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First published online 17 February 2004
doi: 10.1242/jcs.00949

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Microtubule motors control membrane dynamics of Salmonella-containing vacuoles

Julie Guignot^1,*, Emmanuelle Caron², Carmen Beuzón³, Cecilia Bucci⁴, Jonathan Kagan⁵, Craig Roy⁵ and David W. Holden^1,

¹ Department of Infectious Diseases, Centre for Molecular Microbiology and Infection, Imperial College London, London, SW7 2AZ, UK
² Department of Biological Sciences, Centre for Molecular Microbiology and Infection, Imperial College London, London, SW7 2AZ, UK
³ Departamento de Biología Celular, Genética y Fisiología, Universidad de Málaga, Campus de Teatinos, Málaga E-29071, Spain
⁴ Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali, Università di Lecce, Via Monteroni, 73100 Lecce, Italy
⁵ Yale University School of Medicine, Boyer Center for Molecular Medicine, 295 Congress Avenue, New Haven, CT 06536-0812, USA

Author for correspondence (e-mail: d.holden{at}imperial.ac.uk)

Accepted 21 October 2003

Infection of host cells by Salmonella enterica serovar Typhimurium (S. typhimurium) leads to the formation of specialised membrane-bound compartments called Salmonella-containing vacuoles (SCVs). Bacteria remain enclosed by the vacuolar membrane as they divide, and by translocating effector proteins across the vacuolar membrane through the SPI-2 type III secretion system, they interfere with host cell processes in ways that promote bacterial growth. One such effector is SifA, which is required to maintain the integrity of the vacuolar membrane and for the formation in epithelial cells of long tubular structures called Sifs that are connected to SCVs. Unknown effector(s) mediate the assembly of a meshwork of F-actin around SCVs. We report that intracellular bacteria also cause a dramatic accumulation of microtubules around S. typhimurium microcolonies in both epithelial cells and macrophages. Although this process appears to be independent of SPI-2-mediated F-actin assembly, it does require bacterial protein synthesis. In epithelial cells, microtubule accumulation is accompanied by the recruitment of both kinesin and dynein. Inhibition of the activity of either motor prevented both Sif formation and the loss of vacuolar membrane from sifA mutant bacteria. It also resulted in morphologically abnormal vacuoles enclosing wild-type bacteria, and impaired their replication. Our experiments indicate that recruitment of dynein to SCVs is dependent on Rab7 activity. We show that the recently described Rab7 effector RILP is also recruited to SCVs in a Rab7-dependent manner. However, overexpression of RILP did not restore dynein recruitment to SCVs in cells expressing dominant negative Rab7, suggesting that RILP requires a functional Rab7 to be activated at the SCV membrane, or that dynein recruitment is mediated by an effector other than RILP. Together, these experiments indicate that microtubule motors play important roles in regulating vacuolar membrane dynamics during intracellular replication of S. typhimurium.

Key words: Dynein, Salmonella, Microtubule, Vacuolar membrane, Rab7

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