{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,27]],"date-time":"2026-09-27T10:39:15Z","timestamp":1790505555784,"version":"4.1.0"},"reference-count":29,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2016,6,18]],"date-time":"2016-06-18T00:00:00Z","timestamp":1466208000000},"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":["31270721"],"award-info":[{"award-number":["31270721"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>The proportion of foodborne disease caused by pathogenic microorganisms is rising worldwide, with staphylococcal food poisoning being one of the main causes of this increase. Juglone is a plant-derived 1,4-naphthoquinone with confirmed antibacterial and antitumor activities. However, the specific mechanism underlying its antibacterial activity against Staphylococcus aureus remains unclear. To elucidate the mechanism underlying its antibacterial activity, isobaric tags for relative and absolute quantitation methods of quantitative proteomics were applied for analysis of the 53 proteins that were differentially expressed after treatment with juglone. Combined with verification experiments, such as detection of changes in DNA and RNA content and quantification of oxidative damage, our results suggested that juglone effectively increased the protein expression of oxidoreductase and created a peroxidative environment within the cell, significantly reducing cell wall formation and increasing membrane permeability. We hypothesize that juglone binds to DNA and reduces DNA transcription and replication directly. This is the first study to adopt a proteomic approach to investigate the antibacterial mechanism of juglone.<\/jats:p>","DOI":"10.3390\/ijms17060965","type":"journal-article","created":{"date-parts":[[2016,6,20]],"date-time":"2016-06-20T12:51:28Z","timestamp":1466427088000},"page":"965","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":62,"title":["Antibacterial Activity of Juglone against Staphylococcus aureus: From Apparent to Proteomic"],"prefix":"10.3390","volume":"17","author":[{"given":"Jiayi","family":"Wang","sequence":"first","affiliation":[{"name":"College of Food Science, Shenyang Agricultural University, 120 Dongling Rd., Shenyang 110866, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuhuan","family":"Cheng","sequence":"additional","affiliation":[{"name":"College of Food Science, Shenyang Agricultural University, 120 Dongling Rd., Shenyang 110866, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rina","family":"Wu","sequence":"additional","affiliation":[{"name":"College of Food Science, Shenyang Agricultural University, 120 Dongling Rd., Shenyang 110866, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Donghua","family":"Jiang","sequence":"additional","affiliation":[{"name":"College of Food Science, Shenyang Agricultural University, 120 Dongling Rd., Shenyang 110866, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bing","family":"Bai","sequence":"additional","affiliation":[{"name":"College of Food Science, Shenyang Agricultural University, 120 Dongling Rd., Shenyang 110866, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dehong","family":"Tan","sequence":"additional","affiliation":[{"name":"College of Food Science, Shenyang Agricultural University, 120 Dongling Rd., Shenyang 110866, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tingcai","family":"Yan","sequence":"additional","affiliation":[{"name":"College of Food Science, Shenyang Agricultural University, 120 Dongling Rd., Shenyang 110866, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiyun","family":"Sun","sequence":"additional","affiliation":[{"name":"College of Food Science, Shenyang Agricultural University, 120 Dongling Rd., Shenyang 110866, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qi","family":"Zhang","sequence":"additional","affiliation":[{"name":"College of Food Science, Shenyang Agricultural University, 120 Dongling Rd., Shenyang 110866, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhaoxia","family":"Wu","sequence":"additional","affiliation":[{"name":"College of Food Science, Shenyang Agricultural University, 120 Dongling Rd., Shenyang 110866, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2016,6,18]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"827965","DOI":"10.1155\/2014\/827965","article-title":"Staphylococcus aureus and staphylococcal food-borne disease: An ongoing challenge in public health","volume":"2014","author":"Kadariya","year":"2014","journal-title":"Biomed. Res. Int."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"743","DOI":"10.3390\/toxins5040743","article-title":"Review of the inhibition of biological activities of food-related selected toxins by natural compounds","volume":"5","author":"Friedman","year":"2013","journal-title":"Toxins"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1111\/j.1574-6976.2011.00311.x","article-title":"Staphylococcus aureus and its food poisoning toxins: Characterization and outbreak investigation","volume":"36","author":"Hennekinne","year":"2012","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"2093","DOI":"10.4315\/0362-028X.JFP-13-190","article-title":"Staphylococcal poisoning foodborne outbreak: Epidemiological investigation and strain genotyping","volume":"76","author":"Gallina","year":"2013","journal-title":"J. Food Prot."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2177","DOI":"10.3390\/toxins2082177","article-title":"Staphylococcal enterotoxins","volume":"2","author":"Pinchuk","year":"2010","journal-title":"Toxins"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"47","DOI":"10.2174\/157341209787314936","article-title":"Noteworthy secondary metabolites naphthoquinones\u2014Their occurrence, pharmacological properties and analysis","volume":"5","author":"Babula","year":"2009","journal-title":"Curr. Pharm. Anal."},{"key":"ref_7","first-page":"76","article-title":"Inhibition effect of juglong on several food deterioration microorganisms","volume":"8","author":"Wu","year":"2009","journal-title":"China Brew."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1080\/07315724.2003.10719272","article-title":"Vitamin c as an antioxidant: Evaluation of its role in disease prevention","volume":"22","author":"Padayatty","year":"2003","journal-title":"J. Am. Coll. Nutr."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1046\/j.1525-1373.1999.d01-145.x","article-title":"Antioxidants and oxidative stress in exercise","volume":"222","author":"Ji","year":"1999","journal-title":"Exp. Biol. Med."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"426","DOI":"10.1080\/07315724.1999.10718880","article-title":"\u0392-carotene and other carotenoids as antioxidants","volume":"18","author":"Paiva","year":"1999","journal-title":"J. Am. Coll. Nutr."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1159\/000343108","article-title":"The discovery of vitamin k and its clinical applications","volume":"61","author":"Ferland","year":"2012","journal-title":"Ann. Nutr. Metab."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1111\/j.1432-1033.1993.tb18040.x","article-title":"L-serine and l-threonine dehydratase from clostridium propionicum two enzymes with different prosthetic groups","volume":"215","author":"Hofmeister","year":"1993","journal-title":"Eur. J. Biochem."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"5402","DOI":"10.1073\/pnas.1100410108","article-title":"Iron enzyme ribulose-5-phosphate 3-epimerase in escherichia coli is rapidly damaged by hydrogen peroxide but can be protected by manganese","volume":"108","author":"Sobota","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1016\/S0045-2068(02)00513-8","article-title":"Biosynthesis of the 7-deazaguanosine hypermodified nucleosides of transfer rna","volume":"31","year":"2003","journal-title":"Bioorg. Chem."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1006\/abbi.1994.1323","article-title":"Effects of nitroxide stable radicals on juglone cytotoxicity","volume":"312","author":"Zhang","year":"1994","journal-title":"Arch. Biochem. Biophys."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.abb.2010.02.002","article-title":"1,4-naphthoquinones as inducers of oxidative damage and stress signaling in hacat human keratinocytes","volume":"496","author":"Klaus","year":"2010","journal-title":"Arch. Biochem. Biophys."},{"key":"ref_17","first-page":"21","article-title":"Role of quinone moiety as antitumour agents: A review","volume":"12","author":"Saify","year":"1999","journal-title":"Pak. J. Pharm. Sci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1007\/s00253-002-1135-0","article-title":"Triacylglycerols in prokaryotic microorganisms","volume":"60","author":"Alvarez","year":"2002","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/S0065-2911(01)44011-2","article-title":"General stress response of bacillus subtilis and other bacteria","volume":"44","author":"Hecker","year":"2001","journal-title":"Adv. Microb. Physiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"2568","DOI":"10.1099\/mic.0.060749-0","article-title":"The mcsb gene of the clpc operon is required for stress tolerance and virulence in staphylococcus aureus","volume":"158","author":"Wozniak","year":"2012","journal-title":"Microbiology"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"2004","DOI":"10.1128\/JB.01733-07","article-title":"Widespread distribution in pathogenic bacteria of di-iron proteins that repair oxidative and nitrosative damage to iron-sulfur centers","volume":"190","author":"Overton","year":"2008","journal-title":"J. Bacteriol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"2877","DOI":"10.1099\/00221287-143-9-2877","article-title":"The staphylococcus aureus scda gene: A novel locus that affects cell division and morphogenesis","volume":"143","author":"Brunskill","year":"1997","journal-title":"Microbiology"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1648","DOI":"10.1128\/JB.188.4.1648-1659.2006","article-title":"Global transcriptome analysis of staphylococcus aureus response to hydrogen peroxide","volume":"188","author":"Chang","year":"2006","journal-title":"J. Bacteriol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"26066","DOI":"10.1074\/jbc.M402989200","article-title":"Identification and characterization of the first class of potent bacterial acetyl-coa carboxylase inhibitors with antibacterial activity","volume":"279","author":"Freiberg","year":"2004","journal-title":"J. Biol. Chem."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1016\/0005-2736(78)90435-2","article-title":"The effect of toluene on the structure and permeability of the outer and cytoplasmic membranes of escherichia coli","volume":"506","author":"Kingma","year":"1978","journal-title":"BBA Biomembr."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1038\/nmeth.1322","article-title":"Universal sample preparation method for proteome analysis","volume":"6","author":"Wisniewski","year":"2009","journal-title":"Nat. Meth."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Sandberg, A., Lindell, G., K\u00e4llstr\u00f6m, B.N., Branca, R.M., Danielsson, K.G., Dahlberg, M., Larson, B., Forshed, J., and Lehti\u00f6, J. (2012). Tumor proteomics by multivariate analysis on individual pathway data for characterization of vulvar cancer phenotypes. Mol. Cell. Proteom. MCP, 11.","DOI":"10.1074\/mcp.M112.016998"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"821","DOI":"10.1021\/pr060474i","article-title":"Technical, experimental, and biological variations in isobaric tags for relative and absolute quantitation (itraq)","volume":"6","author":"Gan","year":"2007","journal-title":"J. Proteome Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"3420","DOI":"10.1093\/nar\/gkn176","article-title":"High-throughput functional annotation and data mining with the blast2go suite","volume":"36","author":"Gotz","year":"2008","journal-title":"Nucleic Acids Res."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/17\/6\/965\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T19:25:42Z","timestamp":1760210742000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/17\/6\/965"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,6,18]]},"references-count":29,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2016,6]]}},"alternative-id":["ijms17060965"],"URL":"https:\/\/doi.org\/10.3390\/ijms17060965","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,6,18]]}}}