{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T06:41:29Z","timestamp":1792737689999,"version":"4.5.0"},"reference-count":100,"publisher":"American Society for Microbiology","issue":"1","license":[{"start":{"date-parts":[[2004,1,1]],"date-time":"2004-01-01T00:00:00Z","timestamp":1072915200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.asm.org\/non-commercial-tdm-license"}],"content-domain":{"domain":["journals.asm.org"],"crossmark-restriction":true},"short-container-title":["Infect Immun"],"published-print":{"date-parts":[[2004,1]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n          <jats:p>\n            <jats:italic>Legionella pneumophila<\/jats:italic>\n            , the gram-negative agent of Legionnaires' disease, possesses type IV pili and a type II protein secretion (Lsp) system, both of which are dependent upon the PilD prepilin peptidase. By analyzing multiple\n            <jats:italic>pilD<\/jats:italic>\n            mutants and various types of Lsp mutants as well as performing\n            <jats:italic>trans<\/jats:italic>\n            -complementation of these mutants, we have confirmed that PilD and type II secretion genes are required for\n            <jats:italic>L. pneumophila<\/jats:italic>\n            infection of both amoebae and human macrophages. Based upon a complete analysis of\n            <jats:italic>lspDE<\/jats:italic>\n            ,\n            <jats:italic>lspF<\/jats:italic>\n            , and\n            <jats:italic>lspG<\/jats:italic>\n            mutants, we found that the type II system controls the secretion of protease, RNase, lipase, phospholipase A, phospholipase C, lysophospholipase A, and tartrate-sensitive and tartrate-resistant acid phosphatase activities and influences the appearance of colonies. Examination of the developing\n            <jats:italic>L. pneumophila<\/jats:italic>\n            genome database indicated that the organism has two other loci (\n            <jats:italic>lspC<\/jats:italic>\n            and\n            <jats:italic>lspLM<\/jats:italic>\n            ) that are predicted to promote secretion and thus a set of genes that is comparable to the type II secretion genes in other gram-negative bacteria. In contrast to\n            <jats:italic>lsp<\/jats:italic>\n            mutants,\n            <jats:italic>L. pneumophila<\/jats:italic>\n            pilus mutants lacking either the PilQ secretin, the PspA pseudopilin, or pilin were not defective for colonial growth, secreted activities, or intracellular replication.\n            <jats:italic>L. pneumophila dot\/icm<\/jats:italic>\n            mutants were also not impaired for type II-dependent exoenzymes. Upon intratracheal inoculation into A\/J mice,\n            <jats:italic>lspDE<\/jats:italic>\n            ,\n            <jats:italic>lspF<\/jats:italic>\n            , and\n            <jats:italic>pilD<\/jats:italic>\n            mutants, but not pilus mutants, exhibited a reduced ability to grow in the lung, as measured by competition assays. The\n            <jats:italic>lspF<\/jats:italic>\n            mutant was also defective in an in vivo kinetic assay. Examination of infected mouse sera revealed that type II secreted proteins are expressed in vivo. Thus, the\n            <jats:italic>L. pneumophila<\/jats:italic>\n            Lsp system is a virulence factor and the only type II secretion system linked to intracellular infection.\n          <\/jats:p>","DOI":"10.1128\/iai.72.1.310-321.2004","type":"journal-article","created":{"date-parts":[[2003,12,20]],"date-time":"2003-12-20T02:48:22Z","timestamp":1071888502000},"page":"310-321","update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":146,"title":["<i>Legionella pneumophila<\/i>\n            Type II Protein Secretion Promotes Virulence in the A\/J Mouse Model of Legionnaires' Disease Pneumonia"],"prefix":"10.1128","volume":"72","author":[{"given":"Ombeline","family":"Rossier","sequence":"first","affiliation":[{"name":"Department of Microbiology and Immunology, Northwestern University Medical School, Chicago, Illinois 60611"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shawn R.","family":"Starkenburg","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, Northwestern University Medical School, Chicago, Illinois 60611"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicholas P.","family":"Cianciotto","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, Northwestern University Medical School, Chicago, Illinois 60611"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"235","reference":[{"key":"e_1_3_2_2_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.68.11.6431-6440.2000"},{"key":"e_1_3_2_3_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0022-2836(05)80360-2"},{"key":"e_1_3_2_4_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.69.1.177-185.2001"},{"key":"e_1_3_2_5_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.68.4.1855-1863.2000"},{"key":"e_1_3_2_6_2","doi-asserted-by":"publisher","DOI":"10.1099\/00221287-148-7-2223"},{"key":"e_1_3_2_7_2","unstructured":"Ausubel F. M. R. Brent R. E. Kingston D. D. Moore J. G. Seidman J. A. Smith and K. Struhl (ed.). 1989. Current protocols in molecular biology. Wiley New York N.Y."},{"key":"e_1_3_2_8_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.2002.02759.x"},{"key":"e_1_3_2_9_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2958.1992.tb01550.x"},{"key":"e_1_3_2_10_2","doi-asserted-by":"publisher","DOI":"10.1128\/jcm.26.2.382-.1988"},{"key":"e_1_3_2_11_2","doi-asserted-by":"publisher","DOI":"10.1128\/jcm.17.2.346-348.1983"},{"key":"e_1_3_2_12_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.280.5372.2114"},{"key":"e_1_3_2_13_2","doi-asserted-by":"publisher","DOI":"10.1128\/jcm.17.5.887-891.1983"},{"key":"e_1_3_2_14_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.1998.00653.x"},{"key":"e_1_3_2_15_2","doi-asserted-by":"publisher","DOI":"10.1099\/00207713-35-1-50"},{"key":"e_1_3_2_16_2","doi-asserted-by":"publisher","DOI":"10.7326\/0003-4819-90-4-656"},{"key":"e_1_3_2_17_2","first-page":"1537","volume":"145","year":"1994","unstructured":"Brieland, J., P. Freeman, R. Kunkel, C. Chrisp, M. Hurley, J. Fantone, and C. Engleberg. 1994. Replicative Legionella pneumophila lung infection in intratracheally inoculated A\/J mice. A murine model of human Legionnaires' disease. Am. J. Pathol.145:1537-1546.","journal-title":"Am. J. Pathol."},{"key":"e_1_3_2_18_2","doi-asserted-by":"publisher","DOI":"10.1128\/iai.64.7.2449-2456.1996"},{"key":"e_1_3_2_19_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.89.11.5188"},{"key":"e_1_3_2_20_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.67.9.4427-4434.1999"},{"key":"e_1_3_2_21_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.69.1.508-517.2001"},{"key":"e_1_3_2_22_2","first-page":"143","volume":"134","year":"1988","unstructured":"Conlan, J. W., A. Williams, and L. A. Ashworth. 1988. In vivo production of a tissue-destructive protease by Legionella pneumophila in the lungs of experimentally infected guinea-pigs. J. Gen. Microbiol.134:143-149.","journal-title":"J. Gen. Microbiol."},{"key":"e_1_3_2_23_2","doi-asserted-by":"publisher","DOI":"10.1128\/jcm.14.3.298-303.1981"},{"key":"e_1_3_2_24_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.96.14.8190"},{"key":"e_1_3_2_25_2","doi-asserted-by":"publisher","DOI":"10.1128\/iai.57.4.1263-1270.1989"},{"key":"e_1_3_2_26_2","doi-asserted-by":"publisher","DOI":"10.1128\/iai.44.2.222-227.1984"},{"key":"e_1_3_2_27_2","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/30.1.235"},{"key":"e_1_3_2_28_2","doi-asserted-by":"publisher","DOI":"10.1016\/0966-842X(96)10041-X"},{"key":"e_1_3_2_29_2","doi-asserted-by":"publisher","DOI":"10.1128\/CMR.15.3.506-526.2002"},{"key":"e_1_3_2_30_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.182.5.1321-1327.2000"},{"key":"e_1_3_2_31_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.70.11.6094-6106.2002"},{"key":"e_1_3_2_32_2","doi-asserted-by":"publisher","DOI":"10.1006\/mpat.1996.0092"},{"key":"e_1_3_2_33_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.68.2.745-755.2002"},{"key":"e_1_3_2_34_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0378-1119(97)00038-3"},{"key":"e_1_3_2_35_2","doi-asserted-by":"publisher","DOI":"10.1128\/iai.65.11.4738-4746.1997"},{"key":"e_1_3_2_36_2","doi-asserted-by":"publisher","DOI":"10.1006\/mpat.1998.0237"},{"key":"e_1_3_2_37_2","doi-asserted-by":"publisher","DOI":"10.1128\/jcm.15.4.646-653.1982"},{"key":"e_1_3_2_38_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.182.8.2184-2190.2000"},{"key":"e_1_3_2_39_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.77.12.7176"},{"key":"e_1_3_2_40_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.67.7.3662-3666.1999"},{"key":"e_1_3_2_41_2","doi-asserted-by":"publisher","DOI":"10.7326\/0003-4819-92-1-45"},{"key":"e_1_3_2_42_2","doi-asserted-by":"publisher","DOI":"10.1084\/jem.168.4.1487"},{"key":"e_1_3_2_43_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.175.20.6695-6703.1993"},{"key":"e_1_3_2_44_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1462-5822.2001.00093.x"},{"key":"e_1_3_2_45_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.2002.03187.x"},{"key":"e_1_3_2_46_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M002149200"},{"key":"e_1_3_2_47_2","doi-asserted-by":"publisher","DOI":"10.1016\/0378-1119(95)00139-W"},{"key":"e_1_3_2_48_2","doi-asserted-by":"publisher","DOI":"10.1128\/iai.57.3.732-738.1989"},{"key":"e_1_3_2_49_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.183.15.4451-4458.2001"},{"key":"e_1_3_2_50_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.2003.03546.x"},{"key":"e_1_3_2_51_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.68.5.2518-2524.2000"},{"key":"e_1_3_2_52_2","doi-asserted-by":"publisher","DOI":"10.1038\/227680a0"},{"key":"e_1_3_2_53_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.1999.01239.x"},{"key":"e_1_3_2_54_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.174.22.7385-7397.1992"},{"key":"e_1_3_2_55_2","doi-asserted-by":"publisher","DOI":"10.1128\/jcm.26.3.586-587.1988"},{"key":"e_1_3_2_56_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.1998.01031.x"},{"key":"e_1_3_2_57_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.68.7.3971-3982.2000"},{"key":"e_1_3_2_58_2","doi-asserted-by":"publisher","DOI":"10.7326\/0003-4819-94-6-739"},{"key":"e_1_3_2_59_2","doi-asserted-by":"publisher","DOI":"10.7326\/0003-4819-90-4-621"},{"key":"e_1_3_2_60_2","doi-asserted-by":"publisher","DOI":"10.1128\/jcm.12.3.395-401.1980"},{"key":"e_1_3_2_61_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.1999.01650.x"},{"key":"e_1_3_2_62_2","doi-asserted-by":"publisher","DOI":"10.1093\/infdis\/167.5.1138"},{"key":"e_1_3_2_63_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2958.1994.tb01057.x"},{"key":"e_1_3_2_64_2","doi-asserted-by":"publisher","DOI":"10.1016\/0378-1119(91)90007-X"},{"key":"e_1_3_2_65_2","doi-asserted-by":"publisher","DOI":"10.1128\/jcm.12.5.718-721.1980"},{"key":"e_1_3_2_66_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1067025"},{"key":"e_1_3_2_67_2","doi-asserted-by":"publisher","DOI":"10.1093\/emboj\/20.21.5962"},{"key":"e_1_3_2_68_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0962-8924(99)01634-7"},{"key":"e_1_3_2_69_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.88.8.3281"},{"key":"e_1_3_2_70_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.1996.431958.x"},{"key":"e_1_3_2_71_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.69.2.977-987.2001"},{"key":"e_1_3_2_72_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2958.1992.tb01525.x"},{"key":"e_1_3_2_73_2","doi-asserted-by":"publisher","DOI":"10.1128\/iai.57.9.2719-2725.1989"},{"key":"e_1_3_2_74_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.70.10.5659-5669.2002"},{"key":"e_1_3_2_75_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.69.7.4276-4286.2001"},{"key":"e_1_3_2_76_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.69.4.2092-2098.2001"},{"key":"e_1_3_2_77_2","doi-asserted-by":"publisher","DOI":"10.1006\/jmbi.1998.1791"},{"key":"e_1_3_2_78_2","unstructured":"Sambrook J. E. F. Fritsch and T. Maniatis (ed.). 1989. Molecular cloning: a laboratory manual 2nd ed. Cold Spring Harbor Laboratory Press Cold Spring Harbor N.Y."},{"key":"e_1_3_2_79_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.2001.02403.x"},{"key":"e_1_3_2_80_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.69.6.3523-3535.2001"},{"key":"e_1_3_2_81_2","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/20.1.41"},{"key":"e_1_3_2_82_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.183.16.4848-4859.2001"},{"key":"e_1_3_2_83_2","doi-asserted-by":"publisher","DOI":"10.1016\/0378-1119(95)00055-B"},{"key":"e_1_3_2_84_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.95.4.1669"},{"key":"e_1_3_2_85_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.66.4.1768-1775.1998"},{"key":"e_1_3_2_86_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.181.5.1395-1402.1999"},{"key":"e_1_3_2_87_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.173.3.1175-1180.1991"},{"key":"e_1_3_2_88_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.90.6.2404"},{"key":"e_1_3_2_89_2","doi-asserted-by":"publisher","DOI":"10.1084\/jem.192.9.1261"},{"key":"e_1_3_2_90_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.micro.54.1.567"},{"key":"e_1_3_2_91_2","doi-asserted-by":"publisher","DOI":"10.1128\/iai.58.8.2585-2592.1990"},{"key":"e_1_3_2_92_2","doi-asserted-by":"publisher","DOI":"10.1128\/iai.63.4.1278-1285.1995"},{"key":"e_1_3_2_93_2","doi-asserted-by":"publisher","DOI":"10.1128\/jcm.22.1.1-4.1985"},{"key":"e_1_3_2_94_2","doi-asserted-by":"publisher","DOI":"10.1128\/iai.33.2.632-635.1981"},{"key":"e_1_3_2_95_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.76.9.4350"},{"key":"e_1_3_2_96_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.183.1.55-62.2001"},{"key":"e_1_3_2_97_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.70.4.1842-1852.2002"},{"key":"e_1_3_2_98_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.279.5352.873"},{"key":"e_1_3_2_99_2","doi-asserted-by":"publisher","DOI":"10.1084\/jem.194.8.1081"},{"key":"e_1_3_2_100_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.66.9.4450-4460.1998"},{"key":"e_1_3_2_101_2","doi-asserted-by":"publisher","DOI":"10.1128\/CMR.1.1.60"}],"container-title":["Infection and Immunity"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/IAI.72.1.310-321.2004","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/IAI.72.1.310-321.2004","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,3,5]],"date-time":"2022-03-05T04:50:38Z","timestamp":1646455838000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.asm.org\/doi\/10.1128\/IAI.72.1.310-321.2004"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2004,1]]},"references-count":100,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2004,1]]}},"alternative-id":["10.1128\/IAI.72.1.310-321.2004"],"URL":"https:\/\/doi.org\/10.1128\/iai.72.1.310-321.2004","relation":{},"ISSN":["0019-9567","1098-5522"],"issn-type":[{"value":"0019-9567","type":"print"},{"value":"1098-5522","type":"electronic"}],"subject":[],"published":{"date-parts":[[2004,1]]},"assertion":[{"value":"2003-09-02","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2003-10-07","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2004-01-01","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}