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© 2004 The American Society for Nutritional Sciences J. Nutr. 134:2930-2934, November 2004

Biochemical and Molecular Actions of Nutrients

Lipoic Acid and Ascorbic Acid Affect Plasma Free Amino Acids Selectively in the Teleost Fish Pacu (Piaractus mesopotamicus)1

Bendik F. Terjesen*,{dagger},**, Kwan Park*,{ddagger}, Marcelo B. Tesser*,{dagger}{dagger}, Maria C. Portella{dagger}{dagger}, Yongfang Zhang* and Konrad Dabrowski*,2

* School of Natural Resources, The Ohio State University, Columbus, OH 43210; {dagger} AKVAFORSK, Institute of Aquaculture Research, Sunndalsøra, Norway; ** Aquaculture Protein Centre, Ås, Norway; {ddagger} Department of Aquatic Life Medicine, College of Ocean Science and Technology, Kunsan National University, Soryong-Dong, Kunsan City, Chonbuk, South Korea; and {dagger}{dagger} São Paulo State University Aquaculture Center, Jaboticabal-SP, Brazil

2To whom correspondence should be addressed. E-mail: dabrowski.1{at}osu.edu.


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Most studies on the antioxidants, lipoic acid (LA) and ascorbic acid (AA), focused on species that, unlike teleost fish, are not scurvy-prone, and are able to synthesize AA. The antioxidant properties of LA may make it useful in aquaculture nutrition, but several effects must first be investigated, and we address here plasma free amino acids (FAA). In mammals, LA and AA in high doses were claimed to alter plasma FAA profile; to our knowledge, however, no data are available in fish. We therefore studied the effects of dietary LA and AA on plasma FAA in the South American teleost fish pacu, which is being used increasingly in aquaculture. LA treatment decreased concentrations of 18 of 23 individual FAA; specifically, dispensable and total FAA were significantly affected. Ornithine was elevated (+26%) in LA-treated fish and significantly decreased ratios of plasma [Arg]/[Orn] and other individual [FAA]/[Orn] were observed. LA and AA both affected sulfur FAA concentrations. Plasma cystine levels were significantly increased in the LA-supplemented groups. AA had little effect on most amino acids, and no interaction with LA was detected. AA supplementation did, however, significantly lower taurine (–42%) and cystathionine (–31%) levels in plasma. No effect on the branched chain:aromatic amino acid ratios was observed. The data indicate that at the dietary level studied, LA and AA independently affect selected plasma FAA in pacu, and suggest that any use of LA in particular as a dietary supplement should take into account an altered plasma FAA profile.

KEY WORDS: • teleost • lipoic acid • ascorbic acid • antioxidant • free amino acids

The antioxidant {alpha}-lipoic acid (1), 1,2-dithiolane-3-pentanoic acid (C8H14O2S2), is both water and lipid soluble, and is present in pro- and eukaryotic organisms (2). In mammals, the R isomer is synthesized by lipoic acid (LA)3 synthase (3,4). LA protects several macromolecules against reactive oxygen species (ROS) (5), and exerts its effects mainly through its reduced form, dihydrolipoic acid, a conversion catalyzed by lipoamide dehydrogenase. Through linkage between its carboxyl group and lysine residues in proteins, LA is an essential cofactor for mitochondrial enzymes, pyruvate dehydrogenase, glycine decarboxylase, {alpha}-keto glutarate dehydrogenase, and branched chain {alpha}-keto dehydrogenase (3,6).

Ascorbic acid (AA) is known for its antioxidant capacity through its actions, for example, on ROS in biological fluids and membranes. Deficiency indicators in scurvy-prone teleost fish include reduced feed efficiency and growth, muscular dystrophy, scoliosis, lens cataracts, and hemorrhages (7). The effects of AA on plasma free amino acid (FAA) levels were investigated (8) in humans, and significant effects of high AA intake manifested differently depending on the particular amino acid in question. For instance, leucine and lysine were elevated, whereas arginine, glutamic acid, and glycine were significantly depressed in plasma (8). There is little information on the effects of LA on general amino acid and nitrogen metabolism in mammals; most research has focused on interactions with ROS, and lipid and carbohydrate metabolism. However, LA-containing enzymes were shown to facilitate BCAA oxidation in plants (9), and humans deficient in lipoamide dehydrogenase develop higher levels of branched-chain FAA in plasma (10). Cats have a low tolerance for LA compared with other mammals, and a high dose led to disrupted plasma and tissue FAA profiles compared with controls (11).

Due to the antioxidant properties of LA and its many positive effects in the treatment of hypertension and diabetes in mammals (4,12), there may be potential for its use as a supplement in fish nutrition. Indiscriminate use of LA, however, was shown to be adverse for cats (11), and the similar carnivorous nature of many cultured teleost species necessitates that studies address several effects of this potential supplement. To our knowledge, neither the metabolism nor the effects or requirements of dietary LA have been studied in fish. Due to the pivotal role of amino acids in the general metabolic pathways in fish (13) and the scarce knowledge of the effects of LA and AA on fish nitrogen metabolism, we address here the effects of these antioxidants on plasma FAA. We studied the South American fish pacu (Piaractus mesopotamicus), which is increasingly being used in aquaculture due to its good consumer acceptance and high growth rate (14).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
    Diet preparation and experimental design. A casein-gelatin-based basal diet was used (Table 1). In this diet, proline and glutamic acid are the dominant amino acids, when calibrated using all dietary amino acids. We showed previously in preliminary reports that pacu utilize this purified diet (AA added), with protein efficiency ratios (PER) averaging 3.1 ± 0.1 (n = 3, 6 wk trial) and feed conversion ratios (FCR, feed/biomass gain) of 0.65 ± 0.02 (15). AA was supplemented to the basal diet at 0 or 0.5 g/kg diet (ascorbyl monophosphate), whereas LA (racemic {alpha}-lipoic acid, Sigma, T5625) was provided at 0 or 1 g/kg diet (using dextrin for replacement). LA supplementation was chosen to be below levels given to rats (16) due to the lower metabolic rate in fish and the long study period required to achieve multiples of initial body weight. Diets were mixed, pelleted, and freeze-dried to obtain pellets of desired sizes.


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  		TABLE 1 Composition of the 4 experimental diets with or without added AA or LA fed to juvenile pacu1

 
Pacu (Piaractus mesopotamicus), cultured from the larval stage (larvae generously provided by Mr. Nestor Gromenida, Formosa, Argentina) in our laboratories, were used. Juvenile pacu (n = 10/tank) with an initial individual weight of 16.6 ± 0.43 g were stocked randomly in 3 replicate glass aquariums for each of the 4 dietary treatments (Table 1), and supplied with dechlorinated tap water at 25.6 ± 1.2°C (range 23.8–27.8°C). The fish were fed 3 times a day at a readjusted-restricted rate (1.9–2.5% body weight/d) for a total of 8 wk, with intermittent biomass measurements every 2 wk. At the last sampling point, fish were fed a meal in the morning (0700 h), and sampling commenced 3 h after feeding. Sampling was conducted randomly across tanks and treatments. After the fish were placed in ice-cold water for 3 min, blood was collected from the caudal vein of 2–3 fish/tank with heparinized syringes, and fish were killed with a sharp blow to the head. The blood was transferred to Eppendorf tubes, placed on ice, centrifuged at 2200 x g (10 min, 4°C) for separation of plasma, and stored at –80°C for later preparation for FAA analysis. This experiment followed the guidelines of the Animal Care and Use Committee at The Ohio State University.

    Analysis. Samples were prepared by diluting plasma with 1:1 (v:v) of 0.1 mol/L HCl containing 200 µmol/L norleucine internal standard (norleucine recovery was 102 ± 11%) (17). Samples were subsequently filtered with Millipore Ultrafree-MC filtration devices (10-kDa cutoff at 2000 x g, 4°C, 90 min). Aliquots of blanks and external standards (Sigma acid/neutral and basic amino acids), the latter supplemented with glutamine, were prepared at the same time by mixing with distilled and deionized H2O, 0.1 mol/L HCl, and norleucine. Samples, standards, and blanks were then stored at –80°C for later analysis. Amino acids were precolumn derivatized with phenylisothiocyanate (17); in addition, we found that derivatized fish plasma samples required a final centrifugation step (10 min, 9000 x g) before injection to remove precipitates. FAA were quantified using a Waters PicoTag RP-HPLC equipped with an application-specific FAA column (3.9 x 30 cm), a Waters 717 autosampler set at 10°C, models 501 pumps, 441 absorbance detector at 254 nm, a gradient controller, and a Waters column heater at 46°C. Integration through the 87-min runs was conducted by ChromPerfect software (Justice Laboratory Software). Eluents, purchased premixed and ready for use (Eluent 1, 2, Waters), were employed throughout. Amino acids were identified from samples spiked with known FAA and from retention times of standards run every 4th sample. Reported cystine values include cystine plus cysteine. Asparagine was detected, but at very low levels, and eluted as a small peak between and close to both the serine and glycine peaks; thus, it was judged not to be quantifiable under these conditions and amino acid profile characteristics. Plasma FAA concentrations (µmol/L) were calculated using both the internal and external standards (17).

    Data analysis. Data are presented as means ± SD. The percentage change was calculated for LA across AA groups and vice versa. Established nomenclature used for indispensable free amino acids (IDAA) and dispensable free amino acids (DAA) in fish was followed (18). Tanks were used as the experimental unit, and no data transformation was conducted. Data, in µmol/L for the FAA, were tested using SPSS version 12.0.1 throughout, except for nonparametric tests (19). Data were tested for homogeneity of variances by Levene’s test. If significant, the nonparametric Kruskal-Wallis test extended for 2-way designs (19) was used to ensure that any significance matched that of the 2-way univariate general linear model (GLM) tests. This occurred in all cases, and effects of LA and AA, and their interactions, were therefore tested by 2-way univariate GLMs. When significant (P < 0.05), Duncan’s multiple comparison tests in the 1-way ANOVA SPSS post-hoc procedure were used.


   RESULTS
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 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Individual weight after 8 wk was 56.9 ± 5.2 g (n = 12) across treatments. Although a slightly lower gain in weight (9%) was noted in groups supplemented with LA, weight gain did not differ between groups (40.3 ± 4.9 g) or FCR (0.73 ± 0.07). No mortality occurred during the experiment.

Dietary LA significantly reduced total plasma FAA concentrations (Fig. 1, Table 2). DAAs were most affected, with plasma concentrations declining ~20%. For 7 of the 13 individual DAA, the decline in concentration was significant, and serine was the DAA most affected by LA dietary treatment (Fig. 1, Table 2). The finding of a significant dietary influence of LA on total FAA levels persisted if proline, which dominated the FAA plasma pool, was excluded from the dataset. Several of the IDAA concentrations tended to decrease with LA supplementation (P = 0.09–0.33) (Table 2, , 3). The branched-chain:aromatic amino acid ratios, indicators of adverse metabolic effects of LA were not affected by LA dietary treatment (P > 0.05). Of the sulfur amino acids, LA increased circulating cystine significantly (Table 2) above the level without LA in the diet.



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  		FIGURE 1 Plasma individual and total FAA and DAA concentrations (panels A–F) of juvenile pacu fed diets with and without AA or LA. Values are means ± SD, n = 3. Statistical significance of AA or LA dietary treatment (two-way) is presented in the symbol legend above each panel (NS: not significant, *P < 0.05, **P < 0.01; see also Table 2). Results from 1-way multiple comparison tests are indicated by letters next to data; means sharing a letter do not differ. Letters a,b,c refer to the leftmost FAA shown (open bars), whereas letters x,y refer to the rightmost FAA (filled bars).

 

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  		TABLE 2 Statistical results of 2-way GLM tests showing the main effect of dietary AA or LA on plasma FAA concentrations in pacu, and the change in FAA concentration by treatment

 

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  		TABLE 3 Plasma individual and total IDAA concentrations in juvenile pacu fed diets with and without AA or LA1

 
Ornithine was an exception to the general decline in DAA upon LA dietary treatment because there was an increase (P = 0.055) in ornithine concentration (Fig. 1, Table 2). When the [Arg]/[Orn] ratios were tested against treatment (not shown), significantly depressed ratios occurred as a result of LA dietary treatment (P < 0.01). Except for the sulfur amino acids, there was a depressed [FAA]/[Orn] ratio after LA treatment for most other FAA, including proline (P < 0.05) and particularly glutamine (P < 0.001).

AA had a smaller effect upon the total FAA and most individual FAA concentrations than did LA; no significant interactions between the 2 supplements were detected (Table 2). However, AA significantly decreased taurine concentrations compared with the level without AA supplementation, and a similar trend was observed for cystathionine (Fig. 1, Table 2).


   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Considerable alterations were observed in the plasma FAA profile of pacu upon dietary LA and AA supplementation. It is unlikely that the reductions in most plasma amino acids by dietary LA were due to elevated amino acid excretion because in fish, this may occur only when they are fed diets in which the amino acid fraction is composed entirely of crystalline amino acids (20). In the present study, the amino acid fraction was almost completely derived from protein (Table 1). In both mammals and birds fed LA-supplemented diets, LA elevates tissue respiration (4,16,21). Future studies are warranted, however, to determine whether LA elevates amino acid catabolism in fish, as may be hypothesized on the basis of the present data demonstrating a slightly reduced weight gain in LA groups, a more pronounced decline in DAA vs. IDAA, and a significantly decreased [Arg]/[Orn] ratio. The present study indicates, however, that in terms of the plasma FAA profile, the LA dosage was not toxic when using criteria for mammals (11) because unlike in cats, the branched chain:aromatic amino acid ratio did not change.

Sulfur amino acids were affected differently than most other amino acids upon LA supplementation. Methionine did not show the decline typical for most IDAA (Table 3). Cystathionine was unaffected by LA treatment, whereas cystine was significantly elevated, and taurine, which is synthesized from cysteine (22), was decreased (Fig. 1). These findings suggest that either LA treatment affected cystine transport out of plasma and/or that total cellular cystine synthesis increased relative to catabolism. Notably, mammalian studies show that LA increases cysteine levels both in vivo and in vitro (23,24). The dietary level of AA used here had no significant effects on most plasma FAA, unlike what was reported for a scurvy-prone mammal at high dosage (8). AA, like LA, did affect plasma sulfur amino acids; however, there was a considerable reduction in both cystathionine and taurine levels in the pacu (Fig. 1). In humans, an opposite response was seen for taurine, and methionine decreased (8). Taurine has antioxidant properties at physiologic concentrations (22,25) and its essentiality in the early life stages of marine fish was suggested (26). Future experiments should investigate whether there exists an interaction between dietary taurine and AA on antioxidant capacity in fish.

It was expected that an interaction between LA and AA would have been detected in the present study because LA is able to recycle AA (27), but this did not occur. However, in the same experimental fish used here, LA decreased the rate of AA depletion in hepatic and gill tissues in pacu fed diets devoid of ascorbate (28). The lack of an interaction effect has not been explained.

Although it is not known to what degree teleost fish can synthesize LA endogenously, LA is likely present predominately as lipoyl-lysine in commercial aquaculture diets rich in fish ingredients. However, there is currently a trend toward replacing fish meal and fish oils with vegetable sources in aquaculture nutrition. Because plant tissues generally have a low LA content compared with animal tissues (2), situations with a higher risk of accumulating ROS, as in concurrent use of high-energy diets rich in lipids (29), could make LA dietary supplementation advantageous. As demonstrated for pacu at these dietary antioxidant and lipid levels, however, both LA and AA have a significant effect on plasma FAA concentrations, and this effect targets especially dispensable and sulfuric amino acids. Thus, when formulating and testing future diets supplemented with LA, protein utilization indices such as PER, apparent net protein utilization, and expression of central enzymes of nitrogen metabolism should be monitored closely. It will also be of interest to investigate the effects of LA on the metabolism of other compound classes in fish, e.g., the carbohydrates.


   FOOTNOTES
 
1 Supported by The Ohio State University Postdoctoral Fellowship Program, The Norwegian Research Council Overseas Fellowship (project no. 120/159934), The CAPES Brazil Scholarship, and The Fulbright Foundation. Back

3 Abbreviations used: AA, ascorbic acid; DAA, dispensable free amino acids; FAA, free amino acids; FCR, feed conversion ratio; IDAA, indispensable free amino acids; LA, lipoic acid; PER, protein efficiency ratio; ROS, reactive oxygen species. Back

Manuscript received 20 July 2004. Initial review completed 3 August 2004. Revision accepted 13 August 2004.


   LITERATURE CITED
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 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 

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2. Navari-Izzo, F., Quartacci, M. & Sgherri, C. (2002) Lipoic acid: a unique antioxidant in the detoxification of activated oxygen species. Plant Physiol. Biochem. 40:463-470.

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15. Tesser, M., Dabrowski, K., Terjesen, B., Pizauro, J. & Portella, M. (2004) Free- and peptide-based arginine supplementation into arginine-deficient diets for South American fish, Piaractus mesopotamicus. World Aquaculture 2004, 2–7 March 2004 2004:63 Honolulu, HI.

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21. Hamano, Y., Sugawara, S., Kamota, Y. & Nagai, E. (1999) Involvement of lipoic acid in plasma metabolites, hepatic oxygen consumption, and metabolic response to ß-agonist in broiler chickens. Br. J. Nutr. 82:497-503.[Medline]

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