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Division of Medical Microbiology, Faculty of Health Sciences, Linköping University, Linköping, Sweden
In addition to direct bactericidal activities, such as phagocytosis
and generation of reactive oxygen species (ROS), neutrophils can
regulate the inflammatory response by undergoing apoptosis. We found
that infection of human neutrophils with Mycobacterium
tuberculosis (Mtb) induced rapid cell death displaying the
characteristic features of apoptosis such as morphologic changes,
phosphatidylserine exposure, and DNA fragmentation. Both a virulent
(H37Rv) and an attenuated (H37Ra) strain of Mtb were equally effective
in inducing apoptosis. Pretreatment of neutrophils with antioxidants or
an inhibitor of NADPH oxidase markedly blocked Mtb-induced apoptosis
but did not affect spontaneous apoptosis. Activation of caspase-3 was
evident in neutrophils undergoing spontaneous apoptosis, but it was
markedly augmented and accelerated during Mtb-induced apoptosis. The
Mtb-induced apoptosis was associated with a speedy and transient
increase in expression of Bax protein, a proapoptotic member of the
Bcl-2 family, and a more prominent reduction in expression of the
antiapoptotic protein Bcl-xL. Pretreatment with an
inhibitor of NADPH oxidase distinctly suppressed the Mtb-stimulated
activation of caspase-3 and alteration of Bax/Bcl-xL
expression in neutrophils. These results indicate that infection with
Mtb causes ROS-dependent alteration of Bax/Bcl-xL
expression and activation of caspase-3, and thereby induces apoptosis
in human neutrophils. Moreover, we found that phagocytosis of
Mtb-induced apoptotic neutrophils markedly increased the production of
proinflammatory cytokine TNF-
by human macrophages. Therefore, the
ROS-dependent apoptosis in Mtb-stimulated neutrophils may represent an
important host defense mechanism aimed at selective removal of infected
cells at the inflamed site, which in turn aids the functional
activities of local macrophages.
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