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The production of NO in hemocytes was also shown to be enhanced by opiate receptors
involved in the silencing of the immune response (Stefano et al. 1993). The presence of
opiates (pain killers, anti-diarrheal and antitussive drugs) in municipal effluents could
also impact the immune system in mollusks. The presence of microorganisms however,
could stimulate phagocytosis. This was also revealed in freshwater fish, spottail shiners
Notropis hudsonius
, collected upstream and downstream of the municipal effluent disper-
sion plume from a large city on the Saint Lawrence River, Canada (Ménard et al. 2010).
This study showed that although phagocytosis was stimulated by the presence of bacteria
in the water column, cells from fish located downstream of the plume of a municipal dis-
charge had relatively lower activity.
In field exposures of
E. complanata
, lysozyme activity was not significantly increased in
downstream sites where hemocyte viability was unaffected (Bouchard et al. 2009; Farcy
et al. 2011). In field exposures to municipal effluents, COX activity in hemocytes was not
impaired (Bouchard et al. 2009). COX is involved in the formation of proinflammatory pros-
taglandins in tissues. Interestingly, COX activity was significantly decreased by exposure
to the filtered effluent, indicating an anti-inflammatory effect consistent with the presence
of COX inhibitors, which are more active after the removal of microorganisms (Gagné et al.
2008b). COX expression could be increased by NO in vertebrates (Dokmeci 2004), and this
seems to be corroborated by the significant induction of NO production and COX activity
in the bivalve hemocytes exposed to the effluent. This further suggests that NO produc-
tion is mainly linked to bacterial load to support oxidative burst after phagocytosis rather
than to exposure to xenobiotics. This agrees with a previous study with these freshwater
mussels exposed to urban waste water (Bouchard et al. 2009), and studies in vertebrates
reporting that bacterial infection causes up-regulation of NO production (Wheeler et al.
1997). Recent studies have revealed that vitellogenin, an estrogen-dependent energy-rich
protein reserve in eggs, can also act at the immune system level by killing bacteria through
an interaction with lipopolysaccharide (LPS) and lipoteichoic acid in fish (Zhang et al.
2005; Shi et al. 2006; Li et al. 2009). This was corroborated in freshwater mussels exposed to
municipal effluents where phagocytosis activity better explained the observed changes in
vitellogenin-like proteins in the freshwater mussels (Bouchard et al. 2009).
6.2.6 Conclusions
The immune system in mussels is essentially based on innate processes dominated by
phagocytosis and antimicrobial peptides. The cellular component consists of granulocytes
and hyalinocytes, the former accounting for most of the phagocytic activity. Bivalves also
release a number of cell mediators involved in inflammation, which contributes to oxida-
tive stress. For example, mussels exhibit NO synthase activity, which is involved in the
oxidative burst after phagocytosis (Banakou and Dailianis 2010). The activity of arachi-
donate COX, which is blocked by nonsteroidal anti-inflammatory drugs, was shown to be
induced by exposure to urban effluents, suggesting the involvement of this enzyme during
oxidative stress events (Gagné et al. 2005). Besides this information and several immune
functions reported in other groups of invertebrates such as natural killer (NK) activity,
anticancer responses have never or rarely been signaled in bivalve mollusks. There is also
a gap in knowledge regarding the role of each subpopulation of hemocytes and how the
immune system is regulated. Furthermore, despite evidence of endocrine and nervous sys-
tems' interaction with hemocyte functions (Homo-Delarche and Dardenne 1993), mecha-
nisms of action are still the object of research. Moreover, several results clearly indicate
that factors other than the level of contamination, such as gender difference sensitivity,
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