Skip to main content

The Interactions Between Pathogens and Dendritic Cells: From Paralysis of Cells to Their Recruitment for Bacterial Colonization

  • Conference paper
  • First Online:
Book cover The Challenge of Highly Pathogenic Microorganisms

Abstract

The encounter between invading microorganisms and dendritic cells (DC) triggers a series of events which include uptake and degradation of the microorganism, induction of a cell maturation process, as well as enhancement of DC migration to the draining lymph nodes. Bacteria of the genera Yersinia and Francisella have developed different strategies to counteract these events as a measure to evade host defense.

We observed that interaction of the Yersinia enterocolitica with DC impairs their maturation into functional immune cells and triggers premature cell death. Y. pestis, has no effects on DC viability or maturation, yet impairs DC functions related to cytoskeleton rearrangement in a virulence plasmid dependent way. DC pulsed with Y. pestis fails to migrate toward the chemokine CCL19. Moreover, while instillation of a virulence plasmid-cured Y. pestis strain into mice airways triggers effective transport of airway DC to the mediastinal lymph node (MdLN), instillation of Y. pestis harboring the plasmid fails to do so.

Interaction of Francisella tularensis live vaccine strain (LVS) with DC leads to impairment of cell maturation but at the same time allows for intracellular bacterial propagation and effective cell migration, thus paving the way to utilization of DC as vehicles for bacterial dissemination. Indeed, airway infection of mice with LVS results in trafficking of bacteria-carrying DC from the respiratory tract to the draining MdLN. Furthermore, impairment of DC migration in vivo by two independent mechanisms reduces bacterial colonization of the lymph node and delays the onset of morbidity and the time to death of the infected mice.

Taken together, these observations attest to the major role of DC in mounting protection against pathogens, which has in turn led to evolution of various bacterial strategies to counteract and even exploit DC functions.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Bar-Haim, E., Gat, O., Markel, G., Cohen, H., Shafferman, A. & Velan, B. (2008) Interrelationship between Dendritic Cell Trafficking and Francisella tularensis Dissemination following Airway Infection. Plos Pathogens, 4, e1000211.

    Google Scholar 

  • Bhavsar, A. P., Guttman, J. A. & Finlay, B. B. (2007) Manipulation of host-cell pathways by bacterial pathogens. Nature, 449, 827–34.

    Article  PubMed  CAS  Google Scholar 

  • Bosio, C. M., Bielefeldt-Ohmann, H. & Belisle, J. T. (2007) Active suppression of the pulmonary immune response by Francisella tularensis Schu4. J Immun, 178, 4538–47.

    PubMed  CAS  Google Scholar 

  • Darling, R. G., Catlett, C. L., Huebner, K. D. & Jarrett, D. G. (2002) Threats in bioterrorism I: CDC category A agents. Emerg Med Clin North Am, 20, 273–309.

    Article  PubMed  Google Scholar 

  • Erfurth, S. E., Grobner, S., Kramer, U., Gunst, D. S. J., Soldanova, I., Schaller, M., Autenrieth, I. B. & Borgmann, S. (2004) Yersinia enterocolitica Induces Apoptosis and Inhibits Surface Molecule Expression and Cytokine Production in Murine Dendritic Cells. Infect Immun, 72, 7045–54.

    Article  PubMed  CAS  Google Scholar 

  • Finlay, B. B. & McFadden, G. (2006) Anti-immunology: evasion of the host immune system by bacterial and viral pathogens. Cell, 124, 767–82.

    Article  PubMed  CAS  Google Scholar 

  • Humphreys, I. R., Stewart, G. R., Turner, D. J., Patel, J., Karamanou, D., Snelgrove, R. J. & Young, D. B. (2006) A role for dendritic cells in the dissemination of mycobacterial infection. Microbes Infect, 8, 1339–46.

    Article  PubMed  CAS  Google Scholar 

  • Kikuchi, T., Kobayashi, T., Gomi, K., Suzuki, T., Tokue, Y., Watanabe, A. & Nukiwa, T. (2004) Dendritic cells pulsed with live and dead Legionella pneumophila elicit distinct immune responses. J Immun, 172, 1727–34.

    PubMed  CAS  Google Scholar 

  • Lai, X. H. & Sjostedt, A. (2003) Delineation of the molecular mechanisms of Francisella tularensis-induced apoptosis in murine macrophages. Infect Immun, 71, 4642–6.

    Article  PubMed  CAS  Google Scholar 

  • Marketon, M. M., Depaolo, R. W., Debord, K. L., Jabri, B. & Schneewind, O. (2005) Plague bacteria target immune cells during infection. Science, 309, 1739–41.

    Article  PubMed  CAS  Google Scholar 

  • Merrell, D. S. & Falkow, S. (2004) Frontal and stealth attack strategies in microbial pathogenesis. Nature, 430, 250–6.

    Article  PubMed  CAS  Google Scholar 

  • Niedergang, F., Didierlaurent, A., Kraehenbuhl, J. P. & Sirard, J. C. (2004) Dendritic cells: the host Achille’s heel for mucosal pathogens? Trends Microbiol, 12, 79–88.

    Article  PubMed  CAS  Google Scholar 

  • Nogueira, C. V., Lindsten, T., Jamieson, A. M., Case, C. L., Shin, S., Thompson, C. B. & Roy, C. R. (2009) Rapid Pathogen-Induced Apoptosis: A Mechanism Used by Dendritic Cells to Limit Intracellular Replication of Legionella pneumophila. PLoS Pathog, 5, e1000478.

    Google Scholar 

  • Pujol, U. & Bliska, J. B. (2005) Turning Yersinia pathogenesis outside in: subversion of macrophage function by intracellular yersiniae. Clin Immunol, 114, 216–26.

    Article  PubMed  CAS  Google Scholar 

  • Roy, C. R. & Mocarski, E. S. (2007) Pathogen subversion of cell-intrinsic innate immunity. Nat Immunol, 8, 1179–87.

    Article  CAS  Google Scholar 

  • Savina, A. & Amigorena, S. (2007) Phagocytosis and antigen presentation in dendritic cells. Immunol Rev, 219, 143–56.

    Article  PubMed  CAS  Google Scholar 

  • Sjostedt, A. (2007) Tularemia: History, epidemiology, pathogen physiology, and clinical manifestations. Ann NY Acad Sci, 1105, 1–29.

    Article  PubMed  Google Scholar 

  • Steinman, R. M. & Hemmi, H. (2006) Dendritic cells: translating innate to adaptive immunity. Curr Top Microbiol Immunol, 311, 17–58.

    Article  PubMed  CAS  Google Scholar 

  • Ueno, H., Klechevsky, E., Morita, R., Aspord, C., Cao, T., Matsui, T., Di Pucchio, T., Connolly, J., Fay, J. W., Pascual, V., Palucka, A. K. & Banchereau, J. (2007) Dendritic cell subsets in health and disease. Immunol Rev, 219, 118–42.

    Article  PubMed  CAS  Google Scholar 

  • Velan, B., Bar-Haim, E., Zauberman, A., Mamroud, E., Shafferman, A. & Cohen, S. (2006) Discordance in the effects of Yersinia pestis on the dendritic cell functions manifested by induction of maturation and paralysis of migration. Infect Immun, 74, 6365–76.

    Article  PubMed  CAS  Google Scholar 

  • Weiss, D. S., Brotcke, A., Henry, T., Margolis, J. J., Chan, K. & Monack, D. M. (2007) In vivo negative selection screen identifies genes required for Francisella virulence. Proc Nat Acad Sci USA, 104, 6037–42.

    Article  PubMed  CAS  Google Scholar 

  • Zauberman, A., Tidhar, A., Levy, Y., Bar-Haim, E., Halperin, G., Flashner, Y., Cohen, S., Shafferman, A. & Mamroud, E. (2009) Yersinia pestis Endowed with Increased Cytotoxicity Is Avirulent in a Bubonic Plague Model and Induces Rapid Protection against Pneumonic Plague. PLoS ONE, 4, e5938.

    Article  PubMed  Google Scholar 

  • Zauberman, A., Velan, B., Mamroud, E., Flashner, Y., Shafferman, A. & Cohen, S. (2007) Disparity between Yersinia pestis and Yersinia enterocolitica O : 8 in YopJ/YopP-dependent functions. Genus Yersinia: Genomics Funct, 603, 312–20.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Baruch Velan .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media B.V.

About this paper

Cite this paper

Velan, B. et al. (2010). The Interactions Between Pathogens and Dendritic Cells: From Paralysis of Cells to Their Recruitment for Bacterial Colonization. In: Shafferman, A., Ordentlich, A., Velan, B. (eds) The Challenge of Highly Pathogenic Microorganisms. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9054-6_9

Download citation

Publish with us

Policies and ethics