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Journal of Bacteriology, June 1999, p. 3433-3437, Vol. 181, No. 11
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.

Growth Phase-Regulated Induction of Salmonella-Induced Macrophage Apoptosis Correlates with Transient Expression of SPI-1 Genes

Urban Lundberg,dagger Ursula Vinatzer,Dagger Daniela Berdnik,§ Alexander von Gabain, and Manuela Baccarini*

Institute of Microbiology and Genetics, Vienna Biocenter, University of Vienna, A-1030 Vienna, Austria

Received 16 July 1998/Accepted 30 March 1999

Invasive Salmonella has been reported to induce apoptosis in a fraction of infected macrophages within 2 to 14 h from the time of infection by a mechanism involving the type III secretion machinery encoded by the Salmonella pathogenicity island 1 (SPI-1). Here, we show that bacteria in the transition from logarithmic to stationary phase cause 90% of the macrophages to undergo phagocytosis-independent, caspase-mediated apoptosis within 30 to 60 min of infection. The ability of Salmonella to induce this rapid apoptosis was growth phase regulated and cell type restricted, with epithelial cells being resistant. Apoptosis induction was also abrogated by disruption of the hilA gene (encoding a regulator of SPI-1 genes) and by the expression of a constitutively active PhoPQ. hilA itself and a subset of SPI-1 genes were transiently expressed during aerobic growth in liquid medium. Interestingly, however, hilA was found to be required only for the expression of the prgH gene, while sipB, invA, and invF were expressed in a hilA-independent manner. The expression of SPI-1 genes and the secretion of invasion-associated proteins correlated temporally with the induction of apoptosis and are likely to represent its molecular basis. Thus, growth phase transition regulates the expression and secretion of virulence determinants and represents the most efficient environmental cue for apoptosis induction reported to date.

* Corresponding author. Mailing address: Vienna Biocenter, Department of Cell- and Microbiology, Institute for Microbiology and Genetics, Dr. Bohr Gasse 9, A-1030 Vienna, Austria. Phone: 43 (1) 4277-54607. Fax: 43 (1) 4277-9546. E-mail: manuela{at}gem.univie.ac.at.

dagger Present address: Department of Bacteriology, Baxter Hyland-Immuno, A-2304 Orth/Donau, Austria.

Dagger Present address: Institute for Medical Biology, A-1090 Vienna, Austria.

§ Present address: Institute of Molecular Pathology, A-1030 Vienna, Austria.

Journal of Bacteriology, June 1999, p. 3433-3437, Vol. 181, No. 11
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.


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