Reports

Salmonella Modulates Vesicular Traffic by Altering Phosphoinositide Metabolism

Lorraine D. Hernandez,^1* Karsten Hueffer,¹ Markus R. Wenk,² Jorge E. Galán¹

Salmonella enterica, the cause of food poisoning and typhoid fever, induces actin cytoskeleton rearrangements and membrane ruffling to gain access into nonphagocytic cells, where it can replicate and avoid innate immune defenses. Here, we found that SopB, a phosphoinositide phosphatase that is delivered into host cells by a type III secretion system, was essential for the establishment of Salmonella's intracellular replicative niche. SopB mediated the formation of spacious phagosomes following bacterial entry and was responsible for maintaining high levels of phosphatidylinositol-three-phosphate [PtdIns(3)P] in the membrane of the bacteria-containing vacuoles. Absence of SopB caused a significant defect in the maturation of the Salmonella-containing vacuole and impaired bacterial intracellular growth.

¹ Section of Microbial Pathogenesis, Yale University School of Medicine, New Haven, CT 06536, USA.
² Department of Cell Biology, Yale University School of Medicine, New Haven, CT 06510, USA.

^* Present address: Department of Human and Animal Infectious Disease, Merck Research Laboratories, Rahway, NJ 07065, USA.

Present address: Department of Biochemistry, National University of Singapore, 8 Medical Drive, Singapore 117597.

To whom correspondence should be addressed. E-mail: jorge.galan{at}yale.edu

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Type III Secretion Decreases Bacterial and Host Survival following Phagocytosis of Yersinia pseudotuberculosis by Macrophages.

Y. Zhang, J. Murtha, M. A. Roberts, R. M. Siegel, and J. B. Bliska (2008)
Infect. Immun. 76, 4299-4310
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SopB promotes phosphatidylinositol 3-phosphate formation on Salmonella vacuoles by recruiting Rab5 and Vps34.

G. V. Mallo, M. Espina, A. C. Smith, M. R. Terebiznik, A. Aleman, B. B. Finlay, L. E. Rameh, S. Grinstein, and J. H. Brumell (2008)
J. Cell Biol. 182, 741-752
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Sorting nexin-1 defines an early phase of Salmonella-containing vacuole-remodeling during Salmonella infection.

M. V. Bujny, P. A. Ewels, S. Humphrey, N. Attar, M. A. Jepson, and P. J. Cullen (2008)
J. Cell Sci. 121, 2027-2036
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Role for Myosin II in Regulating Positioning of Salmonella-Containing Vacuoles and Intracellular Replication.

J. A. Wasylnka, M. A. Bakowski, J. Szeto, M. B. Ohlson, W. S. Trimble, S. I. Miller, and J. H. Brumell (2008)
Infect. Immun. 76, 2722-2735
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Pseudomonas aeruginosa Induces Membrane Blebs in Epithelial Cells, Which Are Utilized as a Niche for Intracellular Replication and Motility.

A. A. Angus, A. A. Lee, D. K. Augustin, E. J. Lee, D. J. Evans, and S. M. J. Fleiszig (2008)
Infect. Immun. 76, 1992-2001
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Type III Secretion Systems and Disease.

B. Coburn, I. Sekirov, and B. B. Finlay (2007)
Clin. Microbiol. Rev. 20, 535-549
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Alteration of Epithelial Structure and Function Associated with PtdIns(4,5)P2 Degradation by a Bacterial Phosphatase.

D. Mason, G. V. Mallo, M. R. Terebiznik, B. Payrastre, B. B. Finlay, J. H. Brumell, L. Rameh, and S. Grinstein (2007)
J. Gen. Physiol. 129, 267-283
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Differential activation and function of Rho GTPases during Salmonella-host cell interactions.

J. C. Patel and J. E. Galan (2006)
J. Cell Biol. 175, 453-463
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Inhibition of Cdc42-dependent signalling in Saccharomyces cerevisiae by phosphatase-dead SigD/SopB from Salmonella typhimurium..

I. Rodriguez-Escudero, R. Rotger, V. J. Cid, and M. Molina (2006)
Microbiology 152, 3437-3452
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Efficient Translocation of EspC into Epithelial Cells Depends on Enteropathogenic Escherichia coli and Host Cell Contact.

J. E. Vidal and F. Navarro-Garcia (2006)
Infect. Immun. 74, 2293-2303
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Phosphoinositide 5-Phosphatase Fig4p Is Required for both Acute Rise and Subsequent Fall in Stress-Induced Phosphatidylinositol 3,5-Bisphosphate Levels..

J. E. Duex, J. J. Nau, E. J. Kauffman, and L. S. Weisman (2006)
Eukaryot. Cell 5, 723-731
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The Vac14p-Fig4p complex acts independently of Vac7p and couples PI3,5P2 synthesis and turnover.

J. E. Duex, F. Tang, and L. S. Weisman (2006)
J. Cell Biol. 172, 693-704
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Type III Secretion: More Systems Than You Think.

P. Troisfontaines and G. R. Cornelis (2005)
Physiology 20, 326-339
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The Salmonella Effector PipB2 Affects Late Endosome/Lysosome Distribution to Mediate Sif Extension.

L. A. Knodler and O. Steele-Mortimer (2005)
Mol. Biol. Cell 16, 4108-4123
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The Salmonella Effector Protein SopB Protects Epithelial Cells from Apoptosis by Sustained Activation of Akt.

L. A. Knodler, B. B. Finlay, and O. Steele-Mortimer (2005)
J. Biol. Chem. 280, 9058-9064
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The Salmonella Pathogenicity Island (SPI)-2 and SPI-1 Type III Secretion Systems Allow Salmonella Serovar typhimurium to Trigger Colitis via MyD88-Dependent and MyD88-Independent Mechanisms.

S. Hapfelmeier, B. Stecher, M. Barthel, M. Kremer, A. J. Muller, M. Heikenwalder, T. Stallmach, M. Hensel, K. Pfeffer, S. Akira, et al. (2005)
J. Immunol. 174, 1675-1685
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