"B5","first-page":"73","article-title":"Fasciolopslasis--a re-emerging infection in Azamgarh (Uttar Pradesh)","volume":"43","author":"Bhatti","year":"2000","journal-title":"Indian J. Pathol. Microbiol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"1249","DOI":"10.1038\/s41598-020-80899-6","article-title":"In silico analysis of epitope-based vaccine candidate against tuberculosis using reverse vaccinology","volume":"11","author":"Bibi","year":"2021","journal-title":"Sci. Rep."},{"key":"B7","doi-asserted-by":"publisher","first-page":"e0157459","DOI":"10.1371\/journal.pone.0157459","article-title":"Northeast India helminth parasite information database (NEIHPID): knowledge base for helminth parasites","volume":"11","author":"Biswal","year":"","journal-title":"PLoS One"},{"key":"B8","doi-asserted-by":"publisher","first-page":"e207","DOI":"10.7717\/peerj.207","article-title":"An integrated pipeline for next generation sequencing and annotation of the complete mitochondrial genome of the giant intestinal fluke, Fasciolopsis buski (Lankester, 1857) Looss, 1899","volume":"1","author":"Biswal","year":"2013","journal-title":"PeerJ"},{"key":"B9","doi-asserted-by":"publisher","first-page":"693","DOI":"10.1080\/23802359.2016.1222249","article-title":"Complete mitochondrial genome annotation of the giant intestinal fluke, Fasciolopsis buski (Indian isolate) as revealed by ion torrent and illuminanext-generation sequencing","volume":"1","author":"Biswal","year":"","journal-title":"Mitochondrial DNA B Resour."},{"key":"B10","doi-asserted-by":"publisher","first-page":"e0205570","DOI":"10.1371\/journal.pone.0205570","article-title":"De novo genome and transcriptome analyses provide insights into the biology of the trematode human parasite Fasciolopsis buski","volume":"13","author":"Biswal","year":"2018","journal-title":"PLoS One"},{"key":"B11","doi-asserted-by":"publisher","first-page":"W402-W407","DOI":"10.1093\/nar\/gkz297","article-title":"The PSIPRED protein analysis workbench: 20 years on","volume":"47","author":"Buchan","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"B12","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1159\/000053656","article-title":"Vaccine strategies against schistosomiasis: from concepts to clinical trials","volume":"124","author":"Capron","year":"2001","journal-title":"Int. Arch. Allergy Immunol."},{"key":"B13","doi-asserted-by":"publisher","first-page":"2005","DOI":"10.1093\/bioinformatics\/btg272","article-title":"Codon adaptation index as a measure of dominating codon bias","volume":"19","author":"Carbone","year":"2003","journal-title":"Bioinformatics"},{"key":"B14","doi-asserted-by":"publisher","first-page":"763","DOI":"10.1017\/S0031182006001119","article-title":"Molecular and immunological characterization of encoding gene and 14-3-3 protein 1 in Fasciola gigantica","volume":"133","author":"Chaithirayanon","year":"2006","journal-title":"Parasitology"},{"key":"B15","doi-asserted-by":"publisher","first-page":"102","DOI":"10.1016\/j.exppara.2013.06.010","article-title":"Vaccine potential of recombinant cathepsin B against Fasciola gigantica","volume":"135","author":"Chantree","year":"2013","journal-title":"Exp. Parasitol."},{"key":"B16","doi-asserted-by":"publisher","first-page":"595","DOI":"10.1128\/CMR.15.4.595-612.2002","article-title":"History of human parasitology","volume":"15","author":"Cox","year":"2002","journal-title":"Clin. Microbiol. Rev."},{"key":"B17","doi-asserted-by":"publisher","first-page":"1068","DOI":"10.1016\/j.pt.2022.09.009","article-title":"Omics tools enabling vaccine discovery against fasciolosis","volume":"38","author":"Cwiklinski","year":"2022","journal-title":"Trends Parasitol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"835","DOI":"10.1016\/s0022-2836(99)80005-9","article-title":"Prediction of rho-independent Escherichia coli transcription terminators. A statistical analysis of their RNA stem-loop structures","volume":"216","author":"d'Aubenton Carafa","year":"1990","journal-title":"J. Mol. Biol."},{"key":"B21","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1186\/1745-6150-8-30","article-title":"Designing of interferon-gamma inducing MHC class-II binders","volume":"8","author":"Dhanda","year":"2013","journal-title":"Biol. Direct"},{"key":"B22","doi-asserted-by":"publisher","first-page":"2278","DOI":"10.1007\/s00894-014-2278-5","article-title":"AllerTOP v.2 - a server for in silico prediction of allergens","volume":"20","author":"Dimitrov","year":"2014","journal-title":"J. Mol. Model."},{"key":"B23","doi-asserted-by":"publisher","first-page":"856","DOI":"10.1016\/j.vaccine.2006.09.032","article-title":"Identifying candidate subunit vaccines using an alignment-independent method based on principal amino acid properties","volume":"25","author":"Doytchinova","year":"","journal-title":"Vaccine"},{"key":"B24","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1186\/1471-2105-8-4","article-title":"VaxiJen: a server for prediction of protective antigens, tumour antigens and subunit vaccines","volume":"8","author":"Doytchinova","year":"","journal-title":"BMC Bioinforma."},{"key":"B25","doi-asserted-by":"publisher","first-page":"276","DOI":"10.1186\/s13071-021-04784-5","article-title":"Fasciola gigantica tegumental calcium-binding EF-hand protein 4 exerts immunomodulatory effects on goat monocytes","volume":"14","author":"Ehsan","year":"2021","journal-title":"Parasit. Vectors"},{"key":"B26","doi-asserted-by":"publisher","first-page":"20130433","DOI":"10.1098\/rstb.2013.0433","article-title":"The contribution of vaccination to global health: past, present and future","volume":"369","author":"Greenwood","year":"2014","journal-title":"Philos. Trans. R. Soc. Lond B Biol. Sci."},{"key":"B27","doi-asserted-by":"publisher","first-page":"W526","DOI":"10.1093\/nar\/gki376","article-title":"JCat: a novel tool to adapt codon usage of a target gene to its potential expression host","volume":"33","author":"Grote","year":"2005","journal-title":"Nucleic Acids Res."},{"key":"B28","doi-asserted-by":"publisher","first-page":"504","DOI":"10.1002\/(sici)1097-0134(19980901)32:4<504::aid-prot8>3.3.co;2-q","article-title":"Structural basis for specificity of papain-like cysteine protease proregions toward their cognate enzymes","volume":"32","author":"Groves","year":"1998","journal-title":"Proteins"},{"key":"B29","doi-asserted-by":"publisher","first-page":"e73957","DOI":"10.1371\/journal.pone.0073957","article-title":"In silico approach for predicting toxicity of peptides and proteins","volume":"8","author":"Gupta","year":"2013","journal-title":"PLoS One"},{"key":"B30","doi-asserted-by":"publisher","first-page":"W384","DOI":"10.1093\/nar\/gkt458","article-title":"GalaxyRefine: protein structure refinement driven by side-chain repacking","volume":"41","author":"Heo","year":"2013","journal-title":"Nucleic Acids Res."},{"key":"B31","first-page":"143","article-title":"A survey of fasciolopsiasis of pigs in Kwangtung Province","volume":"7","author":"Hsu","year":"1964","journal-title":"Acta Veterinaria Zootechnica Sinica"},{"key":"B32","doi-asserted-by":"publisher","first-page":"1511","DOI":"10.1038\/nprot.2012.085","article-title":"Template-based protein structure modeling using the RaptorX web server","volume":"7","author":"K\u00e4llberg","year":"2012","journal-title":"Nat. Protoc."},{"key":"B33","doi-asserted-by":"publisher","first-page":"2159","DOI":"10.1002\/prot.24403","article-title":"How good is automated protein docking?","volume":"81","author":"Kozakov","year":"2013","journal-title":"Proteins"},{"key":"B34","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1038\/nprot.2016.169","article-title":"The ClusPro web server for protein-protein docking","volume":"12","author":"Kozakov","year":"2017","journal-title":"Nat. Protoc."},{"key":"B35","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1002\/pro.3289","article-title":"PDBsum: structural summaries of PDB entries","volume":"27","author":"Laskowski","year":"2018","journal-title":"Protein Sci."},{"key":"B36","doi-asserted-by":"publisher","first-page":"2200","DOI":"10.1093\/bioinformatics\/btp386","article-title":"SOLpro: accurate sequence-based prediction of protein solubility","volume":"25","author":"Magnan","year":"2009","journal-title":"Bioinformatics"},{"key":"B37","doi-asserted-by":"publisher","first-page":"3216","DOI":"10.1016\/b978-1-4557-4801-3.00290-3","article-title":"Trematodes (schistosomes and liver, intestinal, and lung flukes)","author":"Maguire","year":"2015","journal-title":"Mandell, Douglas, Bennett\u2019s Princ. Pract. Infect. Dis."},{"key":"B38","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1093\/trstmh\/trab002","article-title":"A road map for neglected tropical diseases 2021-2030","volume":"115","author":"Malecela","year":"2021","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"B39","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1128\/CVI.00338-07","article-title":"Leucine aminopeptidase is an immunodominant antigen of Fasciola hepatica excretory and secretory products in human infections","volume":"15","author":"Marcilla","year":"2008","journal-title":"Clin. Vaccine Immunol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"1255","DOI":"10.1016\/j.ijpara.2005.07.010","article-title":"Fascioliasis and other plant-borne trematode zoonoses","volume":"35","author":"Mas-Coma","year":"2005","journal-title":"Int. J. Parasitol."},{"key":"B41","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1016\/j.meegid.2017.02.007","article-title":"A novel design of a multi-antigenic, multistage and multi-epitope vaccine against Helicobacter pylori: an in silico approach","volume":"49","author":"Meza","year":"2017","journal-title":"Infect. Genet. Evol."},{"key":"B42","doi-asserted-by":"publisher","first-page":"161","DOI":"10.2307\/3271232","article-title":"The development of Fasciolopsis buski Lankester","volume":"8","author":"Nakagawa","year":"1922","journal-title":"J. Parasitol."},{"key":"B43","doi-asserted-by":"publisher","first-page":"e8795","DOI":"10.7717\/peerj.8795","article-title":"An immunoinformatics approach for the design of a multi-epitope subunit vaccine for urogenital schistosomiasis","volume":"8","author":"Onile","year":"2020","journal-title":"PeerJ"},{"key":"B44","doi-asserted-by":"publisher","first-page":"422","DOI":"10.4049\/jimmunol.177.1.422","article-title":"Mycobacterium tuberculosis LprA is a lipoprotein agonist of TLR2 that regulates innate immunity and APC function","volume":"177","author":"Pecora","year":"2006","journal-title":"J. Immunol."},{"key":"B45","doi-asserted-by":"publisher","first-page":"711650","DOI":"10.3389\/fimmu.2021.711650","article-title":"Promising technologies in the field of helminth vaccines","volume":"12","author":"Perera","year":"2021","journal-title":"Front. Immunol."},{"key":"B46","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1186\/s12860-020-00335-5","article-title":"Regulation of the Fasciola hepatica newly excysted juvenile cathepsin L3 (FhCL3) by its propeptide: a proposed \u2018clamp-like\u2019 mechanism of binding and inhibition","volume":"21","author":"Pritsch","year":"2020","journal-title":"BMC Mol. Cell Biol."},{"key":"B47","doi-asserted-by":"publisher","first-page":"xx","DOI":"10.20546\/ijcmas.2019.802.xx","article-title":"Review on zoonotic parasitic diseases of northeast India - epidemiology and clinical features","volume":"8","author":"Rajendran","year":"2019","journal-title":"Int. J. Curr. Microbiol. App. Sci."},{"key":"B48","doi-asserted-by":"publisher","first-page":"2757","DOI":"10.14202\/vetworld.2021.2757-2763","article-title":"A review of Fasciolopsis buski distribution and control in Indonesia","volume":"14","author":"Ridha","year":"2021","journal-title":"Vet. World"},{"key":"B49","first-page":"272","volume-title":"Foundations of parasitology","author":"Roberts","year":"2009"},{"key":"B50","first-page":"72","article-title":"Morphological and microtopographical strain variations among Fasciolopsis buski originating from different geographical areas","volume":"38","author":"Roy","year":"1993","journal-title":"Acta Parasitol."},{"key":"B51","doi-asserted-by":"publisher","first-page":"40","DOI":"10.1002\/prot.21078","article-title":"Prediction of continuous B-cell epitopes in an antigen using recurrent neural network","volume":"65","author":"Saha","year":"","journal-title":"Proteins"},{"key":"B52","doi-asserted-by":"publisher","first-page":"W202","DOI":"10.1093\/nar\/gkl343","article-title":"AlgPred: prediction of allergenic proteins and mapping of IgE epitopes","volume":"34","author":"Saha","year":"","journal-title":"Nucleic Acids Res."},{"key":"B53","doi-asserted-by":"publisher","first-page":"621706","DOI":"10.3389\/fimmu.2021.621706","article-title":"Immunoinformatics design of multi-epitope peptide-based vaccine against schistosoma mansoni using transmembrane proteins as a target","volume":"12","author":"Sanches","year":"2021","journal-title":"Front. Immunol."},{"key":"B54","first-page":"r126","article-title":"Epidemiology and morbidity of food-borne intestinal trematode infections","volume":"91","author":"Sen-Hai","year":"1994","journal-title":"Trop. Dis. Bull."},{"key":"B55","doi-asserted-by":"publisher","first-page":"590","DOI":"10.14202\/vetworld.2015.590-598","article-title":"Role of parasitic vaccines in integrated control of parasitic diseases in livestock","volume":"8","author":"Sharma","year":"2015","journal-title":"Vet. World"},{"key":"B56","doi-asserted-by":"publisher","first-page":"4409","DOI":"10.1038\/s41598-019-40833-x","article-title":"In-silico design of a multi-epitope vaccine candidate against onchocerciasis and related filarial diseases","volume":"9","author":"Shey","year":"2019","journal-title":"Sci. Rep."},{"key":"B57","doi-asserted-by":"publisher","first-page":"99","DOI":"10.3390\/pathogens10020099","article-title":"Computational design and preliminary serological analysis of a novel multi-epitope vaccine candidate against onchocerciasis and related filarial diseases","volume":"10","author":"Shey","year":"2021","journal-title":"Pathogens"},{"key":"B58","doi-asserted-by":"publisher","first-page":"516","DOI":"10.1016\/j.exppara.2008.01.009","article-title":"14-3-3 proteins in Echinococcus: their role and potential as protective antigens","volume":"119","author":"Siles-Lucas","year":"2008","journal-title":"Exp. Parasitol."},{"key":"B59","doi-asserted-by":"publisher","first-page":"16219","DOI":"10.1038\/s41598-020-73371-y","article-title":"Designing a multi-epitope peptide based vaccine against SARS-CoV-2","volume":"10","author":"Singh","year":"2020","journal-title":"Sci. Rep."},{"key":"B60","doi-asserted-by":"publisher","first-page":"506","DOI":"10.1016\/j.pt.2010.06.001","article-title":"Cathepsin B proteases of flukes: the key to facilitating parasite control?","volume":"26","author":"Smooker","year":"2010","journal-title":"Trends Parasitol."},{"key":"B61","doi-asserted-by":"publisher","first-page":"9896","DOI":"10.1074\/jbc.M708521200","article-title":"Structural and functional relationships in the virulence-associated cathepsin L proteases of the parasitic liver fluke, Fasciola hepatica","volume":"283","author":"Stack","year":"2008","journal-title":"J. Biol. Chem."},{"key":"B62","doi-asserted-by":"publisher","first-page":"542","DOI":"10.1016\/s0176-6724(86)80148-1","article-title":"Effects of praziquantel on human intestinal flukes (Fasciolopsis buski and Heterophyes heterophyes)","volume":"262","author":"Taraschewski","year":"1986","journal-title":"Zentralbl Bakteriol. Mikrobiol. Hyg. A"},{"key":"B63","doi-asserted-by":"publisher","first-page":"615","DOI":"10.1007\/978-1-4939-9030-6_39","article-title":"Characterization of calcium-binding proteins from parasitic worms","volume":"1929","author":"Thomas","year":"2019","journal-title":"Methods Mol. Biol."},{"key":"B64","doi-asserted-by":"publisher","first-page":"23345","DOI":"10.1038\/srep23345","article-title":"A model to assess the efficacy of vaccines for control of liver fluke infection","volume":"6","author":"Turner","year":"2016","journal-title":"Sci. Rep."},{"key":"B75","first-page":"73","article-title":"Glutathione S-transferase in helminth parasites","volume":"40","author":"Vibanco-P\u00e9rez","year":"1998","journal-title":"Revista latinoamericana de microbiologia"},{"key":"B65","doi-asserted-by":"publisher","first-page":"216","DOI":"10.1186\/s13071-016-1500-y","article-title":"Protection against Schistosoma mansoni infection using a Fasciola hepatica-derived fatty acid binding protein from different delivery systems","volume":"9","author":"Vicente","year":"2016","journal-title":"Parasit. Vectors"},{"key":"B66","doi-asserted-by":"publisher","first-page":"W430","DOI":"10.1093\/nar\/gkw306","article-title":"RaptorX-Property: a web server for protein structure property prediction","volume":"44","author":"Wang","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"B67","doi-asserted-by":"publisher","first-page":"W407","DOI":"10.1093\/nar\/gkm290","article-title":"ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins","volume":"35","author":"Wiederstein","year":"2007","journal-title":"Nucleic Acids Res."},{"key":"B68","doi-asserted-by":"publisher","first-page":"781","DOI":"10.1042\/bj2990781","article-title":"The secreted cathepsin L-like proteinases of the trematode, Fasciola hepatica, contain 3-hydroxyproline residues","volume":"299","author":"Wijffels","year":"1994","journal-title":"Biochem. J."},{"key":"B69","doi-asserted-by":"publisher","first-page":"531","DOI":"10.1385\/1-59259-584-7:531","article-title":"Protein identification and analysis tools in the ExPASy server","volume":"112","author":"Wilkins","year":"1999","journal-title":"Methods Mol. Biol."},{"key":"B70","doi-asserted-by":"publisher","first-page":"735","DOI":"10.1089\/ars.2012.4670","article-title":"Thioredoxin glutathione reductase-dependent redox networks in platyhelminth parasites","volume":"19","author":"Williams","year":"2013","journal-title":"Antioxid. Redox Signal"},{"key":"B71","doi-asserted-by":"publisher","first-page":"345","DOI":"10.1093\/nar\/gkg040","article-title":"The protein information resource","volume":"31","author":"Wu","year":"2003","journal-title":"Nucleic Acids Res."}],"container-title":["Frontiers in Genetics"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fgene.2024.1451853\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,1,22]],"date-time":"2025-01-22T07:11:46Z","timestamp":1737529906000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fgene.2024.1451853\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,1,22]]},"references-count":69,"alternative-id":["10.3389\/fgene.2024.1451853"],"URL":"https:\/\/doi.org\/10.3389\/fgene.2024.1451853","relation":{},"ISSN":["1664-8021"],"issn-type":[{"value":"1664-8021","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,1,22]]},"article-number":"1451853"}}