{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,17]],"date-time":"2026-09-17T23:36:31Z","timestamp":1789688191853,"version":"4.0.1"},"reference-count":67,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2021,8,27]],"date-time":"2021-08-27T00:00:00Z","timestamp":1630022400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000199","name":"U.S. Department of Agriculture","doi-asserted-by":"publisher","award":["2018-67016-28297"],"award-info":[{"award-number":["2018-67016-28297"]}],"id":[{"id":"10.13039\/100000199","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["0619793"],"award-info":[{"award-number":["0619793"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["0923535"],"award-info":[{"award-number":["0923535"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Toxins"],"abstract":"<jats:p>Salmonellosis is among the most reported foodborne illnesses in the United States. The Salmonellaenterica Typhimurium DT104 phage type, which is associated with multidrug-resistant disease in humans and animals, possesses an ADP-ribosylating toxin called ArtAB. Full-length artAB has been found on a number of broad-host-range non-typhoidal Salmonella species and serovars. ArtAB is also homologous to many AB5 toxins from diverse Gram-negative pathogens, including cholera toxin (CT) and pertussis toxin (PT), and may be involved in Salmonella pathogenesis, however, in vitro cellular toxicity of ArtAB has not been characterized. artAB was cloned into E. coli and initially isolated using a histidine tag (ArtABHIS) and nickel chromatography. ArtABHIS was found to bind to African green monkey kidney epithelial (Vero) cells using confocal microscopy and to interact with glycans present on fetuin and monosialotetrahexosylganglioside (GM1) using ELISA. Untagged, or native, holotoxin (ArtAB), and the pentameric receptor-binding subunit (ArtB) were purified from E. coli using fetuin and d-galactose affinity chromatography. ArtAB and ArtB metabolic and cytotoxic activities were determined using Vero and Chinese hamster ovary (CHO) epithelial cells. Vero cells were more sensitive to ArtAB, however, incubation with both cell types revealed only partial cytotoxicity over 72 h, similar to that induced by CT. ArtAB induced a distinctive clustering phenotype on CHO cells over 72 h, similar to PT, and an elongated phenotype on Vero cells, similar to CT. The ArtB binding subunit alone also had a cytotoxic effect on CHO cells and induced morphological rounding. Results indicate that this toxin induces distinctive cellular outcomes. Continued biological characterization of ArtAB will advance efforts to prevent disease caused by non-typhoidal Salmonella.<\/jats:p>","DOI":"10.3390\/toxins13090599","type":"journal-article","created":{"date-parts":[[2021,8,31]],"date-time":"2021-08-31T22:58:15Z","timestamp":1630450695000},"page":"599","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Cellular Activity of Salmonella Typhimurium ArtAB Toxin and Its Receptor-Binding Subunit"],"prefix":"10.3390","volume":"13","author":[{"given":"Elise","family":"Overgaard","sequence":"first","affiliation":[{"name":"Biomolecular Sciences Graduate Program, Boise State University, Boise, ID 83725, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brad","family":"Morris","sequence":"additional","affiliation":[{"name":"Department of Biology, Boise State University, Boise, ID 83725, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4593-6713","authenticated-orcid":false,"given":"Omid","family":"Mohammad Mousa","sequence":"additional","affiliation":[{"name":"Department of Biology, Boise State University, Boise, ID 83725, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emily","family":"Price","sequence":"additional","affiliation":[{"name":"Idaho Veterans Research and Education Foundation, Infectious Diseases Section, Boise, ID 83702, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adriana","family":"Rodriguez","sequence":"additional","affiliation":[{"name":"Department of Biology, Boise State University, Boise, ID 83725, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leyla","family":"Cufurovic","sequence":"additional","affiliation":[{"name":"Department of Biology, Boise State University, Boise, ID 83725, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8545-3014","authenticated-orcid":false,"given":"Richard S.","family":"Beard","sequence":"additional","affiliation":[{"name":"Biomolecular Research Center, Boise State University, Boise, ID 83725, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8954-5810","authenticated-orcid":false,"given":"Juliette K.","family":"Tinker","sequence":"additional","affiliation":[{"name":"Biomolecular Sciences Graduate Program, Boise State University, Boise, ID 83725, USA"},{"name":"Department of Biology, Boise State University, Boise, ID 83725, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,8,27]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"509","DOI":"10.15585\/mmwr.mm6917a1","article-title":"Preliminary Incidence and Trends of Infections with Pathogens Transmitted Commonly Through Food\u2014Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 2016\u20132019","volume":"69","author":"Tack","year":"2020","journal-title":"MMWR Morb. Mortal. Wkly. Rep."},{"key":"ref_2","unstructured":"World Health Organization, and Food and Agriculture Organization of the United Nations (2016). Interventions for the Control of Non-Typhoidal Salmonella spp. in Beef and Pork: Meeting Report and Systematic Review, World Health Organization."},{"key":"ref_3","unstructured":"CDC (2019). Antibiotic Resistance Threats in the United States, U.S. Department of Health and Human Services."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"964","DOI":"10.1016\/j.tim.2019.05.002","article-title":"Salmonella enterica.","volume":"27","author":"Knodler","year":"2019","journal-title":"Trends Microbiol."},{"key":"ref_5","unstructured":"Morningstar-Shaw, B.R., Mackie, B.S.A., Barker, D.K., and Palmer, E.A. (2016). Salmonella Serotypes Isolated from Animals and Related Sources, National Center for Emerging and Zoonotic Infectious Diseases, Division of Foodborne, Waterborne, and Environmental Disease, CDC."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1368","DOI":"10.3389\/fmicb.2019.01368","article-title":"Embracing Diversity: Differences in Virulence Mechanisms, Disease Severity, and Host Adaptations Contribute to the Success of Nontyphoidal","volume":"10","author":"Cheng","year":"2019","journal-title":"Front Microbiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"2516","DOI":"10.1128\/AEM.03821-15","article-title":"Global Genomic Epidemiology of Salmonella enterica Serovar Typhimurium DT104","volume":"82","author":"Leekitcharoenphon","year":"2016","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"4673","DOI":"10.1128\/IAI.69.7.4673-4677.2001","article-title":"In vitro and in vivo assessment of Salmonella enterica serovar Typhimurium DT104 virulence","volume":"69","author":"Allen","year":"2001","journal-title":"Infect. Immun."},{"key":"ref_9","first-page":"559","article-title":"Salmonella Typhimurium DT104: A virulent and drug-resistant pathogen","volume":"39","author":"Poppe","year":"1998","journal-title":"Can. Vet. J."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"3089","DOI":"10.1099\/mic.0.27933-0","article-title":"The artAB genes encode a putative ADP-ribosyltransferase toxin homologue associated with Salmonella enterica serovar Typhimurium DT104","volume":"151","author":"Saitoh","year":"2005","journal-title":"Microbiology"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"294","DOI":"10.1016\/j.chom.2013.08.001","article-title":"Cholera toxin disrupts barrier function by inhibiting exocyst-mediated trafficking of host proteins to intestinal cell junctions","volume":"14","author":"Guichard","year":"2013","journal-title":"Cell Host. Microbe."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1111\/j.1462-5822.2006.00813.x","article-title":"Pertussis toxin transiently affects barrier integrity, organelle organization and transmigration of monocytes in a human brain microvascular endothelial cell barrier model","volume":"9","author":"Heusipp","year":"2007","journal-title":"Cell Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Cheng, R.A., and Wiedmann, M. (2019). The ADP-Ribosylating Toxins of Salmonella. Toxins, 11.","DOI":"10.3390\/toxins11070416"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2653","DOI":"10.1038\/s41598-017-02517-2","article-title":"Characterization of pertussis-like toxin from Salmonella spp. that catalyzes ADP-ribosylation of G proteins","volume":"7","author":"Tamamura","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"3710","DOI":"10.1099\/mic.0.028399-0","article-title":"Salmonella enterica serotype Typhimurium DT104 ArtA-dependent modification of pertussis toxin-sensitive G proteins in the presence of [32P]NAD","volume":"155","author":"Uchida","year":"2009","journal-title":"Microbiology"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"15562","DOI":"10.1074\/jbc.272.24.15562","article-title":"Proteolytic activation of cholera toxin and Escherichia coli labile toxin by entry into host epithelial cells. Signal transduction by a protease-resistant toxin variant","volume":"272","author":"Lencer","year":"1997","journal-title":"J. Biol. Chem."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"5954","DOI":"10.1021\/bi100474z","article-title":"Identification and characterization of the carbohydrate ligands recognized by pertussis toxin via a glycan microarray and surface plasmon resonance","volume":"49","author":"Millen","year":"2010","journal-title":"Biochemistry"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"584","DOI":"10.1177\/1060028017698162","article-title":"Vaxchora: A Single-Dose Oral Cholera Vaccine","volume":"51","author":"Cabrera","year":"2017","journal-title":"Ann. Pharmacother."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Gregg, K.A., and Merkel, T.J. (2019). Pertussis Toxin: A Key Component in Pertussis Vaccines?. Toxins, 11.","DOI":"10.3390\/toxins11100557"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1111\/j.1749-6632.1996.tb21127.x","article-title":"Cholera toxin B subunit as transmucosal carrier-delivery and immunomodulating system for induction of antiinfectious and antipathological immunity","volume":"778","author":"Czerkinsky","year":"1996","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1446","DOI":"10.2174\/138920112800784835","article-title":"Bacteria and their toxins tamed for immunotherapy","volume":"13","author":"Adkins","year":"2012","journal-title":"Curr. Pharm. Biotechnol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/S0198-8859(97)00081-5","article-title":"Delivery of antigens to the MHC class I pathway using bacterial toxins","volume":"54","author":"Goletz","year":"1997","journal-title":"Hum. Immunol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.it.2003.11.008","article-title":"New tools for antigen delivery to the MHC class I pathway","volume":"25","author":"Dadaglio","year":"2004","journal-title":"Trends Immunol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1870","DOI":"10.1093\/molbev\/msw054","article-title":"MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets","volume":"33","author":"Kumar","year":"2016","journal-title":"Mol. Biol. Evol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"15143","DOI":"10.1074\/jbc.M117.796094","article-title":"Structure-function analyses of a pertussis-like toxin from pathogenic E. coli reveal a distinct mechanism of inhibition of timeric G-proteins","volume":"292","author":"Littler","year":"2017","journal-title":"J. Biol. Chem."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1186\/s13059-018-1540-z","article-title":"SKESA: Strategic k-mer extension for scrupulous assemblies","volume":"19","author":"Souvorov","year":"2018","journal-title":"Genome Biol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1038\/nature12377","article-title":"Structure and function of the Salmonella Typhi chimaeric A2B5 typhoid toxin","volume":"499","author":"Song","year":"2013","journal-title":"Nature"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"e01255-20","DOI":"10.1128\/mSphere.01255-20","article-title":"The Majority of Typhoid Toxin-Positive","volume":"6","author":"Gaballa","year":"2021","journal-title":"mSphere"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"648","DOI":"10.1038\/nature07428","article-title":"Incorporation of a non-human glycan mediates human susceptibility to a bacterial toxin","volume":"456","author":"Byres","year":"2008","journal-title":"Nature"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1592","DOI":"10.1038\/s41564-017-0033-2","article-title":"Evolution of host adaptation in the Salmonella typhoid toxin","volume":"2","author":"Gao","year":"2017","journal-title":"Nat. Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1290","DOI":"10.1016\/j.cell.2014.10.057","article-title":"Host adaptation of a bacterial toxin from the human pathogen Salmonella Typhi","volume":"159","author":"Deng","year":"2014","journal-title":"Cell"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"W296","DOI":"10.1093\/nar\/gky427","article-title":"SWISS-MODEL: Homology modelling of protein structures and complexes","volume":"46","author":"Waterhouse","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1186\/1471-2105-9-40","article-title":"I-TASSER server for protein 3D structure prediction","volume":"9","author":"Zhang","year":"2008","journal-title":"BMC Bioinform."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"6375","DOI":"10.1021\/bi952314i","article-title":"Cholera toxin binding affinity and specificity for gangliosides determined by surface plasmon resonance","volume":"35","author":"Kuziemko","year":"1996","journal-title":"Biochemistry"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2520","DOI":"10.1073\/pnas.72.7.2520","article-title":"Interaction of cholera toxin and membrane GM1 ganglioside of small intestine","volume":"72","author":"Holmgren","year":"1975","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1139\/o89-061","article-title":"Single-step purification of pertussis toxin and its subunits by heat-treated fetuin-sepharose affinity chromatography","volume":"67","author":"Chong","year":"1989","journal-title":"Biochem. Cell Biol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"13734","DOI":"10.1021\/bi061175+","article-title":"The pertussis toxin S1 subunit is a thermally unstable protein susceptible to degradation by the 20S proteasome","volume":"45","author":"Pande","year":"2006","journal-title":"Biochemistry"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/S0092-1157(85)80034-2","article-title":"The standardization of an assay for pertussis toxin and antitoxin in microplate culture of Chinese hamster ovary cells","volume":"13","author":"Gillenius","year":"1985","journal-title":"J. Biol. Stand."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"514","DOI":"10.1128\/iai.21.2.514-517.1978","article-title":"Stimulation of cyclic AMP secretion in Vero cells by enterotoxins of Escherichia coli and Vibrio cholerae","volume":"21","author":"Stavric","year":"1978","journal-title":"Infect. Immun."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"pdb.prot087379","DOI":"10.1101\/pdb.prot087379","article-title":"Crystal Violet Assay for Determining Viability of Cultured Cells","volume":"2016","author":"Feoktistova","year":"2016","journal-title":"Cold Spring Harb. Protoc."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"8122","DOI":"10.1016\/S0021-9258(18)92950-9","article-title":"Protease treatment of pertussis toxin identifies the preferential cleavage of the S1 subunit","volume":"266","author":"Krueger","year":"1991","journal-title":"J. Biol. Chem."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"674","DOI":"10.1093\/infdis\/139.6.674","article-title":"Origin of the enzymatically active A1 fragment of cholera toxin","volume":"139","author":"Gill","year":"1979","journal-title":"J. Infect. Dis."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/S0969-2126(00)00007-1","article-title":"The crystal structure of pertussis toxin","volume":"2","author":"Stein","year":"1994","journal-title":"Structure"},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Carbonetti, N.H., Mays, R.M., Artamonova, G.V., Plaut, R.D., and Worthington, Z.E. (2005). Proteolytic cleavage of pertussis toxin S1 subunit is not essential for its activity in mammalian cells. BMC Microbiol., 5.","DOI":"10.1186\/1471-2180-5-7"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Plaut, R.D., Scanlon, K.M., Taylor, M., Teter, K., and Carbonetti, N.H. (2016). Intracellular disassembly and activity of pertussis toxin require interaction with ATP. Pathog. Dis., 74.","DOI":"10.1093\/femspd\/ftw065"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"e00428-19","DOI":"10.1128\/IAI.00428-19","article-title":"Bimodal Response to Shiga Toxin 2 Subtypes Results from Relatively Weak Binding to the Target Cell","volume":"87","author":"Cherubin","year":"2019","journal-title":"Infect. Immun."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"2494","DOI":"10.1038\/s41598-018-20861-9","article-title":"Cellular recovery from exposure to sub-optimal concentrations of AB toxins that inhibit protein synthesis","volume":"8","author":"Cherubin","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"4176","DOI":"10.1128\/iai.62.10.4176-4185.1994","article-title":"Importance of ADP-ribosylation in the morphological changes of PC12 cells induced by cholera toxin","volume":"62","author":"Glineur","year":"1994","journal-title":"Infect. Immun."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1007\/BF01875376","article-title":"Mechanism of action of cholera toxin: Effect of receptor density and multivalent binding on activation of adenylate cyclase","volume":"54","author":"Fishman","year":"1980","journal-title":"J. Membr. Biol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1007\/BF01666023","article-title":"A tissue culture method for the selection of bacterial enterotoxins","volume":"6","author":"Maneval","year":"1981","journal-title":"J. Tissue Cult. Methods"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"720","DOI":"10.1093\/infdis\/135.5.720","article-title":"Characterization of the Chinese hamster ovary cell assay for the enterotoxins of Vibrio cholerae and Escherichia coli and for specific antisera, and toxoid","volume":"135","author":"Guerrant","year":"1977","journal-title":"J. Infect. Dis."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1128\/jcm.7.5.479-485.1978","article-title":"Assay method for Vibrio cholerae and Escherichia coli enterotoxins by automated counting of floating chinese hamster ovary cells in culture medium","volume":"7","author":"Nozawa","year":"1978","journal-title":"J. Clin. Microbiol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"2812","DOI":"10.1038\/s41598-019-38726-0","article-title":"Proteomic analysis of cholera toxin adjuvant-stimulated human monocytes identifies Thrombospondin-1 and Integrin-\u03b21 as strongly upregulated molecules involved in adjuvant activity","volume":"9","author":"Terrinoni","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1198","DOI":"10.1128\/iai.40.3.1198-1203.1983","article-title":"Induction of a novel morphological response in Chinese hamster ovary cells by pertussis toxin","volume":"40","author":"Hewlett","year":"1983","journal-title":"Infect. Immun."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1128\/iai.55.1.24-28.1987","article-title":"Role of the A subunit of pertussis toxin in alteration of Chinese hamster ovary cell morphology","volume":"55","author":"Burns","year":"1987","journal-title":"Infect. Immun."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"ftw001","DOI":"10.1093\/femspd\/ftw001","article-title":"The chromosomal nature of LT-II enterotoxins solved: A lambdoid prophage encodes both LT-II and one of two novel pertussis-toxin-like toxin family members in type II enterotoxigenic Escherichia coli","volume":"74","author":"Jobling","year":"2016","journal-title":"Pathog. Dis."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"410","DOI":"10.1016\/j.micinf.2005.07.005","article-title":"Cytotoxic effect of Shiga toxin-2 holotoxin and its B subunit on human renal tubular epithelial cells","volume":"8","author":"Creydt","year":"2006","journal-title":"Microbes Infect."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1111\/j.1574-695X.1998.tb01141.x","article-title":"Affinity purification of recombinant cholera toxin B subunit oligomer expressed in Bacillus brevis for potential human use as a mucosal adjuvant","volume":"20","author":"Yasuda","year":"1998","journal-title":"FEMS Immunol. Med. Microbiol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1002\/eji.1830210236","article-title":"Effect of bacterial toxins on human B cell activation. II. Mitogenic activity of the B subunit of cholera toxin","volume":"21","author":"Dugas","year":"1991","journal-title":"Eur. J. Immunol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1002\/jcp.1041330227","article-title":"Mitogenic and antimitogenic effects of cholera toxin-mediated cyclic AMP levels in 3T3 cells","volume":"133","author":"Smets","year":"1987","journal-title":"J. Cell. Physiol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1111\/1523-1747.ep12510580","article-title":"Effects of cholera toxin on proliferation of cultured human keratinocytes in relation to intracellular cyclic AMP levels","volume":"79","author":"Okada","year":"1982","journal-title":"J. Invest. Dermatol."},{"key":"ref_62","first-page":"2615","article-title":"Cholera toxin triggers apoptosis in human lung cancer cell lines","volume":"57","author":"Allam","year":"1997","journal-title":"Cancer Res."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1093\/intimm\/8.5.731","article-title":"Cross-linking of cell surface ganglioside GM1 induces the selective apoptosis of mature CD8+ T lymphocytes","volume":"8","author":"Nashar","year":"1996","journal-title":"Int. Immunol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"212001","DOI":"10.1103\/PhysRevLett.108.212001","article-title":"Observation of spin correlation in tt events from pp collisions at radicals=7 TeV using the ATLAS detector","volume":"108","author":"Aad","year":"2012","journal-title":"Phys. Rev. Lett."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"14662","DOI":"10.1073\/pnas.011442598","article-title":"Identification of motifs in cholera toxin A1 polypeptide that are required for its interaction with human ADP-ribosylation factor 6 in a bacterial two-hybrid system","volume":"97","author":"Jobling","year":"2000","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_66","first-page":"275","article-title":"The rapid generation of mutation data matrices from protein sequences","volume":"8","author":"Jones","year":"1992","journal-title":"Comput. Appl. Biosci."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1016\/j.pep.2010.04.021","article-title":"Purification and characterization of Yersinia enterocolitica and Yersinia pestis LcrV-cholera toxin A(2)\/B chimeras","volume":"74","author":"Tinker","year":"2010","journal-title":"Protein Expr. Purif."}],"container-title":["Toxins"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6651\/13\/9\/599\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:54:05Z","timestamp":1760165645000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6651\/13\/9\/599"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,8,27]]},"references-count":67,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2021,9]]}},"alternative-id":["toxins13090599"],"URL":"https:\/\/doi.org\/10.3390\/toxins13090599","relation":{},"ISSN":["2072-6651"],"issn-type":[{"value":"2072-6651","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,8,27]]}}}