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Yersinia enterocolitica Impairs Activation of Transcription Factor NF-B: Involvement in the Induction of Programmed Cell Death and in the Suppression of the Macrophage Tumor Necrosis Factor Production

Klaus Ruckdeschel^*, Suzanne Harb^*, Andreas Roggenkamp, Mathias Hornef, Robert Zumbihl, Stephan Köhler^*, Jürgen Heesemann, and Bruno Rouot^*

From the ^* Institut National de la Santé et de la Recherche Médicale U431, Université Montpellier II, 34095 Montpellier Cedex 05, France; and the Max von Pettenkofer-Institut für Hygiene und Medizinische Mikrobiologie, 80336 München, Germany

In this study, we investigated the activity of transcription factor NF-B in macrophages infected with Yersinia enterocolitica. Although triggering initially a weak NF-B signal, Y. enterocolitica inhibited NF-B activation in murine J774A.1 and peritoneal macrophages within 60 to 90 min. Simultaneously, Y. enterocolitica prevented prolonged degradation of the inhibitory proteins IB- and IB-β observed by treatment with lipopolysaccharide (LPS) or nonvirulent, plasmid-cured yersiniae. Analysis of different Y. enterocolitica mutants revealed a striking correlation between the abilities of these strains to inhibit NF-B and to suppress the tumor necrosis factor (TNF-) production as well as to trigger macrophage apoptosis. When NF-B activation was prevented by the proteasome inhibitor MG-132, nonvirulent yersiniae as well as LPS became able to trigger J774A.1 cell apoptosis and inhibition of the TNF- secretion. Y. enterocolitica also impaired the activity of NF-B in epithelial HeLa cells. Although neither Y. enterocolitica nor TNF- could induce HeLa cell apoptosis alone, TNF- provoked apoptosis when activation of NF-B was inhibited by Yersinia infection or by the proteasome inhibitor MG-132. Together, these data demonstrate that Y. enterocolitica suppresses cellular activation of NF-B, which inhibits TNF- release and triggers apoptosis in macrophages. Our results also suggest that Yersinia infection confers susceptibility to programmed cell death to other cell types, provided that the appropriate death signal is delivered.

¹ Abbreviations used in this paper: DTT, 1,4 dithiothreitol; EMSA, electrophoretic mobility shift assay; ERK, extracellular signal–regulated kinase; JNK, c-Jun NH₂-terminal kinase; MAPK, mitogen-activated protein kinase; MEK1, MAPK-ERK kinase 1.

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