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1 July 2006

Volume 194, Number 1
The Journal of Infectious Diseases 2006;194:86–94
© 2006 by the Infectious Diseases Society of America. All rights reserved.
0022-1899/2006/19401-0013$15.00
DOI: 10.1086/504686
MAJOR ARTICLE

Resident CD11c+ Lung Cells Are Impaired by Anthrax Toxins after Spore Infection

Aurélie Cleret,1

Anne Quesnel‐Hellmann,1

Jacques Mathieu,2

Dominique Vidal,1 and

Jean‐Nicolas Tournier1

1Unité d’Immunobiologie, Département de Biologie des Agents Transmissibles, and 2Unité de Radiobiologie et Inflammation, Département de Radiobiologie et de Radiopathologie, Centre de Recherche du Service de Santé des Armées, La Tronche, France

Bacillus anthracis secretes 2 toxins: lethal toxin (LT) and edema toxin (ET). We investigated their role in the physiopathologic mechanisms of inhalational anthrax by evaluating murine lung dendritic cell (LDC) functions after infection with B. anthracis strains secreting LT, ET, or both or with a nontoxinogenic strain. Three lung cell populations gated on CD11c/CD11b expression were obtained after lung digestion: (1) CD11chigh/CD11blow (alveolar macrophages), (2) CD11cintermediate (int)/CD11bint (LDCs), and (3) CD11clow/CD11bhigh (interstitial macrophages or monocytes). After infection with LT‐secreting strains, a decrease in costimulatory molecule expression on LDCs was observed. All CD11c+ cells infected with a nontoxinogenic strain secreted tumor necrosis factor (TNF)–α, interleukin (IL)–10, and IL‐6. LT‐secreting strains inhibited overall cytokine secretion, whereas the ET‐secreting strain inhibited only TNF‐α secretion and increased IL‐6 secretion. Similar results were obtained after preincubation with purified toxins. Our results suggest that anthrax toxins secreted during infection impair LDC function and suppress the innate immune response.

Received 18 November 2005; accepted 4 February 2006; electronically published 26 May 2006.

Reprints or correspondence: Dr. Jean‐Nicolas Tournier, Unité d’Immunobiologie, Département de Biologie des Agents Transmissibles, CRSSA, 24 ave. des maquis du Grésivaudan, 38702 La Tronche, France ().

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Shuchi Midha, Rakesh Bhatnagar. (2009) Anthrax protective antigen administered by DNA vaccination to distinct subcellular locations potentiates humoral and cellular immune responses. European Journal of Immunology 39:1, 159-177
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Ping-Jen (Joe) Chou, Catherine A. Newton, Izabella Perkins, Herman Friedman, Thomas W. Klein. (2009) Suppression of Dendritic Cell Activation by Anthrax Lethal Toxin and Edema Toxin Depends on Multiple Factors Including Cell Source, Stimulus Used, and Function Tested. DNA and Cell Biology 27:12, 637-648
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Núria Reig, Aimin Jiang, Rachael Couture, Fayyaz S. Sutterwala, Yasunori Ogura, Richard A. Flavell, Ira Mellman, F. Gisou van der Goot. (2008) Maturation modulates caspase-1-independent responses of dendritic cells to Anthrax Lethal Toxin. Cellular Microbiology 10:5, 1190-1207
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Keer Sun, Dennis W Metzger. (2008) Inhibition of pulmonary antibacterial defense by interferon-γ during recovery from influenza infection. Nature Medicine 14:5, 558-564
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Jean-Nicolas Tournier, Anne Quesnel-Hellmann, Aurélie Cleret, Dominique R. Vidal. (2007) Contribution of toxins to the pathogenesis of inhalational anthrax. Cellular Microbiology 9:3, 555-565
Online publication date: 1-Apr-2007.
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Karla D Passalacqua, Nicholas H Bergman. (2007) Bacillus anthracis: interactions with the host and establishment of inhalational anthrax. Future Microbiology 1:4, 397-415
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  • Presented in part: 12th International Congress of Mucosal Immunology, Boston, MA, 25–30 June 2005 (abstract 53928).

    Potential conflicts of interest: none reported.

    Financial support: Délégation Générale pour l’Armement (grant CO 010808); Service de Santé des Armées (135OP3B LFR EMA).

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