{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,21]],"date-time":"2026-07-21T20:01:47Z","timestamp":1784664107460,"version":"3.55.0"},"reference-count":47,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2025,1,17]],"date-time":"2025-01-17T00:00:00Z","timestamp":1737072000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32200078"],"award-info":[{"award-number":["32200078"]}],"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":["2024YFE0102600"],"award-info":[{"award-number":["2024YFE0102600"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"the Intergovernmental International Science and Technology Innovation Cooperation Key Project of China\u2019s National Key R&amp;D Program","award":["32200078"],"award-info":[{"award-number":["32200078"]}]},{"name":"the Intergovernmental International Science and Technology Innovation Cooperation Key Project of China\u2019s National Key R&amp;D Program","award":["2024YFE0102600"],"award-info":[{"award-number":["2024YFE0102600"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Listeria monocytogenes is one of the most important foodborne pathogens that can cause invasive listeriosis. In this study, the virulence levels of 26 strains of L. monocytogenes isolated from food and clinical samples in Shanghai, China, between 2020 and 2022 were analyzed. There were significant differences among isolates in terms of their mortality rate in Galleria mellonella, cytotoxicity to JEG-3 cells, hemolytic activity, and expression of important virulence genes. Compared with other STs, both the ST121 (food source) and ST1930 (clinic source) strains exhibited higher G. mellonella mortality. The 48 h mortality in G. mellonella of lineage II strains was significantly higher than that in lineage I. Compared with other STs, ST1930, ST3, ST5, and ST1032 exhibited higher cytotoxicity to JEG-3 cells. Based on the classification of sources (food and clinical strains) and serogroups (II a, II b, and II c), there were no significant differences observed in terms of G. mellonella mortality, cytotoxicity, and hemolytic activity. In addition, ST121 exhibited significantly higher hly, inlA, inlB, prfA, plcA, and plcB gene expression compared with other STs. A gray relation analysis showed a high correlation between the toxicity of G. mellonella and the expression of the hly and inlB genes; in addition, L. monocytogenes may have a consistent virulence mechanism involving hemolysis activity and cytotoxicity. Through the integration of in vivo and in vitro infection models with information on the expression of virulence factor genes, the differences in virulence between strains or subtypes can be better understood.<\/jats:p>","DOI":"10.3390\/microorganisms13010191","type":"journal-article","created":{"date-parts":[[2025,1,17]],"date-time":"2025-01-17T10:27:58Z","timestamp":1737109678000},"page":"191","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Comparative Analysis of In Vivo and In Vitro Virulence Among Foodborne and Clinical Listeria monocytogenes Strains"],"prefix":"10.3390","volume":"13","author":[{"given":"Hui","family":"Yan","sequence":"first","affiliation":[{"name":"School of Health Science and Engineering, University of Shanghai for Science and Technology, Shanghai 200093, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Biyao","family":"Xu","sequence":"additional","affiliation":[{"name":"Shanghai Municipal Center for Disease Control and Prevention, Shanghai 200051, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0003-2812-5526","authenticated-orcid":false,"given":"Binru","family":"Gao","sequence":"additional","affiliation":[{"name":"School of Health Science and Engineering, University of Shanghai for Science and Technology, Shanghai 200093, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0000-6661-0061","authenticated-orcid":false,"given":"Yunyan","family":"Xu","sequence":"additional","affiliation":[{"name":"School of Health Science and Engineering, University of Shanghai for Science and Technology, Shanghai 200093, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xuejuan","family":"Xia","sequence":"additional","affiliation":[{"name":"School of Health Science and Engineering, University of Shanghai for Science and Technology, Shanghai 200093, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6981-0878","authenticated-orcid":false,"given":"Yue","family":"Ma","sequence":"additional","affiliation":[{"name":"School of Health Science and Engineering, University of Shanghai for Science and Technology, Shanghai 200093, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaojie","family":"Qin","sequence":"additional","affiliation":[{"name":"School of Health Science and Engineering, University of Shanghai for Science and Technology, Shanghai 200093, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9019-0001","authenticated-orcid":false,"given":"Qingli","family":"Dong","sequence":"additional","affiliation":[{"name":"School of Health Science and Engineering, University of Shanghai for Science and Technology, Shanghai 200093, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6517-5835","authenticated-orcid":false,"given":"Takashi","family":"Hirata","sequence":"additional","affiliation":[{"name":"Graduate School of Agriculture, Kyoto University, Kyoto 606-8501, Japan"},{"name":"Faculty of Rehabilitation, Shijonawate Gakuen University, Osaka 574-0011, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4895-3241","authenticated-orcid":false,"given":"Zhuosi","family":"Li","sequence":"additional","affiliation":[{"name":"School of Health Science and Engineering, University of Shanghai for Science and Technology, Shanghai 200093, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,1,17]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2231","DOI":"10.1007\/s00248-023-02269-9","article-title":"Listeria monocytogenes an Emerging Pathogen: A Comprehensive Overview on Listeriosis, Virulence Determinants, Detection, and Anti-Listerial Interventions","volume":"86","author":"Ravindhiran","year":"2023","journal-title":"Microb. Ecol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"115114","DOI":"10.1016\/j.lwt.2023.115114","article-title":"Growth and survival characteristics of Listeria monocytogenes of different sources and subtypes","volume":"184","author":"Cheng","year":"2023","journal-title":"LWT"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Ranjbar, R., and Halaji, M. (2018). Epidemiology of Listeria monocytogenes prevalence in foods, animals and human origin from Iran: A systematic review and meta-analysis. BMC Public Health, 18.","DOI":"10.1186\/s12889-018-5966-8"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"986","DOI":"10.1016\/j.foodcont.2008.11.013","article-title":"Survey of Listeria monocytogenes in ready-to-eat products: Prevalence by brands and retail establishments for exposure assessment of listeriosis in Northern Spain","volume":"20","author":"Garrido","year":"2009","journal-title":"Food Control"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"13626","DOI":"10.1074\/jbc.RA118.003888","article-title":"Structural basis of VHH-mediated neutralization of the food-borne pathogen Listeria monocytogenes","volume":"293","author":"King","year":"2018","journal-title":"J. Biol. Chem."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"e01165-20","DOI":"10.1128\/AEM.01165-20","article-title":"Differential Modulation of Listeria monocytogenes Fitness, In Vitro Virulence, and Transcription of Virulence-Associated Genes in Response to the Presence of Different Microorganisms","volume":"86","author":"Zilelidou","year":"2020","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1038\/nrmicro.2017.126","article-title":"Listeria monocytogenes: Towards a complete picture of its physiology and pathogenesis","volume":"16","author":"Radoshevich","year":"2018","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1080\/19490976.2017.1290759","article-title":"Listeriolysin S: A bacteriocin from epidemic Listeria monocytogenes strains that targets the gut microbiota","volume":"8","author":"Quereda","year":"2017","journal-title":"Gut Microbes"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"5706","DOI":"10.1073\/pnas.1523899113","article-title":"Bacteriocin from epidemic Listeria strains alters the host intestinal microbiota to favor infection","volume":"113","author":"Quereda","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1973","DOI":"10.1084\/jem.20170495","article-title":"Commensal microbes provide first line defense against Listeria monocytogenes infection","volume":"214","author":"Becattini","year":"2017","journal-title":"J. Exp. Med."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"M\u00f8retr\u00f8, T., Wagner, E., Heir, E., Langsrud, S., and Fagerlund, A. (2024). Genomic analysis of Listeria monocytogenes CC7 associated with clinical infections and persistence in the food industry. Int. J. Food Microbiol., 410.","DOI":"10.1016\/j.ijfoodmicro.2023.110482"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/j.ijmm.2010.05.002","article-title":"Listeria monocytogenes lineages: Genomics, evolution, ecology, and phenotypic characteristics","volume":"301","author":"Orsi","year":"2011","journal-title":"Int. J. Med. Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"3819","DOI":"10.1128\/JCM.42.8.3819-3822.2004","article-title":"Differentiation of the major Listeria monocytogenes serovars by multiplex PCR","volume":"42","author":"Doumith","year":"2004","journal-title":"J. Clin. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1007\/s002849900315","article-title":"Identification and characterization of nucleotide sequence differences in three virulence-associated genes of Listeria monocytogenes strains representing clinically important serotypes","volume":"36","author":"Vines","year":"1998","journal-title":"Curr. Microbiol."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Dom\u00ednguez, A.V., Ledesma, M.C., Dom\u00ednguez, C.I., Cisneros, J.M., Lepe, J.A., and Smani, Y. (2023). In Vitro and In Vivo Virulence Study of Listeria monocytogenes Isolated from the Andalusian Outbreak in 2019. Trop. Med. Infect. Dis., 8.","DOI":"10.3390\/tropicalmed8010058"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Myintzaw, P., Pennone, V., McAuliffe, O., Begley, M., and Callanan, M. (2023). Association of Virulence, Biofilm, and Antimicrobial Resistance Genes with Specific Clonal Complex Types of Listeria monocytogenes. Microorganisms, 11.","DOI":"10.3390\/microorganisms11061603"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1001","DOI":"10.1023\/A:1025849532417","article-title":"Incidence of Listeria monocytogenes in food and environmental samples in Italy between 1990 and 1999: Serotype distribution in food, environmental and clinical samples","volume":"18","author":"Gianfranceschi","year":"2003","journal-title":"Eur. J. Epidemiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"2509","DOI":"10.1080\/21505594.2021.1975526","article-title":"Pathogenicity and virulence of Listeria monocytogenes: A trip from environmental to medical microbiology","volume":"12","author":"Quereda","year":"2021","journal-title":"Virulence"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3201\/eid1901.120393","article-title":"Listeriosis Outbreaks and Associated Food Vehicles, United States, 1998\u20132008","volume":"19","author":"Cartwright","year":"2013","journal-title":"Emerg. Infect. Dis."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Zhang, X.A., Niu, Y.L., Liu, Y.Z., Lu, Z., Wang, D., Cui, X., Chen, Q., and Ma, X.C. (2019). Isolation and Characterization of Clinical Listeria monocytogenes in Beijing, China, 2014\u20132016. Front. Microbiol., 10.","DOI":"10.3389\/fmicb.2019.00981"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Rugna, G., Carra, E., Bergamini, F., Franzini, G., Faccini, S., Gattuso, A., Morganti, M., Baldi, D., Naldi, S., and Serraino, A. (2021). Distribution, virulence, genotypic characteristics and antibiotic resistance of Listeria monocytogenes isolated over one-year monitoring from two pig slaughterhouses and processing plants and their fresh hams. Int. J. Food Microbiol., 336.","DOI":"10.1016\/j.ijfoodmicro.2020.108912"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"753","DOI":"10.1089\/fpd.2014.1747","article-title":"Characterization of Listeria monocytogenes Strains Isolated During 2011\u20132013 from Human Infections in Switzerland","volume":"11","author":"Althaus","year":"2014","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Baba, H., Kanamori, H., Kakuta, R., Sakurai, H., Oshima, K., Aoyagi, T., and Kaku, M. (2021). Genomic characteristics of listeria monocytogenes causing invasive listeriosis in Japan. Diagn. Microbiol. Infect. Dis., 99.","DOI":"10.1016\/j.diagmicrobio.2020.115233"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Rychli, K., Stessl, B., Szakmary-Br\u00e4ndle, K., Strauss, A., Wagner, M., and Schoder, D. (2018). Listeria monocytogenes Isolated from Illegally Imported Food Products into the European Union Harbor Different Virulence Factor Variants. Genes, 9.","DOI":"10.3390\/genes9090428"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"114232","DOI":"10.1016\/j.foodres.2024.114232","article-title":"Growth, biofilm formation, and motility of Listeria monocytogenes strains isolated from food and clinical samples located in Shanghai (China)","volume":"184","author":"Gao","year":"2024","journal-title":"Food Res. Int."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Martinez, M.R., Wiedmann, M., Ferguson, M., and Datta, A.R. (2017). Assessment of Listeria monocytogenes virulence in the Galleria mellonella insect larvae model. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0184557"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"110348","DOI":"10.1016\/j.foodcont.2024.110348","article-title":"Effects of nisin and sesamol on biofilm formation and virulence of Listeria monocytogenes","volume":"160","author":"Wu","year":"2024","journal-title":"Food Control"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Wang, Z., Du, J., Ma, W., Diao, X., Liu, Q., and Liu, G. (2024). Bacteriocins attenuate Listeria monocytogenes\u2013induced intestinal barrier dysfunction and inflammatory response. Appl. Microbiol. Biotechnol., 108.","DOI":"10.1007\/s00253-024-13228-w"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"107558","DOI":"10.1016\/j.foodcont.2020.107558","article-title":"Antibiofilm activity of shikonin against Listeria monocytogenes and inhibition of key virulence factors","volume":"120","author":"Li","year":"2021","journal-title":"Food Control"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2\u2212\u0394\u0394CT Method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1186\/s13567-017-0496-4","article-title":"Role in virulence of phospholipases, listeriolysin O and listeriolysin S from epidemic Listeria monocytogenes using the chicken embryo infection model","volume":"49","author":"Quereda","year":"2018","journal-title":"Vet. Res."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"3862","DOI":"10.1128\/AEM.02164-05","article-title":"Differential inlA and inlB expression and interaction with human intestinal and liver cells by Listeria monocytogenes strains of different origins","volume":"72","author":"Werbrouck","year":"2006","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"14733","DOI":"10.1073\/pnas.1614028114","article-title":"Structural basis for glutathione-mediated activation of the virulence regulatory protein PrfA in Listeria","volume":"113","author":"Hall","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"510","DOI":"10.1016\/j.lwt.2016.11.080","article-title":"Effect of lemongrass essential oil on Listeria monocytogenes gene expression","volume":"77","author":"Hadjilouka","year":"2017","journal-title":"LWT-Food Sci. Technol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"ftaa056","DOI":"10.1093\/femspd\/ftaa056","article-title":"Galleria mellonella as an infection model: An in-depth look at why it works and practical considerations for successful application","volume":"78","author":"Pereira","year":"2020","journal-title":"Pathog. Dis."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1080\/21505594.2019.1621649","article-title":"Galleria mellonella as a consol idated in vivo model hosts: New developments in antibacterial strategies and novel drug testing","volume":"10","author":"Cutuli","year":"2019","journal-title":"Virulence"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"ftaa059","DOI":"10.1093\/femspd\/ftaa059","article-title":"Utilising Galleria mellonella larvae for studying in vivo activity of conventional and novel antimicrobial agents","volume":"78","author":"Piatek","year":"2020","journal-title":"Pathog. Dis."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1128\/AEM.01301-09","article-title":"Galleria mellonella as a model system for studying Listeria pathogenesis","volume":"76","author":"Mukherjee","year":"2010","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Pouillot, R., Kiermeier, A., Guillier, L., Cadavez, V., and Sanaa, M. (2024). Updated Parameters for Listeria monocytogenes Dose\u2013Response Model Considering Pathogen Virulence and Age and Sex of Consumer. Foods, 13.","DOI":"10.3390\/foods13050751"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"3456","DOI":"10.1099\/mic.0.040782-0","article-title":"Molecular pathogenesis of Listeria monocytogenes in the alternative model host Galleria mellonella","volume":"156","author":"Joyce","year":"2010","journal-title":"Microbiology"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1016\/S1286-4579(01)01413-7","article-title":"Pathogenicity islands and virulence evolution in Listeria","volume":"3","author":"Kreft","year":"2001","journal-title":"Microbes Infect."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Vadia, S., Arnett, E., Haghighat, A.-C., Wilson-Kubalek, E.M., Tweten, R.K., and Seveau, S. (2011). The Pore-Forming Toxin Listeriolysin O Mediates a Novel Entry Pathway of L. monocytogenes into Human. Hepatocytes. PLoS Pathog., 7.","DOI":"10.1371\/journal.ppat.1002356"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Petri\u0161i\u010d, N., Kozorog, M., Aden, S., Podobnik, M., and Anderluh, G. (2021). The molecular mechanisms of listeriolysin O-induced lipid membrane damage. Biochim. Biophys. Acta (BBA)\u2014Biomembr., 1863.","DOI":"10.1016\/j.bbamem.2021.183604"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"971","DOI":"10.1016\/j.micinf.2013.09.012","article-title":"In vitro and in vivo models to study human listeriosis: Mind the gap","volume":"15","author":"Disson","year":"2013","journal-title":"Microbes Infect."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"955","DOI":"10.1046\/j.1365-2958.2001.02704.x","article-title":"Synergy between the N- and C-terminal domains of InlB for efficient invasion of non-phagocytic cells by Listeria monocytogenes","volume":"42","author":"Cossart","year":"2001","journal-title":"Mol. Microbiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1016\/j.jip.2009.09.005","article-title":"Comparative analysis of the virulence of invertebrate and mammalian pathogenic bacteria in the oral insect infection model Galleria mellonella","volume":"103","author":"Fedhila","year":"2010","journal-title":"J. Invertebr. Pathol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1016\/j.mib.2011.01.005","article-title":"Regulation of Listeria virulence: PrfA master and commander","volume":"14","author":"Cain","year":"2011","journal-title":"Curr. Opin. Microbiol."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/13\/1\/191\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,8]],"date-time":"2025-10-08T10:30:30Z","timestamp":1759919430000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/13\/1\/191"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,1,17]]},"references-count":47,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,1]]}},"alternative-id":["microorganisms13010191"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms13010191","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,1,17]]}}}