J. gen. Virol. (1982), 58, 47-61. Printed in Great Britain
Key words: inhibition of virus entry/chtoroquine/amantadine/SFV
47
Inhibition of Semliki Forest Virus Penetration by Lysosomotropic Weak
Bases
By ARI HELENIUS,*t MARK MARSHt AND JUDY WHITEr
European Molecular Biology Laboratory, Postfach 102209, 6900 Heidelberg, Federal
Republic of Germany
(Accepted 27 July 1981)
SUMMARY
The effect of five lysosomotropic weak bases (chloroquine, amantadine,
tributylamine, methylamine and NH4CI) on Semliki Forest virus (SFV) infection has
been studied in BHK-21 cells. When present at concentrations equal to or greater
than 0-1, 0.5, 2, 15 and 15 mM respectively, the agents inhibited SFV infection by
more than 90%. The effect was reversible and involved a process occurring within
the first 60 min of virus-cell contact. The agents did not have a direct virucidal effect
nor did they affect virus binding to the cells, receptor-mediated endocytosis of
prebound virus, intracellular distribution of virus after endocytosis, or the low
pH-induced membrane fusion activity of the virus spike glycoproteins. The step
blocked by chloroquine and NH4CI occurred intracellularly and was identified as the
release of the virus nucleocapsid into the cytoplasm or the uncoating process. On the
basis of these results, our previous studies on SFV entry, and the known effects of
lipophilic amines on lysosomes, we conclude that the agents affect entry by a
common mechanism: they prevent the transfer of the virus nucleocapsid into the
cytoplasm by increasing the lysosomal pH above the critical value needed to trigger
a low pH-dependent fusion reaction between the membranes of the tysosome and the
virus.
INTRODUCTION
Semliki Forest virus (SFV), an alphavirus, infects cells by an endocytotic route. The
viruses are internalized by receptor-mediated endocytosis in coated vesicles and delivered
into intracellular vacuoles (Helenius et al., 1980a, b; Marsh & Helenius, 1980). Our results
suggest that the virus genome penetrates into the cytoplasm by fusion between the virus
membrane and the limiting membrane of the secondary lysosome to which the viruses are
directed (Helenius et al., 1980 a, b; White & Helenius, 1980). The fusion reaction is probably
triggered by the low pH in the lysosomes (Helenius et al., 1980a, b; White & Helenius, 1980;
White et al., 1980). Experiments using a lysosomotropic weak base, chloroquine, indicated
that lysosomes are important in the endocytotic infection route observed at neutral pH
(Helenius et al., 1980a, b; Talbot & Vance, 1980). In addition, infection could be induced
directly through the plasma membrane, but only when the pH of the medium is adjusted to 6
or below. In this case the membrane of the virus fuses with the plasma membrane and the
nucleocapsid is introduced into the cytoplasm (White et al., 1980).
In this paper we have studied the effect of five lysosomotropic weak bases: chloroquine,
t Present address: Yale University School of Medicine, 333 Cedar Street, New Haven, Connecticut 06510,
U.S.A.
0022 1317/82/0000-4648 $02.00 © 1982 SGM