© 2003 Blackwell Publishing Ltd 113
Parasite Immunology , 2003, 25, 113–118
Blackwell Publishing Ltd. ORIGINAL ARTICLE SOCS-1 mice are resistant to malaria
The lack of suppressor of cytokine signalling-1 (SOCS1) protects
mice from the development of cerebral malaria caused by
Plasmodium berghei ANKA
DENISE V. R. BULLEN, DIANA S. HANSEN, MARY-ANNE V. SIOMOS, LOUIS SCHOFIELD, WARREN S. ALEXANDER &
EMANUELA HANDMAN
The Walter & Eliza Hall Institute of Medical Research and Cooperative Research Centre for Cellular Growth Factors, 1G Royal Parade,
Victoria 3050, Australia
Abbreviations : SOCS , suppressor of cytokine signalling
SUMMARY
Cerebral malaria is a severe complication of infection with
Plasmodium berghei ANKA involving the Th1 cytokines
TNF-α and IFN-γ. Suppressor of cytokine signalling-1
(SOCS1) is an important component in the regulatory cas-
cade controlling inflammatory responses and signalling
through IFN-γ. Contrary to the expectation that SOCS1-
deficient mice, in which IFN-γ responses are uncontrolled
and which are more sensitive to IFN-γ, may show heightened
susceptibility, mice lacking SOCS1 were protected from
cerebral malaria. Unlike the controls and despite similar par-
asitaemia, infected SOCS1 null mice showed no inflammation
or haemorrhaging in the brains. Mice lacking SOCS1 exhib-
ited decreased splenic cellularity and a reduced ratio of
CD4 : CD8 lymphocytes, which were maintained during
infection. However, the ratio of IFN-γ to IL-4 mRNA expres-
sion during infection was similar in SOCS1 –/– and control
mice suggesting that a dramatic shift in the ratio of Th1 : Th2
responses does not account for the resistance to disease.
Resistance conferred by the lack of SOCS1 is specific
since the related SOCS2, also implicated in Th1-mediated
responses, did not seem to be involved in the development of
disease. Understanding the mechanism by which SOCS1 defi-
ciency protects mice from cerebral malaria may allow the
manipulation of its activity and alleviate pathology.
Keywords inflammation, cytokines, parasitic protozoan, Th1/
Th2 cells
Abbreviations: SOCS, suppressor of cytokine signalling
INTRODUCTION
Cerebral malaria in the human population is a complication
of Plasmodium falciparum malaria and affects approximately
1% of infected individuals. In mice, P. berghei ANKA infec-
tions lead to development of a cerebral disease with many
similarities to that observed in humans infected with P. fal-
ciparum (1,2). Susceptible mouse strains, such as C57BL/6,
infected with P. berghei ANKA develop neurological symp-
toms with fitting and coma within 6 –10 days of infection,
leading to death in about 90% of mice. These manifestations
of cerebral disease become evident quite early in infection
whereas parasitaemia is relatively low (5–20%) (3,4). This
model has provided several key insights into the mechanisms
underlying cerebral malaria which have subsequently been
confirmed in human disease, including the important roles of
IFN- γ and TNF- α , Th1 lymphocytes and cytokine-induced
changes in the brain microvascular endothelium (2,4–7).
The suppressors of cytokine signalling (SOCS) are a
family of negative regulators involved in the control of intra-
cellular signal transduction in many cell types (8–10). Since
SOCS1 is a negative regulator of IFN- γ signalling (8,11) we
set out to examine the role of SOCS1 in the development
and pathology of cerebral malaria in vivo using mice that
lack the gene for SOCS1. However, SOCS1 –/– mice die
within 3 weeks of birth from an IFN- γ -dependent liver dis-
ease. A recently developed treatment protocol in which
IFN- γ -neutralizing antibody is administered at birth for
7 days only was found to prevent neonatal lethality and
resulted in mice that were healthy for up to 5 weeks of age
(12). We therefore infected antibody-treated SOCS1 –/–
mice and their antibody-treated wild-type (SOCS1 +/+) or
heterozygous (SOCS1 +/–) littermates with P. berghei
ANKA parasites. We found that whereas 90% of SOCS1
+/+ and +/– mice developed cerebral malaria, mice lacking
SOCS1 were resistant.
Correspondence: Dr Emanuela Handman, The Walter & Eliza Hall
Institute of Medical Research, 1G Royal Parade, Victoria 3050,
Australia (e-mail: handman@wehi.edu.au).
Received : 1 July 2002
Accepted for publication: 23 January 2003