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Infection and Immunity, March 2001, p. 1613-1624, Vol. 69, No. 3
0019-9567/01/$04.00+0   DOI: 10.1128/IAI.69.3.1613-1624.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Cell Vacuolation Caused by Vibrio cholerae Hemolysin

Paula Figueroa-Arredondo,1,2,3,* John E. Heuser,4 Natalia S. Akopyants,1 J. Hiroshi Morisaki,4 Silvia Giono-Cerezo,2 Fernando Enríquez-Rincón,3 and Douglas E. Berg1

Departments of Molecular Microbiology and of Genetics1 and Department of Cell Biology,4 Washington University School of Medicine, St. Louis, Missouri 63110, and Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas del IPN, Carpio y Plan de Ayala, México, D.F. 11340,2 and Departamento de Biología Celular, CINVESTAV-IPN, México, D.F. 07360,3 Mexico

Received 10 April 2000/Returned for modification 16 May 2000/Accepted 19 October 2000

Non-O1 strains of Vibrio cholerae implicated in gastroenteritis and diarrhea generally lack virulence determinants such as cholera toxin that are characteristic of epidemic strains; the factors that contribute to their virulence are not understood. Here we report that at least one-third of diarrhea-associated nonepidemic V. cholerae strains from Mexico cause vacuolation of cultured Vero cells. Detailed analyses indicated that this vacuolation was related to that caused by aerolysin, a pore-forming toxin of Aeromonas; it involved primarily the endoplasmic reticulum at early times (~1 to 4 h after exposure), and resulted in formation of large, acidic, endosome-like multivesicular vacuoles (probably autophagosomes) only at late times (~16 h). In contrast to vacuolation caused by Helicobacter pylori VacA protein, that induced by V. cholerae was exacerbated by agents that block vacuolar proton pumping but not by endosome-targeted weak bases. It caused centripetal redistribution of endosomes, reflecting cytoplasmic alkalinization. The gene for V. cholerae vacuolating activity was cloned and was found to correspond to hlyA, the structural gene for hemolysin. HlyA protein is a pore-forming toxin that causes ion leakage and, ultimately, eukaryotic cell lysis. Thus, a distinct form of cell vacuolation precedes cytolysis at low doses of hemolysin. We propose that this vacuolation, in itself, contributes to the virulence of V. cholerae strains, perhaps by perturbing intracellular membrane trafficking or ion exchange in target cells and thereby affecting local intestinal inflammatory or other defense responses.

* Corresponding author. Present address: Department of Microbiology and Molecular Genetics, Harvard Medical School, Harvard University, 200 Longwood Ave., Boston MA 02115. Phone: (617) 432-5098. Fax: (617) 738-7364. E-mail: paula_figueroa{at}hms.harvard.edu.

Infection and Immunity, March 2001, p. 1613-1624, Vol. 69, No. 3
0019-9567/01/$04.00+0   DOI: 10.1128/IAI.69.3.1613-1624.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


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