{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,10]],"date-time":"2026-10-10T13:20:04Z","timestamp":1791638404062,"version":"4.3.4"},"reference-count":42,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2022,7,31]],"date-time":"2022-07-31T00:00:00Z","timestamp":1659225600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Ministry of Science and Technology of Taiwan","award":["110-2221-E-019-006-"],"award-info":[{"award-number":["110-2221-E-019-006-"]}]},{"name":"Ministry of Science and Technology of Taiwan","award":["111-2221-E-019-005-MY2"],"award-info":[{"award-number":["111-2221-E-019-005-MY2"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biology"],"abstract":"<jats:p>High-pressure processing (HPP) is a prevailing non-thermal food preservation technology. The inactivation mechanisms of Listeria monocytogenes under HPP at 200 and 400 MPa for 3 min were investigated by label-free quantitative proteomic analysis and functional enrichment analysis in the Kyoto Encyclopedia of Genes and Genomes. HPP treatment at 400 MPa exhibited significant effects on proteins involved in translation, carbon, carbohydrate, lipid and energy metabolism, and peptidoglycan biosynthesis. HPP increased most ribosomal subunits and initiation factors, suggesting it might shift ribosomal biogenesis to translation initiation. However, protein synthesis was impaired by the shortage of proteins responsible for elongation, termination and recycling. HPP stimulated several ATP-dependent Clp proteases, and the global transcriptional regulator Spx, associating with activation of the stress-activated sigma factor Sigma B (\u03c3B) and the transcriptional activator positive regulatory factor A (PrfA) regulons. The quantitative proteomics approaches provide fundamental information on L. monocytogenes under different HPP pressures, and provide theoretical support for HPP against Listeriosis illness and for promotion of safer ready-to-eat foods.<\/jats:p>","DOI":"10.3390\/biology11081152","type":"journal-article","created":{"date-parts":[[2022,7,31]],"date-time":"2022-07-31T21:49:02Z","timestamp":1659304142000},"page":"1152","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Differential Proteomic Analysis of Listeria monocytogenes during High-Pressure Processing"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1689-5999","authenticated-orcid":false,"given":"Yi-An","family":"Chen","sequence":"first","affiliation":[{"name":"Department of Food Science, National Taiwan Ocean University, Keelung 20224, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3435-0725","authenticated-orcid":false,"given":"Guan-Wen","family":"Chen","sequence":"additional","affiliation":[{"name":"Department of Food Science, National Taiwan Ocean University, Keelung 20224, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1537-6724","authenticated-orcid":false,"given":"Hao-Hsiang","family":"Ku","sequence":"additional","affiliation":[{"name":"Institute of Food Safety and Risk Management, National Taiwan Ocean University, Keelung 20224, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7873-132X","authenticated-orcid":false,"given":"Tsui-Chin","family":"Huang","sequence":"additional","affiliation":[{"name":"Graduate Institute of Cancer Biology and Drug Discovery, College of Medical Science and Technology, Taipei Medical University, Taipei 11031, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2742-0676","authenticated-orcid":false,"given":"Hsin-Yi","family":"Chang","sequence":"additional","affiliation":[{"name":"Graduate Institute of Medical Sciences, Department of Research and Development, National Defense Medical Center, Taipei 11490, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cheng-I","family":"Wei","sequence":"additional","affiliation":[{"name":"Department of Nutrition &Food Science, University of Maryland, College Park, MD 20742, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yung-Hsiang","family":"Tsai","sequence":"additional","affiliation":[{"name":"Department of Seafood Science, National Kaohsiung University of Science and Technology, Kaohsiung 811, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6234-9190","authenticated-orcid":false,"given":"Tai-Yuan","family":"Chen","sequence":"additional","affiliation":[{"name":"Department of Food Science, National Taiwan Ocean University, Keelung 20224, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,7,31]]},"reference":[{"key":"ref_1","unstructured":"Centers for Disease Control and Prevention (CDC) (2020, August 31). Listeria (Listeriosis), Available online: https:\/\/www.cdc.gov\/listeria\/prevention.html."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.foodcont.2016.12.016","article-title":"A review of Listeria monocytogenes: An updated on outbreaks, virulence, dose-response, ecology, and risk assessments","volume":"75","author":"Buchanan","year":"2017","journal-title":"Food Control"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"European Food Safety Authority and European Centre for Disease Prevention and Control (EFSA and ECDC) (2019). The European Union one health 2018 zoonoses report. EFSA J., 17, 5926.","DOI":"10.2903\/j.efsa.2019.5926"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Daher, D., Le Gourrierec, S., and P\u00e9rez Lamela, C. (2017). Effect of high pressure processing on the microbial inactivation in fruit preparation and other vegetable based beverages. Agriculture, 7.","DOI":"10.3390\/agriculture7090072"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1234","DOI":"10.1016\/j.lwt.2015.07.029","article-title":"Comparative study between Serrano and Iberian dry-cured hams in relation to the application of high hydrostatic pressure and temporal sensory perceptions","volume":"64","author":"Lorido","year":"2015","journal-title":"LWT Food Sci. Technol."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Meloni, D. (2019). High-hydrostatic-pressure (HHP) processing technology as a novel control method for Listeria monocytogenes occurrence in Mediterranean-Style dry-fermented sausages. Foods, 8.","DOI":"10.3390\/foods8120672"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"102476","DOI":"10.1016\/j.ifset.2020.102476","article-title":"Extending shelf life of desalted cod by high pressure processing","volume":"69","author":"Rode","year":"2021","journal-title":"Innov. Food Sci. Emerg. Technol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"108583","DOI":"10.1016\/j.foodcont.2021.108583","article-title":"Inactivation of microbial loads and retardation of quality loss in Asian hard clam (Meretrix lusoria) using high-hydrostatic-pressure processing during refrigerated storage","volume":"133","author":"Lin","year":"2022","journal-title":"Food Control"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1016\/j.foodchem.2015.08.019","article-title":"Differential proteomics to explore the inhibitory effects of acidic, slightly acidic electrolysed water and sodium hypochlorite solution on Vibrio parahaemolyticus","volume":"194","author":"Chen","year":"2016","journal-title":"Food Chem."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1410","DOI":"10.1021\/acs.jproteome.6b00645","article-title":"Assessment of label-free quantitation in discovery proteomics and impact of technological factors and natural variability of protein abundance","volume":"16","author":"Mojovsky","year":"2017","journal-title":"J. Proteome Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"462","DOI":"10.1099\/mic.0.2007\/010314-0","article-title":"Differential gene expression of Listeria monocytogenes during high hydrostatic pressure processing","volume":"154","author":"Bowman","year":"2008","journal-title":"Microbiology"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Duru, I.C., Bucur, F.I., Andreevskaya, M., Nikparvar, B., Ylinen, A., Grigore-Gurgu, L., Rode, T.M., Crauwels, P., Laine, P., and Paulin, L. (2021). High-pressure processing-induced transcriptome response during recovery of Listeria monocytogenes. BMC Genom., 22.","DOI":"10.1186\/s12864-021-07407-6"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1016\/j.foodcont.2018.03.015","article-title":"Label free-based proteomic analysis of proteins in Bacillus cereus spores regulated by high pressure processing and slightly acidic electrolyzed water treatment","volume":"90","author":"Wang","year":"2018","journal-title":"Food Control"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"110494","DOI":"10.1016\/j.foodres.2021.110494","article-title":"Combined impact of high-pressure processing and slightly acidic electrolysed water on Listeria monocytogenes proteomes","volume":"147","author":"Chen","year":"2021","journal-title":"Food Res. Int."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1144","DOI":"10.1016\/j.jprot.2011.10.028","article-title":"Dynamic proteomic changes in Campylobacter jejuni 81\u2013176 after high pressure shock and subsequent recovery","volume":"75","author":"Chevret","year":"2012","journal-title":"J. Proteom."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"765","DOI":"10.1002\/1615-9861(200206)2:6<765::AID-PROT765>3.0.CO;2-V","article-title":"High pressure effects step-wise altered protein expression in Lactobacillus sanfranciscensis","volume":"2","author":"Drews","year":"2002","journal-title":"Proteomics"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"D607","DOI":"10.1093\/nar\/gky1131","article-title":"STRING v11: Protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets","volume":"47","author":"Szklarczyk","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1002\/pro.4172","article-title":"KEGG mapping tools for uncovering hidden features in biological data","volume":"31","author":"Kanehisa","year":"2022","journal-title":"Protein Sci."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1111\/1467-9868.00293","article-title":"Estimating the number of clusters in a data Set via the Gap statistic","volume":"63","author":"Tibshirani","year":"2001","journal-title":"J. R. Stat. Soc. Ser. B"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1080\/87559129.2015.1094816","article-title":"Susceptibility of Listeria monocytogenes to high pressure processing; A review","volume":"32","author":"Ferreira","year":"2016","journal-title":"Food Rev. Int."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"250","DOI":"10.1016\/j.foodcont.2013.12.007","article-title":"Responses of microorganisms to high hydrostatic pressure processing","volume":"40","author":"Huang","year":"2014","journal-title":"Food Control"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Nguyen, H.T.M., Akanuma, G., Hoa, T.T.M., Nakai, Y., Kimura, K., Yamamoto, K., and Inaoka, T. (2020). Ribosome reconstruction during recovery from high-hydrostatic-pressure induced injury in Bacillus subtilis. Appl. Environ. Microbiol., 86.","DOI":"10.1128\/AEM.01640-19"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1099\/13500872-145-2-419","article-title":"The effects of hydrostatic pressure on ribosome conformation in Escherichia coli: An in vivo study using differential scanning calorimetry","volume":"145","author":"Niven","year":"1999","journal-title":"Microbiology"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"479","DOI":"10.3136\/fstr.25.479","article-title":"Injury and recovery of Escherichia coli cells in phosphate-buffered saline after high hydrostatic pressure treatment","volume":"25","author":"Morimatsu","year":"2019","journal-title":"Food Sci. Technol. Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/j.celrep.2017.06.028","article-title":"Post-termination ribosome intermediate acts as the gateway to ribosome recycling","volume":"20","author":"Prabhakar","year":"2017","journal-title":"Cell Rep."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"8510","DOI":"10.1128\/JB.01259-07","article-title":"Dissection of 16S rRNA methyltransferase (KsgA) function in Escherichia coli","volume":"189","author":"Inoue","year":"2008","journal-title":"J. Bacteriol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1454","DOI":"10.1261\/rna.051383.115","article-title":"Mutation of ribosomal protein S5 suppress a defect in late-30S ribosomal subunit biogenesis caused by lack of the RbfA biogenesis factor","volume":"21","author":"Nord","year":"2015","journal-title":"RNA"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Maksimova, E.M., Korepanov, A.P., Kravchenko, O.V., Baymukhametov, T.N., Myasnikov, A.G., Vassilenko, K.S., Afonina, Z.A., and Stolboushkina, E.A. (2021). RbfA is involved in two important stages of 30S subunit assembly: Formation of the central pseudoknot and docking of helix 44 to the decoding center. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22116140"},{"key":"ref_29","first-page":"359","article-title":"RbfA and IF3 couple ribosome biogenesis and translation initiation to increase stress tolerance","volume":"48","author":"Sharma","year":"2020","journal-title":"Nucleic Acids Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1128\/MMBR.00013-07","article-title":"Ribosome biogenesis and the translation process in Escherichia coli","volume":"71","author":"Kaczanowska","year":"2007","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"382","DOI":"10.1111\/mmi.12105","article-title":"Nus transcription elongation factors and RNase III modulate small ribosome subunit biogenesis in Escherichia coli","volume":"87","author":"Bubunenko","year":"2012","journal-title":"Mol. Microbiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1159\/000517718","article-title":"Contribution of the Clp protease to bacterial survival and mitochondrial homoeostasis","volume":"31","author":"Illigmann","year":"2021","journal-title":"Microb. Physiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"3135","DOI":"10.3389\/fmicb.2018.03135","article-title":"CtsR, the master regulator of stress-response in Oenococcus oeni, is a heat sensor interacting with ClpL1","volume":"9","author":"Darsonval","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1227","DOI":"10.1046\/j.1365-2958.2003.03636.x","article-title":"The CtsR regulator of Listeria monocytogenes contains a variant glycine repeat region that affects piezotolerance, stress resistance, motility and virulence","volume":"49","author":"Karatzas","year":"2003","journal-title":"Mol. Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1165","DOI":"10.1128\/JB.186.4.1165-1174.2004","article-title":"ClpB, a novel member of the Listeria monocytogenes CtsR regulon, is involved in virulence but not in general stress tolerance","volume":"186","author":"Chastanet","year":"2004","journal-title":"J. Bacteriol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1878","DOI":"10.1002\/pmic.200402086","article-title":"Comparative proteome approach to characterize the high-pressure stress response of Lactobacillus sanfranciscensis DSM 20451T","volume":"6","author":"Scheyhing","year":"2006","journal-title":"Proteomics"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"4938","DOI":"10.1128\/IAI.69.8.4938-4943.2001","article-title":"Stress-induced ClpP serine protease of Listeria monocytogenes is essential for induction of listeriolysin O-dependent protective immunity","volume":"69","author":"Gaillot","year":"2001","journal-title":"Infect. Immun."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1111\/mmi.14508","article-title":"Listeria monocytogenes SpxA1 is a global regulator required to activate genes encoding catalase and heme biosynthesis enzymes for aerobic growth","volume":"114","author":"Cesinger","year":"2020","journal-title":"Mol. Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Gaballa, A., Guariglia-Oropeza, V., Wiedmann, M., and Boor, K.J. (2019). Cross talk between SigB and PrfA in Listeria monocytogenes facilitates transitions between extra- and intracellular environments. Microbiol. Mol. Biol. Rev., 83.","DOI":"10.1128\/MMBR.00034-19"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"819","DOI":"10.1099\/mic.0.000808","article-title":"Flick of a switch: Regulatory mechanisms allowing Listeria monocytogenes to transition from a saprophyte to a killer","volume":"165","author":"Tiensuu","year":"2019","journal-title":"Microbiology"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Uhlig, F., and Hyland, N.P. (2022). Making sense of quorum sensing at the intestinal mucosal interface. Cells, 11.","DOI":"10.3390\/cells11111734"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"62","DOI":"10.3389\/fcimb.2019.00062","article-title":"The AI-2\/luxS quorum sensing system affects the growth characteristics, biofilm formation, and virulence of Haemophilus parasuis","volume":"9","author":"Zhang","year":"2019","journal-title":"Front. Cell Infect. Microbiol."}],"container-title":["Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-7737\/11\/8\/1152\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:00:22Z","timestamp":1760140822000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-7737\/11\/8\/1152"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,7,31]]},"references-count":42,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2022,8]]}},"alternative-id":["biology11081152"],"URL":"https:\/\/doi.org\/10.3390\/biology11081152","relation":{},"ISSN":["2079-7737"],"issn-type":[{"value":"2079-7737","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,7,31]]}}}