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Infection and Immunity, December 1998, p. 5711-5724, Vol. 66, No. 12
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

Brucella abortus Transits through the Autophagic Pathway and Replicates in the Endoplasmic Reticulum of Nonprofessional Phagocytes

Javier Pizarro-Cerdá,1 Stéphane Méresse,1 Robert G. Parton,2 Gisou van der Goot,3 Alberto Sola-Landa,4 Ignacio Lopez-Goñi,4 Edgardo Moreno,1,dagger and Jean-Pierre Gorvel1,*

Centre d'Immunologie INSERM-CNRS de Marseille-Luminy, Marseille, France1; Centre for Microscopy and Microanalysis, University of Queensland, Brisbane, Australia2; Department of Biochemistry, University of Geneva, Geneva, Switzerland3; and Departmento de Microbiologia, Universidad de Navarra, Pamplona, Spain4

Received 5 June 1998/Returned for modification 17 August 1998/Accepted 1 September 1998

Brucella abortus is an intracellular pathogen that replicates within a membrane-bounded compartment. In this study, we have examined the intracellular pathway of the virulent B. abortus strain 2308 (S2308) and the attenuated strain 19 (S19) in HeLa cells. At 10 min after inoculation, both bacterial strains are transiently detected in phagosomes characterized by the presence of early endosomal markers such as the early endosomal antigen 1. At ~1 h postinoculation, bacteria are located within a compartment positive for the lysosome-associated membrane proteins (LAMPs) and the endoplasmic reticulum (ER) marker sec61beta but negative for the mannose 6-phosphate receptors and cathepsin D. Interestingly, this compartment is also positive for the autophagosomal marker monodansylcadaverin, suggesting that S2308 and S19 are located in autophagic vacuoles. At 24 h after inoculation, attenuated S19 is degraded in lysosomes, while virulent S2308 multiplies within a LAMP- and cathepsin D-negative but sec61beta - and protein disulfide isomerase-positive compartment. Furthermore, treatment of infected cells with the pore-forming toxin aerolysin from Aeromonas hydrophila causes vacuolation of the bacterial replication compartment. These results are compatible with the hypothesis that pathogenic B. abortus exploits the autophagic machinery of HeLa cells to establish an intracellular niche favorable for its replication within the ER.

* Corresponding author. Mailing address: Centre d'Immunologie INSERM-CNRS de Marseille-Luminy, Case 906-13288 Marseille Cedex 9, France. Phone: (33) 4 91 26 94 66. Fax: (33) 4 91 26 94 30. E-mail: gorvel{at}ciml.univ-mrs.fr.

dagger Present address: Programa de Investigación en Enfermedades Tropicales, Escuela de Medicina Veterinaria, Universidad Nacional, Heredia, Costa Rica.

Infection and Immunity, December 1998, p. 5711-5724, Vol. 66, No. 12
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.


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