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Infection and Immunity, December 2002, p. 6926-6932, Vol. 70, No. 12
0019-9567/02/$04.00+0     DOI: 10.1128/IAI.70.12.6926-6932.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Rapid Translocation of Polarized MDCK Cell Monolayers by Leptospira interrogans, an Invasive but Nonintracellular Pathogen

Michele A. Barocchi,1 Albert I. Ko,2,3 Mitermayer Galvão Reis,2 Kent L. McDonald,4 and Lee W. Riley1*

Division of Infectious Diseases and Immunity, School of Public Health,1 UC Berkeley Electron Microscopy Laboratory, University of California, Berkeley, Berkeley, California 94720,4 Gonçalo Moniz Research Center, Oswaldo Cruz Foundation, Brazilian Ministry of Health, 40001 Salvador, Bahia, Brazil,2 Division of International Medicine and Infectious Diseases, Weil Medical College of Cornell University, New York, New York 100213

Received 25 February 2002/ Returned for modification 3 April 2002/ Accepted 22 July 2002

Pathogenic spirochetes of the genus Leptospira are a major cause of human zoonotic infectious disease worldwide. After gaining entry through the skin, the organism causes disease by hematogenously disseminating to multiple organs. The mechanism by which it penetrates the mammalian cell barriers to disseminate is not well understood. In this study, we used a low-passage-number isolate of Leptospira interrogans to elucidate the invasive potential of this spirochete. Quantification of bacteria by dark-field microscopy revealed that pathogenic spirochetes were able to translocate through polarized MDCK cell monolayers at a rate significantly greater than that of nonpathogenic Leptospira or a recognized invasive bacterial pathogen, Salmonella. In contrast to Salmonella, L. interrogans did not alter transepithelial electrical resistance during cell translocation. Both transmission and scanning electron microscopy revealed tight association of the extracellular spirochetes with the host cell plasma membrane, without membrane perturbations suggestive of cytoskeletal rearrangement. Spirochetes were not observed within intercellular junctions or membrane-bound compartments inside cells. They were found within the cytoplasm of only 8% of the counted cells. These results indicate that Leptospira is an invasive but not a facultative intracellular organism. We propose that the rapid translocation of mammalian cells by pathogenic Leptospira is a mechanism designed to evade killing by host cells that permits the organism to quickly reach the bloodstream and disseminate to multiple organs.

* Corresponding author. Mailing address: Division of Infectious Diseases and Immunity, School of Public Health, University of California, Berkeley, 140 Earl Warren Hall, Berkeley, CA 94720-7360. Phone: (510) 642-9200. Fax: (510) 642-6350. E-mail: lwriley{at}uclink4.berkeley.edu.

Editor: B. B. Finlay

Infection and Immunity, December 2002, p. 6926-6932, Vol. 70, No. 12
0019-9567/02/$04.00+0     DOI: 10.1128/IAI.70.12.6926-6932.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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