The Journal of Experimental Medicine
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Published online 26 April 2004 doi:10.1084/jem.20031706
Rockefeller University Press, 0022-1007 $8.00
JEM, Volume 199, Number 9, 1201-1211
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Legionella Subvert the Functions of Rab1 and Sec22b to Create a Replicative Organelle

Jonathan C. Kagan, Mary-Pat Stein, Marc Pypaert, and Craig R. Roy

Section of Microbial Pathogenesis, Boyer Center for Molecular Medicine, Yale University School of Medicine, New Haven, CT 06536

Address correspondence to Craig R. Roy, Section of Microbial Pathogenesis, Boyer Center for Molecular Medicine, Yale University School of Medicine, 295 Congress Ave., New Haven, CT 06536. Phone: (203) 737-2408; Fax: (203) 737-2630; email: craig.roy{at}yale.edu

Legionella pneumophila is a bacterial pathogen that infects eukaryotic host cells and replicates inside a specialized organelle that is morphologically similar to the endoplasmic reticulum (ER). To better understand the molecular mechanisms governing transport of the Legionella-containing vacuole (LCV), we have identified host proteins that participate in the conversion of the LCV into a replicative organelle. Our data show that Rab1 is recruited to the LCV within minutes of uptake. Rab1 recruitment to the LCV precedes remodeling of this compartment by ER-derived vesicles. Genetic inhibition studies demonstrate that Rab1 is important for the recruitment of ER-derived vesicles to the LCV and that inhibiting Rab1 function abrogates intracellular growth of Legionella. Morphological studies indicate that the Sec22b protein is located on ER-derived vesicles recruited to the LCV and that Sec22b is delivered to the LCV membrane. Sec22b function was found to be important for biogenesis of the specialized organelle that supports Legionella replication. These studies demonstrate that Legionella has the ability to subvert Rab1 and Sec22b function to facilitate the transport and fusion of ER-derived vesicles with the LCV, resulting in the formation of a specialized organelle that can support bacterial replication.

Key Words: brefeldin A • ARF1 • Sar1 • phagosome • endoplasmic reticulum

The online version of this article contains supplemental material.

Abbreviations used in this paper: ARF, ADP ribosylation factor; BMM, bone marrow–derived macrophage; CHO, Chinese hamster ovary; FSG, fish skin gelatin; GFP, green fluorescent protein; GTPase, guanosine triphosphatase; LCV, Legionella-containing vacuole; SEAP, secreted alkaline phosphatase; SNARE, soluble N-ethylmaleimide-sensitive factor attachment protein receptor; t-SNARE, SNARE found on target membrane; v-SNARE, SNARE found on vesicle membrane.


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