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Originally published In Press as doi:10.1074/jbc.M101573200 on March 14, 2001

J. Biol. Chem., Vol. 276, Issue 23, 19706-19714, June 8, 2001
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Yersinia enterocolitica YopP-induced Apoptosis of Macrophages Involves the Apoptotic Signaling Cascade Upstream of Bid*

Geertrui DeneckerDagger §, Wim Declercq§, Cecile A. W. GeuijenDagger §||, Anne BolandDagger ¶¶, Rachid BenabdillahDagger , Maria van Gurp, Marie-Paule SoryDagger **, Peter Vandenabeele, and Guy R. CornelisDagger Dagger Dagger

From the Dagger  Microbial Pathogenesis Unit, Christian de Duve Institute of Cellular Pathology, Université catholique de Louvain, Avenue Hippocrate 74, B-1200 Brussels and the  Department of Molecular Biology, Flanders Interuniversitary Institute for Biotechnology and University of Ghent, K. L. Ledeganckstraat 35, 9000 Ghent, Belgium

Yersinia enterocolitica induces apoptosis in macrophages by injecting the plasmid-encoded YopP (YopJ in other Yersinia species). Recently it was reported that YopP/J is a member of an ubiquitin-like protein cysteine protease family and that the catalytic core of YopP/J is required for its inhibition of the MAPK and NF-kappa B pathways. Here we analyzed the YopP/J-induced apoptotic signaling pathway. YopP-mediated cell death could be inhibited by addition of the zVAD caspase inhibitor, but not by DEVD or YVAD. Generation of truncated Bid (tBid) was the first apoptosis-related event that we observed. The subsequent translocation of tBid to the mitochondria induced the release of cytochrome c, leading to the activation of procaspase-9 and the executioner procaspases-3 and -7. Inhibition of the postmitochondrial executioner caspases-3 and -7 did not affect Bid cleavage. Bid cleavage could not be observed in a yopP-deficient Y. enterocolitica strain, showing that this event requires YopP. Disruption of the catalytic core of YopP abolished the rapid generation of tBid, thereby hampering induction of apoptosis by Y. enterocolitica. This finding supports the idea that YopP/J induces apoptosis by directly acting on cell death pathways, rather than being the mere consequence of gene induction inhibition in combination with microbial stimulation of the macrophage.

* This work was supported by the Belgian Fonds National de la Recherche Scientifique Médicale (convention 3.4595.97), the Direction Générale de la Recherche Scientifique-Communauté Française de Belgique (Action de Recherche Concertée 99/04-236), the Interuniversitaire Attractiepolen (number P4/26), European Community-Research Technology and Development Grant QLRT-199-00739, and the Fonds voor Wetenschappelijk Onderzoek Vlaanderen (number 3G000601). C. G. was a recipient of a Marie-Curie fellowship from the European Union (contract ERBFMBICT972047).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

§ Contributed equally to this work.

|| Present address: Division of Cell Biology, Cancer Inst., Plesmanstraat 121, 1066 CX Amsterdam, The Netherlands.

** Present address: Laboratoire de Bacteriologie Moléculaire, Université Libre de Bruxelles, Route de lennik 808, CP614, 1070 Bruxelles, Belgium.

¶¶ Present address: UMR1582, Institut Gustave Roussy, 94805 Villejuif, France.

Dagger Dagger To whom correspondence should be addressed. Tel.: 32-2-764-7449; Fax: 32-2-764-7498; E-mail: cornelis@mipa.ucl.ac.be.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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