© 2006 DIPAV-Università degli Studi di Milano 73
Journal compilation © 2006 Blackwell Publishing Ltd
Parasite Immunology , 2007, 29, 73–79 DOI: 10.1111/j.1365-3024.2006.00915.x
Blackwell Publishing Ltd ORIGINAL ARTICLE WSP inhibits PMNs apoptosis
Wolbachia surface protein (WSP) inhibits apoptosis in human
neutrophils
C. BAZZOCCHI, S. COMAZZI, R. SANTONI, C. BANDI, C. GENCHI & M. MORTARINO
Dipartimento di Patologia Animale Igiene e Sanità Pubblica Veterinaria, Sezione di Patologia Generale e Parassitologia, Università di Milano,
Milano, Italy
SUMMARY
Polymorphonuclear cells (PMNs) are essential for the innate
immune response against invading bacteria. At the same time,
modulation of PMNs’ apoptosis or cell death by bacteria has
emerged as a mechanism of pathogenesis. Wolbachia bacteria
are Gram-negative endosymbionts of filarial nematodes and
arthropods, phylogenetically related to the genera Anaplasma,
Ehrlichia and Neorickettsia ( family Anaplasmataceae).
Although several pathogens are known to interfere with
apoptosis, there is only limited information on specific
proteins that modulate this phenomenon. This is the first
evidence for the anti-apoptotic activity of a surface protein of
Wolbachia from filarial nematode parasites (the Wolbachia
surface protein, WSP). The inhibition of apoptosis was
demonstrated on purified human PMNs in vitro by different
methods. TUNEL assay showed that the percentage of dead
cells was reduced after stimulation with WSP; Annexin V-FITC
binding assay confirmed that cell death was due mainly to
apoptosis and not to necrosis. Reduced caspase-3 activity in
stimulated cells also confirmed an inhibition of the apoptotic
process.
Keywords apoptosis, filariasis, immunopathology, PMN,
Wolbachia surface protein
INTRODUCTION
Polymorphonuclear cells (PMNs) are essential in initiation
and execution of the acute inflammatory response and
subsequent resolution of bacterial infection. PMNs are the
first cells that migrate into tissues in response to invading
organisms, and they phagocytose microbial pathogens, trigger-
ing a cytokine network resulting in the development of
inflammatory and specific immune responses. PMNs are
known to have the shortest in vivo half-life among leucocytes
and die rapidly in vitro, showing changes characteristic of
cells undergoing programmed cell death or apoptosis (1).
The exposure of PMNs to agents known to regulate
inflammatory reactions (such as cytokines and bacterial
products) can influence cell survival and the physiological
process of apoptosis (2). Inflammatory mediators delay
apoptosis of PMNs, which contributes to the persistence
of inflammation (3). Furthermore, agonists of toll-like
receptors (TLRs), such as lipopolysaccharide (LPS, TLR4
ligand), peptidoglycan (TLR2 ligand) and CpG motives (TLR9
ligand), are shown to delay the apoptosis of PMNs both in
whole blood and in purified cells (4). Bacterial synthetic
lipopeptides, derived from major constituents of the wall
of diverse bacteria that are implicated in the pathogenesis
of human sepsis, have also recently been shown to delay
apoptosis in human neutrophils, through inhibition of
caspase-3 activity (5).
Wolbachia is a Gram-negative bacterial endosymbiont of
filarial nematodes (6). These parasites infect more than 150
million people in tropical areas and cause diseases of eyes,
skin and the lymphatic system, such as river blindness and
elephantiasis. Wolbachia are abundant in all developmental
stages of filarial nematodes, including the lateral cords of
both sexes and the reproductive apparatus of adult females
(7). Furthermore, the obligatory relationship between
filariae and their abundant endobacteria has been exploited
to develop a novel chemotherapeutic approach using tetra-
cycline derivates that cause developmental block, long-term
worm sterility and adult worm death (8–10).
Correspondence: Dr Michele Mortarino, DIPAV, Sezione di Patologia
Generale e Parassitologia, Università di Milano, Via Celoria 10,
20133 Milano, Italy (e-mail: michele.mortarino@unimi.it).
Received: 15 February 2006
Accepted for publication: 3 August 2006