1887

Abstract

YadB and YadC are putative trimeric autotransporters present only in the plague bacterium and its evolutionary predecessor, . Previously, was found to promote invasion of epithelioid cells by grown at 37 °C. In this study, we found that also promotes uptake of 37 °C-grown by mouse monocyte/macrophage cells. We tested whether might be required for lethality of the systemic stage of plague in which the bacteria would be pre-adapted to mammalian body temperature before colonizing internal organs and found no requirement for early colonization or growth over 3 days. We tested the hypothesis that YadB and YadC function on ambient temperature-grown in the flea vector or soon after infection of the dermis in bubonic plague. We found that did not promote uptake by monocyte/macrophage cells if the bacteria were grown at 28 °C, nor was there a role of in colonization of fleas by grown at 21 °C. However, the presence of did promote recoverability of the bacteria from infected skin for 28 °C-grown . Furthermore, the gene for the proinflammatory chemokine CXCL1 was upregulated in expression if the infecting lacked but not if was present. Also, was not required for recoverability if the bacteria were grown at 37 °C. These findings imply that thermally induced virulence properties dominate over effects of during plague but that has a unique function early after transmission of to skin.

Funding
This study was supported by the:
  • PHS (NIAID) (Award R21 AI083861)
  • PHS (NIAID) (Award R01 AI48491)
  • University of Kentucky Faculty Research Support
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.073205-0
2014-02-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/2/396.html?itemId=/content/journal/micro/10.1099/mic.0.073205-0&mimeType=html&fmt=ahah

References

  1. Armstrong D. A., Major J. A., Chudyk A., Hamilton T. A. ( 2004). Neutrophil chemoattractant genes KC and MIP-2 are expressed in different cell populations at sites of surgical injury. J Leukoc Biol 75:641–648 [View Article][PubMed]
    [Google Scholar]
  2. Beesley E. D., Brubaker R. R., Janssen W. A., Surgalla M. J. ( 1967). Pesticins. 3. Expression of coagulase and mechanism of fibrinolysis. J Bacteriol 94:19–26 [View Article][PubMed]
    [Google Scholar]
  3. Chouikha I., Hinnebusch B. J. ( 2012). Yersinia–flea interactions and the evolution of the arthropod-borne transmission route of plague. Curr Opin Microbiol 15:239–246 [View Article][PubMed]
    [Google Scholar]
  4. Chromy B. A., Choi M. W., Murphy G. A., Gonzales A. D., Corzett C. H., Chang B. C., Fitch J. P., McCutchen-Maloney S. L. ( 2005). Proteomic characterization of Yersinia pestis virulence. J Bacteriol 187:8172–8180 [View Article][PubMed]
    [Google Scholar]
  5. Cowan C., Jones H. A., Kaya Y. H., Perry R. D., Straley S. C. ( 2000). Invasion of epithelial cells by Yersinia pestis: evidence for a Y. pestis-specific invasin. Infect Immun 68:4523–4530 [View Article][PubMed]
    [Google Scholar]
  6. Du Y., Rosqvist R., Forsberg A. ( 2002). Role of fraction 1 antigen of Yersinia pestis in inhibition of phagocytosis. Infect Immun 70:1453–1460 [View Article][PubMed]
    [Google Scholar]
  7. Felek S., Tsang T. M., Krukonis E. S. ( 2010). Three Yersinia pestis adhesins facilitate Yop delivery to eukaryotic cells and contribute to plague virulence. Infect Immun 78:4134–4150 [View Article][PubMed]
    [Google Scholar]
  8. Forman S. F., Wulff C. R., Myers-Morales T., Cowan C., Perry R. D., Straley S. C. ( 2008). yadBC of Yersinia pestis, a new virulence determinant for bubonic plague. Infect Immun 76:578–587 [View Article][PubMed]
    [Google Scholar]
  9. Han Y., Zhou D., Pang X., Song Y., Zhang L., Bao J., Tong Z., Wang J., Guo Z. & other authors ( 2004). Microarray analysis of temperature-induced transcriptome of Yersinia pestis. Microbiol Immunol 48:791–805 [View Article][PubMed]
    [Google Scholar]
  10. Hinnebusch B. J. ( 2005). The evolution of flea-borne transmission in Yersinia pestis. Curr Issues Mol Biol 7:197–212[PubMed]
    [Google Scholar]
  11. Hinnebusch B. J., Perry R. D., Schwan T. G. ( 1996). Role of the Yersinia pestis hemin storage (hms) locus in the transmission of plague by fleas. Science 273:367–370 [View Article][PubMed]
    [Google Scholar]
  12. Hinnebusch B. J., Rosso M.-L., Schwan T. G., Carniel E. ( 2002). High-frequency conjugative transfer of antibiotic resistance genes to Yersinia pestis in the flea midgut. Mol Microbiol 46:349–354 [View Article][PubMed]
    [Google Scholar]
  13. Hu P., Elliott J., McCready P., Skowronski E., Garnes J., Kobayashi A., Brubaker R. R., Garcia E. ( 1998). Structural organization of virulence-associated plasmids of Yersinia pestis. J Bacteriol 180:5192–5202[PubMed]
    [Google Scholar]
  14. Kukkonen M., Lähteenmäki K., Suomalainen M., Kalkkinen N., Emödy L., Lång H., Korhonen T. K. ( 2001). Protein regions important for plasminogen activation and inactivation of α2-antiplasmin in the surface protease Pla of Yersinia pestis. Mol Microbiol 40:1097–1111 [View Article][PubMed]
    [Google Scholar]
  15. Leo J. C., Grin I., Linke D. ( 2012). Type V secretion: mechanism(s) of autotransport through the bacterial outer membrane. Philos Trans R Soc Lond B Biol Sci 367:1088–1101 [View Article][PubMed]
    [Google Scholar]
  16. Lukaszewski R. A., Kenny D. J., Taylor R., Rees D. G., Hartley M. G., Oyston P. C. ( 2005). Pathogenesis of Yersinia pestis infection in BALB/c mice: effects on host macrophages and neutrophils. Infect Immun 73:7142–7150 [View Article][PubMed]
    [Google Scholar]
  17. Marketon M. M., DePaolo R. W., DeBord K. L., Jabri B., Schneewind O. ( 2005). Plague bacteria target immune cells during infection. Science 309:1739–1741 [View Article][PubMed]
    [Google Scholar]
  18. McDonough K. A., Falkow S. ( 1989). A Yersinia pestis-specific DNA fragment encodes temperature-dependent coagulase and fibrinolysin-associated phenotypes. Mol Microbiol 3:767–775 [View Article][PubMed]
    [Google Scholar]
  19. Miller J. H. ( 1972). Appendix I. Formulas and recipes. Experiments in Molecular Genetics Plainview, NY: Cold Spring Harbor Laboratory Press;433
    [Google Scholar]
  20. Montminy S. W., Khan N., McGrath S., Walkowicz M. J., Sharp F., Conlon J. E., Fukase K., Kusumoto S., Sweet C. & other authors ( 2006). Virulence factors of Yersinia pestis are overcome by a strong lipopolysaccharide response. Nat Immunol 7:1066–1073 [View Article][PubMed]
    [Google Scholar]
  21. Motin V. L., Georgescu A. M., Fitch J. P., Gu P. P., Nelson D. O., Mabery S. L., Garnham J. B., Sokhansanj B. A., Ott L. L. & other authors ( 2004). Temporal global changes in gene expression during temperature transition in Yersinia pestis. J Bacteriol 186:6298–6305 [View Article][PubMed]
    [Google Scholar]
  22. Parkhill J. M., Wren B. W., Thomson N. R., Titball R. W., Holden M. T., Prentice M. B., Sebaihia M., James K. D., Churcher C. & other authors ( 2001). Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413:523–527 [View Article][PubMed]
    [Google Scholar]
  23. Perry R. D., Fetherston J. D. ( 1997). Yersinia pestis–etiologic agent of plague. Clin Microbiol Rev 10:35–66[PubMed]
    [Google Scholar]
  24. Pujol C., Bliska J. B. ( 2005). Turning Yersinia pathogenesis outside in: subversion of macrophage function by intracellular yersiniae. Clin Immunol 114:216–226 [View Article][PubMed]
    [Google Scholar]
  25. Sebbane F., Lemaître N., Sturdevant D. E., Rebeil R., Virtaneva K., Porcella S. F., Hinnebusch B. J. ( 2006). Adaptive response of Yersinia pestis to extracellular effectors of innate immunity during bubonic plague. Proc Natl Acad Sci U S A 103:11766–11771 [View Article][PubMed]
    [Google Scholar]
  26. Sodeinde O. A., Subrahmanyam Y. V., Stark K., Quan T., Bao Y., Goguen J. D. ( 1992). A surface protease and the invasive character of plague. Science 258:1004–1007 [View Article][PubMed]
    [Google Scholar]
  27. Straley S. C., Bowmer W. S. ( 1986). Virulence genes regulated at the transcriptional level by Ca2+ in Yersinia pestis include structural genes for outer membrane proteins. Infect Immun 51:445–454[PubMed]
    [Google Scholar]
  28. Sun W., Olinzock J., Wang S., Sanapala S., Curtiss R. III ( 2013). Evaluation of YadC protein delivered by live attenuated Salmonella as a vaccine against plague. Pathog Dis 69:1–13[PubMed]
    [Google Scholar]
  29. Suomalainen M., Lobo L. A., Brandenburg K., Lindner B., Virkola R., Knirel Y. A., Anisimov A. P., Holst O., Korhonen T. K. ( 2010). Temperature-induced changes in the lipopolysaccharide of Yersinia pestis affect plasminogen activation by the pla surface protease. Infect Immun 78:2644–2652 [View Article][PubMed]
    [Google Scholar]
  30. Surgalla M. J., Beesley E. D. ( 1969). Congo red-agar plating medium for detecting pigmentation in Pasteurella pestis. Appl Microbiol 18:834–837[PubMed]
    [Google Scholar]
  31. Tateda K., Moore T. A., Newstead M. W., Tsai W. C., Zeng X., Deng J. C., Chen G., Reddy R., Yamaguchi K., Standiford T. J. ( 2001). Chemokine-dependent neutrophil recruitment in a murine model of Legionella pneumonia: potential role of neutrophils as immunoregulatory cells. Infect Immun 69:2017–2024 [View Article][PubMed]
    [Google Scholar]
  32. Tsai W. C., Strieter R. M., Mehrad B., Newstead M. W., Zeng X., Standiford T. J. ( 2000). CXC chemokine receptor CXCR2 is essential for protective innate host response in murine Pseudomonas aeruginosa pneumonia. Infect Immun 68:4289–4296 [View Article][PubMed]
    [Google Scholar]
  33. Vadyvaloo V., Jarrett C., Sturdevant D. E., Sebbane F., Hinnebusch B. J. ( 2010). Transit through the flea vector induces a pretransmission innate immunity resistance phenotype in Yersinia pestis. PLoS Pathog 6:e1000783 [View Article][PubMed]
    [Google Scholar]
  34. Viboud G. I., Bliska J. B. ( 2005). Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu Rev Microbiol 59:69–89 [View Article][PubMed]
    [Google Scholar]
  35. Ye Z., Kerschen E. J., Cohen D. A., Kaplan A. M., van Rooijen N., Straley S. C. ( 2009). Gr1+ cells control growth of YopM-negative Yersinia pestis during systemic plague. Infect Immun 79:3791–3806 [View Article][PubMed]
    [Google Scholar]
  36. Ye Z., Uittenbogaard A. M., Cohen D. A., Kaplan A. M., Ambati J., Straley S. C. ( 2011). Distinct CCR2+ Gr1+ cells control growth of the Yersinia pestis ΔyopM mutant in liver and spleen during systemic plague. Infect Immun 79:674–687 [View Article][PubMed]
    [Google Scholar]
  37. Zhang S.-S., Park C. G., Zhang P., Bartra S. S., Plano G. V., Klena J. D., Skurnik M., Hinnebusch B. J., Chen T. ( 2008). Plasminogen activator Pla of Yersinia pestis utilizes murine DEC-205 (CD205) as a receptor to promote dissemination. J Biol Chem 283:31511–31521 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.073205-0
Loading
/content/journal/micro/10.1099/mic.0.073205-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error