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Infection and Immunity, September 1998, p. 4068-4072, Vol. 66, No. 9
Laboratoire de Parasitologie,
Received 17 February 1998/Returned for modification 1 April
1998/Accepted 5 June 1998
Reactive nitrogen intermediates were synthesized spontaneously in
cultures of macrophages from Trypanosoma brucei
brucei-infected mice by an inducible nitric oxide (NO) synthase.
This was inhibited by the addition of nitro-L-arginine. In
this paper, we report the kinetics of the fixation of
macrophage-derived NO on bovine serum albumin by using an enzyme-linked
immunosorbent assay. S nitrosylation was confirmed by the Saville
reaction, using mercuric chloride. It is known that reactive oxygen
intermediates (ROI) are also synthesized by stimulated macrophages. The
fact that NO is able to bind cysteine only under aerobic conditions led us to investigate the role of macrophage-derived ROI in the formation of S-nitrosylated proteins by activated macrophages. The
immunoenzymatic signal decreased by 66 and 30% when superoxide
dismutase and catalase, respectively, were added to the culture medium
of macrophages from infected mice. In addition, the decrease in
S-nitrosylated albumin formation correlated with the protection of
extracellular trypanosomes from the cytostatic and cytotoxic activity
of NO. Melatonin, a hydroxyl radical scavenger resulting from the
decomposition of peroxynitrous acid, had no effect. All these data
support the concept that an interaction between NO and ROI promoted the
production of S-nitroso-albumin by activated macrophages
from infected mice.
Nitric oxide (NO) is an important
bioregulatory mediator and possesses many physiological functions. NO
and reactive nitrogen intermediates (RNI) are implicated in
macrophage-derived cytostasis/cytotoxicity against tumor cells
(15) and various intracellular and extracellular pathogens
(1, 21, 22, 54) but also in the mechanisms of
immunosuppression (45). NO circulates in plasma as
S-nitrosothiols (16), mainly
S-nitroso-albumin (49), and previous studies have
elucidated the role of these intermediates in the long-distance effects
of NO. Endothelium-derived relaxing-factor activities (19, 25,
34), inhibition of platelet functions (51), apoptosis (33), and anti-parasite activities of NO (36) are
mediated through nitrosylated albumin. However, the mechanism of the in vivo formation of S-nitrosothiols remains unclear. It has been established that, under anaerobic conditions, NO does not react with
cysteine, glutathione (26, 58), or serum albumin (6, 26). Therefore, RNI species seem to be needed for the
nitrosylation process.
Macrophages from Trypanosoma brucei brucei-infected mice
produce high levels of NO (30). In addition, reactive oxygen
intermediates (ROI), such as superoxide anion
(O2 Mice.
Female Swiss mice (8 to 12 weeks old) were purchased
from Iffa Credo (Saint-Germain-sur-l'Arbresle, France).
Parasites.
The Antat 1.1.E. clone of T. b.
brucei (Institute of Tropical Medicine, Antwerp, Belgium) was used
in all the experiments. Parasites (5 × 103 per mice)
were injected intraperitoneally, and trypanosomes were purified from
the blood of infected mice by chromatography on a DEAE-cellulose
column, as previously described (28).
Cells.
Peritoneal cells from control mice or from
10-day-infected mice were collected after intraperitoneal injection of
Dulbecco's modified Eagle's medium (DMEM; BioWhittaker, Verviers,
Belgium) supplemented with HEPES (20 mM), L-glutamine (2 mM), sodium pyruvate (2 mM), and gentamicin (10 µg/ml). Macrophages
were purified by washing nonadherent cells after a 1-h incubation and
cultured at 37°C in a 5% CO2-enriched atmosphere.
Cocultures of macrophages and trypanosomes.
Macrophages
(106 per ml) from control or T. b.
brucei-infected mice were cocultured with T. b. brucei
(105 per ml) in supplemented Dulbecco modified Eagle medium
containing BSA (4 mg/ml) in 24-well plates (Nunc Inc., Naperville,
Ill.). Superoxide dismutase (SOD) (100 U/ml; Sigma Chemical Co., St. Louis, Mo.), catalase (100 U/ml; Sigma), melatonin (1 or 10 µg/ml), and nitro-L-arginine (L-NA) (1 mM; Sigma) were
added when required. Parasites were counted daily.
Enzyme-linked immunosorbent assay (ELISA).
Macrophages
(106 per ml) were plated in 24-well plates. Cells were
incubated in Hanks balanced salt solution without calcium, magnesium,
or phenol red (Life Technologies, Paisley, Scotland) but supplemented
with BSA (4 mg/ml), L-arginine (1 mM), L-NA
(1 mM), SOD (100 U/ml), and/or catalase (100 U/ml). Enzymes heated at 70°C for 1 h were used as controls. Supernatants were
collected at the indicated times and coated in polystyrene well plates
(Maxisorb; Nunc). Anti-NO acetylated cysteine antibody (Ab) (1/1,000)
(36) or anti-nitrotyrosine Ab (1/100 to 1/1,000)
(Transduction Laboratories, Lexington, Ky.) and horseradish
peroxidase-labeled goat anti-rabbit immunoglobulin (Diagnostic Pasteur,
Paris, France) were used. o-Phenylenediamine was used as the
chromogen. The optical density was measured at 492 nm. Mercuric
chloride (HgCl2; 1 mM) was used in supernatants before
coating to confirm the S nitrosylation (43).
Assay for H2O2 release.
H2O2 release was induced by using phorbol
12-myristate 13-acetate (PMA) in cultures of macrophages (5 × 105 macrophages per well) from control or T. b.
brucei-infected mice. The concentration of
H2O2 in each cell supernatant was measured by
spectrofluorimetry in the presence of scopoletin and peroxidase (41, 53).
Measurement of nitrite production.
In each cell culture
supernatant, the concentration of nitrite
(NO2 Kinetics of the S nitrosylation of BSA by NO from macrophages of
infected mice.
Nitrite accumulation was detected by the Griess
reaction, in culture supernatants of macrophages from T. b.
brucei-infected mice (Table 1).
After a 6-h incubation, the presence of S-nitroso-BSA in
these supernatants was revealed by ELISA. A decrease in NO production
and an inhibition of protein nitrosylation were induced by adding
L-NA to cultures. The addition of HgCl2
abolished the immunoenzyme signal and confirmed the S nitrosylation of
BSA. When supernatants from control macrophages were used with
or without L-NA or HgCl2, nitrite and
S-nitroso-BSA were not detected. In addition, nitrotyrosine
was not detected by ELISA in activated or control macrophage
supernatants at the indicated times (data not shown).
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Murine Macrophages Use Oxygen- and Nitric
Oxide-Dependent Mechanisms To Synthesize S-Nitroso-Albumin
and To Kill Extracellular Trypanosomes
ABSTRACT
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Abstract
Introduction
Materials & Methods
Results
Discussion
References
INTRODUCTION
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Abstract
Introduction
Materials & Methods
Results
Discussion
References
) and
O2-derived hydrogen peroxide
(H2O2), are synthesized as a result of the
oxidative burst (47) by macrophages from T. b.
brucei-infected mice (12) or macrophages exposed to
opsonized T. b. brucei (55). Since NO reacts
with ROI (50), we investigated the interaction of the
L-arginine
NO metabolism with the NADPH oxidase pathway leading to S nitrosylation of bovine serum albumin (BSA), resulting in
the death of extracellular parasites.
MATERIALS AND METHODS
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Abstract
Introduction
Materials & Methods
Results
Discussion
References
), the stable oxidized derivative of NO
(18), was determined spectrophotometrically at 540 nm after
reaction with the Griess reagent as previously described
(14).
RESULTS
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Abstract
Introduction
Materials & Methods
Results
Discussion
References
TABLE 1.
NO2 production and
S-nitroso-BSA formation in supernatants of murine
macrophages after a 6-h incubation
View larger version (23K):
[in a new window]
FIG. 1.
Representative data of the kinetics of
NO2 and S-nitroso-BSA production
by macrophages from T. b. brucei-infected mice. Activated
macrophages were cultured with or without L-NA.
Supernatants were collected at the indicated times.
NO2 and S-nitroso-BSA
concentrations were determined for each sample.
Effect of oxygen-derived species on S-nitroso-BSA formation. After a 4-h incubation, the concentration of S-nitroso-BSA decreased by 66 and 21% in SOD- and catalase-treated macrophage cultures from infected mice, respectively (Fig. 2A), whereas nitrite production was unaffected (Fig. 2B). The two enzymes used together had no synergistic effect with respect to SOD or catalase alone. Heated enzymes, used as controls, had no effect on BSA nitrosylation. Supernatants from control macrophage cultures treated with SOD and/or catalase, with or without L-NA, did not contain S-nitroso-BSA.
|
) or supplemented with SOD (100 U/ml) (
), catalase (100 U/ml)
(
), or SOD plus catalase (
). Each point represents the mean ± standard error of the mean of three experiments, each performed on
two mice. OD, optical density.
H2O2 release by macrophages. The production of H2O2 was observed in the first 4 h of culture when adherent macrophages from infected mice were stimulated with PMA (1.1 ± 0.22 nmol/106 cells/5 min). When these macrophages were cultured for 10 h, a dramatic decrease in H2O2 release was observed (0.14 ± 0.07 nmol/106 cells/5 min). Supernatants from control macrophages or macrophages of T. b. brucei-infected mice not treated with PMA did not contain H2O2 (0.04 ± 0.02 nmol/106 cells/5 min).
Effect of SOD and catalase on trypanosome survival. Previous studies had shown the involvement of nitrosylated albumin in trypanostatic and trypanocidal activity. Observation of the inhibition of S-nitroso-BSA formation in the presence of SOD and catalase led us to test the effect of these two enzymes on trypanosome survival. Parasites were cocultured with macrophages from infected mice. Two days later, a parasite count revealed that the trypanocidal activity of NO was partially inhibited by SOD and catalase (Fig. 3). These two enzymes used together acted more efficiently to protect trypanosomes. Nevertheless, SOD and catalase were not as efficient as L-NA in inhibiting the antiparasite effect. L-NA, SOD, and catalase had no effect on trypanosomes cocultured with control macrophages or with activated macrophages in a BSA-free medium (data not shown).
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Role of melatonin in the protection of trypanosomes. Melatonin, a specific hydroxyl radical (OH) scavenger (32), was used in cocultures of macrophages and trypanosomes. As shown in Fig. 4, trypanosome lysis was not compromised by the addition of melatonin (1 or 10 µg/ml) to supernatants of stimulated macrophages. Melatonin added to control macrophages had no effect on trypanosome growth. These data indicate either that stimulated macrophages did not produce OH or that cell-derived OH in culture were not involved in the cytotostatic and cytotoxic effect of macrophages on extracellular trypanosomes.
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) or with L-NA (
).
A parasite count was performed daily, and the results represent the
mean ± standard deviation of two experiments.
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DISCUSSION |
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Abstract
Introduction
Materials & Methods
Results
Discussion
References
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Our results demonstrate that (i) biosynthesis of S-nitroso-BSA in macrophage supernatants is a rapid and transitory mechanism and (ii) interaction between NO and ROI from activated macrophages is involved in the synthesis of S-nitroso-BSA, which has antiparasite effects.
Previous studies have shown that NO is transported to extracellular targets by proteins such as albumin (46) or hemoglobin (11, 23). These intermediates may release NO to other thiol-containing species by transnitrosylation (25, 39, 44). The first part of our results confirmed that NO products of macrophages from T. b. brucei-infected mice yield S-nitroso-BSA under physiological conditions, in agreement with the spectrophotometric findings of Simon et al. (48). However, the mechanism of NO binding to thiols remains unclear. Biochemical investigations have demonstrated that NO cannot react directly with thiols. S nitrosylation is more probably due to RNI, the reactive products of NO and O2 or ROI (50, 57). However, all these data were obtained in cell-free experiments.
Our kinetic study showed that the S-nitroso-BSA level in
culture supernatants reached its maximum after 6 h of incubation and then decreased. Then, although NO2
accumulated continuously, the S-nitroso-BSA concentration
gradually decreased. Consequently, we have concluded that NO is not a
limiting factor in the S-nitrosylation process. We have also
shown that the in vitro production of
H2O2 by macrophages of parasitized mice was a
transitory phenomenon. This decrease in ROI generation was probably due
to the inhibition of NADPH oxidase by an NO- and/or R-S-NO-dependent
mechanism. Several studies have shown that NO inactivates NADPH
oxidase and consequently impairs ROI production in phagocytes (5,
9, 38). In murine microglial cell cultures, the gamma
interferon-mediated suppression of the oxidative burst was reversed by
an NO synthase inhibitor. The addition of
S-nitroso-N-acetylpenicillamine, an NO-releasing
compound, caused a gradual reduction in the oxidative burst during the
first few hours in culture (27). The NADPH oxidase is
composed of membrane-bound proteins, including cytochrome
b558, that may be gradually altered through the
effects of RNI (4, 40). This time dependence of ROI led us
to speculate that the NADPH oxidase metabolism pathway was involved in
S-nitroso-BSA biosynthesis. Indeed, when SOD or SOD plus
catalase was used in cultures of macrophages from infected mice, the
formation of S-nitrosylated albumin was significantly inhibited, but
catalase alone had less effect than did SOD or SOD plus catalase. This
suggests that macrophage-derived ROI, and more particularly
O2, are involved in the formation of
S-nitroso-BSA. The question raised in these experiments is
how O2 and/or H2O2
interact with NO to favor S nitrosylation.
Peroxynitrite (ONOO) is produced by the reaction of NO
with O2. Its formation in an extracellular
environment leads to protein oxidation and to a decrease in the yield
of nitrosothiols (56), but it is not involved in S
nitrosylation (58). However, our results indicate that NO
and O2 are both involved in the formation of
S-nitroso-BSA. In addition, an immunoenzymatic assay was
unable to detect nitrotyrosine, an ONOO marker
(20), in stimulated macrophage supernatants. The protonated form of ONOO, peroxynitrous acid (ONOOH), may be
indirectly implicated in the S-nitrosylation mechanism since
NO2 is produced by the decomposition of ONOOH (ONOOH OH + NO2). This radical may also be formed by oxidation of NO by H2O2
(H2O2 + NO NO2 + H2O). NO2 reacts with NO to form nitrous
anhydride (N2O3), which decomposes rapidly in
aqueous solutions (N2O3 + H2O 2 NO2 + 2 H+). The molecule
N2O3 has been shown to be a good nitrosylating agent of intracellular thiol molecules (26). All these data led us to hypothesize that S-nitrosylated compounds, such as
S-nitroso-glutathione, formed in the intracellular medium by
an ROI-dependent mechanism could transfer NO to extracellular BSA.
However, RNI, resulting from the interaction between ROI and NO may
also be released by activated macrophages in the extracellular medium
and could be involved in the S nitrosylation.
The effect of ROI on the killing of extracellular trypanosomes was also investigated. ROI may act directly or indirectly, through RNI or nitrosylated albumin, on trypanosome development. Although macrophage-derived ROI mediate the killing of intracellular parasites (17). SOD or catalase had no significant effect on the growth of trypanosomes cocultured with activated macrophages in BSA-free medium. In a medium with BSA, the addition of SOD and/or catalase to macrophage cultures led to a decrease in S-nitroso-BSA formation and an inhibition of the trypanostatic effect of NO. Catalase alone has a similar protective effect on the growth of trypanosomes to that of SOD, although the inhibition of S-nitroso-BSA synthesis by SOD was more marked than that of catalase. Recently, it was shown that NO and R-S-NO cooperate with H2O2 to favor cell lysis (8, 31). Thus, one hypothesis would be that the cytotoxic activity of H2O2 on trypanosomes is potentiated by the presence of S-nitroso-BSA. We also hypothesized that the strong oxidizing species, OH, resulting from the decomposition of HONOO, may also act as an extracellular trypanostatic/trypanocidal agent. However, melatonin, an OH scavenger, had no protective activity. It is thus likely that the main trypanostatic effect is due to S-nitroso-BSA rather than ROI. The fact that interaction between NO and ROI was needed to kill different pathogens was also established (29, 35). We propose that this interaction acts through the formation of S-nitroso-BSA.
Although ONOO has been proposed as a cytotoxic factor
against various pathogens (42, 52), the killing of
Gardia trophozoites was not shown to be affected by this
anion (7). In addition, immunocytochemical testing was
unable to detect nitrotyrosine on the surface of trypanosomes after a
24-h incubation with activated macrophages (data not shown). The
trypanostatic and trypanocidal effects may thus be explained by a
transnitrosylation mechanism rather than ONOO activity,
since R-S-NO was found, in vitro, by using anti-NO-acetylated cysteine
Ab on the surface of trypanosomes cocultured with activated macrophages
(unpublished data). However, it was not possible to distinguish between
S-nitroso-BSA bound on the parasites and S-nitroso proteins
of trypanosomes. The cytostatic and cytotoxic activity of NO was
probably linked to the release of NO from S-nitroso-BSA on
other thiol-containing proteins or Fe-S clusters. The antiproliferative activity of NO is usually attributed to its effect on numerous enzymes,
including protein kinase C (10), ribonucleotide reductase (13), or glyceraldehyde-3-phosphate dehydrogenase (37,
59). The modification of a single highly reactive cysteine led to
a complete inhibition of phosphoenolpyruvate carboxykinase, a key enzyme in the energy metabolism of trypanosomes which lack functional mitochondria (24). Trypanothione reductase, which represents up to 13% of the total soluble proteins and is considered equivalent to glutathione reductase in mammals, has two cysteines which are essential for overall catalysis (2). Moreover, cysteine
residues are conserved in variant surface glycoproteins and non-variant surface glycoprotein surface proteins of trypanosomes (3). All these data show the importance of cysteine integrity for
trypanosomes. Furthermore, trypanosomes are lower eucaryotes, which
constitute simpler but adequate models for studying the effects and
targets of S nitrosylation in mammalian cells.
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ACKNOWLEDGMENTS |
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This work was supported by grants from Le Conseil Regional d'Aquitaine and La Ligue Nationale Contre le Cancer (Comité Pyrénées Atlantique).
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FOOTNOTES |
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* Corresponding author. Mailing address: Laboratoire de Parasitologie, Université de Bordeaux II, Bat 1B, 146 rue Léo Saignat, 33076 Bordeaux Cédex, France. Phone: 33-557-57-17-73. Fax: 33-556-84-66-31. E-mail: Philippe.Vincendeau{at}parasito.u-bordeaux2.fr.
Editor: S. H. E. Kaufmann
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Abstract
Introduction
Materials & Methods
Results
Discussion
References
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Infection and Immunity, September 1998, p. 4068-4072, Vol. 66, No. 9
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