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Originally published In Press as doi:10.1074/jbc.M105606200 on September 28, 2001

J. Biol. Chem., Vol. 276, Issue 48, 44435-44443, November 30, 2001
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GTPases of the Rho Subfamily Are Required for Brucella abortus Internalization in Nonprofessional Phagocytes
DIRECT ACTIVATION OF Cdc42*

Caterina Guzmán-VerriDagger §, Esteban Chaves-OlarteDagger ||, Christoph von Eichel-Streiber**, Ignacio López-GoñiDagger Dagger , Monica Thelestam§, Staffan Arvidson§, Jean-Pierre Gorvel§§, and Edgardo MorenoDagger ¶¶

From the Dagger  Programa de Investigación en Enfermedades Tropicales, Escuela de Medicina Veterinaria, Universidad Nacional, P. O. Box 304, 3000 Heredia, Costa Rica, the § Microbiology & Tumorbiology Center, Karolinska Institute, S-17177 Stockholm, Sweden, the || Centro de Investigación en Enfermedades Tropicales, Facultad de Microbiología, Universidad de Costa Rica, 1000 San José, Costa Rica, the ** Institut für Medizinische Mikrobiologie und Hygiene, Verfügungsgebaude für Forschung und Entwicklung, Johannes Gutenberg-Universität Mainz, Obere Zahlbacher Straße 63, 55101 Mainz, Federal Republic of Germany, the Dagger Dagger  Departamento de Microbiología, Universidad de Navarra, P. O. Box 177, 31080 Pamplona, Spain, and §§ INSERM-CNRS, Centre d'Immunologie de Marseille-Luminy, 13288 Marseille Cedex 9, France

Members of the genus Brucella are intracellular alpha -Proteobacteria responsible for brucellosis, a chronic disease of humans and animals. Little is known about Brucella virulence mechanisms, but the abilities of these bacteria to invade and to survive within cells are decisive factors for causing disease. Transmission electron and fluorescence microscopy of infected nonprofessional phagocytic HeLa cells revealed minor membrane changes accompanied by discrete recruitment of F-actin at the site of Brucella abortus entry. Cell uptake of B. abortus was negatively affected to various degrees by actin, actin-myosin, and microtubule chemical inhibitors. Modulators of MAPKs and protein-tyrosine kinases hampered Brucella cell internalization. Inactivation of Rho small GTPases using clostridial toxins TcdB-10463, TcdB-1470, TcsL-1522, and TcdA significantly reduced the uptake of B. abortus by HeLa cells. In contrast, cytotoxic necrotizing factor from Escherichia coli, known to activate Rho, Rac, and Cdc42 small GTPases, increased the internalization of both virulent and non-virulent B. abortus. Expression of dominant-positive Rho, Rac, and Cdc42 forms in HeLa cells promoted the uptake of B. abortus, whereas expression of dominant-negative forms of these GTPases in HeLa cells hampered Brucella uptake. Cdc42 was activated upon cell contact by virulent B. abortus, but not by a noninvasive isogenic strain, as proven by affinity precipitation of active Rho, Rac, and Cdc42. The polyphasic approach used to discern the molecular events leading to Brucella internalization provides new alternatives for exploring the complexity of the signals required by intracellular pathogens for cell invasion.

* This work was supported in part by Research Contract ICA4-CT-1999-10001 from the European Community, Research and Technological Development Projects NOVELTARGETVACCINES, Ministerio de Ciencia y Tecnología/Consejo Nacional de Ciencia y Tecnología (Costa Rica), Vicerrectoría de Investigación from the Universidad de Costa Rica, American Society for Microbiology Microbial Resources Center award, and Grant AGL2000-0305-C02-01 from the Ministerio de Ciencia y Tecnología (Spain).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.

Recipient of a grant from the Swedish International Development Agency as part of the Karolinska International Research Training Program.

¶¶ To whom correspondence should be addressed. Tel.: 506-2380761; Fax: 506-2381298; E-mail: emoreno@ns.medvet.una.ac.cr.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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