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Originally published In Press as doi:10.1074/jbc.M105508200 on November 7, 2001

J. Biol. Chem., Vol. 277, Issue 3, 2258-2265, January 18, 2002
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Nramp1 Modifies the Fusion of Salmonella typhimurium-containing Vacuoles with Cellular Endomembranes in Macrophages*

Patricia Cuellar-MataDagger §, Nada Jabado||, Jun Liu**, Wendy FuruyaDagger , B. Brett FinlayDagger Dagger §§, Philippe Gros§§, and Sergio GrinsteinDagger §§¶¶

From the Dagger  Division of Cell Biology, Hospital for Sick Children, Toronto M5G 1X8, Ontario, the  Department of Biochemistry, McGill University, Montreal H3G 1Y6, Quebec, the ** Department of Molecular and Medical Genetics, University of Toronto, Toronto M5S 1A8, Ontario, and the Dagger Dagger  Biotechnology Laboratory, University of British Columbia, Vancouver V6T 1Z3, British Columbia, Canada

Salmonella survive and replicate within mammalian cells by becoming secluded within specialized membrane-bound vacuoles inaccessible to the host defense mechanisms. Delayed acidification of the vacuole and its incomplete fusion with lysosomes have been implicated in intracellular Salmonella survival. Nramp1 confers to macrophages resistance to a variety of intracellular pathogens, including Salmonella, but its precise mode of action is not understood. We investigated whether Nramp1 affects the maturation and acidification of Salmonella-containing vacuoles (SCV). A mouse-derived macrophage line (RAW/Nramp1-) devoid of Nramp1 and therefore susceptible to infection was compared with isogenic clones stably transfected with Nramp1 (RAW/Nramp1+). Intravacuolar pH, measured in situ, was similar in Nramp1-expressing and -deficient cells. SCV acquired LAMP1 and fused with preloaded fluid-phase markers in both cell types. In contrast, although few vacuoles in RAW/Nramp1- acquired mannose 6-phosphate receptor, many more contained M6PR in RAW/Nramp1+ cells. Shortly after closure, SCV in RAW/Nramp1- became inaccessible to extracellular markers, suggesting inability to fuse with newly formed endosomes. Expression of Nramp1 markedly increased the access to extracellularly added markers. We propose that Nramp1 counteracts the ability of Salmonella to become secluded in a compartment that limits access of bactericidal agents, allowing the normal degradative pathway of the macrophage to proceed.

* This work was supported in part by the Arthritis Society of Canada, by the Canadian Institutes of Health Research (CIHR), and by National Institutes of Health NIAID Grant AI-35237.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.

§ Supported by the Consejo Nacional de Ciencia y Tecnologia (Mexico) and the University of Guanajuato (Mexico).

|| Recipient of a Human Frontier Science Program fellowship.

§§ International Scholar of the Howard Hughes Medical Institute and recipient of a CIHR Distinguished Scientist award.

¶¶ Current holder of the Pitblado Chair in Cell Biology. To whom correspondence should be addressed. Tel.: 416-813-5727; Fax: 416-813-5028; E-mail: sga@sickkids.on.ca.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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