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Infection and Immunity, August 2002, p. 4369-4378, Vol. 70, No. 8
0019-9567/02/$04.00+0     DOI: 10.1128/IAI.70.8.4369-4378.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Effect of Acid Adaptation on the Fate of Listeria monocytogenes in THP-1 Human Macrophages Activated by Gamma Interferon

Maria Pia Conte,1 Gloria Petrone,1 Assunta Maria Di Biase,1 Catia Longhi,1 Michela Penta,1 Antonella Tinari,2 Fabiana Superti,2 Giulia Fabozzi,3 Paolo Visca,3,4 and Lucilla Seganti1*

Department of Public Health Sciences, University "La Sapienza," 00185 Rome,1 Laboratory of Ultrastructure, Istituto Superiore di Sanità, 00161 Rome,2 Molecular Microbiology Unit, National Institute for Infectious Diseases IRCCS "Lazzaro Spallanzani," 00149 Rome,3 Department of Biology, University Roma Tre, 00146 Rome, Italy4

Received 23 January 2002/ Returned for modification 2 April 2002/ Accepted 23 April 2002

In Listeria monocytogenes the acid tolerance response (ATR) takes place through a programmed molecular response which ensures cell survival under unfavorable conditions. Much evidence links ATR with virulence, but the molecular determinants involved in the reactivity to low pHs and the behavior of acid-exposed bacteria within host cells are still poorly understood. We have investigated the effect of acid adaptation on the fate of L. monocytogenes in human macrophages. Expression of genes encoding determinants for cell invasion and intracellular survival was tested for acid-exposed bacteria, and invasive behavior in the human myelomonocytic cell line THP-1 activated with gamma interferon was assessed. Functional approaches demonstrated that preexposure to an acidic pH enhances the survival of L. monocytogenes in activated human macrophages and that this effect is associated with an altered pattern of expression of genes involved in acid resistance and cell invasion. Significantly decreased transcription of the plcA gene, encoding a phospholipase C involved in vacuolar escape and cell-to-cell spread, was observed in acid-adapted bacteria. This effect was due to a reduction in the quantity of the bicistronic plcA-prfA transcript, concomitant with an increase in the level(s) of the monocistronic prfA mRNA(s). The transcriptional shift from distal to proximal prfA promoters resulted in equal levels of the prfA transcript (and, as a consequence, of the inlA, hly, and actA transcripts) under neutral and acidic conditions. In contrast, the sodC and gad genes, encoding a cytoplasmic superoxide dismutase and the glutamate-based acid resistance system, respectively, were positively regulated at a low pH. Morphological approaches confirmed the increased intracellular survival and growth of acid-adapted L. monocytogenes cells both in vacuoles and in the cytoplasm of interferon gamma-activated THP-1 macrophages. Our data indicate that preexposure to a low pH has a positive impact on subsequent challenge of L. monocytogenes with macrophagic cells.

* Corresponding author. Mailing address: Department of Public Health Sciences, University "La Sapienza," P.le Aldo Moro 5, 00185 Rome, Italy. Phone: 39 06 49914629. Fax: 39 06 49914626. E-mail: lucilla.seganti{at}uniroma1.it.

Editor: A. D. O'Brien

Infection and Immunity, August 2002, p. 4369-4378, Vol. 70, No. 8
0019-9567/02/$04.00+0     DOI: 10.1128/IAI.70.8.4369-4378.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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