{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T15:01:37Z","timestamp":1791298897361,"version":"4.1.0"},"reference-count":32,"publisher":"Springer Science and Business Media LLC","issue":"1","content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Microbiol"],"published-print":{"date-parts":[[2012,12]]},"abstract":"<jats:title>Abstract<\/jats:title>\n          <jats:sec>\n            <jats:title>Background<\/jats:title>\n            <jats:p>Plague is caused by <jats:italic>Yersinia pestis<\/jats:italic>, a bacterium that disseminates inside of the host at remarkably high rates. Plague bacilli disrupt normal immune responses in the host allowing for systematic spread that is fatal if left untreated. How <jats:italic>Y. pestis<\/jats:italic> disseminates from the site of infection to deeper tissues is unknown. Dissemination studies for plague are typically performed in mice by determining the bacterial burden in specific organs at various time points. To follow bacterial dissemination during plague infections in mice we tested the possibility of using bioluminescence imaging (BLI), an alternative non-invasive approach. Fully virulent <jats:italic>Y. pestis<\/jats:italic> was transformed with a plasmid containing the <jats:italic>luxCDABE<\/jats:italic> genes, making it able to produce light; this <jats:italic>lux<\/jats:italic>-expressing strain was used to infect mice by subcutaneous, intradermal or intranasal inoculation.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Results<\/jats:title>\n            <jats:p>We successfully obtained images from infected animals and were able to follow bacterial dissemination over time for each of the three different routes of inoculation. We also compared the radiance signal from animals infected with a wild type strain and a \u0394<jats:italic>caf1<\/jats:italic> \u0394<jats:italic>psaA<\/jats:italic> mutant that we previously showed to be attenuated in colonization of the lymph node and systemic dissemination. Radiance signals from mice infected with the wild type strain were larger than values obtained from mice infected with the mutant strain (linear regression of normalized values, P\u2009&lt;\u20090.05).<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Conclusions<\/jats:title>\n            <jats:p>We demonstrate that BLI is useful for monitoring dissemination from multiple inoculation sites, and for characterization of mutants with defects in colonization or dissemination.<\/jats:p>\n          <\/jats:sec>","DOI":"10.1186\/1471-2180-12-147","type":"journal-article","created":{"date-parts":[[2012,7,24]],"date-time":"2012-07-24T10:29:12Z","timestamp":1343125752000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":35,"title":["Bioluminescence imaging to track bacterial dissemination of Yersinia pestis using different routes of infection in mice"],"prefix":"10.1186","volume":"12","author":[{"given":"Rodrigo J","family":"Gonzalez","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eric H","family":"Weening","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Richard","family":"Frothingham","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gregory D","family":"Sempowski","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Virginia L","family":"Miller","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2012,7,24]]},"reference":[{"issue":"2","key":"1670_CR1","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1078\/1438-4639-00259","volume":"207","author":"BP Zietz","year":"2004","unstructured":"Zietz BP, Dunkelberg H: The history of the plague and the research on the causative agent Yersinia pestis. Int J Hyg Envir Heal. 2004, 207 (2): 165-178. 10.1078\/1438-4639-00259.","journal-title":"Int J Hyg Envir Heal"},{"issue":"6","key":"1670_CR2","doi-asserted-by":"publisher","first-page":"2242","DOI":"10.1128\/IAI.01477-08","volume":"77","author":"D Zhou","year":"2009","unstructured":"Zhou D, Yang R: Molecular Darwinian evolution of virulence in Yersinia pestis. Infect Immun. 2009, 77 (6): 2242-2250. 10.1128\/IAI.01477-08.","journal-title":"Infect Immun"},{"issue":"1","key":"1670_CR3","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1128\/CMR.10.1.35","volume":"10","author":"RD Perry","year":"1997","unstructured":"Perry RD, Fetherston JD: Yersinia pestis\u2013etiologic agent of plague. Clin Microbiol Rev. 1997, 10 (1): 35-66.","journal-title":"Clin Microbiol Rev"},{"issue":"Pt 11","key":"1670_CR4","doi-asserted-by":"publisher","first-page":"1461","DOI":"10.1099\/jmm.0.46697-0","volume":"55","author":"AP Anisimov","year":"2006","unstructured":"Anisimov AP, Amoako KK: Treatment of plague: promising alternatives to antibiotics. J Med Microbiol. 2006, 55 (Pt 11): 1461-1475.","journal-title":"J Med Microbiol"},{"key":"1670_CR5","doi-asserted-by":"publisher","first-page":"505","DOI":"10.1146\/annurev.ento.50.071803.130337","volume":"50","author":"KL Gage","year":"2005","unstructured":"Gage KL, Kosoy MY: Natural history of plague: perspectives from more than a century of research. Annu Rev Entomol. 2005, 50: 505-528. 10.1146\/annurev.ento.50.071803.130337.","journal-title":"Annu Rev Entomol"},{"issue":"1","key":"1670_CR6","doi-asserted-by":"publisher","first-page":"e3","DOI":"10.1371\/journal.pmed.0050003","volume":"5","author":"NC Stenseth","year":"2008","unstructured":"Stenseth NC, Atshabar BB, Begon M, Belmain SR, Bertherat E, Carniel E, Gage KL, Leirs H, Rahalison L: Plague: past, present, and future. PLoS Med. 2008, 5 (1): e3-10.1371\/journal.pmed.0050003.","journal-title":"PLoS Med"},{"issue":"8","key":"1670_CR7","doi-asserted-by":"publisher","first-page":"e667","DOI":"10.1016\/j.ijid.2009.11.011","volume":"14","author":"I Bitam","year":"2010","unstructured":"Bitam I, Dittmar K, Parola P, Whiting MF, Raoult D: Fleas and flea-borne diseases. Int J Infect Dis. 2010, 14 (8): e667-e676. 10.1016\/j.ijid.2009.11.011.","journal-title":"Int J Infect Dis"},{"issue":"10","key":"1670_CR8","doi-asserted-by":"publisher","first-page":"3233","DOI":"10.1128\/AAC.00306-06","volume":"50","author":"M Galimand","year":"2006","unstructured":"Galimand M, Carniel E, Courvalin P: Resistance of Yersinia pestis to antimicrobial agents. Antimicrob Agents Chemother. 2006, 50 (10): 3233-3236. 10.1128\/AAC.00306-06.","journal-title":"Antimicrob Agents Chemother"},{"key":"1670_CR9","doi-asserted-by":"publisher","first-page":"256","DOI":"10.1111\/j.1600-065X.2008.00674.x","volume":"225","author":"ST Smiley","year":"2008","unstructured":"Smiley ST: Immune defense against pneumonic plague. Immunol Rev. 2008, 225: 256-271. 10.1111\/j.1600-065X.2008.00674.x.","journal-title":"Immunol Rev"},{"issue":"9568","key":"1670_CR10","doi-asserted-by":"publisher","first-page":"1196","DOI":"10.1016\/S0140-6736(07)60566-2","volume":"369","author":"MB Prentice","year":"2007","unstructured":"Prentice MB, Rahalison L: Plague. Lancet. 2007, 369 (9568): 1196-1207. 10.1016\/S0140-6736(07)60566-2.","journal-title":"Lancet"},{"issue":"2","key":"1670_CR11","first-page":"85","volume":"46","author":"J Wimsatt","year":"2009","unstructured":"Wimsatt J, Biggins DE: A review of plague persistence with special emphasis on fleas. J Vec Born Dis. 2009, 46 (2): 85-99.","journal-title":"J Vec Born Dis"},{"issue":"5741","key":"1670_CR12","doi-asserted-by":"publisher","first-page":"1739","DOI":"10.1126\/science.1114580","volume":"309","author":"MM Marketon","year":"2005","unstructured":"Marketon MM, DePaolo RW, DeBord KL, Jabri B, Schneewind O: Plague bacteria target immune cells during infection. Science (New York, NY). 2005, 309 (5741): 1739-1741. 10.1126\/science.1114580.","journal-title":"Science (New York, NY)"},{"issue":"9","key":"1670_CR13","doi-asserted-by":"publisher","first-page":"927","DOI":"10.1038\/nm0905-927","volume":"11","author":"FR DeLeo","year":"2005","unstructured":"DeLeo FR, Hinnebusch BJ: A plague upon the phagocytes. Nat Med. 2005, 11 (9): 927-928. 10.1038\/nm0905-927.","journal-title":"Nat Med"},{"issue":"1","key":"1670_CR14","doi-asserted-by":"publisher","first-page":"94","DOI":"10.1016\/j.mib.2008.12.005","volume":"12","author":"H Matsumoto","year":"2009","unstructured":"Matsumoto H, Young GM: Translocated effectors of Yersinia. Curr Opin Microbiol. 2009, 12 (1): 94-100. 10.1016\/j.mib.2008.12.005.","journal-title":"Curr Opin Microbiol"},{"issue":"2","key":"1670_CR15","doi-asserted-by":"publisher","first-page":"e1688","DOI":"10.1371\/journal.pone.0001688","volume":"3","author":"F Guinet","year":"2008","unstructured":"Guinet F, Av\u00e9 P, Jones L, Huerre M, Carniel E: Defective innate cell response and lymph node infiltration specify Yersinia pestis infection. PLoS One. 2008, 3 (2): e1688-10.1371\/journal.pone.0001688.","journal-title":"PLoS One"},{"issue":"5","key":"1670_CR16","doi-asserted-by":"publisher","first-page":"1427","DOI":"10.1016\/S0002-9440(10)62360-7","volume":"166","author":"F Sebbane","year":"2005","unstructured":"Sebbane F, Gardner D, Long D, Gowen BB, Hinnebusch BJ: Kinetics of disease progression and host response in a rat model of bubonic plague. Am J Pathol. 2005, 166 (5): 1427-1439. 10.1016\/S0002-9440(10)62360-7.","journal-title":"Am J Pathol"},{"issue":"5","key":"1670_CR17","doi-asserted-by":"publisher","first-page":"545","DOI":"10.1101\/gad.1047403","volume":"17","author":"TF Massoud","year":"2003","unstructured":"Massoud TF, Gambhir SS: Molecular imaging in living subjects: seeing fundamental biological processes in a new light. Genes Dev. 2003, 17 (5): 545-580. 10.1101\/gad.1047403.","journal-title":"Genes Dev"},{"key":"1670_CR18","doi-asserted-by":"publisher","first-page":"S15","DOI":"10.1016\/S1472-9792(09)70006-X","volume":"89","author":"Y Kong","year":"2009","unstructured":"Kong Y, Subbian S, Cirillo SLG, Cirillo JD: Application of optical imaging to study of extrapulmonary spread by tuberculosis. Tuberculosis (Edinb). 2009, 89: S15-S17.","journal-title":"Tuberculosis (Edinb)"},{"issue":"6","key":"1670_CR19","doi-asserted-by":"publisher","first-page":"1073","DOI":"10.1038\/mt.2008.76","volume":"16","author":"C Zincarelli","year":"2008","unstructured":"Zincarelli C, Soltys S, Rengo G, Rabinowitz JE: Analysis of AAV serotypes 1\u20139 mediated gene expression and tropism in mice after systemic injection. Mol Ther. 2008, 16 (6): 1073-1080. 10.1038\/mt.2008.76.","journal-title":"Mol Ther"},{"issue":"12","key":"1670_CR20","doi-asserted-by":"publisher","first-page":"1391","DOI":"10.1016\/j.ijpara.2008.04.002","volume":"38","author":"KV Hyland","year":"2008","unstructured":"Hyland KV, Asfaw SH, Olson CL, Daniels MD, Engman DM: Bioluminescent imaging of Trypanosoma cruzi infection. Int J Parasitol. 2008, 38 (12): 1391-1400. 10.1016\/j.ijpara.2008.04.002.","journal-title":"Int J Parasitol"},{"issue":"10","key":"1670_CR21","doi-asserted-by":"publisher","first-page":"2315","DOI":"10.1111\/j.1462-5822.2007.00995.x","volume":"9","author":"M Hutchens","year":"2007","unstructured":"Hutchens M, Luker GD: Applications of bioluminescence imaging to the study of infectious diseases. Cell Microbiol. 2007, 9 (10): 2315-2322. 10.1111\/j.1462-5822.2007.00995.x.","journal-title":"Cell Microbiol"},{"key":"1670_CR22","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1146\/annurev.bioeng.4.111901.093336","volume":"4","author":"CH Contag","year":"2002","unstructured":"Contag CH, Bachmann MH: Advances in in vivo bioluminescence imaging of gene expression. Annu Rev Biomed Eng. 2002, 4: 235-260. 10.1146\/annurev.bioeng.4.111901.093336.","journal-title":"Annu Rev Biomed Eng"},{"issue":"1 Spec No","key":"1670_CR23","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1016\/0378-1119(95)00676-1","volume":"173","author":"JW Hastings","year":"1996","unstructured":"Hastings JW: Chemistries and colors of bioluminescent reactions: a review. Gene. 1996, 173 (1 Spec No): 5-11.","journal-title":"Gene"},{"issue":"42","key":"1670_CR24","doi-asserted-by":"publisher","first-page":"16669","DOI":"10.1073\/pnas.0607898104","volume":"104","author":"MC Lane","year":"2007","unstructured":"Lane MC, Alteri CJ, Smith SN, Mobley HLT: Expression of flagella is coincident with uropathogenic Escherichia coli ascension to the upper urinary tract. Proc Natl Acad Sci U S A. 2007, 104 (42): 16669-16674. 10.1073\/pnas.0607898104.","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"4","key":"1670_CR25","doi-asserted-by":"publisher","first-page":"e34714","DOI":"10.1371\/journal.pone.0034714","volume":"7","author":"T Nham","year":"2012","unstructured":"Nham T, Filali S, Danne C, Derbise A, Carniel E: Imaging of Bubonic Plague Dynamics by In Vivo Tracking of Bioluminescent Yersinia pestis. PLoS One. 2012, 7 (4): e34714-10.1371\/journal.pone.0034714.","journal-title":"PLoS One"},{"issue":"36","key":"1670_CR26","doi-asserted-by":"publisher","first-page":"13514","DOI":"10.1073\/pnas.0603456103","volume":"103","author":"JS Cathelyn","year":"2006","unstructured":"Cathelyn JS, Crosby SD, Lathem WW, Goldman WE, Miller VL: RovA, a global regulator of Yersinia pestis, specifically required for bubonic plague. Proc Natl Acad Sci U S A. 2006, 103 (36): 13514-13519. 10.1073\/pnas.0603456103.","journal-title":"Proc Natl Acad Sci U S A"},{"key":"1670_CR27","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1007\/0-306-48416-1_13","volume":"529","author":"F Guinet","year":"2003","unstructured":"Guinet F, Carniel E: A technique of intradermal injection of Yersinia to study Y. pestis physiopathology. Adv Exp Med Biol. 2003, 529: 73-78.","journal-title":"Adv Exp Med Biol"},{"issue":"1\u20132","key":"1670_CR28","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1016\/j.jim.2006.01.022","volume":"312","author":"W Van den Broeck","year":"2006","unstructured":"Van den Broeck W, Derore A, Simoens P: Anatomy and nomenclature of murine lymph nodes: Descriptive study and nomenclatory standardization in BALB\/cAnNCrl mice. J Immunol Methods. 2006, 312 (1\u20132): 12-19.","journal-title":"J Immunol Methods"},{"issue":"49","key":"1670_CR29","doi-asserted-by":"publisher","first-page":"17786","DOI":"10.1073\/pnas.0506840102","volume":"102","author":"WW Lathem","year":"2005","unstructured":"Lathem WW, Crosby SD, Miller VL, Goldman WE: Progression of primary pneumonic plague: a mouse model of infection, pathology, and bacterial transcriptional activity. Proc Natl Acad Sci U S A. 2005, 102 (49): 17786-17791. 10.1073\/pnas.0506840102.","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"2","key":"1670_CR30","doi-asserted-by":"publisher","first-page":"644","DOI":"10.1128\/IAI.00981-10","volume":"79","author":"EH Weening","year":"2011","unstructured":"Weening EH, Cathelyn JS, Kaufman G, Lawrenz MB, Price P, Goldman WE, Miller VL: The dependence of the Yersinia pestis capsule on pathogenesis is influenced by the mouse background. Infect Immun. 2011, 79 (2): 644-652. 10.1128\/IAI.00981-10.","journal-title":"Infect Immun"},{"issue":"8","key":"1670_CR31","doi-asserted-by":"publisher","first-page":"3083","DOI":"10.1073\/pnas.1112729109","volume":"109","author":"PA Price","year":"2012","unstructured":"Price PA, Jin J, Goldman WE: Pulmonary infection by Yersinia pestis rapidly establishes a permissive environment for microbial proliferation. Proc Natl Acad Sci U S A. 2012, 109 (8): 3083-3088. 10.1073\/pnas.1112729109.","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"8","key":"1670_CR32","doi-asserted-by":"publisher","first-page":"789","DOI":"10.1179\/136485905X65161","volume":"99","author":"A Arbaji","year":"2005","unstructured":"Arbaji A, Kharabsheh S, Al-Azab S, Al-Kayed M, Amr ZS, Abu Baker M, Chu MC: A 12-case outbreak of pharyngeal plague following the consumption of camel meat, in north-eastern Jordan. Ann Trop Med Parasitol. 2005, 99 (8): 789-793. 10.1179\/136485905X65161.","journal-title":"Ann Trop Med Parasitol"}],"container-title":["BMC Microbiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/1471-2180-12-147.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,9,1]],"date-time":"2021-09-01T19:35:37Z","timestamp":1630524937000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcmicrobiol.biomedcentral.com\/articles\/10.1186\/1471-2180-12-147"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2012,7,24]]},"references-count":32,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2012,12]]}},"alternative-id":["1670"],"URL":"https:\/\/doi.org\/10.1186\/1471-2180-12-147","relation":{},"ISSN":["1471-2180"],"issn-type":[{"value":"1471-2180","type":"electronic"}],"subject":[],"published":{"date-parts":[[2012,7,24]]},"assertion":[{"value":"11 May 2012","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"24 July 2012","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"24 July 2012","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}}],"article-number":"147"}}