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Articles

Selenium from Selenium-Rich Spirulina Is Less Bioavailable than Selenium from Sodium Selenite and Selenomethionine in Selenium-Deficient Rats¹

Unité Nutrition, Laboratoire Génie Biologique et Sciences des Aliments, Université Montpellier II, 34095 Montpellier, France and ^* Group of Bio-inorganic Analytical Chemistry, CNRS-UMR 5034, Hélioparc, 64053 Pau, France

²To whom correspondence should be addressed. E-mail: rouanet{at}arpb.univ-montp2.fr.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
The bioavailabilty of selenium (Se) from selenium-rich Spirulina (SeSp) was assessed in Se-deficient rats by measuring tissue Se accumulation and glutathione peroxidase (GSH-Px) activity. For 42 d, rats were subjected to dietary Se depletion by consumption of a Torula yeast (TY)-based diet with no Se; controls were fed the same diet supplemented with 75 µg Se/kg diet as sodium selenite. Se-deficient rats were then repleted with Se (75 µg/kg) by the addition of sodium selenite, selenomethionine (SeMet) or SeSp to the TY basal diet. Selenium speciation in SeSp emphasized the quasi-absence of selenite (2% of total Se); organic Se comprised SeMet (18%), with the majority present in the form of two selenoproteins (20–30 kDa and 80 kDa). Gross absorption of Se from SeSp was significantly lower than from free SeMet and sodium selenite. SeMet was less effective than sodium selenite in restoring Se concentration in the liver but not in kidney. SeSp was always much less effective. Similarly, Se from SeSp was less effective than the other forms of Se in restoring GSH-Px activity, except in plasma and red blood cells where no differences were noted among the three sources. This was confirmed by measuring the bioavailability of Se by slope-ratio analysis using selenite as the reference form of Se. Although Se from SeSp did not replenish Se concentration and GSH-Px activity in most tissues to the same degree as the other forms of Se, we conclude that it is biologically useful and differently metabolized due to its chemical form.

KEY WORDS: • selenium • Spirulina • rats • glutathione peroxidase

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Selenium (Se), an essential trace element for animals (1 ,2) and humans (3) , is obtained mainly from cereal products, fish, poultry and meat, almost exclusively in organic compounds. At least 13 different selenoproteins have now been identified (4 ,5) , but only glutathione peroxidase ( GSH-Px),³ selenoprotein P and Type I iodothyronine 5'-deiodinase have been well characterized in animals. Thus, selenium plays a vital part in many metabolic functions as a key component of GSH-Px, which is involved in the removal of hydrogen peroxide and lipid peroxides generated in cells (6) during oxidative processes. The Se responsiveness of an endemic cardiomyopathy called Keshan disease, which is found in areas of China with low soil Se, emphasized the human essentiality of this element as recently as 1979 (7 ,8) . A correlation between the lack of Se in food and different diseases such as cardiovascular disease (9) , cancer (10 ,11) , rheumatoid arthritis (12) and cataract (13) has been proposed. Although human Se deficiency has also been reported in patients subjected to long-term parenteral nutrition (14 ,15) , Se deficiency in humans is relatively rare and many populations with low Se intakes show no apparent ill-effects.

The major forms of selenium occurring in foodstuffs are the organic, protein-associated forms, selenomethionine (SeMet, plant and animal sources) and selenocysteine (SeCys, animal sources). Selenate is also present in some foodstuffs (16) , and in selenium-deficient areas, inorganic selenium salts (selenite, selenate) are added to the food (17) . The activity of selenoproteins depends on an adequate selenium supply from the diet. Because Se enters the food chain through plants, its availability may vary with climatic and soil fertilization conditions. Moreover, Se in foodstuffs is not always available for intestinal absorption, and there are differences both between and within species (18 19 20 21) . The metabolism of selenium varies according to the form of selenium ingested. It was demonstrated (22) that SeMet and selenate are more diffusible than selenocysteine and selenite under simulated gastrointestinal conditions, contributing to their high absorption in vivo. Moreover, reutilization of organic selenium is one of the most important differences in the metabolism of SeMet and selenite (23) .

It is very important to know the bioavailability of selenium present in the diet to establish nutritional Se status in relation to dietary intake and to intervene promptly in cases of Se deficiency. In the present study, we examined the bioavailability of Se from SeMet, sodium selenite (Na₂SeO₃) and from enriched Spirulina platensis, a blue-green alga which is commercially available for human consumption, and now used as a health food source of Se for humans (24) . We reported previously that Spirulina grown in the presence of selenium showed health benefits in rats fed high cholesterol diets (25) . The ability to control its chemical composition by varying cultivation conditions makes Spirulina a vegetable that can easily be enriched with Se by way of the aquatic medium. This work investigated the ability of Se-enriched Spirulina (SeSp) to provide biologically available Se to rats. Experiments using Se-deficient rats were conducted to measure tissue uptake of the element and GSH-Px activity.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Spirulina selenium fortification.

This step was performed at Aquamer S.A. (Mèze, France). Algae (Spirulina platensis) were grown in a 130-L photobioreactor under continuous lighting on Zarouk’s medium at 22°C and pH 10.5 in the presence of SeO₂. This medium contained NaHCO₃, 16.8 g/L; K₂HPO₄, 0.5 g/L; NaNO₃, 2.5 g/L; K₂SO₄, 1.0 g/L; NaCl, 1.0 g/L; MgSO₄ · 7H₂O, 0.2 g/L; CaCl₂, 0.04 g/L; FeSO₄ · 7H₂O, 0.01 g/L; EDTA, 0.08 g/L; H₃BO₃, 2.86 mg/L; MnCl₂ · 4H₂O, 1.81 mg/L; ZnSO₄ · 7H₂O, 220 µg/L; CuSO₄ · 5H₂O, 79 µg/L; MoO₃, 15 µg/L; and Na₂MoO₄, 21 µg/L and was supplied with light aeration (30 L/min) and the addition of 0.03% CO₂. At the end of the growth, the biomass was recovered and filtered through a 20-µm membrane, thoroughly washed with distilled water, frozen and lyophilized.

Characterization of selenium speciation in fortified Spirulina.

Selenium speciation was characterized by a sequential extraction with reagent solutions designed to selectively leach different classes of selenium species into an aqueous phase. The latter was subsequently characterized by size exclusion HPLC with Se-specific detection by inductively coupled plasma mass spectrometry (ICP-MS) (26) . A 0.2-g sample was taken for analysis. It was extracted sequentially as follows: 1) 5 mL of hot water (85–90°C) by agitation for 1 h for water-soluble selenospecies; 2) 5 mL of 4% Driselase in 30 mmol/L Tris-HCl buffer (pH 7.0) in the presence of 1 mmol/L phenylmethylsulfonyl fluoride by agitation for 1 h at 25°C for selenium associated with cell wall; 3) 5 mL of 30 mmol/L Tris-HCl buffer (pH 7.0) containing 4% SDS by agitation for 1 h at 25°C for water-insoluble selenoproteins; and 4) 5 mL of phosphate buffer (pH 7.5) by incubation for 16 h at 37°C with a mixture containing 20 mg of Pronase and 10 mg of lipase to break the residual selenoproteins. Selenium was determined by ICP-MS in the supernatant remaining after the centrifugation. The final residue was dissolved completely in 2 mL of 250 g/L tetramethylammonium hydroxide in water to determine the residual Se. A 100-µL aliquot of extract (10-fold diluted) was injected on a Superdex Peptide HR 10/30 column (Pharmacia, Uppsala, Sweden) and eluted at 0.75 mL/min with 30 mmol/L Tris-HCl buffer (pH 7.5). ⁷⁸Se, ⁸⁰Se and ⁸²Se were monitored on-line using an ELAN 6000 ICP MS spectrometer (PE-SCIEX, Thornhill, Canada).

Animals and diets.

Male Sprague-Dawley rats (Iffa Credo, L’Arbresle, France) weighing 68 g were used. Rats were housed individually in stainless steel metabolic cages and had free access to deionized water. They were kept under light from 0700 to 1900 h, and the room temperature was 23 ± 1°C, with constant humidity. Rats were fed a Torula yeast (TY)-based selenium-deficient diet throughout the 98-d experiment (Table 1 ). They were maintained by pair-feeding to the food intake of the group with the lowest intake over the experimental periods, i.e., each group received daily a quantity of food equal to that eaten by this group the day before. Rats were weighed weekly. On arrival and just before the beginning of the experimental period, five rats were selected at random and killed to establish baseline values for tissue GSH-Px activity and Se concentration. At the start of the experiment, rats (n = 70) were divided into two dietary groups on the basis of average body weight. The control group (n = 20) received the TY diet to which was added 75 µg Se/kg as Na₂SeO₃. This suboptimal level was chosen to generate nonplateauing GSH-Px activities (27) . In fact, the use of the optimal Se level (100 µg/kg) most likely would prevent detection of any metabolic differences that might have been detected with a level lower than the dietary Se requirement. The remaining rats (n = 50) were fed the TY Se-deficient basal diet (Se-deficient dietary group) which contained 7 µg Se/kg. After 42 d, five rats from each group were anesthetized by an intraperitoneal injection of pentobarbital, and tissues (liver, kidney and blood) were removed for Se bioassays and GSH-Px activity to ascertain that the Se-deficient diet had depleted Se. The repletion period lasted from d 43 to 98. The rats from the Se-deficient group were randomly divided into three groups of 15 and fed diets containing 75 µg Se/kg as Na₂SeO₃, SeMet or SeSp. Five rats of each group were killed at d 7, 28 and 56 of the repletion period. Five animals from the control group were also killed at the same times.

Rats were handled according to NIH guidelines (28) . They were deprived of food overnight and anesthetized with pentobarbital (60 g/L pentobarbital , 60 mg/kg body) before tissues were excised. The liver was perfused with 0.15 mol/L KCl to remove residual blood, rapidly excised, rinsed in ice-cold saline, blotted dry, weighed, sectioned for analyses and stored in liquid nitrogen. Kidneys were also removed, washed in ice-cold saline, blotted, weighed and frozen immediately in liquid nitrogen.

Liver and kidney were homogenized in 5 volumes of ice-cold 0.1 mol/L potassium phosphate buffer (pH 7.4), and the homogenate was centrifuged at 13000 x g for 15 min at 4°C. The supernatant was then centrifuged at 105000 x g for 60 min at 4°C and the cytosol was stored at -80°C for subsequent assay of GSH-Px activity. Glutathione peroxidase activity was measured by the method of Wendel (29) using 0.2 mmol/L hydrogen peroxide as the substrate and including 1.0 mmol/L sodium azide to inhibit catalase; thus, only Se-dependent GSH-Px activity was measured. The cytosolic protein content was determined by a commercial protein assay (Sigma, Saint Quentin Fallavier, France) according to Smith et al. (30) and using bovine serum albumin as the standard.

Blood was withdrawn by cardiac puncture and aliquots were transferred to heparinized tubes, then centrifuged at 1000 x g for 10 min to separate plasma and erythrocytes. The erythrocytes obtained were washed with saline and hemolyzed in 9 volumes of hypotonic buffer (5 mmol/L sodium phosphate buffer, pH 7.0).

Feces were collected from each rat during the last 5 d of the repletion period for intestinal absorption measurements.

Selenium was analyzed by ICP-MS after samples were digested in nitric acid and hydrogen peroxide.

Assessment of Se bioavailability.

The bioavailability of Se from sodium selenite, SeMet and SeSp was assessed by using sodium selenite–fed control rats as the reference. The deposition of Se and the increase in GSH-Px activity in different tissues were used as the responses to time of repletion (T). Because this response R can be described by the equation, R = mT + k, the relative bioavailability of Se from the three sources was estimated by the slope-ratio technique, which compares the slope of the time-response plots observed for SeMet and SeSp to that observed for sodium selenite.

Statistical analyses.

Data are shown as the means ± SEM, n = 5. Data were subjected to logarithmic transformation where necessary to achieve homogeneity of variances. Statistical analyses of data were performed by one-way ANOVA followed by Fisher’s Protected Least Significant Difference post-hoc procedure using a StatView 512 + microcomputer program (Brain Power, Calabasas, CA). Differences were considered significant when P < 0.05.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
The concentration of Se in the fortified algae was 223 ± 9 µg/g. The speciation of this selenium is characterized in Figure 1 . Water-soluble selenium accounted for 23% of the total selenium. Selenite corresponded to only 10% of the water-soluble Se (2% of total Se), indicating that algae had metabolized the SeO₂ from the culture medium. Most of the water-soluble selenium was present as a macromolecule of 60–80 kDa. The attack with Driselase (an enzyme preparation containing laminarinase, xylanase and cellulase) liberated an additional 18% of Se (bound to cell walls) that eluted at the elution volume of selenomethionine. The majority of Se in Spirulina (40%) was present in the form of selenoproteins, which can be solubilized by a solution of SDS. Figure 1 c shows that these proteins represent two molecular mass fractions, one close to the excluded volume of 80 kDa and the other in the 20–30 kDa range. Leaching with SDS did not allow all of the selenoproteins present in the sample to solubilize. A proteolytic attack of the residue allowed recovery in the aqueous phase of an additional 12% present in the form of a macromolecular compound but also Se(IV) and selenomethionine. The remaining 7% of selenium was resistant to the above reagents.

View larger version (21K): [in this window] [in a new window]   Figure 1. Speciation of selenium in Spirulina by size-exclusion HPLC-inductively coupled plasma mass spectrometry (ICP-MS) after sequential extraction. Extractions were with (A) hot water, (B) Driselase solution (mixture of laminarinase, xylanase and cellulase), (C) SDS solution and (D) lipase-pronase solution. Dotted lines mark the elution volumes of Se(VI), Se(IV) and selenomethionine standards.

View larger version (72K): [in this window] [in a new window]   Figure 2. Percentage of dietary selenium absorbed by Se-deficient rats after the 56-d period of repletion with DL-selenomethionine (SeMet), sodium selenite (selenite) or Se-rich Spirulina. Values are means ± SEM, n = 5. Bars with different index letters differ, P < 0.05.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

Selenium consumed in foods and supplements exists in a number of organic and inorganic forms, including selenomethionine (plant and animal sources and supplements), selenocysteine (SeCys) (mainly animal sources), selenite and selenate (mainly supplements). Bioavailability and tissue distribution depend on the form ingested. For instance, SeMet is more effective in increasing Se status because it is nonspecifically incorporated into proteins in place of methionine (34) . It must, however, be catabolized to an inorganic precursor before entering the available Se pool. Selenite is a more available metabolic source of Se than SeMet because it needs only to be reduced to selenide to provide selenophosphate, the precursor of SeCys, which is the active form of Se in selenoproteins (35) . Despite this, organic forms are often preferred in interventions, partly because they are less acutely toxic (36) . However, the supplemental form of Se should not accumulate excessively in the body. This work shows that SeSp meets this criterion for a good supplemental form of Se because it does not replenish the Se pool to the same extent as sodium selenite, for example, and consequently it does not accumulate in the tissues studied (kidney, liver). It must be pointed out that SeMet as well as selenoproteins from Spirulina must be digested for intestinal absorption and subsequent metabolism; selenite does not. The blue green algae Spirulina belongs to the cyanobacteria family; in this regard, it is closely related to bacteria, in which the Se metabolism incorporates SeCys into proteins; such a process also occurs in mammals (37) . Elsewhere, we could consider that these microalgae belong too to the plant kingdom. This dual-property makes spirulina an ubiquitous material which could contain Se into forms identical to SeMet (plant and animal sources) and SeCys (animal sources) and probably other metabolites. In fact, selenium speciation in Spirulina seems to be distinctly different from that in selenized yeast and allium plants. Moreover, low-molecular-mass compounds (amino acids and oligopeptides), which account for the majority of Se in yeast and garlic (38) , are present only in small amounts in the microalgae investigated. Few previous studies feeding rats Se as high selenium garlic (in the form of seleno-methyl selenocysteine) (39) and high selenium broccoli (40) , in the same chemical form as in garlic (41) , reported that these organic forms of Se tended to incorporate less into most tissues than Se fed as SeMet. Our results are consistent with such findings, although Isp and Lisk (39) fed 3 mg Se/kg diet and Finley (40) refed rats with 100 µg Se/kg diet for 63 d vs. 75 µg Se/kg diet for 56 d in our study. Moreover, Finley used L-SeMet, whereas we chose DL-SeMet. The lower dietary Se level (75 µg/kg diet) and reduced intestinal absorption of Se from SeSp could in part explain our results. Moreover, several forms of Se were present in these algae; SeMet accounted for a small part of Se, the majority of which was linked to cell walls and therefore not readily available to the body. It is likely that the effects observed were to a great extent due to the proteins detected (20–30 kDa and 80 kDa).

Although kidney is the tissue in which Se is most concentrated (42) , GSH-Px activity predominates in the liver (43) . This difference would suggest that renal Se is used in activities other than GSH-Px activity. Selenium-dependent glutathione peroxidase and phospholipid hydroperoxide glutathione peroxidase have been shown to be very active in renal membranes (44) . The selenoprotein type I iodothyronine 5'-nucleotidase is localized on the cytosolic surface of the renal cell basolateral plasma membrane (45) ; the plasma GSH-Px (i.e., GSH-Px_ec) is synthesized mainly in the proximal renal tubules and appears to be secreted through the tubule basolateral membrane (46) . Because kidney is the site of synthesis for these selenoproteins, this could explain in part the high uptake of Se by this tissue and its need for a reserve at a site in which Se accumulation is not toxic for cells (47) . Thus, kidney could serve as a storage site before the release of seleniated molecules into the bloodstream or as Se reserve for the body after glomerular filtration and reabsorption. Although Se from SeSp was the least effective in restoring kidney Se concentration and GSH-Px activity, the similar plasma GSH-Px_ec activities obtained for all of the treatment groups after 56 d would suggest that this Se source is able to supply sufficient Se for this purpose and explain why renal Se is used in other activities than GSH-Px, a protein relatively low in the hierarchy of Se use.

In this study we reported that Se from SeSp was less effective than organic and inorganic supplements in restoring GSH-Px activity and Se concentrations in several tissues and organs of Se-depleted rats. Plasma and erythrocyte GSH-Px activities were exceptions because no effect of a particular chemical form was observed, as has been reported (48) . However, it must be pointed out that for each tissue studied, GSH-Px activity increased after refeeding with SeSp, although the increase was not as rapid as with other sources. Thus, Se from SeSp is less bioavailable than selenite and SeMet. As clearly stated by Finley et al. (49) , bioavailability can be used synonymously with biological usefulness. Therefore, Se-enriched Spirulina represents a useful source of selenium.

This work was devoted to Se bioavailability from Spirulina; to our knowledge, it is the first study relative to this microalgae and contributes novel data concerning this potentially beneficial Se supplement. The primary public impetus for Se supplementation is the potential benefit for reduction of cancer. Ip and co-workers (39 ,50 51 52) as well as the study by Finley et al. (49) of colon cancer and high selenium broccoli demonstrated that cancer reduction is not a function of tissue selenium concentrations or GSH-Px activities and that the least bioavailable Se compounds may exhibit potent biological activities. Thus, the anticancer effect of a Se-containing compound may be more closely related to its ability to produce antitumorigenic metabolites, such as methyl selenol (52) . It is very important, therefore, to define more precisely the forms of Se present in Se-Spirulina to permit identification of the most active anticarcinogenic component(s) and to recommend such a source as a Se supplement. Before such a study can be conducted, due to the several forms of selenium in Spirulina, fractionation of the algae is in progress currently to identify more clearly the chemical forms of Se in the issuing fractions.

	ACKNOWLEDGMENTS

 
We would like to thank Bruno Baroux (Aquamer S.A.) for the selenium fortification of Spirulina and Jean-Claude Baccou (Plant Physiology and Technology Unit) for his help.

	FOOTNOTES

 
¹ Supported in part by the Région Languedoc Roussillon.

³ Abbreviations used: GSH-Px, glutathione peroxidase; GSH-Px_ec, extracellular GSH-Px; ICP-MS, inductively coupled plasma mass spectrometry; SeSp, Se-enriched Spirulina; TY, Torula yeast.

Manuscript received January 29, 2001. Initial review completed February 20, 2001. Revision accepted May 23, 2001.

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