Combinatorial Chemistry & High Throughput Screening, 2005, 8, 81-88 81
The New Permeability Pathways: Targets and Selective Routes for the
Development of New Antimalarial Agents
Henry M. Staines*
,1
, J. Clive Ellory
1
and Kelly Chibale
2
1
University Laboratory of Physiology, Parks Road, Oxford OX1 3PT, UK
2
Department of Chemistry, University of Cape Town, Rondebosch 7701, South Africa
Abstract: The malaria parasite, Plasmodium falciparum, spends part of its complex life cycle within the red
blood cells of a human host. During this time, the parasite alters the permeability of the red blood cell’s plasma
membrane to allow the uptake of nutrients, the removal of “waste” and volume and ion regulation of the
infected cell. The increased permeability is due to the induction of new permeability pathways (NPP), which are
obvious chemotherapeutic antimalarial targets and/or selective routes for drugs, which target the internal
parasite. This review covers our present understanding of the NPP, the methods used to screen for putative
inhibitors of the NPP, the current repertoire of NPP inhibitors and the problems that need to be addressed to
realise the potential of the NPP as antimalarial targets. In addition, the review will cover the use of the NPP as
specific drug delivery routes.
Keywords: Malaria, Channel, Anion, Antimalarial.
1. INTRODUCTION external medium for normal growth [4]. These must first
cross the RBC plasma membrane before they are accessible
to the parasite. In the case of glucose (the parasite’s primary
energy source), the native glucose transporter (GLUT1) is
capable of supplying the parasite’s requirements [5].
However, there is no native transport pathway for the
vitamin, pantothenate (required by the parasite for the
production of co-enzyme A). As the NPP are permeable to
pantothenate [6], they are thought to aid nutrient uptake.
As part of its life cycle, the malaria parasite, Plasmodium
falciparum, invades the red blood cells (RBCs) of its human
host. In so doing, the parasite passes through the host
plasma membrane and, at the same time, surrounds its own
plasma membrane with a second membrane called the
parasitophorous vacuole membrane (PVM). Within the
RBC, P. falciparum takes approximately 48 hours to
mature, divide and release up to 32 new parasites (at a
metabolic rate far in excess of that of the host RBC). Secondly, to produce energy (in the form of ATP), the
parasite utilises glycolysis primarily. The major by-product
of this process is lactate and this is potentially toxic to the
parasite if left to accumulate. Besides a small degree of
diffusion of the protonated from, the RBC has two native
transport pathways for the removal of lactate (the anion
exchanger, Band 3, and the monocarboxylate transporter).
However, it has been calculated that these pathways are not
capable of clearing parasite-derived lactate and so a third
route (i.e. the NPP) is required for metabolite removal [7,
8].
Approximately 15 hours into this asexual reproductive
phase, the permeability of the host RBC’s plasma membrane
increases to a range of relatively low molecular weight
solutes including sugars, amino acids, nucleosides and
inorganic ions. This occurs due to the induction of new
permeability pathways (NPP) by the internal parasite. It has
yet to be clarified to which compartment the NPP lead. A
simple sequential model of solute trafficking, as suggested
by Desai [1], would predict that the NPP lead to the RBC
cytosol but other models have been hypothesised including
the localisation of the NPP to points of contact between the
host plasma membrane and the, so called, tubovesicular
membrane (a network of tubular membranes extending from
the PVM) [2]. The latter would predict that the NPP lead to
the compartment between the PVM and the parasite plasma
membrane. The evidence behind these models and more
contentious models are discussed in greater detail by Kirk
[3].
Thirdly, the parasite obtains some of the amino acids it
requires for protein production from digestion of the host
RBC’s cytosol (predominantly haemoglobin). Only a
relatively small proportion of the amino acids produced by
this process are used by the parasite [9]. If left to
accumulate, an amino acid concentration gradient would
form, which would draw water into the infected cell and
swell it (ultimately lysing the cell before the parasite has
divided). The NPP have, therefore, been proposed to aid
amino acid release and provide the parasite with a
mechanism for regulating the volume of the infected RBC
[10].
1.1. Why Induce the NPP?
Four reasons have been postulated for why the parasite
induces the NPP. Firstly, the parasite has an essential
requirement for the presence of several nutrients in the
Finally, a RBC maintains a low Na
+
concentration
within its cytosol compared with the external milieu. This
inward Na
+
gradient can be used to facilitate the transport of
solutes, against their own concentration gradients, across the
cell membrane (known as secondary active transport due to
the need for a primary active transport process to produce the
*Address correspondence to this author at the University Laboratory of
Physiology, Parks Road, Oxford OX1 3PT, UK; Tel: ++44 1865 285828;
Fax: ++44 1865 272469; E-mail: henry.staines@physiol.ox.ac.uk
1386-2073/05 $50.00+.00 © 2005 Bentham Science Publishers Ltd.