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© 2004 The American Society for Nutritional Sciences J. Nutr. 134:128-131, January 2004

Nutrient Metabolism
Research Communication

Acute Ingestion of Dietary Proteins Improves Post-Exercise Liver Glutathione in Rats in a Dose-Dependent Relationship with their Cysteine Content

François Mariotti1, Karine L. Simbelie, Lina Makarios-Lahham, Jean-François Huneau, Benoit Laplaize*, Daniel Tomé and Patrick C. Even

UMR INRA-INAPG 914 Physiologie de la Nutrition et du Comportement Alimentaire, Institut National Agronomique Paris-Grignon, 75005 Paris, France and * Armor Proteines, 35460 Saint Brice en Coglès, France

1To whom correspondence should be addressed. E-mail: mariotti{at}inapg.inra.fr.


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Dietary sulfur amino acids affect glutathione synthesis, but their acute effect under conditions of oxidative stress is unknown. We assessed the effect of the selective ingestion of {alpha}-lactalbumin, a cysteine-rich protein, on glutathione homeostasis before a single bout of exhaustive exercise. One hour before a 2-h run on a treadmill, untrained rats ingested a meal enriched with either milk protein (TMP), {alpha}-lactalbumin–enriched milk protein ({alpha}-LAC), glucose (GLUC) or milk protein plus 150 mg N-acetyl-L-cysteine, a pharmacologic cysteine donor (NAC). Glutathione status was monitored in the blood and measured postexercise in the liver and heart. A group of fed sedentary rats was used as a control (CON). Blood total glutathione levels declined over time in all test groups. Although postexercise heart glutathione did not differ among groups, postexercise liver glutathione was curvilinearly related to prior cysteine intake (R2 = 0.999, P < 0.05). In {alpha}-LAC rats, liver glutathione was 60–80% higher than in GLUC or CON rats (P < 0.05) and did not differ from that of NAC rats. Cysteine from dietary proteins exhibits a considerable, dose-dependent and acute stimulatory effect on liver glutathione during exercise but does not immediately benefit whole-body glutathione homeostasis, presumably because of an overlap between the postprandial and exercise-related states.

KEY WORDS: • cysteine • {alpha}-lactalbumin • glutathione • exercise • liver

Glutathione ({gamma}-glutamyl-cysteinyl-glycine) is the most abundant low-molecular-weight thiol in mammalian tissues; it is involved in a variety of physiologic functions, including xenobiotic detoxification and antioxidant defense (1). In its antioxidant role, glutathione status (i.e., total glutathione and its redox state) reflects the ability of the body to cope with reactive oxygen/nitrogen species and to limit oxidative stress. An altered glutathione status has repeatedly been reported under conditions of chronic or acute oxidative challenge related to both normal and pathophysiologic states (1,2). In particular, sustained exercise can be regarded as a physiologic model in which prooxidant/antioxidant homeostasis in healthy humans is rapidly challenged by the increased production of reactive oxygen/nitrogen species (3–5). Oxidative stress has been associated with reduced physical performance and muscle fatigue and damage, especially in untrained individuals (3,6,7). In rats, liver glutathione status has been reported to be related to the degree of oxidative stress after a bout of exercise (8,9).

Proglutathione strategies in health and disease rely on pharmacologic approaches (4). However, recent data showed that because sulfur amino acids in the diet provide cysteine, the limiting amino acid for glutathione synthesis, they affect the glutathione synthesis rate and glutathione levels in the body (10–13). The stimulatory effect is less marked with graded proportions of protein in the diet than after the addition of sulfur amino acids to a standard diet (11,12,14), suggesting that this effect may be more closely related to protein quality (amino acid composition) than to protein quantity. Similarly, long-term supplementation with {alpha}-lactalbumin, a cysteine-rich whey protein, improves lymphocyte glutathione and muscle performance in healthy humans (15). Interestingly, one study reported that the selective ingestion of a methionine-supplemented meal was particularly effective in increasing liver glutathione in resting rats (12), whereas postabsorptive exercise was reported to reduce liver glutathione (9). Because the liver is the principal contributor to de novo glutathione synthesis and controls the distribution of glutathione toward the peripheral organs (1,16), we designed a study to address the acute effect of preingesting a cysteine-rich dietary protein on glutathione status after exhaustive exercise, a condition of oxidative stress that challenges glutathione homeostasis.


   MATERIALS AND METHODS
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 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
    Animal and diets. All experimental procedures complied strictly with French guidelines concerning the care and use of laboratory animals. Male Wistar rats (n = 40; Depré, France), weighing 200–220 g, were housed in individual cages kept in a temperature-controlled room (22 ± 1°C) under a 12-h light:dark cycle, with lights on at 0600 h. The experimental diets were prepared under strict laboratory conditions by the Unité de Preparation des Aliments Expérimentaux (Experimental Foods Preparation Unit, Institut National de la Recherche Agronomique-UPAE, Jouy-en-Josas, France).

    Experimental design. The experiment described below was designed for a group of 5 rats, and was repeated 8 times to achieve 7 rats in each group, accounting for one dropout per group. During the first week, the 5 rats had free access to a standard, semisynthetic powdered food containing 14 g/100 g milk protein [P14 diet, as previously described, (17)]. The mean food intake of the first group of rats measured during wk 1 was taken as the reference ad libitum intake for all rats throughout the study. At the end of wk 1, the rats were implanted with a chronic jugular catheter, which ended in the vena cava according to an adaptation of the method described by Burvin et al. (18). During wk 2, the rats were fed 50% of the reference ad libitum intake delivered at 1800 h and then had free access to the diet for 30 min, from 1100 to 1130 h. During this week, the rats were accustomed, but not trained, to running on a 6-lane treadmill, through two brief (10-min), low-speed sequences on the treadmill. The experimental day was chosen as d 1 or 3 of wk 3. At 1100 h on that day, 4 rats received one of the isoenergetic meals, comprising 1 g of their usual diet (the 14% protein diet) mixed with either 2 g milk protein (TMP),1 2 g {alpha}-lactalbumin–enriched milk protein ({alpha}-LAC), 1.8 g glucose (GLUC) or 2 g milk protein plus 150 mg N-acetyl-L-cysteine (NAC, Table 1). The GLUC and NAC groups were intended to serve as negative and positive control, respectively, for the amount of cysteine in the meals compared with the TMP and {alpha}-LAC meals (Table 1). TMP and {alpha}-LAC protein were kindly provided by Armor Proteines (Saint-Brice en Coglès, France). The meals were completely ingested by the rats between 1100 and 1130 h. The exercise began at 1200 h and lasted for 2 h. After a 30-min warm-up period, during which the treadmill speed was gradually increased, the rats were made to run at ~60% VO2max on the treadmill (20 m/min, 10% grade). Blood samples (245 µL) were drawn at 1100 (baseline), 1200 (pre-exercise), 1240, 1330 and 1400 h, via the permanently implanted catheter. After each blood sample collection, the catheter was washed with citrated physiologic serum [Citric Acid anhydrous+ Citric Acid Trisodium Salt Dihydrate Sigma Ultra (Sigma, Saint-Quentin-Fallavier, France)+ NaCl (9 g/L solution; B. Braun Medical, Boulogne, France)]. The rats were killed at 1400 h by a pentobarbital overdose (40 mg/kg body weight) through the catheter, and the liver and heart were rapidly removed. The fifth rat received 3 g of the usual diet but was kept sedentary, and then killed at the end of the experiment (control group, Table 1).


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  		TABLE 1 Composition of the test meals

 
    Sample processing. The 250-µL blood samples were dropped into prechilled tubes, containing 10 µL of an antiprotease solution composed of EDTA and aprotinin (Trasylol, 10000 U; Bayer, Leverkusen, Germany). Two 40-µL aliquots were immediately added with 200 µL of 10 mmol hydrochloric acid and subjected to three cycles of rapid freezing (-80°C) and thawing (room temperature). After centrifugation (4°C, 10000 x g, 5 min), the 200-µL supernatant was deproteinized on ice by the addition of 100 µL of 20% sulfosalicylic acid and centrifuged (4°C, 7000 x g, 15 min). The supernatant was kept overnight at 4°C before glutathione determination. The liver and heart were weighed, divided in portions, frozen in liquid nitrogen and stored at -80°C. Liver and heart samples were homogenized (1:10, v/v) with 9 g/L NaCl (4°C) and 300 µL was then deproteinized on ice by the addition of 100 µL of 20% sulfosalicylic acid and centrifuged (4°C, 7000 x g, 15min). The supernatant was used immediately for glutathione assays.

    Glutathione assays. Whole blood, liver and heart were analyzed for total and oxidized glutathione (GSSG) using an enzymatic method described by Anderson (19), with the following minor adaptations: the test sample volume was 20 µL, liver and heart samples were diluted by a factor of four and 5 µL GSSG reductase (266 kU/L after dilution; Sigma, Saint-Quentin-Fallavier, France) was used for each assay.

    Statistical analysis. Data are expressed as means ± SEM. The kinetics of blood total glutathione, its reduced and oxidized forms and their ratio were analyzed using mixed models for repeated-measure analysis (SAS Institute, Cary, NC) with time and meal as independent factors. Total, reduced, oxidized and reduced:oxidized glutathione in the liver and heart were analyzed for the effect of meal type using a mixed model with the animal as a random effect nested into the treatment (fixed) effect. For all data, multiple comparisons were made using ad hoc contrasts under the mixed models. Linear and nonlinear regressions were performed using Sigma Plot (SPSS, Chicago, IL). A P-value < 0.05 was considered to be significant.


   RESULTS
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 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
    Blood glutathione kinetics. Blood total glutathione (Fig. 1) declined significantly over time (P < 0.001), but the nature of the meal did not influence total blood glutathione. One hour after the meal (at the start of exercise), blood glutathione tended to be slightly lower than baseline (pooled values, 948 ± 27 vs. 1009 ± 34 µmol/L, P = 0.054). By the end of the exercise period, blood glutathione (862 ± 37 µmol/L) had decreased significantly compared with the levels seen at baseline or at the start of exercise (P < 0.01). The statistical trends were similar for reduced glutathione (data not shown). Similarly, the meal type did not affect the GSH:GSSG ratio (Fig. 1); however, the ratio changed over time (P < 0.001) and 1 h after the meal (pooled values, 14.3 ± 1.1), it was significantly higher than at baseline (11.5 ± 0.7, P < 0.01). At the end of the exercise period, the GSH:GSSG ratio (15.8 ± 1.1) differed from baseline (P < 0.001) but not from the pre-exercise value (P = 0.16).



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  		FIGURE 1 Total glutathione (upper panel) and the reduced:oxidized glutathione ratio (GSH:GSSG ratio, lower panel) in the blood of rats, drawn via a permanently implanted catheter, before meal ingestion (t = 0), before exercise (t = 60 min), during exercise (t = 90 and 150 min) and immediately after exercise (t = 180 min). As their final meal, rats ingested 1 g of the usual diet mixed with 1.8 g glucose (GLUC), 2 g milk protein (TMP), 2 g {alpha}-lactalbumin-enriched milk protein ({alpha}-LAC) or 2 g milk protein + 150 mg N-acetyl-cysteine (NAC). Data are means ± SEM, n = 7. Time affected both variables, P < 0.01. Pooled means at a time without a common letter differ, P < 0.05

 
    Liver glutathione. At the end of the experiment, liver total glutathione (Fig. 2) was higher in test rats than in the control group (P < 0.01). Within the test groups, meal type significantly affected the liver glutathione concentration at the end of the exercise period. Liver glutathione was significantly higher in the NAC group than in the TMP and GLUC groups, and significantly higher in the {alpha}-LAC group than in the GLUC group. Liver glutathione concentrations were not correlated with sulfur amino acid intake or methionine levels in the last meal (linear regression, R2 = 0.89; P = 0.057; R2 = 0.42; P = 0.35, respectively) and no nonlinear relationship could be found. In contrast, liver total glutathione had a marked curvilinear relationship with cysteine intake (simple exponential rise to maximum, R2 = 0.999; P < 0.02; Fig. 2). All test groups had higher GSH:GSSG ratios than the control group (205 ± 17 in pooled test groups vs. 54 ± 21 in the control group, P < 0.01) but the test groups did not differ due to meal type (data not shown).



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  		FIGURE 2 Liver total glutathione after a single bout of exhaustive exercise in rats that ingested as their last meal 1 g of the usual diet mixed with 1.8 g glucose (GLUC), 2 g milk protein (TMP), 2 g {alpha}-lactalbumin-enriched milk protein ({alpha}-LAC) or 2 g milk protein + 150 mg N-acetyl-cysteine (NAC) as a function of the amount of cysteine ingested in the last meal. The control group (CON) received 3 g of the control diet as their last meal and was kept sedentary. Data are means ± SEM, n = 7. *Means of exercised rats differed from the control, P < 0.05. Means of exercised rats without a common letter differ, P < 0.05. The broken line shows the single exponential growth regression for postexercise liver glutathione vs. cysteine intake (R2 = 0.999; P < 0.02).

 
    Heart glutathione. At the end of the experiment, heart glutathione in the control group (2.16 ± 0.27 µmol/g) was higher than in all of the test groups taken together (1.66 ± 0.06 µmol/g) and in the TMP (1.52 ± 0.03 µmol/g) and {alpha}-LAC (1.61 ± 0.08 µmol/g) groups, and tended to be higher than in GLUC (1.68 ± 0.09 µmol/g, P = 0.058) group. There were no differences among the test groups. The heart GSH:GSSG ratio did not differ among the groups (pooled groups, 99 ± 25).


   DISCUSSION
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 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
The principal result of this study is that all groups of rats had higher liver glutathione concentrations after exercise, and postexercise liver glutathione was clearly linked to the amount of cysteine in the last meal, in a curvilinear dose-dependent relationship.

In contrast, it was shown that in food-deprived or postabsorptive rats, a single bout of exhaustive exercise lowers liver glutathione and cysteine (8,9,20). Other studies suggested that, in this context as in many other situations of stress, cysteine availability probably limits glutathione synthesis (21). A large body of evidence also suggests that the liver glutathione pool is both the most markedly challenged and the most critical for glutathione homeostasis during exercise (3,21,22). During our study, the effect of dietary cysteine delivery to the liver was important in rats that had ingested the {alpha}-lactalbumin–enriched meal before exercise (~60–80% increase in liver glutathione compared with the fed, sedentary rats, or to exercised rats ingesting the glucose-based meal, an isoenergetic negative control). Furthermore, after that meal, liver glutathione did not differ significantly from that after a milk protein meal enriched with N-acetyl-cysteine (a positive, pharmacologic control), probably because as substantiated by the exponential-rise-to-maximum curve fit on the dose-response, the cysteine effect was almost maximal with the amount provided by the {alpha}-lactalbumin-enriched meal. The promotion of high liver glutathione levels helps to relieve marked oxidative stress in the liver during exercise (9,20), as indicated in the present study by the high GSH:GSSG ratio in the liver at the end of the exercise. This study showed that a single cysteine intake as part of proteins can have a large effect on liver glutathione during exercise, and that the effect was important with an {alpha}-lactalbumin–rich meal because of its high cysteine content.

Surprisingly, our study also showed that the important stimulatory effect of the nature of the last meal on liver glutathione status had a very limited extrahepatic effect. Even though the blood GSH:GSSG ratio increased during the experiment, blood glutathione decreased over time, regardless of the meal type. Although different kinds of acute exercise may have variable effects on glutathione homeostasis, blood glutathione usually remains stable during exercise, likely because of an increase in liver output (4). Therefore, it is unclear why the changes in hepatic glutathione did not affect circulating glutathione concentration. Because heart glutathione concentrations were low after exercise and unrelated to meal type, we can rule out the possibility that peripheral tissues might have taken up most of the liver-derived glutathione. It is more likely that liver glutathione sinusoidal efflux was markedly inhibited during exercise. In this situation, increased liver glutathione output is thought to be triggered by major hormonal modifications, including vasopressin secretion and {alpha}-adrenergic stimulation, with lower insulin and higher glucagon and catecholamine levels (8,23). Because exercise took place 1 h after the last meal, the absorptive period may have impaired the exercise-related hormonal regulation of glutathione efflux. This adds support to the similar hypothesis put forward by Ji et al. (24) who reported that carbohydrate supplementation during exercise prevented an exercise-induced rise in blood glutathione in humans. In addition, the very high sulfur amino acid influx might have inhibited liver glutathione efflux in a dose-dependent fashion (25), which would explain why we found no difference in the blood glutathione status as a function of the type of the last meal. In contrast, an overwhelming effect of the postprandial state could also have favored glutathione synthesis in the liver. Additional data are required to test this hypothesis.

This study therefore demonstrates that liver glutathione synthesis is markedly sensitive to the acute dietary supply of cysteine via selected proteins, thus opening new opportunities to explore nutritional strategies that allow an oxidative challenge and/or the disruption of glutathione homeostasis to be rapidly prevented in different situations. Immediately after a single bout of exercise starting soon after ingestion of a meal, cysteine in dietary proteins dose-dependently improves liver glutathione. Virtually maximal stimulation may be attained with dietary proteins that are rich in cysteine, such as {alpha}-lactalbumin. This may not translate into immediate benefits for body glutathione homeostasis probably because of broad and complex conflicting regulations between the postprandial and exercise-related states. Nevertheless, in addition to the above-mentioned protective effect in the liver, a high liver glutathione concentration after exercise may allow the delivery of glutathione during the recovery period, when oxidative stress is sustained and inflammatory pathways are activated (4). Last, a high glutathione reserve in the liver should be beneficial during repeated bouts of exercise performed in the subsequent postabsorptive state (9,26,27). Further studies are warranted to determine the extent to which a dietary supply of cysteine might support glutathione homeostasis and the prooxidant/antioxidant balance in the body, as a function of the delay between meal ingestion and the onset of exercise.


   FOOTNOTES
 
2 Abbreviations used: GLUC, glucose-based meal; GSH, reduced glutathione; GSSG, oxidized glutathione; NAC, total milk protein–based meal plus N-acetyl-cysteine; TMP, total milk protein–based meal; {alpha}-LAC, {alpha}-lactalbumin–based meal. Back

Manuscript received 27 August 2003. Initial review completed 22 September 2003. Revision accepted 7 October 2003.


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 DISCUSSION
 LITERATURE CITED
 

1. Sen, C. K. (1997) Nutritional biochemistry of cellular glutathione. J. Nutr. Biochem. 8:660-672.

2. Li, J., Quan, N. & Bray, T. M. (2002) Supplementation of N-acetylcysteine normalizes lipopolysaccharide-induced nuclear factor {kappa}B activation and proinflammatory cytokine production during early rehabilitation of protein malnourished mice. J. Nutr. 132:3286-3292.[Abstract/Free Full Text]

3. Ji, L. L. (1999) Antioxidants and oxidative stress in exercise. Proc. Soc. Exp. Biol. Med. 222:283-292.[Abstract/Free Full Text]

4. Sen, C. K. & Packer, L. (2000) Thiol homeostasis and supplements in physical exercise. Am. J. Clin. Nutr. 72:653S-669S.[Abstract/Free Full Text]

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7. Oh-ishi, S., Kizaki, T., Ookawara, T., Sakurai, T., Izawa, T., Nagata, N. & Ohno, H. (1997) Endurance training improves the resistance of rat diaphragm to exercise-induced oxidative stress. Am. J. Respir. Crit. Care Med. 156:1579-1585.[Abstract/Free Full Text]

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10. Bella, D. L., Hirschberger, L. L., Hosokawa, Y. & Stipanuk, M. H. (1999) Mechanisms involved in the regulation of key enzymes of cysteine metabolism in rat liver in vivo. Am. J. Physiol. 276:E326-E335.

11. Stipanuk, M. H., Londono, M., Lee, J. I., Hu, M. & Yu, A. F. (2002) Enzymes and metabolites of cysteine metabolism in nonhepatic tissues of rats show little response to changes in dietary protein or sulfur amino acid levels. J. Nutr. 132:3369-3378.[Abstract/Free Full Text]

12. Morand, C., Rios, L., Moundras, C., Besson, C., Rémésy, C. & Demigné, C. (1997) Influence of methionine availability on glutathione synthesis and delivery by the liver. J. Nutr. Biochem. 8:246-255.

13. Jain, A., Madsen, D. C., Auld, P. A., Frayer, W. W., Schwartz, M. K., Meister, A. & Martensson, J. (1995) L-2-Oxothiazolidine-4-carboxylate, a cysteine precursor, stimulates growth and normalizes tissue glutathione concentrations in rats fed a sulfur amino acid-deficient diet. J. Nutr. 125:851-856.

14. Hum, S., Koski, K. G. & Hoffer, L. J. (1992) Varied protein intake alters glutathione metabolism in rats. J. Nutr. 122:2010-2018.

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