{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,29]],"date-time":"2026-04-29T23:35:37Z","timestamp":1777505737147,"version":"3.51.4"},"reference-count":73,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2010,4,26]],"date-time":"2010-04-26T00:00:00Z","timestamp":1272240000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/3.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Toxins"],"abstract":"<jats:p>Photobacterium damselae subsp. piscicida (Phdp) is a Gram-negative pathogen agent of an important fish septicemia. The key virulence factor of Phdp is the plasmid-encoded exotoxin AIP56, which is secreted by exponentially growing pathogenic strains. AIP56 has 520 amino acids including an N-terminal cleavable signal peptide of 23 amino acid residues, two cysteine residues and a zinc-binding region signature HEXXH that is typical of most zinc metallopeptidases. AIP56 induces in vitro and in vivo selective apoptosis of fish macrophages and neutrophils through a caspase-3 dependent mechanism that also involves caspase-8 and -9. In vivo, the AIP56-induced phagocyte apoptosis progresses to secondary necrosis with release of cytotoxic phagocyte molecules including neutrophil elastase. Fish injected with recombinant AIP56 die with a pathology similar to that seen in the natural infection.<\/jats:p>","DOI":"10.3390\/toxins2040905","type":"journal-article","created":{"date-parts":[[2010,4,26]],"date-time":"2010-04-26T11:03:39Z","timestamp":1272279819000},"page":"905-918","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":20,"title":["AIP56: A Novel Bacterial Apoptogenic Toxin"],"prefix":"10.3390","volume":"2","author":[{"given":"Manuel T.","family":"Silva","sequence":"first","affiliation":[{"name":"IBMC-Instituto de Biologia Molecular e Celular, Rua do Campo Alegre, 823. 4150-180 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5960-0647","authenticated-orcid":false,"given":"Nuno M. S.","family":"Dos Santos","sequence":"additional","affiliation":[{"name":"IBMC-Instituto de Biologia Molecular e Celular, Rua do Campo Alegre, 823. 4150-180 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4044-6328","authenticated-orcid":false,"given":"Ana","family":"Do Vale","sequence":"additional","affiliation":[{"name":"IBMC-Instituto de Biologia Molecular e Celular, Rua do Campo Alegre, 823. 4150-180 Porto, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2010,4,26]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1814","DOI":"10.1128\/jb.88.6.1814-1815.1964","article-title":"Pasteurella Sp. from an Epizootic of White Perch (Roccus Americanus) in Chesapeake Bay Tidewater Areas","volume":"88","author":"Snieszko","year":"1964","journal-title":"J. Bacteriol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1606","DOI":"10.1128\/jb.96.5.1606-1610.1968","article-title":"Morphology, physiology, and serology of a Pasteurella species pathogenic for white perch. (Roccus americanus)","volume":"96","author":"Janssen","year":"1968","journal-title":"J. Bacteriol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1099\/00207713-45-1-139","article-title":"Small-subunit rRNA sequences and whole DNA relatedness concur for the reassignment of Pasteurella piscicida (Snieszko et al.) Janssen and Surgalla to the genus Photobacterium as Photobacterium damsela subsp. piscicida comb. nov","volume":"45","author":"Gauthier","year":"1995","journal-title":"Int. J. Syst. Bacteriol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"908","DOI":"10.1099\/00207713-47-3-908","article-title":"Taxonomic note: necessary correction of specific epithets formed as substantives (nouns) \u2018in apposition\u2019","volume":"47","year":"1997","journal-title":"Int. J. Syst. Bacteriol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/0959-8030(93)90028-A","article-title":"Pathogenesis of Gram-negative bacterial infections in warmwater fish","volume":"3","author":"Thune","year":"1993","journal-title":"Annu. Rev. Fish Dis."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/S0959-8030(96)90005-8","article-title":"Phenotypic and pathobiological characteristics of Pasteurella piscicida","volume":"6","author":"Toranzo","year":"1996","journal-title":"Ann. Rev. Fish Dis."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1007\/s10123-002-0051-6","article-title":"Photobacterium damselae subsp. piscicida: an integrated view of a bacterial fish pathogen","volume":"5","author":"Romalde","year":"2002","journal-title":"Int. Microbiol."},{"key":"ref_8","first-page":"75","article-title":"Update on bacterial vaccines: Photobacterium damselae subsp. piscicida","volume":"121","author":"Mydtlyng","year":"2005","journal-title":"Progress in Fish Immunology"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1016\/0044-8486(87)90231-6","article-title":"Fish pasteurellosis of cultured striped bass (Morone saxatilis) in coastal Alabama","volume":"65","author":"Hawke","year":"1987","journal-title":"Aquaculture"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0044-8486(91)90284-E","article-title":"Pasteurellosis in cultured gilthead seabream (Sparus aurata): first report in Spain","volume":"99","author":"Toranzo","year":"1991","journal-title":"Aquaculture"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"2491","DOI":"10.1099\/00221287-138-12-2491","article-title":"Pathogenic activities of live cells and extracellular products of the fish pathogen Pasteurella piscicida","volume":"138","author":"Santos","year":"1992","journal-title":"J. Gen. Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/0959-8030(93)90029-B","article-title":"Major bacterial diseases affecting mariculture in Japan","volume":"3","author":"Kusuda","year":"1993","journal-title":"Annu. Rev. Fish Dis."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"177","DOI":"10.3354\/dao021177","article-title":"Sequential pathology of experimental pasteurellosis in gilthead seabream Sparus aurata. A light- and electron-microscopic study","volume":"21","author":"Noya","year":"1995","journal-title":"Dis. Aquat. Org."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1577\/1548-8667(1997)009<0026:FROFPF>2.3.CO;2","article-title":"First report of fish pasteurellosis from Malta","volume":"9","author":"Bakopoulos","year":"1997","journal-title":"J. Aquat. Anim. Health"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1111\/j.1365-2109.2004.01086.x","article-title":"Histopathological findings after sea bass (Dicentrarhus labrax L.) exposure to extracellular products of Photobacterium damselae subsp. piscicida produced in vivo","volume":"35","author":"Poulos","year":"2004","journal-title":"Aquaculture Res."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1046\/j.1365-2761.2003.00513.x","article-title":"The effect of in vivo growth on the cellular and extracellular components of the marine bacterial pathogen Photobacterium damsela subsp. piscicida","volume":"27","author":"Bakopoulos","year":"2004","journal-title":"J. Fish Dis."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/S1050-4648(02)00144-4","article-title":"Apoptosis of sea bass (Dicentrarchus labrax L.) neutrophils and macrophages induced by experimental infection with Photobacterium damselae subsp. piscicida","volume":"15","author":"Marques","year":"2003","journal-title":"Fish Shellfish Immunol."},{"key":"ref_18","unstructured":"Gudding, R., Lillehaug, A., Midtlyng, P.J., and Brown, F. (1997). Fish Vaccinology, Karger."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1025","DOI":"10.1111\/j.1365-2958.2005.04893.x","article-title":"AIP56, a novel plasmid-encoded virulence factor of Photobacterium damselae subsp. piscicida with apoptogenic activity against sea bass macrophages and neutrophils","volume":"58","author":"Silva","year":"2005","journal-title":"Mol. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1046\/j.1365-2761.1997.00299.x","article-title":"The effect of iron limitation growth conditions on the cell and extracellular components of the fish pathogen Pasteurella piscicida","volume":"20","author":"Bakopoulos","year":"1997","journal-title":"J. Fish Dis."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"303","DOI":"10.2323\/jgam.52.303","article-title":"Analysis of a gene (vch) encoding hemolysin isolated and sequenced from Vibrio campbellii","volume":"52","author":"Hedreyda","year":"2006","journal-title":"J. Gen. Appl. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1111\/j.1365-2583.2009.00950.x","article-title":"Characteristics of the genome of Arsenophonus nasoniae, son-killer bacterium of the wasp Nasonia","volume":"19 (Suppl 1)","author":"Darby","year":"2010","journal-title":"Insect. Mol. Biol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"9063","DOI":"10.1073\/pnas.0900194106","article-title":"Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors","volume":"106","author":"Degnan","year":"2009","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"832","DOI":"10.1038\/359832a0","article-title":"Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin","volume":"359","author":"Schiavo","year":"1992","journal-title":"Nature"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/S0041-0101(00)00163-X","article-title":"Tetanus and botulinum neurotoxins: turning bad guys into good by research","volume":"39","author":"Rossetto","year":"2001","journal-title":"Toxicon"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/protein\/10.1.1","article-title":"Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites","volume":"10","author":"Nielsen","year":"1997","journal-title":"Protein Eng."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"783","DOI":"10.1016\/j.jmb.2004.05.028","article-title":"Improved prediction of signal peptides: SignalP 3.0","volume":"340","author":"Bendtsen","year":"2004","journal-title":"J. Mol. Biol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1089","DOI":"10.1046\/j.1365-2958.1997.3101672.x","article-title":"Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution","volume":"23","author":"Hacker","year":"1997","journal-title":"Mol. Microbiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"988","DOI":"10.1111\/j.1462-5822.2006.00846.x","article-title":"Systemic macrophage and neutrophil destruction by secondary necrosis induced by a bacterial exotoxin in a Gram-negative septicaemia","volume":"9","author":"Silva","year":"2007","journal-title":"Cell. Microbiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1016\/S0074-7696(08)62312-8","article-title":"Cell death: the significance of apoptosis","volume":"68","author":"Wyllie","year":"1980","journal-title":"Int. Rev. Cytol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1006\/meth.1999.0825","article-title":"Assessment of apoptosis in xenobiotic-induced immunotoxicity","volume":"19","author":"Pallardy","year":"1999","journal-title":"Methods"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/S0022-1759(00)00233-7","article-title":"Flow cytometry of apoptotic cell death","volume":"243","author":"Vermes","year":"2000","journal-title":"J. Immunol. Methods"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1754","DOI":"10.1016\/j.molimm.2006.07.293","article-title":"First molecular cloning and characterisation of caspase-9 gene in fish and its involvement in a gram negative septicaemia","volume":"44","author":"Reis","year":"2007","journal-title":"Mol. Immunol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"774","DOI":"10.1016\/j.molimm.2006.04.028","article-title":"Molecular cloning and characterisation of sea bass (Dicentrarchus labrax L.) caspase-3 gene","volume":"44","author":"Reis","year":"2007","journal-title":"Mol. Immunol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1038\/bjc.1972.33","article-title":"Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics","volume":"26","author":"Kerr","year":"1972","journal-title":"Br. J. Cancer"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1016\/j.it.2006.03.005","article-title":"Apoptotic cell removal in development and tissue homeostasis","volume":"27","author":"Henson","year":"2006","journal-title":"Trends Immunol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"294","DOI":"10.1016\/j.gde.2007.05.009","article-title":"Pathways regulating apoptosis during patterning and development","volume":"17","author":"Domingos","year":"2007","journal-title":"Curr. Opin. Genet. Dev."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1038\/icb.1977.38","article-title":"Death of cells by apoptosis following attachment of specifically allergized lymphocytes in vitro","volume":"55","author":"Don","year":"1977","journal-title":"Aust. J. Exp. Biol. Med. Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1002\/path.1711260307","article-title":"Morphological aspects of glucocorticoid-induced cell death in human lymphoblastoid cells","volume":"126","author":"Robertson","year":"1978","journal-title":"J. Pathol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"5245","DOI":"10.1242\/dev.127.24.5245","article-title":"Mesenchymal cells engulf and clear apoptotic footplate cells in macrophageless PU.1 null mouse embryos","volume":"127","author":"Wood","year":"2000","journal-title":"Development"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1016\/S0960-9822(00)00598-4","article-title":"Differences between the clearance of apoptotic cells by professional and non-professional phagocytes","volume":"10","author":"Parnaik","year":"2000","journal-title":"Curr. Biol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1007\/s10495-008-0187-8","article-title":"Secondary necrosis in multicellular animals: an outcome of apoptosis with pathogenic implications","volume":"13","author":"Silva","year":"2008","journal-title":"Apoptosis"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"806","DOI":"10.1038\/364806a0","article-title":"Lethal effect of the anti-Fas antibody in mice","volume":"364","author":"Ogasawara","year":"1993","journal-title":"Nature"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"S5","DOI":"10.1164\/ajrccm.160.supplement_1.4","article-title":"Granulocyte apoptosis and its role in the resolution and control of lung inflammation","volume":"160","author":"Haslett","year":"1999","journal-title":"Am. J. Respir. Crit. Care Med."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1161","DOI":"10.1083\/jcb.200410057","article-title":"Persistence of apoptotic cells without autoimmune disease or inflammation in CD14-\/- mice","volume":"167","author":"Devitt","year":"2004","journal-title":"J. Cell Biol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"320","DOI":"10.1002\/jcp.10105","article-title":"Induction of neutrophil apoptosis and secondary necrosis during endotoxin-induced pulmonary inflammation in mice","volume":"191","author":"Medan","year":"2002","journal-title":"J. Cell Physiol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1164\/rccm.200207-698OC","article-title":"Alveolar macrophages have a protective antiinflammatory role during murine pneumococcal pneumonia","volume":"167","author":"Knapp","year":"2003","journal-title":"Am. J. Respir. Crit. Care Med."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1560","DOI":"10.1126\/science.1087621","article-title":"Phosphatidylserine receptor is required for clearance of apoptotic cells","volume":"302","author":"Li","year":"2003","journal-title":"Science"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1164\/rccm.200612-1804OC","article-title":"Impairment of apoptotic cell engulfment by pyocyanin, a toxic metabolite of Pseudomonas aeruginosa","volume":"177","author":"Bianchi","year":"2008","journal-title":"Am. J. Respir. Crit. Care Med."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1146\/annurev.micro.53.1.155","article-title":"The induction of apoptosis by bacterial pathogens","volume":"53","author":"Weinrauch","year":"1999","journal-title":"Annu. Rev. Microbiol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/S0378-1135(01)00467-9","article-title":"Leukotoxins of gram-negative bacteria","volume":"84","author":"Narayanan","year":"2002","journal-title":"Vet. Microbiol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1023\/B:APPT.0000031448.64969.fa","article-title":"Modulation of phagocyte apoptosis by bacterial pathogens","volume":"9","author":"DeLeo","year":"2004","journal-title":"Apoptosis"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1007\/s12026-008-8049-6","article-title":"Neutrophil apoptosis and the resolution of infection","volume":"43","author":"Kennedy","year":"2009","journal-title":"Immunol. Res."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1069","DOI":"10.1007\/s10495-006-0040-x","article-title":"Cytochemical and ultrastructural study of anoikis and secondary necrosis in enterocytes detached in vivo","volume":"12","author":"Silva","year":"2007","journal-title":"Apoptosis"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1083\/jcb.124.4.619","article-title":"Disruption of epithelial cell-matrix interactions induces apoptosis","volume":"124","author":"Frisch","year":"1994","journal-title":"J. Cell. Biol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1038\/sj.cdd.4400883","article-title":"Death receptor-induced apoptotic and necrotic cell death: differential role of caspases and mitochondria","volume":"8","author":"Denecker","year":"2001","journal-title":"Cell. Death Differ."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1016\/S0925-4439(00)00098-3","article-title":"Evaluation of oxidative stress during apoptosis and necrosis caused by carbon tetrachloride in rat liver","volume":"1535","author":"Sun","year":"2001","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1111","DOI":"10.1006\/bbrc.2001.4918","article-title":"In vivo and in vitro evidence for extracellular caspase activity released from apoptotic cells","volume":"283","author":"Hentze","year":"2001","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1196\/annals.1368.043","article-title":"Nucleosomal DNA fragments in autoimmune diseases","volume":"1075","author":"Holdenrieder","year":"2006","journal-title":"Ann. N.Y. Acad. Sci."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1172\/JCI112869","article-title":"Tissue injury in inflammation. Oxidants, proteinases, and cationic proteins","volume":"79","author":"Henson","year":"1987","journal-title":"J. Clin. Invest."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1056\/NEJM198902093200606","article-title":"Tissue destruction by neutrophils","volume":"320","author":"Weiss","year":"1989","journal-title":"N. Engl. J. Med."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0014-2999(02)02182-9","article-title":"The role of neutrophil elastase in acute lung injury","volume":"451","author":"Kawabata","year":"2002","journal-title":"Eur. J. Pharmacol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"1238","DOI":"10.1016\/j.biocel.2008.03.003","article-title":"Proteases and cystic fibrosis","volume":"40","author":"Voynow","year":"2008","journal-title":"Int. J. Biochem. Cell Biol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1189\/jlb.0809549","article-title":"When two is better than one: macrophages and neutrophils work in concert in innate immunity as complementary and cooperative partners of a myeloid phagocyte system","volume":"87","author":"Silva","year":"2010","journal-title":"J. Leukoc. Biol."},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Silva, M.T. (2010). Neutrophils and macrophages work in concert as inducers and effectors of adaptive immunity against extracellular and intracellular microbial pathogens. J. Leukoc. Biol.","DOI":"10.1189\/jlb.1109767"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/S1438-4221(00)80096-X","article-title":"Apoptosis as a common bacterial virulence strategy","volume":"290","author":"Monack","year":"2000","journal-title":"Int. J. Med. Microbiol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1038\/nature06247","article-title":"Manipulation of host-cell pathways by bacterial pathogens","volume":"449","author":"Bhavsar","year":"2007","journal-title":"Nature"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"735","DOI":"10.1038\/embor.2008.131","article-title":"The type VI secretion toolkit","volume":"9","author":"Cascales","year":"2008","journal-title":"EMBO Rep."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"5785","DOI":"10.1128\/IAI.71.10.5785-5793.2003","article-title":"The Pseudomonas aeruginosa autoinducer N-3-oxododecanoyl homoserine lactone accelerates apoptosis in macrophages and neutrophils","volume":"71","author":"Tateda","year":"2003","journal-title":"Infect. Immun."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"3643","DOI":"10.4049\/jimmunol.174.6.3643","article-title":"Pyocyanin production by Pseudomonas aeruginosa induces neutrophil apoptosis and impairs neutrophil-mediated host defenses in vivo","volume":"174","author":"Allen","year":"2005","journal-title":"J. Immunol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"7142","DOI":"10.1128\/IAI.73.11.7142-7150.2005","article-title":"Pathogenesis of Yersinia pestis infection in BALB\/c mice: effects on host macrophages and neutrophils","volume":"73","author":"Lukaszewski","year":"2005","journal-title":"Infect. Immun."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"4827","DOI":"10.1128\/IAI.00246-09","article-title":"Francisella tularensis induces extensive caspase-3 activation and apoptotic cell death in the tissues of infected mice","volume":"77","author":"Wickstrum","year":"2009","journal-title":"Infect. Immun."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1574-6968.2009.01791.x","article-title":"Programmed cell death and the pathogenesis of tissue injury induced by type A Francisella tularensis","volume":"301","author":"Parmely","year":"2009","journal-title":"FEMS Microbiol. Lett."}],"container-title":["Toxins"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6651\/2\/4\/905\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T22:02:14Z","timestamp":1760220134000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6651\/2\/4\/905"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2010,4,26]]},"references-count":73,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2010,4]]}},"alternative-id":["toxins2040905"],"URL":"https:\/\/doi.org\/10.3390\/toxins2040905","relation":{},"ISSN":["2072-6651"],"issn-type":[{"value":"2072-6651","type":"electronic"}],"subject":[],"published":{"date-parts":[[2010,4,26]]}}}