50 © 2009 The Authors
Journal compilation © 2009 Blackwell Publishing Ltd
Parasite Immunology , 2009, 31, 50–56 DOI: 10.1111/j.1365-3024.2008.001073.x
Blackwell Publishing Ltd
Effect of Nippostrongylus brasiliensis L3 ES on inflammatory mediator
gene transcription in lipopolysaccharide lung inflammation
M. ZHAO, D. M. BROWN, J. MACCALLUM & L. PROUDFOOT
School of Life Sciences, Napier University, Edinburgh, UK
SUMMARY
The anti-inflammatory properties of parasitic helminths have
been largely linked to their excretory–secretory (ES) products.
Some studies have noted a lack of TNF-α production and limited
recruitment of neutrophils into the lungs after Nippostrongylus
brasiliensis infection. We previously reported that instillation
of ES from L3 larvae of N. brasiliensis to the lungs could
inhibit the recruitment of neutrophils on a background of
LPS-induced inflammation. A similar reduction in neutrophil
recruitment was observed in this study. This reduction was
associated with the significant inhibition in gene transcription
of the adhesion molecule, ICAM-1, and the chemokine, MIP-
2 in bronchoalveolar lavage (BAL) cells. The LPS-stimulated
gene transcription of the pro-inflammatory cytokines TNF-α
and IL-1β was also significantly reduced by L3 ES. Inducible
nitric oxide synthase (iNOS) is normally elevated in classically
activated macrophages, however, in this case gene transcrip-
tion of iNOS was inhibited by L3 ES and may suggest a pheno-
type change to anti-inflammatory. The general inhibition of
pro-inflammatory mediators observed in this study suggests
that infective stage L3 larvae excrete and/or secrete inhibitory
products capable of modifying the normally potent LPS
inflammatory response.
Keywords anti-inflammatory, bronchoalveolar lavage (BAL),
chemokines, cytokines, lung, Nippostrongylus brasiliensis
INTRODUCTION
Parasitic nematode infection can cause significant disease in
humans and animals but at the same time has a Th2-like,
anti-inflammatory phenotype which may be of benefit to the
host. Nematode excretory–secretory (ES) products are known
to contain a number of different immunomodulatory
molecules which could interfere with, or modulate, the
inflammatory process (1,2). There has also been interest
in development of parasitic nematodes, or their ES, as
therapeutic agents. The pig whipworm Trichuris suis has
been used in trials to treat inflammatory bowel disease (3)
and an ES product of a filarial nematode has recently
been demonstrated to have dramatic modulatory effects in a
mouse model of rheumatoid arthritis (4) and on mast cell
degranulation (5).
The subject of our study is Nippostrongylus brasiliensis, a
parasitic nematode of the rat, which is widely used as a
model for human parasitic hookworm disease as it follows
a similar migratory route through the lungs and induces
immunological responses comparable with human infection
(6). The delay in recruitment of inflammatory leucocytes to
the rat lung in our previous study of N. brasiliensis infection
(7) led us to the belief that anti-inflammatory mechanisms
could be active in the parasite ES. This idea was encouraged
by our experiments (8) using ES from L3 larvae (L3 ES) of
N. brasiliensis, which indicated that parasite products could
interfere with neutrophil recruitment to the lung in response
to bacterial lipopolysaccharide (LPS). Neutrophil recruit-
ment to sites of acute inflammation is an important step
in the eradication of invading pathogens such as bacteria,
however, the role of neutrophils in helminth infection
remains unclear.
In the present investigation, we examined the extent of
an anti-inflammatory effect of N. brasiliensis ES in a rat
model of lung inflammation using LPS. LPS is a highly
potent activator of the innate immune response (9) and
its interaction with lung cells will lead to induction of a
succession of inflammatory mediators. Neutrophils interact
with chemokines, cytokines and adhesion molecules for
Correspondence: Dr Lorna Proudfoot, School of Life Sciences,
Napier University, 10 Colinton Road, Edinburgh, EH10 5DT, UK
(e-mail: l.proudfoot@napier.ac.uk).
Received: 22 July 2008
Accepted for publication: 3 October 2008