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

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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^, 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 haveexamined the intracellular pathway of the virulent B. abortusstrain 2308 (S2308) and the attenuated strain 19 (S19) in HeLacells. At 10 min after inoculation, both bacterial strains aretransiently detected in phagosomes characterized by the presenceof early endosomal markers such as the early endosomal antigen1. At ~1 h postinoculation, bacteria are located within a compartmentpositive for the lysosome-associated membrane proteins (LAMPs)and the endoplasmic reticulum (ER) marker sec61 $beta$ but negativefor the mannose 6-phosphate receptors and cathepsin D. Interestingly,this compartment is also positive for the autophagosomal markermonodansylcadaverin, suggesting that S2308 and S19 are locatedin autophagic vacuoles. At 24 h after inoculation, attenuatedS19 is degraded in lysosomes, while virulent S2308 multiplieswithin a LAMP- and cathepsin D-negative but sec61 $beta$ - and proteindisulfide isomerase-positive compartment. Furthermore, treatmentof infected cells with the pore-forming toxin aerolysin from Aeromonashydrophila causes vacuolation of the bacterial replication compartment.These results are compatible with the hypothesis that pathogenicB. abortus exploits the autophagic machinery of HeLa cells toestablish an intracellular niche favorable for its replicationwithin theER.

^* Corresponding author. Mailing address: Centre d'Immunologie INSERM-CNRS de Marseille-Luminy, Case 906-13288 Marseille Cedex9, France. Phone: (33) 4 91 26 94 66. Fax: (33) 4 91 26 94 30.E-mail: gorvel{at}ciml.univ-mrs.fr.

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

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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