TRENDS in Parasitology Vol.17 No.5 May 2001
http://parasites.trends.com 1471-4922/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S0169-4758(00)01862-7
219 Opinion
Falciparum malaria infects several million
individuals and kills nearly a million children in
Africa each year
1
. This situation is expected to worsen
because of the spread of drug-resistant parasites and
insecticide-resistant vectors. Despite important
advances, such as the circumsporozoite protein
(CSP)-based vaccine called RTS,S (Ref. 2), the goal of
a safe and broadly effective malaria vaccine remains
unfulfilled. The parasite’s complex life-cycle offers
several targets for intervention in the human host
and the mosquito vector, and vaccines against
sporozoite, intrahepatic, blood and sexual stages of
the parasite are currently in development
3
. Targeting
intrahepatic parasites for vaccine development has
specific advantages, including the relatively low
parasite burden at this stage of infection, the putative
presentation of antigens by liver cell MHC class I
molecules and an array of potential effector
mechanisms against liver-stage antigens.
Plasmodium falciparum liver-stage antigen-1 (LSA-
1) is expressed specifically in liver-stage parasites
4
,
unlike other identified pre-erythrocytic antigens.
Investigation of its immunological significance is
restricted to human studies because no homologue in
mouse or non-human primate malarias has been
identified. In this article, we discuss the
immunobiology of hepatic stage parasites, evidence
relating immune responses against this stage to
protection, and the rationale for development of liver-
stage vaccines based on LSA-1.
LSA-1 and the biology of liver-stage parasites
Sporozoite invasion occurs by a series of incompletely
characterized molecular interactions that involve
sporozoite antigens such as CSP (Ref. 5) and
thrombospondin-related anonymous protein (TRAP)
6,7
.
CSP and TRAP are carried into the hepatocyte, but are
detected in decreasing amounts as liver-stage
development progresses
8,9
. By contrast, synthesis of
LSA-1 begins soon after sporozoite invasion of the
hepatocyte and increases throughout the liver cycle
8
.
Consequently, LSA-1 might be processed and
presented to the immune system in a way that differs
from that of sporozoite antigens. LSA-1 appears as part
of a flocculent mass within the parasitophorous
vacuole of the hepatocyte and surrounds the
developing merozoite
8,10
(Fig. 1). When the hepatocyte
ruptures, merozoites are released in this flocculent
mass
11
into the liver sinusoid where they invade red
blood cells. LSA-1 is a 200 kDa protein
8
that contains a
central region with 86 copies of a 17 amino acid (aa)
repeat
8,10
, flanked by N- and C-terminal non-repeat
regions containing B and T epitopes
8,12
(Fig. 2). Unlike
many other vaccine candidates, the sequence of LSA-1
is generally conserved across strains
8,13
. This might
suggest a crucial role during liver schizogony, perhaps
protecting the merozoite surface.
Protective immunity targeting the infected hepatocyte
Although the homologue of LSA-1 has not been
identified in rodent parasites, studies in mice have
Pre-erythrocytic
immunity to
Plasmodium
falciparum : the case
for an LSA-1 vaccine
Jonathan D. Kurtis, Michael R. Hollingdale,
Adrian J.F. Luty, David E. Lanar, Urszula Krzych
and Patrick E. Duffy
A vaccine is urgently needed to stem the global resurgence of Plasmodium
falciparum malaria. Vaccines targeting the erythrocytic stage are often viewed
as an anti-disease strategy. By contrast, infection might be completely averted
by a vaccine against the liver stage, a pre-erythrocytic stage during which the
parasite multiplies 10 000-fold w ithin hepatocytes. Sterilizing immunity can be
conferred by inoculating humans with irradiated pre-erythrocytic parasites,
and a recombinant pre-erythrocytic vaccine partially protects humans from
infection. Liver-stage antigen-1, one of a few proteins known to be expressed by
liver-stage parasites, holds particular promise as a vaccine. Studies of naturally
exposed populations have consistently related immune responses against this
antigen to protection.
Jonathan D. Kurtis
David E. Lanar
Urszula Krzych
Patrick E. Duffy*
Walter Reed Army
Institute of Research, Dept
of Immunology, Silver
Spring, MD 20910, USA.
*e-mail: patrick.duffy@
na.amedd.army.mil
Michael R. Hollingdale
Gates Malaria
Programme, London
School of Hygiene and
Tropical Medicine,
London, UK WC1E 7HT.
Adrian J.F. Luty
University of Tübingen,
Dept of Parasitology,
72074 Tübingen,
Germany.
Fig. 1. Electron micrograph showing immunogold localization of
LSA-1. Plasmodium falciparum merozoites developing in a chimpanzee
hepatocyte (H) are identified by their nuclei (N) and rhoptries (R). The
parasitophorous vacuole (PV), enclosed within the vacuolar membrane
(PVM), is filled with flocculent material containing LSA-1. Micrograph
courtesy of Jacques Meis, University of Nijmegen, The Netherlands.
Scale bar = 0.5 μm.