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Infection and Immunity, June 2002, p. 3199-3207, Vol. 70, No. 6
0019-9567/02/$04.00+0     DOI: 10.1128/IAI.70.6.3199-3207.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Apoptosis in Acute Shigellosis Is Associated with Increased Production of Fas/Fas Ligand, Perforin, Caspase-1, and Caspase-3 but Reduced Production of Bcl-2 and Interleukin-2

Rubhana Raqib,1* Caroline Ekberg,2 Protim Sharkar,1 Pradip K. Bardhan,1 Arturo Zychlinsky,3 Philippe J. Sansonetti,4 and Jan Andersson5

International Centre for Diarrhoeal Diseases Research, Bangladesh, Dhaka, Bangladesh,1 Department of Immunology, Stockholm University, Stockholm,2 Center for Infectious Medicine, Karolinska Institutet, Huddinge University Hospital, Huddinge, Sweden,5 Max Planck Institute for Infection Biology, Berlin, Germany,3 Unite de Pathogenie Microbienne Moleculaire, Institut Pasteur, Paris, France4

Received 29 October 2001/ Returned for modification 9 January 2002/ Accepted 2 March 2002

Shigella dysenteriae type 1-induced apoptotic cell death in rectal tissues from patients infected with Shigella dysenteriae type 1 was studied by the terminal deoxynucleotidyltransferase-mediated dUTP-biotin nick end labeling (TUNEL) technique and annexin V staining. Expression of proteins and cytokines participating in the apoptotic process (caspase-1, caspase-3, Fas [CD95], Fas ligand [Fas-L], perforin, granzyme A, Bax, WAF-1, Bcl-2, interleukin-2 [IL-2], IL-18, and granulocyte-macrophage colony-stimulating factor) in tissue in the acute and convalescent stages of dysentery was quantified at the single-cell level by in situ immunostaining. Apoptotic cell death in the lamina propria was markedly up-regulated at the acute stage (P < 0.05), where an increased number of necrotic cells were also seen. Phenotypic analysis of apoptotic cells revealed that 43% of T cells (CD3), 10% of granulocytes (CD15), and 5% of macrophages (CD56) underwent apoptosis. Increased activity of caspase-1 persisted in the rectum up to 1 month after onset. More-extensive expression of Fas, Fas-L, perforin, caspase-3, and IL-18, but not IL-2, at the acute stage than at the convalescent stage was observed. Increased expression of caspase-3 and IL-18 in tissues with severe inflammation compared to expression in those with mild inflammation was evident, implying a possible role in the perpetuation of inflammation. Significantly reduced cell death during convalescence was associated with a significant up-regulation of Bcl-2, Bax, and WAF-1 expression in the rectum compared to that in the acute phase of infection. Thus, induction of apoptosis at the local site in the early phase of S. dysenteriae type 1 infection was associated with a significant up-regulation of Fas/Fas-L and perforin and granzyme A expression and a down-regulation of Bcl-2 and IL-2, which promote cell survival.

* Corresponding author. Mailing address: Immunology, Laboratory Sciences Division, ICDDR,B, International Center for Health & Population Research, Mohakhali, Dhaka-1212, Bangladesh. Phone: 880 2 8811751. Fax: 880 2 8812529, 8826050, or 8823116. E-mail: rubhana{at}icddrb.org.

Editor: W. A. Petri, Jr.

Infection and Immunity, June 2002, p. 3199-3207, Vol. 70, No. 6
0019-9567/02/$04.00+0     DOI: 10.1128/IAI.70.6.3199-3207.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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