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and IL-10 Modulate the Induction of Apoptosis by Virulent Mycobacterium tuberculosis in Murine Macrophages1
*
Grupo de Inmunología Celular e Inmunogenética, Laboratorio Central de Investigaciones, Centro de Investigaciones Médicas. Facultad de Medicina, Universidad de Antioquia, Medellín, Colombia;
Laboratoire d’Infectiologie, Centre de Recherche du Centre Hospitalier de l’Université de Québec (Pavillon Centre Hospitalier de l’Université Laval), Université Laval, Ste.-Foy, Québec, Canada; and
Department of Biochemistry, McGill University, Montreal, Québec, Canada
The Bcg/Nramp1 gene controls early resistance and
susceptibility of macrophages to mycobacterial infections. We
previously reported that Mycobacterium tuberculosis-infected
(Mtb) B10R (Bcgr) and B10S
(Bcgs) macrophages
differentially produce nitric oxide (NO-), leading to
macrophage apoptosis. Since TNF-
and IL-10 have opposite effects on
many macrophage functions, we determined the number of cells producing
TNF- and IL-10 in Mtb-infected or purified protein
derivative-stimulated B10R and B10S macrophages lines, and
Nramp1+/+ and
Nramp1-/- peritoneal macrophages and
correlated them with Mtb-mediated apoptosis.
Mtb infection and purified protein derivative treatment
induced more TNF-+Nramp1+/+ and
B10R, and more IL-10+Nramp1-/-
and B10S cells. Treatment with mannosylated lipoarabinomannan, which
rescues macrophages from Mtb-induced apoptosis, augmented
the number of IL-10 B10R+ cells. Anti-TNF- inhibited
apoptosis, diminished NO- production, p53, and caspase 1
activation and increased Bcl-2 expression. In contrast, anti-IL-10
increased caspase 1 activation, p53 expression, and apoptosis, although
there was no increment in NO- production. Murine rTNF-
induced apoptosis in noninfected B10R and B10S macrophages that was
reversed by murine rIL-10 in a dose-dependent manner with concomitant
inhibition of NO- production and caspase 1 activation.
NO- and caspase 1 seem to be independently activated in
that aminoguanidine did not affect caspase 1 activation and the
inhibitor of caspase 1, Tyr-Val-Ala-Asp-acylooxymethylketone, did not
block NO- production; however, both treatments inhibited
apoptosis. These results show that Mtb activates TNF--
and IL-10-dependent opposite signals in the induction of macrophage
apoptosis and suggest that the TNF--IL-10 ratio is controlled by the
Nramp1 background of resistance/susceptibility and may
account for the balance between apoptosis and macrophage
survival.
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