{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,15]],"date-time":"2025-11-15T10:16:06Z","timestamp":1763201766378},"reference-count":58,"publisher":"Public Library of Science (PLoS)","issue":"9","license":[{"start":{"date-parts":[[2013,9,5]],"date-time":"2013-09-05T00:00:00Z","timestamp":1378339200000},"content-version":"unspecified","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0073390","type":"journal-article","created":{"date-parts":[[2013,9,5]],"date-time":"2013-09-05T21:14:58Z","timestamp":1378415698000},"page":"e73390","update-policy":"http:\/\/dx.doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":22,"title":["Grape Extracts Inhibit Multiple Events in the Cell Biology of Cholera Intoxication"],"prefix":"10.1371","volume":"8","author":[{"given":"Srikar","family":"Reddy","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Michael","family":"Taylor","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mojun","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Patrick","family":"Cherubin","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sandra","family":"Geden","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Supriyo","family":"Ray","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"David","family":"Francis","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ken","family":"Teter","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2013,9,5]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"622","DOI":"10.1128\/MMBR.56.4.622-647.1992","article-title":"Structure and function of cholera toxin and the related <italic>Escherichia coli<\/italic> heat-labile enterotoxin","volume":"56","author":"BD Spangler","year":"1992","journal-title":"Microbiol Rev"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1080\/09687680410001663267","article-title":"Cholera toxin: a paradigm for multi-functional engagement of cellular mechanisms (Review)","volume":"21","author":"L De Haan","year":"2004","journal-title":"Mol Membr Biol"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1016\/S0140-6736(03)15328-7","article-title":"Cholera","volume":"363","author":"DA Sack","year":"2004","journal-title":"Lancet"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"310","DOI":"10.3390\/toxins2030310","article-title":"Cholera toxin: an intracellular journey into the cytosol by way of the endoplasmic reticulum","volume":"2","author":"NLB Wernick","year":"2010","journal-title":"Toxins"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"905","DOI":"10.1083\/jcb.141.4.905","article-title":"Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains","volume":"141","author":"PA Orlandi","year":"1998","journal-title":"J Cell Biol"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"16249","DOI":"10.1074\/jbc.M109834200","article-title":"Uncoupling of the cholera toxin-G(M1) ganglioside receptor complex from endocytosis, retrograde Golgi trafficking, and downstream signal transduction by depletion of membrane cholesterol","volume":"277","author":"AA Wolf","year":"2002","journal-title":"J Biol Chem"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"860","DOI":"10.1083\/jcb.93.3.860","article-title":"Internalization and degradation of cholera toxin by cultured cells: relationship to toxin action","volume":"93","author":"PH Fishman","year":"1982","journal-title":"J Cell Biol"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"12010","DOI":"10.1016\/S0021-9258(19)50301-5","article-title":"Brefeldin A blocks the response of cultured cells to cholera toxin. Implications for intracellular trafficking in toxin action","volume":"268","author":"PA Orlandi","year":"1993","journal-title":"J Biol Chem"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"4783","DOI":"10.1091\/mbc.E03-06-0354","article-title":"Gangliosides that associate with lipid rafts mediate transport of cholera and related toxins from the plasma membrane to endoplasmic reticulm","volume":"14","author":"Y Fujinaga","year":"2003","journal-title":"Mol Biol Cell"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"2941","DOI":"10.1172\/JCI116917","article-title":"Entry of cholera toxin into polarized human intestinal epithelial cells. Identification of an early brefeldin A sensitive event required for A1-peptide generation","volume":"92","author":"WI Lencer","year":"1993","journal-title":"J Clin Invest"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1016\/S0014-5793(96)01447-0","article-title":"Reduction of protein disulfide bonds in an oxidizing environment. The disulfide bridge of cholera toxin A-subunit is reduced in the endoplasmic reticulum","volume":"401","author":"I Majoul","year":"1997","journal-title":"FEBS Lett"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"4591","DOI":"10.1016\/S0021-9258(19)67333-3","article-title":"Protein-disulfide isomerase-mediated reduction of the A subunit of cholera toxin in a human intestinal cell line","volume":"272","author":"PA Orlandi","year":"1997","journal-title":"J Biol Chem"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"22090","DOI":"10.1074\/jbc.M111.237966","article-title":"Protein disulfide isomerase displaces the cholera toxin A1 subunit from the holotoxin without unfolding the A1 subunit","volume":"286","author":"M Taylor","year":"2011","journal-title":"J Biol Chem"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"937","DOI":"10.1016\/S0092-8674(01)00289-6","article-title":"Protein disulfide isomerase acts as a redox-dependent chaperone to unfold cholera toxin","volume":"104","author":"B Tsai","year":"2001","journal-title":"Cell"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"8839","DOI":"10.1021\/bi101201c","article-title":"Contribution of subdomain structure to the thermal stability of the cholera toxin A1 subunit","volume":"49","author":"T Banerjee","year":"2010","journal-title":"Biochemistry"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"1083","DOI":"10.1016\/j.jmb.2009.09.013","article-title":"Stabilization of the tertiary structure of the cholera toxin A1 subunit inhibits toxin dislocation and cellular intoxication","volume":"393","author":"S Massey","year":"2009","journal-title":"J Mol Biol"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"1114","DOI":"10.1016\/j.jmb.2007.10.025","article-title":"Conformational instability of the cholera toxin A1 polypeptide","volume":"374","author":"AH Pande","year":"2007","journal-title":"J Mol Biol"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"e18825","DOI":"10.1371\/journal.pone.0018825","article-title":"A therapeutic chemical chaperone inhibits cholera intoxication and unfolding\/translocation of the cholera toxin A1 subunit","volume":"6","author":"M Taylor","year":"2011","journal-title":"PLoS ONE"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"861","DOI":"10.1111\/j.1600-0854.2008.00729.x","article-title":"The recognition and retrotranslocation of misfolded proteins from the endoplasmic reticulum","volume":"9","author":"K Nakatsukasa","year":"2008","journal-title":"Traffic"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"6172","DOI":"10.1128\/IAI.70.11.6172-6179.2002","article-title":"Inhibition of endoplasmic reticulum-associated degradation in CHO cells resistant to cholera toxin, <italic>Pseudomonas aeruginosa<\/italic> exotoxin A, and ricin","volume":"70","author":"K Teter","year":"2002","journal-title":"Infect Immun"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1034\/j.1600-0854.2003.00070.x","article-title":"A class of mutant CHO cells resistant to cholera toxin rapidly degrades the catalytic polypeptide of cholera toxin and exhibits increased endoplasmic reticulum-associated degradation","volume":"4","author":"K Teter","year":"2003","journal-title":"Traffic"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"11051","DOI":"10.1021\/bi971383p","article-title":"Accumulating evidence suggests that several AB-toxins subvert the endoplasmic reticulum-associated protein degradation pathway to enter target cells","volume":"36","author":"B Hazes","year":"1997","journal-title":"Biochemistry"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"1222","DOI":"10.1093\/embo-reports\/kvf239","article-title":"Role of ubiquitination in retro-translocation of cholera toxin and escape of cytosolic degradation","volume":"3","author":"C Rodighiero","year":"2002","journal-title":"EMBO Rep"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"5271","DOI":"10.1128\/IAI.61.12.5271-5278.1993","article-title":"Monoclonal immunoglobulin A antibodies directed against cholera toxin prevent the toxin-induced chloride secretory response and block toxin binding to intestinal epithelial cells in vitro","volume":"61","author":"FM Apter","year":"1993","journal-title":"Infect Immun"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"991","DOI":"10.1046\/j.1471-4159.2001.00489.x","article-title":"Cholesterol depletion by methyl-beta-cyclodextrin blocks cholera toxin transport from endosomes to the Golgi apparatus in hippocampal neurons","volume":"78","author":"H Shogomori","year":"2001","journal-title":"J Neurochem"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"1750","DOI":"10.1091\/mbc.01-12-0592","article-title":"Inhibitors of COP-mediated transport and cholera toxin action inhibit simian virus 40 infection","volume":"13","author":"AA Richards","year":"2002","journal-title":"Mol Biol Cell"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"22838","DOI":"10.1074\/jbc.M101184200","article-title":"Involvement of ADP-ribosylation factor 1 in cholera toxin-induced morphological changes of Chinese hamster ovary cells","volume":"276","author":"N Morinaga","year":"2001","journal-title":"J Biol Chem"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"4739","DOI":"10.1128\/IAI.05503-11","article-title":"Structural and functional interactions between the cholera toxin A1 subunit and ERdj3\/HEDJ, a chaperone of the endoplasmic reticulum","volume":"79","author":"S Massey","year":"2011","journal-title":"Infect Immun"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1016\/S0014-5793(03)01217-1","article-title":"BiP-dependent export of cholera toxin from endoplasmic reticulum-derived microsomes","volume":"554","author":"A Winkeler","year":"2003","journal-title":"FEBS Lett"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"1410","DOI":"10.1128\/AEM.02230-08","article-title":"Novel cell-based method to detect Shiga toxin 2 from <italic>Escherichia coli<\/italic> O157:H7 and inhibitors of toxin activity","volume":"75","author":"B Quinones","year":"2009","journal-title":"Appl Environ Microbiol"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"23303","DOI":"10.1074\/jbc.M502093200","article-title":"Differential activities of plant polyphenols on the binding and internalization of cholera toxin in vero cells","volume":"280","author":"N Morinaga","year":"2005","journal-title":"J Biol Chem"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"3042","DOI":"10.1073\/pnas.052709499","article-title":"Identification in traditional herbal medications and confirmation by synthesis of factors that inhibit cholera toxin-induced fluid accumulation","volume":"99","author":"H Oi","year":"2002","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1111\/j.1348-0421.2002.tb02693.x","article-title":"Inhibition by apple polyphenols of ADP-ribosyltransferase activity of cholera toxin and toxin-induced fluid accumulation in mice","volume":"46","author":"T Saito","year":"2002","journal-title":"Microbiol Immunol"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/S0304-4165(99)00102-6","article-title":"Epigallocatechin gallate and gallocatechin gallate in green tea catechins inhibit extracellular release of Vero toxin from enterohemorrhagic <italic>Escherichia coli<\/italic> O157:H7","volume":"1472","author":"Y Sugita-Konishi","year":"1999","journal-title":"Biochim Biophys Acta"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"30395","DOI":"10.1074\/jbc.M112.385575","article-title":"Lipid rafts alter the stability and activity of the cholera toxin A1 subunit","volume":"287","author":"S Ray","year":"2012","journal-title":"J Biol Chem"},{"key":"ref36","doi-asserted-by":"crossref","unstructured":"Taylor M, Banerjee T, VanBennekom N, Teter K (2012) Detection of toxin translocation into the host cytosol by surface plasmon resonance. Journal of Visualized Experiments 59: doi: 10.3791\/3686.","DOI":"10.3791\/3686"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"4113","DOI":"10.1021\/bi00362a019","article-title":"Use of substituted (benzylidineamino)guanidines in the study of guanidino group specific ADP-ribosyltransferase","volume":"25","author":"G Soman","year":"1986","journal-title":"Biochemistry"},{"key":"ref38","doi-asserted-by":"crossref","first-page":"622","DOI":"10.3390\/ijms11020622","article-title":"Biological activities of polyphenols from grapes","volume":"11","author":"EQ Xia","year":"2010","journal-title":"Int J Mol Sci"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"4360","DOI":"10.1021\/jf049613b","article-title":"Polyphenol screening of pomace from red and white grape varieties (<italic>Vitis vinifera<\/italic> L.) by HPLC-DAD-MS\/MS","volume":"52","author":"D Kammerer","year":"2004","journal-title":"J Agric Food Chem"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1089\/109662003772519831","article-title":"Polyphenolics in grape seeds-biochemistry and functionality","volume":"6","author":"J Shi","year":"2003","journal-title":"J Med Food"},{"key":"ref41","first-page":"401","article-title":"Chemical characterization of commercial dietary ingredients from <italic>Vitis vinifera<\/italic> L. Anal Chim Acta","volume":"563","author":"M Monagas","year":"2006"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1002\/mnfr.200600173","article-title":"Overview of antibacterial, antitoxin, antiviral, and antifungal activities of tea flavonoids and teas","volume":"51","author":"M Friedman","year":"2007","journal-title":"Mol Nutr Food Res"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1186\/1472-6882-9-47","article-title":"Studies on the antidiarrhoeal activity of <italic>Aegle marmelos<\/italic> unripe fruit: validating its traditional usage","volume":"9","author":"S Brijesh","year":"2009","journal-title":"BMC Complement Altern Med"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"4808","DOI":"10.1016\/j.vaccine.2009.05.081","article-title":"Co-administration of cholera toxin and apple polyphenol extract as a novel and safe mucosal adjuvant strategy","volume":"27","author":"N Yoshino","year":"2009","journal-title":"Vaccine"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.toxicon.2010.03.009","article-title":"Resveratrol, a natural polyphenolic compound, inhibits cholera toxin-induced cyclic AMP accumulation in Vero cells","volume":"56","author":"N Morinaga","year":"2010","journal-title":"Toxicon"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"5855","DOI":"10.1016\/S0021-9258(18)50491-9","article-title":"Enzymic activity of cholera toxin. II. Relationships to proteolytic processing, disulfide bond reduction, and subunit composition","volume":"254","author":"JJ Mekalanos","year":"1979","journal-title":"J Biol Chem"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"1742","DOI":"10.1021\/bi0112816","article-title":"Analysis of cholera toxin-ganglioside interactions by flow cytometry","volume":"41","author":"S Lauer","year":"2002","journal-title":"Biochemistry"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"2626","DOI":"10.1016\/j.febslet.2010.04.008","article-title":"Protein toxins from plants and bacteria: probes for intracellular transport and tools in medicine","volume":"584","author":"K Sandvig","year":"2010","journal-title":"FEBS Lett"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"3054","DOI":"10.3168\/jds.S0022-0302(93)77645-6","article-title":"Review and update of casein chemistry","volume":"76","author":"HE Swaisgood","year":"1993","journal-title":"J Dairy Sci"},{"key":"ref50","first-page":"156","article-title":"Docking of selected natural polyphenols to ARF activated A1 subunit of cholera toxin","volume":"56","author":"C Podlipnik","year":"2009","journal-title":"Acta Chim Slov"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"1743","DOI":"10.1016\/j.metabol.2009.05.030","article-title":"Effect of grape seed extract on blood pressure in subjects with the metabolic syndrome","volume":"58","author":"B Sivaprakasapillai","year":"2009","journal-title":"Metabolism"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1089\/10966200152053677","article-title":"MegaNatural((R)) Gold Grapeseed Extract: In Vitro Antioxidant and In Vivo Human Supplementation Studies","volume":"4","author":"JA Vinson","year":"2001","journal-title":"J Med Food"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"1593","DOI":"10.1021\/jf010897z","article-title":"Polyphenol\/peptide binding and precipitation","volume":"50","author":"AJ Charlton","year":"2002","journal-title":"J Agric Food Chem"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/j.micpath.2007.01.007","article-title":"Inhibitory effects of various plant polyphenols on the toxicity of Staphylococcal alpha-toxin","volume":"42","author":"O Choi","year":"2007","journal-title":"Microb Pathog"},{"key":"ref55","doi-asserted-by":"crossref","first-page":"317S","DOI":"10.1093\/ajcn\/81.1.317S","article-title":"Polyphenols and disease risk in epidemiologic studies","volume":"81","author":"IC Arts","year":"2005","journal-title":"Am J Clin Nutr"},{"key":"ref56","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1021\/np960040+","article-title":"Natural polyphenols (vegetable tannins) as drugs: possible modes of action","volume":"59","author":"E Haslam","year":"1996","journal-title":"J Nat Prod"},{"key":"ref57","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1111\/j.1523-5378.2005.00315.x","article-title":"Inhibitory effects of polyphenols on gastric injury by <italic>Helicobacter pylori<\/italic> VacA toxin","volume":"10","author":"K Yahiro","year":"2005","journal-title":"Helicobacter"},{"key":"ref58","doi-asserted-by":"crossref","first-page":"418","DOI":"10.1038\/sj.embor.7400118","article-title":"Potent inhibitors of anthrax lethal factor from green tea","volume":"5","author":"I Dell\u2019Aica","year":"2004","journal-title":"EMBO Rep"}],"container-title":["PLoS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0073390","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,3,5]],"date-time":"2022-03-05T16:35:33Z","timestamp":1646498133000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0073390"}},"subtitle":[],"editor":[{"given":"Adam J.","family":"Ratner","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2013,9,5]]},"references-count":58,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2013,9,5]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0073390","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2013,9,5]]}}}