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The Journal of Nutrition Vol. 128 No. 1 January 1998,
pp. 97-105
Laboratoire d'Etude du Métabolisme Azoté, INRA Clermont-Ferrand Theix, 63122 Saint Genès Champanelle, France and * Clintec Technologie, 92352 Le Plessis Robinson, France
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ABSTRACT |
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Abstract
Introduction
Methods
Results
Discussion
References
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In vivo cysteine metabolism during the inflammatory state has been studied minimally. We investigated cysteine metabolism (i.e. taurine, sulfate and glutathione formation) using a single dose of [35S] cysteine in septic rats that had been injected with live Escherichia coli into the tail vein and in control, pair-fed rats. Cysteine metabolites were separated by ion exchange chromatography, and radioactivity was counted in the different fractions. Radioactivity incorporated in tissue proteins was also measured after protein precipitation. [35S]Sulfate production was significantly lower in septic rats than in pair-fed rats. [35S]Taurine contents were significantly lower only in kidneys, spleen and gastrointestinal tract of septic rats. The higher production of [35S] taurine in the livers (the major site of taurine production) of septic rats could have a protective effect against oxidation. Glutathione concentrations were also significantly greater in liver, spleen, kidneys and gastrocnemius muscle of septic rats, presumably in order to combat oxidative stress induced by sepsis. [35S]Cysteine incorporation in glutathione was significantly higher in spleen and kidneys but not in liver of septic rats compared to pair-fed rats. This could be explained by the fact that, in liver, a greater amount of labeled glutathione had been utilized for host defense, or by a high level in glutathione turnover. Finally, [35S]cysteine incorporation into protein, in septic rats, was significantly greater than in pair-fed rats in spleen, lung and particulary in whole plasma proteins other than albumin, which mainly represent the acute-phase proteins. These data suggest an increased requirement for cysteine during sepsis in rats.
KEY WORDS: cysteine · glutathione · rats · sulfate · taurine
Metabolic alterations observed in critically ill patients and in septic animals are characterized by a marked loss of weight, an acute-phase protein response, muscle protein wasting and an important nitrogen loss (Ash et al. 1989, Breuillé et al. 1991 Preferential retention of sulfur amino acids, however, occurs during an inflammatory response. Following fracture and burns, urinary nitrogen excretion is enhanced to a greater extent than is sulfur excretion (Larson et al. 1982 One of the major metabolic uses of cysteine is glutathione synthesis. Glutathione (L-glutamyl-L-cysteinyl-glycine) is an important cellular reductant involved in detoxification of reactive oxygen species (Meister and Anderson 1983 This study was designed to investigate cysteine metabolism in septic rats. Cysteine catabolism was studied after an injection of L-[35S]cysteine by measuring in various tissues the formation of [35S]sulfates, which are the end products of cysteine degradation. To explore cysteine utilization, the formation of [35S]taurine and glutathione concentrations as de novo-synthesized [35S]glutathione were determined in various tissues. Incorporation of [35S]cysteine in tissue proteins was also measured.
Animals.
All procedures were performed according to current legislation on animal experimentation in France. Fifteen male Sprague Dawley rats, 270-290 g body weight, were obtained from Iffa-Credo (Lyon France). They were maintained in individual cages at 22°C with a 12-h light:dark cycle (lights on at 0700 h). During a 6-d period of acclimatization, all rats had free access to water and to a semiliquid diet containing the following (in g/kg diet): water, 450; herring flour, 80.5; wheat starch, 367.2; agar-agar, 17.5; corn oil, 10; peanut oil, 25.8; CaHPO4, 32; NaCl, 3.1; K2CO3, 1.2; MgCl2, 2.6; and commercial vitamin mixture,5 10; also containing trace elements including the following (in mg/kg diet): MnCO3, 170; CuSO4·5H2O, 80; ZnSO4·7H2O, 26; Al2(SO4)3, K2SO4·24H2O, 144; NaF, 22; KI, 0.5; CoCO3, 0.4; SeO2, 0.2. Thus, food protein concentration was 12 g/100 g dry matter. Food consumption was recorded daily by measuring the amounts of dry matter offered and left.
Experimental design.
At the end of the acclimatization period, rats weighed about 300 g. They were randomly assigned to two groups. Between 1400 and 1500 h, live Escherichia coli (7 × 108 bacteria/rat) were injected into the lateral tail vein of nine rats as described previously (Voisin et al. 1996
Tissue analyses.
The gastrocnemius muscle, liver, spleen, lungs, heart, kidneys and gastrointestinal tract (GIT)6 were quickly excised. Tissues were washed in cold serum, wiped, weighed and frozen in liquid nitrogen. Lungs, heart and GIT were stored at Glutathione determination.
For total glutathione measurement, frozen powdered tissues were homogenized in a solution containing 0.2 mol perchloric acid and 5 mmol EDTA per L. The homogenate was then centrifuged for 20 min at 8000 × g, and the supernatant was assayed for GSH + GSSG content using a standard enzymatic recycling procedure as described by Robinson et al. (1992) Expression of results and statistical methods.
In the soluble fraction and in the glutathione fraction, results are expressed as Bq/kBq injected. In the insoluble fration, results are expressed as Bq/MBq injected.
Rat body and tissue weights.
Infection induced an acute body weight loss, and the rats lost 40 g in two days (Fig. 2). This loss was significantly higher than in pair-fed rats, which lost only 30 g.
Distribution of radioactivity in the soluble fraction.
Radioactivity was abundant in liver and kidneys (Table 2). The recovery of radioactivity (percentage of the injected dose) in the soluble fraction of kidneys, GIT, lungs, heart and gastrocnemius, did not differ among groups. In contrast, total radioactivity was greater in liver (+75%) and spleen (+147%) of infected rats compared to pair-fed rats.
Effect of infection on [35S] repartition in the soluble fractions of tissues.
The amount of radioactivity (Bq/g) found in the taurine fraction of heart, lungs, and gastrocnemius did not differ between the pair-fed group and the septic group (Table 3). In contrast, in spleen, kidneys and GIT, the amount of radioactivity found in taurine was lower in septic rats than in pair-fed rats. In liver, there was significantly more radioactivity in the taurine fraction of septic rats than in the taurine fraction of pair-fed rats. When expressed as the percentage of total soluble radioactivity (Table 4), the results were similar to those in Table 3.
Tissue glutathione.
The concentrations of total glutathione (reduced and oxidized) were significantly higher in infected rats than in pair-fed rats in most tissues studied: liver (7.16 ± 1.14 vs. 3.93 ± 1.29 µmol/g); spleen (3.28 ± 0.16 vs. 2.29 ± 0.24 µmol/g); kidneys (2.92 ± 0.92 vs. 2.01 ± 0.25 µmol/g); gastrocnemius muscle (1.07 ± 0.11 vs. 0.70 ±0.09 µmol/g) (Fig. 3). This resulted in a higher amount of total glutathione in liver (+146%), in spleen (+177%), in kidneys (+44%) and in gastrocnemius (+35%, despite an 11% weight loss) of infected rats compared to pair-fed rats. In contrast, GSH concentration in GIT was significantly lower in septic than in pair-fed rats (1.64 ± 0.32 vs. 2.26 ± 0.3 µmol/g; Fig 3).
Distribution of radioactivity in tissue proteins.
Incorporation of [35S]cysteine in kidneys, heart and GIT proteins was not different between septic and pair-fed rats (Table 6). In spleen, lung and plasma proteins (without albumin), the incorporated radioactivity was significantly greater in septic than in pair-fed rats. Radioactivity incorporated in liver and gastrocnemius proteins and in albumin was significantly less in septic than in pair-fed rats.
In vivo cysteine metabolism, the formation of taurine, sulfates and glutathione, was investigated in various tissues of septic and control, pair-fed rats. Rats were given a single injection of [35S]cysteine, and the appearance of radioactivity as cysteine metabolites was determined in various tissues one hour after the injection. Concentrations of cysteine metabolites in tissues were not measured, so we could not calculate specific radioactivity or metabolite flux. Further studies are needed to confirm the interpretation of our results. Furthermore, radioactivity found in one tissue may not only reflect cysteine metabolism of that tissue; indeed, once cysteine metabolites are formed in one tissue, they can be transported via the blood to other tissues. Thus our results probably reflect both cysteine metabolism and cysteine metabolite exchange between tissues. However, in spite of this limitation, these results demonstrate that cysteine metabolism was modified during sepsis. Cysteine catabolism was lower, and cysteine utilization for taurine formation and GSH synthesis was higher in septic rats than in pair-fed rats.
The authors thank M. Sallas and C. Lafarge for animal care and D. Bonin and H. Lafarge for literature management.
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
, Jepson et al. 1986, Long et al. 1977). The negative nitrogen balance occurring in response to sepsis is greater than can be accounted for by anorexia. Once specific amino acid requirements have been met by muscle protein degradation, the excess amino acids are catabolized, which results in nitrogen loss.
). A reduction in the excretion of urinary inorganic sulfate has been described following tumor necrosis factor injection in rats (Hunter et al. 1993). Grimble et al. (1992) suggested that cysteine plays a key role in the amino acid economy of the body under inflammatory conditions. In septic rats, we have demonstrated that whole body content of cysteine + cystine is significantly increased, and whole body cysteine catabolism is dramatically decreased compared to pair-fed rats (Breuillé et al. 1996). That study suggested that specific perturbations of cysteine metabolism occur during sepsis. Although cysteine metabolism has been studied in vitro (Coloso et al. 1990, Coloso and Stipanuk 1989, Ensunsa et al. 1993, Stipanuk et al. 1990) and in vivo (Garcia and Stipanuk 1992, Weinstein et al. 1988) there is still little information about in vivo cysteine catabolism during inflammatory states.
). Previous studies have shown that glutathione concentration was increased in livers of septic rats compared to pair-fed rats (Breuillé et al. 1994a). The increase in glutathione concentration observed in livers of septic rats may protect against oxidative damage induced by sepsis (Ogilvie et al. 1991). Glutathione production is regulated by the availability of cysteine (Reed and Orrenius 1977, Stipanuk et al. 1992, Tateishi et al. 1974, Thor et al. 1979). Therefore the lower cysteine catabolism observed during sepsis (Breuillé et al. 1996) could be due to an increased utilization of this amino acid for glutathione synthesis. Furthermore, protein synthesis in liver and in the whole body is greater in septic rats than in pair-fed rats (Breuillé et al. 1994b). Although newly synthesized proteins are not especially rich in cysteine, the greater protein synthesis observed in septic rats could also contribute to an increased utilization of cysteine during sepsis.
MATERIALS AND METHODS
Abstract
Introduction
Methods
Results
Discussion
References
), and six rats were likewise injected with saline. There was no mortality in the infected group.
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Fig 1.
Food consumption of septic rats before and during the infection. Food consumption was recorded daily by measuring the amounts of dry matter offered and left before infection (days 
2, 1) and during infection (days 0, 1, 2).Values are means ± SD, n = 9. *Significantly different from day 1, P < 0.05.
20°C. Gastrocnemius, kidneys, spleen and liver were stored at 80°C. Tissue [35S] distribution in cysteine degradation end products (taurine and sulfates) was measured in septic and pair-fed rats. Total glutathione [i.e. reduced glutathione (GSH) plus oxidized glutathione (GSSG)] concentration was measured in gastrocnemius, kidneys, spleen and liver.
-mercaptoethanol/L. The acid-soluble fraction containing free amino acids was separated from the protein precipitate by centrifugation (20 min, 8000 × g). The soluble fraction was then chromatographed on Dowex 50X8 and Dowex 1X2 columns for separation of different [35S]-containing fractions, as described by Tanaka et al. (1990). The assembled columns were washed with acetic acid solution (0.1 mol/L); the effluent was the taurine fraction. After washing the columns they were disassembled, and then the Dowex 50X8 column was eluted with ammonia (3 mol/L); the eluate was the amino acid fraction (containing cysteine, cystine, GSH and GSSG). The Dowex 1X2 column was eluted with HCl (2 mol/L); the eluate was the acidic fraction (containing sulfates). The radioactivity in each fraction was measured using a liquid scintillation counter (Betamatic IV, Kontron).
by the colorimetric reaction with bicinchoninic acid. Radioactivity incorporated into proteins was also measured in weighed aliquots using a liquid scintillation counter (Betamatic IV, Kontron).
and modified by Cayol et al. (1995). Blue-Sepharose columns were equilibrated with a pH 7.0 buffer solution of 0.05 mol Tris-HCl and 0.1 mol KCl per L, then a 0.5-mL sample of plasma was applied. The column was washed with 20 mL of the same buffer solution adjusted to pH 7.4, until the absorbance at 280 nm return to baseline; the effluent was the fraction containing most of the positive acute-phase proteins. The bound albumin was eluted with 20 mL of pH 7.4 buffer of 0.05 mol Tris-HCl and 1.5 mol KCl per L; the eluate contained the albumin fraction. Proteins contained in the effluent fraction were precipitated with trichloracetic acid, 0.6 mol/L. The precipitate was washed twice to remove free amino acids. The radioactivity in each protein fraction was measured after solubilization in NaOH, as described above.
. In this procedure, GSH is oxidized by 5,5
-dithio-bis 2-nitrobenzoic acid to form glutathione disulfide and 5-thio-2-nitrobenzoic acid. Glutathione disulfide is then reduced back to GSH in a reaction catalyzed by GSSG reductase in the presence of NADPH. Thus, a cycle between GSH and GSSG is achieved that is linked to 5-thio-2-nitrobenzoic acid production. The rate of 5-thio-2-nitrobenzoic acid formation depends on the original sample concentration of GSH and GSSG and can be spectrophotometrically monitored at 412 nm. A standard curve generated with a known amount of GSH was used to derive the original specimen concentration of total GSH.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
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Fig 2.
Body weights of septic and pair-fed rats. Values are means ± SD. Septic rats n = 9; pair-fed rats n = 6. *Significantly different from pair-fed rats, P < 0.05. 
Significantly different from day 0, P < 0.05.
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Table 1.
Tissue weights of pair-fed and septic rats1,2
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Table 2.
Tissue relative weights and incorporation of radioactivity in the tissue soluble fraction of pair-fed and septic rats1,2,3
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Table 3.
Distribution of radioactivity in the anionic, taurine and cationic fractions in tissues of pair-fed and septic rats1,2
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Table 4.
Distribution of radioactivity in the anionic, taurine and cationic fraction in tissues of pair-fed and septic rats1,2
46%), kidneys (73%), spleen (35%), lungs (23%) and heart (28%) (Table 4).
). The weight of the gastrocnemius muscle was 11% lower in septic rats (Table 1). Similar atrophy was observed in other muscles with the same or different fiber composition including soleus, tibialis and extensor digitorum longus (Voisin et al. 1996). We have assumed that this degree of atrophy can be extrapolated to the whole skeletal muscle. We have estimated that whole skeletal muscle represented 40% of body weight in septic rats. [35S]Taurine was significantly greater in septic rats compared to control rats. In the whole body without liver, [35S]taurine levels were significantly lower in septic rats compared to pair-fed rats. In contrast, the levels of [35S]sulfates were dramatically lower in septic rats than in pair-fed ones. Radioactivity incorporated in the cationic fraction containing cysteine, cystine and glutathione was dramatically greater in septic rats than in pair-fed rats (Table 5).
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Table 5.
Distribution of radioactivity in the anionic, taurine and cationic fractions in whole tissues of pair-fed and septic rats1,2
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Fig 3.
Total glutathione concentrations in liver, spleen, kidneys, gastrocnemius and gastrointestinal tract (GIT) of septic and pair-fed rats. Total glutathione was determined enzymatically. Data are means ± SD. Septic rats n = 9; pair-fed rats n = 6. *Significantly different from pair-fed rats, P < 0.05.
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Fig 4.
Incorporation of radioactivity in reduced glutathionone (GSH) in liver, kidneys and spleen of septic and pair-fed rats. Reduced glutathione was separated by HPLC, and radioactivity incorporated in each fraction was counted in a liquid scintillation counter. Data are means ± SD and are expressed as Bq/(g tissue·kBq injected). Septic rats n = 9; pair-fed rats n = 6. *Significantly different from pair-fed rats, P < 0.05.
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Table 6.
Incorporation of radioactivity in tissue proteins of pair-fed
and septic rats1,2
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
). The large amount of radioactivity incorporated into the soluble fraction of liver, kidneys and GIT of pair-fed rats (Table 2) are consistent with Garcia's results (1992). In vitro and in vivo studies have demonstrated that the liver removes cysteine from plasma (Garcia and Stipanuk 1992) and releases taurine and sulfates formed during cysteine catabolism (Coloso et al. 1990). In contrast, cysteine catabolism in kidney cells and in enterocytes yield sulfates without taurine (Coloso and Stipanuk 1989, Stipanuk et al. 1990). In our study, taurine found in kidneys (Tables 3 and 4) may result from plasma taurine uptake (Garcia and Stipanuk 1992). In the GIT, the presence of radioactive taurine may be explained by deconjugation of bile acids and reabsorption of taurine. The large amount of radioactivity associated with sulfates in kidneys and GIT (Tables 3 and 4) may also be explained by both cysteine catabolism and sulfate removal from plasma (Garcia and Stipanuk 1992). In rat muscle, there is no uptake of taurine or sulfates from plasma (Garcia and Stipanuk 1992). Thus, cysteine catabolites present in muscle cells are formed in situ. Sulfate and taurine production in the muscle of pair-fed rats was consistent with the results of Ensusa et al. (1993), which demonstrated that, in rat hindquarters, 80% of cysteine catabolism occurred mainly by sulfate production. To our knowledge, cysteine metabolism in spleen, lung and heart has never been studied. From our results, it seems that cysteine catabolism occurs mainly by the sulfate pathway in heart and spleen, and by the two metabolic routes in lungs.
).
) and may play an important function as a modulator of calcium flux (Hayes 1985, Huxtable et al. 1980). A constant level of taurine in this tissue during infection could be essential for stimulating myocardial perfomance that is decreased during sepsis (Abel 1989). In lungs, Banks et al. (1992) have shown that taurine offers protection against oxidative damage in animal models of lung inflammation. Thus, the maintenance of taurine concentration in lungs would be essential to fight oxidative damage that occurs during sepsis (Bersten and Sibbald 1989). In contrast, the amount of labeled taurine measured in spleen, GIT and kidneys was less in septic rats than in pair-fed rats, probably due to decreased taurine uptake from plasma, since there is no taurine production in these tissues (Coloso and Stipanuk 1989, Stipanuk et al. 1990). In liver, the level of [35S]taurine was higher in the infected than in the pair-fed rats. Taurine produced in liver, which is the major organ for its synthesis (Coloso et al. 1990), could be excreted into blood (Garcia and Stipanuk 1992) and removed by other tissues such as the lungs. Furthermore, taurine may also be removed from plasma by lymphocytes, in which >60% of the free amino acids pool is taurine (Gaull 1986). The phagocyte antimicrobial action depends on H2O2 production by the peroxidosis oxidation system. Hydrogen peroxide can react with Cl
to form hypochlorous acid, which is a powerful oxidant. Taurine can react with hypochlorous acid to form taurine chloramine, which is less reactive than hypochlorous acid (Wright et al. 1986). Taurine could also play an antioxidant role (Wright et al. 1986) in these cells. It is then possible that the activation of immune cells during infection leads to an increased requirement for taurine and therefore for cysteine.
, which showed that GSH synthesis was increased in erythrocytes of pigs after inflammation was induced by turpentine injection. The amount of GSH in the liver of the infected rats was higher than in the pair-fed rats. This would suggest that GSH is more actively synthesized in those rats. This was not clearly confirmed by a much higher radioactivity in liver GSH one hour after [35S]cysteine administration. We may conclude that liver GSH was not extensively exported in infected rats. However, the kinetics of GSH labeling may have been different in the two groups. Higher GSH synthesis and exportation rates would result in an earlier maximum and a more rapid decrease of radioactivity as hepatic GSH (Atkins 1969). It is difficult to make definitive conclusions; however, the higher levels of radioactivity in the cationic fractions of the other tissues from infected rats suggest that part of this radioactivity corresponded to an uptake of GSH synthesized in liver. Furthermore, the increased GSH utilization observed during an inflammatory stress (Jahoor et al. 1995) could also lead to a greater loss of de novo-synthesized GSH in livers of septic rats.
, 1984). In septic rats, in spite of anorexia, GSH concentrations were dramatically greater in liver, spleen, kidneys and gastrocnemius when compared to pair-fed rats and even to control rats that had free access to food [liver, 5.8 ± 1.1 µmol/g (Breuillé et al. 1994a); kidneys, 2.4 ± 0.2 µmol/g; spleen, 2.8 ± 0.2 µmol/g; muscle, 0.9 ± 0.1 µmol/g.] One of the multiple functions of GSH is as an antioxidant (Meister 1983). The higher GSH concentration observed in septic rats 2 d postinfection could then be explained by an increase in the requirement for antioxidant to fight the oxidative stress induced by sepsis (Peralta et al. 1993, Sakaguchi et al. 1981). However, as observed in pigs subjected to turpentine-elicited inflammation (Jahoor et al. 1995), we observed a lower concentration of GSH in GIT of septic rats. This could be a consequence of decreased GSH synthesis rate or of increased GSH utilization. GSH is essential for the protection of GIT integrity and for maintenance of normal GIT function (Vincenzini et al. 1991). The decrease in GSH concentration observed in the GIT of septic rats could then be a major cause of lesions, like the described presence of abnormally swollen and distorted mitochondria throughout the cytoplasm in GIT of critically ill rats (Yoshida et al. 1992).
) and a significant decrease in muscle protein synthesis (Breuillé et al. 1994b). Liver protein synthesis was also increased in rats two days after an injection of live E. coli. This synthesis represents about one-third of whole body protein synthesis compared to 15% in control rats (Breuillé et al. 1994b). However, our results failed to show greater incorporation of [35S]cysteine in liver proteins. The liver synthesizes both exported and nonexported proteins. Since the secretion time of exported proteins is ~20 min, our measurement, made one hour after the injection of cysteine, would not take these proteins into account. However, the incorporation of labeled cysteine was 100% greater in whole plasma proteins other than albumin (mainly positive acute-phase proteins) and was significantly lower in albumin (negative acute-phase proteins) in septic rats than in pair-fed rats. Sepsis induces a dramatic increase in acute-phase protein concentration in plasma. In our model, orosomucoid is increased more than 50 times and fibrinogen is increased twofold 2 d after infection (Voisin et al. 1996) probably due to increased synthesis. Cysteine represents 1.5% of total amino acids in alpha-1-acid glycoprotein (Ricca and Taylor 1981) and 2.3% in fibrinogen (Blombaeck et al. 1965) of rats, whereas cysteine represents about 1.3% of total amino acids in muscle proteins (Reeds et al. 1994). Although acute-phase proteins are not rich in cysteine, the increase of these proteins and of proteins in various tissues results in an additional need for cysteine.
). This enhanced proteolysis supplies more cysteine, thus avoiding a decrease in cysteine concentration. Cysteine can also be synthesized de novo from methionine transsulfuration. If the cysteine requirement is increased, one could expect a higher rate of methionine transsulfuration, inducing lower tissue and plasma methionine concentrations. However, plasma and liver methionine concentrations were similar in septic and pair-fed rats (43 ± 5 vs. 48 ± 5 mmol/L and 83 ± 20 vs. 84 ± 20 µmol/g, respectivley; unpublished data). This could mean that methionine transsulfuration is impaired during sepsis or that methionine supplied by muscle proteolysis is sufficient to meet the methionine requirement. In the same way, plasma glycine concentrations were not different in septic and pair-fed rats (342 ± 61 vs. 335 ± 51 mmol/L; unpublished data) suggesting also that the requirement for glycine in glutathione synthesis is met during the acute phase of sepsis in rats.
ACKNOWLEDGMENTS
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FOOTNOTES |
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-tocopheryl acetate, 12.5; cholecalciferol, 0.015; menadione, 0.15; ascorbic acid, 80; myo-inositol, 15; choline HCl, 136; and p-aminobenzoic acid, 5. Purchased from UAR (Villemoisson, Epinay-sur-Orge, France).
Manuscript received 16 April 1997. Initial reviews completed 16 May 1997. Revision accepted 18 August 1997.
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Abstract
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Methods
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References
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