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Article

The Rhamnogalacturonan-II Dimer Decreases Intestinal Absorption and Tissue Accumulation of Lead in Rats¹

Maha Tahiri^*, Patrice Pellerin, Jean Claude Tressol^*, Thierry Doco, Denise Pépin^**, Yves Rayssiguier^* and Charles Coudray^*2

^* Centre de Recherche en Nutrition Humaine d’Auvergne CRNH, Unité Maladies Métaboliques et Micronutriments, INRA, Centre de Clermont-Ferrand/Theix, 63122, Saint Genès Champanelle, France; Institut des Produits de la Vigne, Unité de Recherches Biopolymères et Arômes, INRA Montpellier, 2, place Viala, 34060 Montpellier Cedex, France; and ^** Laboratoire d’Hydrologie, Institut Louise Blanquet, Faculté de Pharmacie, Université d’Auvergne, 63000 Clermont-Ferrand, France

²To whom correspondence should be addressed.

	ABSTRACT

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The rhamnogalacturonan-II dimer (dRG-II) forms strong complexes in vitro with lead (Pb) and other selected cations. We examined the in vivo bioavailability of Pb complexed with dRG-II and the effect of unleaded dRG-II on the intestinal absorption and tissue retention of Pb in rats. Forty male Wistar rats were divided into four groups. Each group consumed a purified control diet for 3 wk or the same diet supplemented with: i) 3 mg of Pb/kg, ii) 0.5 g of leaded dRG-II/kg, or iii) 0.5 g of leaded dRG-II/kg and 4.5 g of unleaded dRG-II/kg. The leaded dRG-II provided ~3 mg of Pb/kg of diet. A chemical balance study was conducted during the last 5 d of the 3-wk study, and blood and organs were sampled for Pb and mineral analyses. The apparent intestinal absorptions of Pb were 62.3, 15.2, 11.8 and -0.1%, and Pb balances were 1.9, 9.6, 5.6 and -0.2 µg/d for the control and the three experimental groups, respectively. The Pb complexed with dRG-II was less available than Pb acetate, as reflected by significantly lower blood and tissue Pb levels. The addition of unleaded dRG-II decreased the intestinal absorption and the tissue retention of Pb significantly. We further found that the apparent absorption and status of magnesium, zinc and iron were unaffected by Pb treatment or dRG-II addition. We conclude that dRG-II may be useful in decreasing toxicity related to chronic Pb exposure. Human studies will be necessary however, to further evaluate the clinical utility of this beneficial effect.

KEY WORDS: • lead • absorption • rhamnogalacturonan-II • fruits • vegetables • rats

	INTRODUCTION

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Lead (Pb)³ is a ubiquitous and toxic metal, and its toxicity remains an important public health problem. Pb can affect the nervous system, blood and blood-forming organs, kidneys and the gastrointestinal tract (Skerfving et al. 1995 ). One of the major remaining sources of Pb contamination is paint and water from older homes. These may be an important source of Pb, especially if Pb is present in pipes. Most other sources of environmental lead do not currently pose a problem.

Nutritional factors are thought to play an important role in Pb accumulation and poisoning (Mahaffey 1977 and 1981 ). Studies in animals have shown that the gastrointestinal absorption of Pb may be enhanced by citrate, ascorbate and vitamin D and decreased by cations such as calcium, iron and zinc (Barton 1980 et al. , Conrad and Barton 1978 , Evans et al. 1943 ). Dietary fiber and some associated substances interact with mineral absorption. Such an effect is dependent on the fiber level and its nature and associated substances in the diet.

Rhamnogalacturonan-II dimer (dRG-II) is a complex pectic polysaccharide present in the cell-wall of many fruits and vegetables (Doco and Brillouet 1993 , Doco et al. 1997 ). We have previously shown that large amounts of Pb are strongly complexed with dRG-II in these vegetable products. In addition, dRG-II is also present in wine, in which it represents a predominant anionic macromolecule. In vitro studies have shown that dRG-II complexes specifically with Pb, strontium and barium but not with essential cations such as calcium, magnesium, iron and zinc (Pellerin et al. 1996 ).

The purpose of this study was to evaluate the availability of Pb from the Pb/dRG-II complex and the in vivo effect of dRG-II on Pb intestinal absorption and its tissue retention in lead-treated rats. We also assessed the in vitro specific complexing capacity of dRG-II by determining the intestinal absorption and status of magnesium, iron and zinc in rats.

	MATERIALS AND METHODS

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Materials and reagents.

Suprapure HNO₃ and H₂O₂ were purchased from Merck (Darmstadt, Germany), and lead acetate was purchased from Sigma Chemical (St. Louis, MO). All other chemicals were of the highest quality available. Distilled water was used throughout. A Plasmaquad II system (Fisons Instruments, Manchester, United Kingdom) with a Meinhard nebulizer was used for Pb measurement and a Perkin Elmer 560 (Perkin Elmer, St.-Quentin en Yvelines, France) was used for magnesium, iron and zinc measurements.

dRG-II preparation.

We isolated dRG-II from an industrial apple retentat residue (Les vergers de Chateaubourg, Chateaubourg, France). Apple residue was treated 3 d by pectinolytic enzymes (Rapidase Liq⁺, 0.08% (v/v); Gist-Brocades, Seclin, France). The supernatant was filtered and concentrated. It was then injected on a DEAE-Fractogel 650M column (18 x 25 cm, Pharmacia, Uppsala, Sweden) equilibrated at 150 mL/min with acetate buffer 30 mmol/L, pH 5. The dRG-II purified fraction was obtained by washing the column with 200 mmol/L NaCl in buffer acetate 30 mmol/L, pH 5. The purified dRG-II was then injected on Superdex 75HR column and the glycosyl residue composition determined (Pellerin et al. 1996 ) to verify the homogeneity of the fraction. The structure of the mRG-II is given in Figure 1 .

View larger version (13K): [in this window] [in a new window]   Figure 1. Structure of the rhamnogalacturonan-II monomer. The figure shows the four oligoglycoside side chains A-D whose residues are numbered according to the model sequence. Abbreviations: 2-O-Me- -L-Fuc p: 2-O-methyl- -L-fucopyranose; -L-Rha p: -L-rhamnopyranose; -L-Fuc p: -L-fucopyranose; 2-O-Me- -D-Xyl p: 2-O-methyl- -D-xylopyranose; -L-Ara p: -L-arabinopyranose; ß-L-Ara f: ß-L-arabinofuranose; ß-D-Api f: ß-D-apiofuranose; -D-Gal p: -D-galactopyranose; -D-GalA p: -D-galacturonic acid; ß-D-GlcA p: ß-D-glucuronic acid; Kdo: 3-deoxy-D-manno-octulosonic acid; ß-D-Dha: 3-deoxy-D-lyxo-heptulosaric acid, ß-L-Ace A: ß-L-aceric acid.

dRG-II (10 g) in HCl/KCl buffer 50 mmol/L at pH 1 was kept at room temperature for 120 min. The pH was then adjusted to 3.7 with 1 mol/L of NaOH, and the solution was dialyzed 72 h against acidified water at pH 3.7. Complex Pb-dRG-II was obtained by treatment of monomer rhamnogalacturonan-II with a solution of 6 mmol/L of Pb(NO₃)₂/boric acid at pH 3.7 for 24 h. To determine the hydrolysis of dRG-II to mRG-II in the first step and the formation of the dRG-II-Pb in the second step, a sample of the reaction mixture was subjected to size-exclusion chromatography on superdex 75 HR column (10 x 600 mm; Pharmacia) with a refractive index detection (Pellerin et al. 1996 ). The dRG-II-PB was dialyzed with acidified water for 48 h and then freeze-dried.

Animals and diet.

Male weaning Wistar rats weighing 70 g, obtained from the colony of laboratory animals of the Institut National de la Recherche Agronomique (INRA de Clermont-Ferrand Theix), were used in this study. The rats were housed under conditions of constant temperature (20–22°C), and humidity (45–50%) in rooms with a fixed 12-h artificial light-dark cycle. The rats were cared for following the guidelines formulated by the European Community for the use of experimental animals (L358–86/609/EEC). Prior to starting the study diet, rats were adapted using a purified diet for 7 d. The diet used was that recommended by the Ad Hoc Committee on Standards for Nutritional Studies in Animals. The composition of this diet is given in Table 1 . Dietary levels of magnesium, iron and zinc in this diet were 680, 57 and 52 mg/kg dry weight, respectively. After the adaptation period, the 40 rats were randomly assigned to four groups of 10. These groups consisted of a control group, and three groups that received Pb. These were: i) Pb group, ii) Pb/RG-II group and iii) Pb/RG-II + RG-II group. The control group continued to receive the purified control diet, and the Pb, the Pb/RG-II and the Pb/RG-II + RG-II groups received the same diet but their water contained 3 mg of Pb as acetate/L, 0.5 g of leaded dRG-II/L, or 0.5 g of leaded dRG-II/L plus 4.5 g of unleaded dRG-II/L, respectively, for 3 wk. The Pb contained in the leaded dRG-II theoretically corresponds to 3 mg of Pb/L of water in the diets Pb/dRG-II and Pb/dRG-II + dRG-II. Powdered diet (100 g) was daily mixed with 100 mL of water to form a semiliquid food prepared on site. During the last 5 d of the experimental period, rats were placed in individual metabolic cages and a balance study was conducted. During this study, dietary feed consumption was recorded and all fecal and urinary excretions were collected for each animal. Rats were killed while under anesthesia using sodium pentobarbital (40 mg/kg, intraperitoneally). Subsequently, blood was collected into heparinized tubes by exsanguination via the abdominal aorta, and tibia, liver and kidney were then removed, rinsed and frozen at -20°C until analysis.

The feces were dried for 72 h at 80°C, weighed and powdered. Urine volume was determined and 10 mL of urine were sampled and acidified with 0.1 mL of 14 mol/L HNO₃. Adequate subsamples of diet, feces, urine, whole blood, liver, tibia and kidney were dried overnight and then dry-ashed at 500°C for 10 h. The ash was dissolved in 0.5 mL of 14 mol/L HNO₃ and 0.2 mL of 10 mol/L H₂O₂ and heated at 110° for 2 h. The temperature was then increased to 130°C until the sample dried. Then, 5 mL of 0.14 mol/L HNO₃ were added to every sample. In each case, an appropriate dilution with 0.14 mol/L HNO₃ was performed prior to analysis. Pb concentrations were determined by inductively coupled plasma/mass spectrometry. The mass spectrometer settings and plasma conditions were optimized with a solution of 10 µg of indium/L and the instrument operating conditions were as follows: radio frequency (RF) generator, 27.12 MHz; forward RF power, 1350 W; reflected RF power, <3W; outer argon flow rate, 14 L/min; intermediate argon flow rate, 0.7 L/min; nebulizer argon flow rate, 0.76 L/min; mass resolution, 0.9 Da at 10% of peak height. Data collection variables were as follows: total replicates per integration, 5; signal integration time per replicate, 30 s; dwell time per sweep, 20.4 s; scanning mode, peak hopping at five points per peak sample and uptake rate at 0.6 mL/min. Zinc, iron and magnesium concentrations were determined by flame atomic absorption at wavelengths of 231.8, 248 and 285 nm, respectively, using a Perkin Elmer 560 atomic absorption spectrometer.

Calculations.

Relative apparent absorption of Pb, Mg, Fe and Zn were calculated according to the following equation: Relative apparent absorption (%) = 100 x {(mineral intake - mineral fecal excretion)/(mineral intake)}. Conventional chemical balance was determined as follows: balance = mineral intake - (fecal excretion + urinary excretion).

Statistical analysis.

The data are expressed as group means ± SEM. ANOVA was used to test for any significant differences among the four groups. If the F-test was significant (P < 0.05), the Student-Newman-Keuls multiple comparisons test was used to determine the specific differences between group means. Parametric ANOVA was used when the SD were homogeneous. If not, the nonparametric ANOVA test Kruskall-Wallis was used. If this last test indicated a significant difference among the four groups (P < 0.05), then the Mann and Whitney test was used to determine specific group differences.

	RESULTS

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The Pb levels of the control, Pb, RG-II/Pb and RG-II/Pb + RG-II diets were 0.15, 3.3, 2.76 and 2.85 mg Pb/kg diet, respectively. The target level was 3 mg Pb/kg diet in the noncontrol diets. Food consumption and growth rate during the experiment did not differ among the groups (Table 2 ). Furthermore, the moderate Pb accumulation induced in the present study did not have any negative effect on hematological variables such as the red and white blood cell counts or hemoglobin level (Table 2) .

As expected, Pb treatment was accompanied by high Pb fecal and urinary excretions in the Pb-treated groups in comparison with the control group (Table 3 ). The relative intestinal absorption (%) of Pb was significantly lower in the group receiving the Pb acetate compared to the control group. However, the absorbed amount of Pb (µg/d) was greater and the Pb balance was more positive in the Pb acetate group than in the control group. Intestinal absorption of Pb complexed to dRG-II was not significantly lower than that of Pb in acetate form (-23%). This finding was confirmed by significantly lower Pb excretion in the urine (-38%). Interestingly, when the unleaded dRG-II was added to the diet (Pb/RG-II + RG-II group), the Pb intestinal absorption approached zero, and the urinary excretion of Pb further decreased (-59%). Consequently, Pb balance was significantly lower than from leaded dRG-II (-37%) and became close to zero.

The brain Pb level was too low to be accurately measured in the present study. As expected, Pb administration in the form of acetate led to a considerable augmentation (>19-fold) in whole blood, kidney and tibia levels of Pb, compared to the control group (Fig. 2 ). Liver was the last sensitive tissue to Pb retention and we found only 1.4 times more Pb level in the Pb-treated rats compared to the control rats. Because Pb complexed with dRG-II was less available than Pb from acetate, Pb tissue levels in the Pb/RG-II group were significantly lower than those observed in the Pb acetate group in all four tissues. Again, the addition of unleaded dRG-II significantly reduced the Pb accumulation in the tissues, compared to both the Pb acetate group and the Pb/RG-II group.

View larger version (28K): [in this window] [in a new window]   Figure 2. Lead concentrations in blood, tibia, kidney and liver of rats fed, or for 3 wk. Powdered diet (100 g) was daily mixed with 100 mL of deionized water to form a semiliquid food prepared on-site. Water containing or not (control diet) 3 mg/L of Pb as acetate form (acetate group), 0.5 g/L of leaded dRG II (Pb/RG-II group), or 0.5 g/L of leaded dRG-II + 4.5 g/L of unleaded dRG-II (Pb/RG-II + RG-II group). A: whole blood; B: tibia; C: kidney and D: liver. Values are group mean ± SEM, n = 10. Means in a panel not sharing a letter differ significantly, P < 0.05.

Neither Pb treatment nor dRG-II addition had a significant effect upon the apparent absorption of magnesium which ranged from 6.6 to 7.5 mg/d, of Zn which ranged from 0.18 to 0.22 mg/d or of Fe which ranged from 0.72 to 0.80 mg/d. In addition, the concentrations of magnesium, zinc and iron in blood, tibia and liver were not affected by 3 wk of Pb or dRG-II treatments (data not shown).

	DISCUSSION

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Total Pb dietary intake for an adult may vary from 20 to 150 µg per day in most countries (Reilly 1998 ). Major efforts have recently been made to decrease food Pb concentrations by focusing on the food industry. Dietary fibers have previously been studied for their potential detoxifying effect on several radionuclides and heavy metals (Rose and Quaterman 1987 ). The dRG-II is a low molecular weight pectic polysaccharide (10,000 Da), present in the cell wall of plants, bound to other polysaccharides from which dRG-II can be released by an endo-a-1,4-polygalacturonase (O’Neill et al. 1990 ). In vitro studies have already demonstrated that dRG-II forms strong specific coordination complexes with specific divalent or trivalent cations (O’Neill et al. 1996 ).

The animal model and the Pb dose we used were chosen so that our study may have physiological and nutritional relevance. Because Pb pharmacokinetics in humans and rats are similar (Bogden 1997 , Leggett 1993 ), rats are a good model for studying Pb metabolism and toxicity. The Pb dose used in this study, 3 mg Pb/kg of diet, about 50 µg of Pb/(rat·d), may be considered a low to moderate dose, compared to Pb doses usually used by other investigators (Bondarev et al. 1979 , Wapnir et al. 1980 ). Consequently, rats of the Pb, Pb/RG-II and Pb/RG-II + RG-II groups did not show any signs of toxicity that are generally related to severe Pb intoxication in either growth or hematological variables. The doses of dRG-II used in this study (0.5 and 5 g/kg) may also be considered as nutritional doses because they correspond to 0.2 to 1 g of dRG-II consumed per day in human diets. Many vegetable and fruit products contain this material. For example, between 100 and 400 mg/L of dRG-II is present in wine or juices (Doco et al. 1997 ). Additionally, in a preliminary study using rats, it was reported that dRG-II is devoid of any toxicity at doses as high as 2 g dRG-II/kg rat weight (CERB society, 18800 Baugy, France, personal communication). This corresponds to about 20 g dRG-II/kg diet.

The in vivo results of the present study confirm the in vitro specificity of dRG-II to complex with cations having specific characteristics. Cations which bind to dRG-II should have some common properties including: a valence of ⁺² or ⁺³; a crystal ionic radius >9.5 nm; an electronic configuration with an incompletely filled subshell; a low energy of ionization; and an affinity for oxygen-donor ligands (Pellerin and O’Neill 1998 ). These cations include Pb⁺², Ba⁺², Sr⁺², La⁺³, Eu⁺³, Ce⁺³, Pr⁺³, Nd⁺²³ whereas the essential cations such as Ca⁺², Mg⁺², Fe⁺², Zn⁺² and Cu⁺² are excluded (O’Neill et al. 1996 ). Our results thus confirm the specific effect of dRG-II on Pb absorption and accumulation without altering those of essential elements.

The Pb acetate-treated rats had a lower apparent absorption percentage of Pb (-76%) compared to controls. This was expected because the Pb level in the diet affects Pb intestinal absorption (Reichlmayr-Lais et al. 1988 ). Further evidence for this was provided by Conrad and Barton (1978) , who reported that increasing amounts of Pb in the diet were associated with decreases in the percentage of radioactive lead tracer that was absorbed. Indeed, in addition to saturable active processes, diffusion processes also occur during Pb absorption which can explain such findings.

Our results show that the Pb availability of Pb complexed with dRG-II was less than that of Pb in the acetate form. This was reflected by lower intestinal apparent absorption, urinary excretion, and net balance of Pb, as well as lower blood, bone, liver and kidney Pb levels. Additionally, the addition of unleaded dRG-II futher decreased the intestinal absorption and the tissue retention of Pb primarily via an increase in fecal Pb excretion. Indeed, Pb fecal excretion in rats receiving Pb acetate, leaded dRG-II or leaded dRG-II plus unleaded dRG-II excreted in their feces 85, 88 and 100% of the Pb they ingested, respectively.

Thus, it appears that Pb complexed with dRG-II is less available for absorption, probably because the strong complex Pb/dRG-II readily survives gastrointestinal conditions, particularly in the upper part of intestine. In vitro studies have shown that Pb/dRG-II complex is stable from pH 2 to 8 (O’Neill et al. 1996 ). Pb absorption occurs primarily in the duodenum, and the ileal uptake of Pb is very low (Henning and Leeper 1984 ). However, dRG-II is completely degraded in the colon by fermentation (data not shown; no dRG-II was recovered in the feces of these rats) and may thus liberate the complexed Pb. This Pb liberated in the colon may be partially absorbed by the passive paracellular pathway, which may explain the small decrease in the intestinal absorption of Pb in this group (Pb/RG-II group). Consequently, these results suggest that the Pb complexed to dRG-II in red wine or in other fruit and vegetable products may be less available than from other sources of Pb.

Also of note are our results showing that additional dRG-II markedly reduced the intestinal absorption and tissue retention of Pb compared to the Pb acetate or to the leaded RG-II groups. The dRG-II may have the potential to complex and eliminate endogenous Pb of the organism. Indeed, Pb excretion from bile is the key excretion pathway for Pb (Alexander et al. 1986 , Conrad and Barton 1978 ). Therefore, substantial amounts of endogenous Pb return to the intestine where it may be complexed by dRG-II and become unavailable for absorption in the upper part of intestine. On the other hand, Pb urinary excretion was positively correlated with Pb dose and negatively with dRG-II levels in the diet. After dRG-II fermentation and degradation, it is not known whether dRG-II or its components may pass into the general circulation with or without complexed Pb. The precise mechanism through which dRG-II exercise its effect remains to be elucidated.

In conclusion, many chelating agents are currently used to manage Pb toxicity. Several of them, however, are nonspecific and have some adverse effects in humans such as inducing essential mineral efficiencies. Because it is both specific and effective in complexing with Pb, dRG-II may be a nutritional product that could be used to decrease Pb intestinal absorption, to prevent Pb accumulation, and perhaps to ameliorate Pb toxicity. However, additional studies in rats and humans are required before developing the dRG-II as a preventive or perhaps as a curative agent in Pb exposure and toxicity in humans.

	ACKNOWLEDGMENTS

 
The authors would like to thank Steven Abrams, M.D. (CNRC, Houston, TX) for editorial assistance, and gratefully acknowledge the statistical assistance of Jean Vernet and the technical assistance of Claudine Lab and Elyett Gueux.

	FOOTNOTES

 
¹ The French Environment Ministry provided financial support for this study (N° EN 98–07).

³ Abbreviations used: dRG-II, Rhamnogalacturonan-II dimers; Pb, lead; RF, radio frequency.

Manuscript received July 16, 1999. Initial review completed August 6, 1999. Revision accepted October 12, 1999.

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