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MBC in Press, published online ahead of print October 26, 2005
Mol. Biol. Cell 10.1091/mbc.E04-12-1096

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Submitted on December 21, 2004
Revised on October 17, 2005
Accepted on October 19, 2005

Visualization of Vacuolar Acidification-induced Transcription of Genes of Pathogens inside Macrophages

Natalia Martin Orozco,*{dagger} Nicolas Touret,*{dagger} Michael L. Zaharik,{ddagger}{sect} Edwin Park,|| Raoul Kopelman,|| Samuel Miller,¶ B. Brett Finlay,{ddagger} Philippe Gros,# and Sergio Grinstein*

*Cell Biology Program, Hospital for Sick Children and Department of Biochemistry, University of Toronto, Toronto, Ontario M5G 1X8, Canada; {ddagger}Biotechnology Laboratory, University of British Columbia, Vancouver, British Columbia V6T1Z3, Canada; ||Department of Chemistry, University of Michigan, Ann Arbor, MI 48109-1055; Department of Microbiology and Laboratory of Medicine, University of Washington Medical School, Seattle, WA 98195; #Department of Biochemistry, Center for the Study of Host Resistance, McGill University, Montreal, Quebec, Canada H3A 2T5

Monitoring Editor: Ralph Isberg

The objective of these studies was to analyze the role of the ionic environment of phagosomal vacuoles in the control of pathogens by macrophages. Digital imaging and flow cytometry were used to follow the induction of the phoP promoter of Salmonella enterica Typhimurium within live macrophages. Manipulating the Mg2+ concentration within the Salmonella-containing vacuole (SCV) was without effect on the early induction of PhoPQ. Moreover, direct measurement of [Mg2+] within the SCV using nanosensor particles showed that, during this initial period of phoP activation, the concentration of the divalent cation is rapidly regulated and stabilizes around 1 mM. Extrusion of other divalent cations via the Nramp1 efflux pump was similarly ruled out as an important contributor to the activation of the regulon. By contrast, induction of PhoP was greatly attenuated when the pH gradient across the SCV membrane was dissipated. A second, more modest pH-independent component of PhoP induction was unmasked by inhibition of the vacuolar proton pump. This second component was eliminated by pretreatment of cells with IFN{gamma}, even though the cytokine augmented the overall PhoP response. These findings demonstrate the existence of at least three separate activators of phoP transcription: resting and IFN{gamma}-stimulated pH-sensitive components, plus a pH-independent component.

{dagger}These authors contributed equally to this work.

{sect}Present address: UBC CDC, 655 West 12th Ave., Vancouver, British Columbia V5Z4R4, Canada.

Address correspondence to: Sergio Grinstein (sga{at}sickkids.ca)




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