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Infection and Immunity, July 2005, p. 3937-3944, Vol. 73, No. 7
0019-9567/05/$08.00+0     doi:10.1128/IAI.73.7.3937-3944.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Survival of Salmonella enterica Serovar Typhimurium within Late Endosomal-Lysosomal Compartments of B Lymphocytes Is Associated with the Inability To Use the Vacuolar Alternative Major Histocompatibility Complex Class I Antigen-Processing Pathway

Roberto Rosales-Reyes,1,2 Celia Alpuche-Aranda,2,{dagger} María de la Luz Ramírez-Aguilar,2 Angel Denisse Castro-Eguiluz,1 and Vianney Ortiz-Navarrete1*,{dagger}

Departamento de Biomedicina Molecular, Centro de Investigación y de Estudios Avanzados (CINVESTAV), México D.F.,1 Departamento de Medicina Experimental, Facultad de Medicina UNAM-HGM, México D.F., Mexico2

Received 9 September 2004/ Returned for modification 17 October 2004/ Accepted 1 March 2005

Gamma interferon (IFN-{gamma})-activated macrophages use an alternative processing mechanism to present Salmonella antigens to CD8+ T lymphocytes. This pathway involves processing of antigen in a vacuolar compartment followed by secretion and loading of antigenic peptides to major histocompatibility complex class I (MHC-I) molecules on macrophage cell surface and bystander cells. In this study, we have shown that B lymphocytes are not able to process Salmonella antigens using this alternative pathway. This is due to differences in Salmonella enterica serovar Typhimurium-containing vacuoles (SCV) when comparing late endosomal-lysosomal processing compartments in B lymphocytes to those in macrophages. The IFN-{gamma}-activated IC21 macrophage cell line and A-20 B-cell line were infected with live or dead Salmonella enterica serovar Typhimurium. The SCV in B cells were in a late endosomal-lysosomal compartment, whereas SCV in macrophages were remodeled to a noncharacteristic late endosomal-lysosomal compartment over time. Despite the difference in SCV within macrophages and B lymphocytes, S. enterica serovar Typhimurium survives more efficiently within the IFN-{gamma}-activated B cells than in activated macrophage cell lines. Similar results were found during in vivo acute infection. We determined that a lack of remodeling of late endosomal-lysosomal compartments by live Salmonella infection in B lymphocytes is associated with the inability to use the alternative MHC-I antigen-processing pathway, providing a survival advantage to the bacterium. Our data also suggest that the B lymphocyte late endosome-lysosome environment allows the expression of Salmonella virulence mechanisms favoring B lymphocytes in addition to macrophages and dendritic cells as a reservoir during in vivo infection.

* Corresponding author. Mailing address: Departamento de Biomedicina Molecular, Centro de Investigación y de Estudios Avanzados (CINVESTAV), Av. IPN No. 2508, Colonia San Pedro Zacatenco, Delegación Gustavo A. Madero, México, DF CP 07360, Mexico. Phone: 52 555 506 13324. Fax: 52 555 747 7134. E-mail: vortiz{at}mail.cinvestav.mx.

Editor: F. C. Fang

{dagger} V.O.-N. and C.A.-A. share senior authorship.

Infection and Immunity, July 2005, p. 3937-3944, Vol. 73, No. 7
0019-9567/05/$08.00+0     doi:10.1128/IAI.73.7.3937-3944.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.





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