© 2002 Blackwell Science Ltd
The Vibrio cholerae haemolysin anion channel is
required for cell vacuolation and death
tioning of the Cystic Fibrosis Transmembrane Regulator
(CFTR) chloride channel and of other cellular proteins
(Hogenauer et al., 2000). The zona occludens toxin alters
the tight junctions that control the paracellular permeabil-
ity of the polarized epithelial monolayer (Marinaro et al.,
1999). The V. cholerae heat-stable toxin causes rapid fluid
accumulation after activation of the guanylyl cyclase and
the influx of Ca
2+
ions across the plasma membrane
(Visweswariah et al., 1992; Hoque et al., 2001).
In addition, many V. cholerae strains secrete a
haemolytic toxin of 63 kDa, termed V. cholerae cytolysin
(VCC) or haemolysin (Honda and Finkelstein, 1979;
Ramamurthy et al., 1993; Dalsgaard et al., 1995). VCC
causes lysis of vertebrate erythrocytes and cultured cells
(Honda and Finkelstein, 1979; Zitzer et al., 1997a). It also
increases the vascular permeability of rabbit skin and it is
lethal to mice (Yamamoto et al., 1984).
VCC forms transmembrane anion-selective pentameric
channels with a diameter of 0.9–1.0 nm, leading to
osmotic swelling of the cell and lysis (Krasilnikov et al.,
1992; Zitzer et al., 1995, 1997a; 1999). The membrane-
permeabilizing action of VCC has been documented in
planar lipid bilayers and liposomes (Krasilnikov et al.,
1992; Zitzer et al., 1993; Menzl et al., 1996). A pathogenic
role for VCC in enteritis is suggested by the observation
that the purified protein elicits fluid accumulation in rabbit
ileal loops (Zitzer et al., 1993). Furthermore, a cytocidal
action of VCC on human intestinal cells was attributed to
VCC oligomerization and pore formation on cell mem-
branes (Zitzer et al., 1997b; 1999). Recently, extensive
cell vacuolation of HeLa and Vero cells was shown to be
induced by V. cholerae filtrates and the vacuolating activ-
ity was linked to VCC (Coelho et al., 2000; Mitra et al.,
2000). Such cell vacuolating effect was reminiscent of that
induced by the VacA cytotoxin of Helicobacter pylori
(Cover and Blaser, 1992; Montecucco and Rappuoli,
2001; Morbiato et al., 2001). On the other hand, some dif-
ferences among the cellular vacuoles induced by the two
toxins were apparent. Vibrio cholerae cytolysin-induced
vacuoles were found to uptake the weak base dye, neutral
red, indicating that they are acidic like VacA-induced
vacuoles. However, the specific vacuolar ATPase proton
pump inhibitor bafilomycin A1, which is able to inhibit
vacuole formation in VacA treated cells, did not prevent
vacuole formation in VCC exposed cells (Cover et al.,
1993; Papini et al., 1993; Coelho et al., 2000; Mitra et al.,
2000; Figueroa-Arredondo et al., 2001).
Cellular Microbiology (2002) 4(7), 397–409
Monica Moschioni,
1
Francesco Tombola,
1
Marina de Bernard,
1
Ana Coelho,
2
Alexander Zitzer,
3
Mario Zoratti
1
and Cesare Montecucco
1
*
1
Centro CNR Biomembrane and Dipartimento di
Scienze Biomediche Sperimentali, Università di Padova,
Via G. Colombo 3, 35121, Padova, Italy.
2
Departamento de Genetica, Universidade Federal do
Rio de Janeiro RJ21944-970, Brazil.
3
Institute of Medical Microbiology and Hygiene,
Johannes Gutenberg University, 55101 Mainz,
Germany.
Summary
Several strains of Vibrio cholerae secrete a
haemolytic toxin of 63 kDa, termed V. cholerae
cytolysin (VCC). This toxin causes extensive vacuo-
lation and death of cells in culture and forms an
anion-selective channel in planar lipid bilayers and in
cells. Here, we identify inhibitors of the VCC anion
channel and show that the formation of the anion
channel is necessary for the development of the
vacuoles and for the cell death induced by this
toxin. Using markers of cell organelles, we show
that vacuoles derive from different intracellular com-
partments and we identify the contribution of late
endosomes and of the trans-Golgi network in vacuole
biogenesis.
Introduction
The Gram-negative bacterium Vibrio cholerae is an
intestinal non-invasive pathogen that adheres to the
apical side of the small intestine (Salyers and Whitt, 1994)
thereby inducing cholera, an acute watery diarrhoea
disease of humans (Kaper et al., 1995). Vibrio cholerae
produces several virulence factors that are involved in
colonization and adhesion and also releases protein
toxins that co-operate to induce the alteration of ion and
water fluxes across the intestinal epithelium, which is the
basis of the massive loss of fluids characteristic of cholera
(Kaper et al., 1995). Cholera toxin enters into epithelial
cells and elevates the cAMP level, which affects the func-
Received 23 January, 2002; revised 9 April, 2002; accepted 9 April,
2002. *For correspondence. E-mail: cesare@civ.bio.unipd.it;
Tel. (+39) 049 8276058; Fax: (+39) 049 8276049.