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Biochemical and Molecular Actions of Nutrients

Spray-Dried Porcine Plasma Reduces the Effects of Staphylococcal Enterotoxin B on Glucose Transport in Rat Intestine^1,2

Carles Garriga, Anna Pérez-Bosque, Concepció Amat, Joy M. Campbell^*, Louis Russell^*, Javier Polo, Joana M. Planas and Miquel Moretó³

Departament de Fisiologia, Facultat de Farmàcia, Universitat de Barcelona, Barcelona, Spain; ^* APC Inc., Ankeny, IA 50021; and APC Europe, S.A., Granollers, Spain

³To whom correspondence should be addressed. E-mail: mmoreto{at}ub.edu.

	ABSTRACT

TOP ABSTRACT METHODS DISCUSSION LITERATURE CITED

 
We investigated the intestinal transport of D-glucose (D-Glc) and 3 essential amino acids in a model of intestinal inflammation, and the effects of dietary supplementation with animal plasma proteins on this function. Wistar Lewis rats were fed a diet containing an isonitrogenous amount of milk protein (control group) or a diet supplemented with either spray-dried animal plasma (SDAP) or immunoglobulin concentrate (IC) from porcine plasma, from d 21 of life (weaning) until d 35. On d 30 and 33, rats were challenged intraperitoneally with Staphylococcus aureus enterotoxin B (SEB; groups SEB, SEB-SDAP, and SEB-IC) and on d 35, brush border membrane vesicles (BBMVs) were prepared and used for transport and binding studies. Administration of SEB reduced D-Glc transport across sodium glucose transporter 1 [SGLT1; 20% reduction in maximal transport rate (V_max); P < 0.05], without affecting the Michaelis constant (K_m). The results from specific phlorizin binding, Western blot, and immunohistochemistry supported the view that the effects of SEB are due to reduced expression of D-Glc transporters in the apical membrane. SEB increased the passive diffusion constant (K_d) for D-Glc 3-fold (P < 0.05). SEB did not affect mediated or passive amino acid fluxes of L-leucine, L-methionine, or L-lysine. Dietary SDAP increased the D-Glc V_max in the SEB group without affecting the passive component. Changes in D-Glc V_max due to SEB and to the dietary treatments were correlated with changes in the number of SGLT1 transporters present in the BBMVs (r = 0.9468; P < 0.05). Dietary IC had no observed effect. We estimate that, in rats challenged with SEB, SDAP supplementation can increase glucose absorption by 8–9% during the interdigestive periods.

KEY WORDS: • Staphylococcus aureus enterotoxin B • intestinal inflammation • glucose transport • spray-dried porcine plasma • immunoglobulin concentrate

Farm animals at weaning are exposed to many stresses (e.g., changing from a liquid to a solid diet) and frequently suffer infections, mainly caused by enterotoxigenic pathogens. Enteric infections may cause intestinal inflammation, villous atrophy, maldigestion, and malabsorption, which contribute to the high rates of mortality (1,2). Rats and mice can also develop intestinal inflammation at weaning, showing increased plasma cytokine concentrations (3) and increased numbers of T-helper secreting lymphocytes (4). In humans, dietary nutrient deficiencies (5) and acute bacterial infections also induce local immunoinflammatory reactions that may impair the absorptive and barrier functions of the intestine (6). Furthermore, infants may be sensitized to dietary antigens even during breast-feeding, which can also alter the barrier function of the gut (7) and eventually have a negative effect on growth.

In weanling pigs, dietary supplementation with spray-dried animal plasma (SDAP)⁴ has shown beneficial effects in growth and performance (8,9). In calves infected with Cryptosporidium parvum, bovine serum concentrate reduced fecal losses and returned villous surface area to normal values (10). SDAP has been proposed as an alternative to antimicrobial medication (11,12). In humans, studies to assess the acceptability and safety of SDAP supplementation show that it may increase the fractional absorption of dietary lipid and of total energy in malnourished children (13). We have recently studied a rat model of mild intestinal inflammation to investigate the effects of dietary supplements on the pathophysiology of bacterial enterotoxins. With this model we demonstrated that dietary SDAP can modulate the immune response of gut-associated lymphoid tissue and prevent Staphylococcus aureus enterotoxin B (SEB)-induced intestinal water secretion (14).

The gastrointestinal tract, particularly the small intestine and its mucosal epithelium, is capable of rapid functional and morphological adaptations in response to evolutionary, genetic, and ontogenetic development and demands (15) as well as to environmental and nutritional challenges (16). Intestinal inflammation represents a pathological situation that can alter gastrointestinal function and morphology.

During intestinal inflammation, the barrier function of the epithelium is altered, and the absorption of nutrients may be impaired. For example, in rabbits with chronic ileal inflammation, both the affinity of apical sodium glucose transporter 1 (SGLT1) for D-glucose (D-Glc) and the activity of basolateral Na⁺/K⁺-ATPase are reduced (17). In C. parvum–infected rats there is also impairment of Na⁺-glucose cotransport, although the effect may be ascribed to a concomitant reduction in villous height (18). Absorption of amino acids is also impaired in a rabbit model (19) and in a rat model (20) of intestinal inflammation. In the present study, we investigated the effects of dietary supplementation with SDAP or immunoglobulin concentrates on the intestinal transport of D-Glc and amino acids in rats challenged with SEB.

	METHODS

TOP ABSTRACT METHODS DISCUSSION LITERATURE CITED

 
    Animals and protocol. Male Wistar Lewis rats (n = 48; Harlan Ibérica) were used. Rats were kept under stable temperature and humidity conditions, with a 12-h light:dark cycle. Intestinal inflammation was induced by the intraperitoneal (i.p.) administration of SEB (Toxin Technologies) dissolved in PBS (3 mmol/L KCl, 137 mmol/L NaCl, 1.5 mmol/L KH₂PO₄, and 17 mmol/L Na₂HPO₄). The protocol consisted of the administration of 2 SEB doses (0.5 mg/kg body wt) on d 30 and 33 (14).

At d 21 after birth, rats were weaned, randomly distributed into 4 groups, and fed the experimental diets until d 35. Rats in the control group were fed a control diet (without plasma proteins but containing an isonitrogenous amount of dried milk protein); rats in the SEB group were fed the control diet and were treated with SEB; rats in the SEB-SDAP group were fed a diet supplemented with 80 g SDAP/kg diet and were treated with SEB; and rats in the SEB-IC group were fed a diet supplemented with 22.7 g porcine immunoglobulin concentrate (IC)/kg diet and were treated with SEB. The SDAP and IC supplements were obtained from the same batch of fresh porcine blood (APC Europe) and the full composition of the diets was identical to that used in a previous study (14).

All protocols used in this study were approved by the ethical committees of the Universitat de Barcelona and of the regional government (Departament d’Agricultura, Ramadaria i Pesca, Generalitat de Catalunya) for the use and handling of experimental animals.

    Brush border membrane vesicle preparation. Brush border membrane vesicles (BBMVs) were prepared using the MgCl₂ precipitation method (21). For each BBMV preparation, the small intestine (except the proximal 5 cm) of 2 rats was used. After successive centrifugations, the final pellet was resuspended in a medium containing 300 mmol/L mannitol, 0.1 mmol/L MgSO₄, 0.41 µmol/L LiN₃, and 20 mmol/L Hepes/Tris (pH 7.4), with a protein concentration of 15–20 g/L. The purity of BBMV preparations was assessed from the enrichment factor of marker enzymes. Sucrase (-D-glucohydrolase, EC 3.2.1.48) activity, the marker of brush border membrane, was determined according to Garriga et al. (22). The activity of the ouabain-sensitive Na⁺/K⁺-ATPase (EC 3.6.1.3) was routinely assayed as a marker of the basolateral membrane as previously described (22). The overall recovery of enzymatic activities was calculated as the sum of recoveries of all fractions. In addition, membrane orientation was studied according to Garriga et al. (22).

    Transport and kinetic studies. The uptakes of D-Glc and L-amino acids were measured at 25°C by a rapid filtration technique, as described elsewhere (22). For the studies of the effect of specific glucose transporter type 2 (GLUT2) inhibitors on initial rates of D-Glc transport, the BBMVs were incubated in a medium in which the NaCl was replaced by KCl to prevent transport across SGLT1.

The kinetic analysis of D-Glc uptake was carried out by nonlinear regression analysis of total D-Glc fluxes from 6 independent experiments, using the Biosoft EnzFitter program (Biosoft). Because the errors associated with experimental fluxes were roughly proportional to their values, the data were proportionally weighted.

The initial rates of L-leucine, L-methionine, and L-lysine uptake were measured by incubating BBMVs for 3 s in a medium containing an aliquot of radiolabeled L-amino acid (L-[³H]-leucine, L-[¹⁴C]-methionine, or L-[¹⁴C]-lysine, New England Nuclear Research Products; final activity: 1.1–2.0 mCi/L), 100 mmol/L mannitol, 100 mmol/L NaCl, 20 mmol/L Hepes/Tris (pH 7.4), 0.1 mmol/L MgSO₄, and 0.41 µmol/L LiN₃. Initial rates were determined at initial concentrations of the substrates that were either low (0.1 mmol/L) or relatively high (10 mmol/L for L-leucine and L-lysine and 1 mmol/L for L-methionine, because of its lower water solubility).

    Phlorizin binding. The specific steady-state phlorizin binding to SGLT1 was assayed to determine the correlation between D-Glc transport rate and the number of SGLT1 transporters present in the BBMVs, using the method described by Garriga et al. (22). Each determination was carried out in triplicate using 4 different BBMV preparations. The specific phlorizin binding was expressed as pmol bound phlorizin/mg protein at a phlorizin concentration of 50 µmol/L (B₅₀).

    Western blot analysis of SGLT1. Measurements of SGLT1 protein abundance in BBMVs of rat small intestine were performed using Western-blot analysis, as previously described (23). Blots were incubated with a rabbit polyclonal antibody raised against the synthetic peptide corresponding to amino acids 564–575 of the deduced amino acid sequence of rabbit intestinal SGLT1 at a 1:5000 dilution for 16 h at 4°C. In simultaneous experiments, nitrocellulose membranes were incubated with the same antibody previously preadsorbed with the antigenic peptide (1 g/L). Hybridization bands were quantified by scanning densitometry.

    Determination of myeloperoxidase activity. Myeloperoxidase (MPO) activity was measured as an indicator of neutrophil infiltration in mucosal samples from the jejunum and was determined as described previously (14). One unit of MPO activity (UMPO) is defined as the amount of enzyme that degrades 1 µmol H₂O₂/min at 25°C.

    Immunohistochemistry. Jejunum fragments (0.5 cm) were fixed with IHC Zinc Fixative® (Becton Dickinson) at 20°C for 24 h, then embedded in OCT compound medium (Miles). Cryostat sections (10 µm; –30°C) were prepared, transferred onto glass slides, and dried overnight at room temperature. Sections were postfixed with acetone at –20°C for 10 min, then permeabilized with Triton® X-100 (Sigma) 0.1% and blocked with 1% bovine serum albumin (v:v; Sigma) at room temperature for 30 min. Sections were then incubated with the same rabbit polyclonal anti-SGLT1 used for Western blot analysis (1:500 dilution in PBS) in a humidified chamber overnight at 4°C. Sections were washed with PBS and incubated with secondary antibody, Alexa 548 conjugated goat anti-rabbit antibody (Molecular Probes; 1:300 dilution in PBS), for 1 h at room temperature. Sections were rinsed in PBS and mounted in Mowiol®-488 (Calbiochem).

    Image acquisition and processing. Sections (4 per rat) were scanned with a confocal scanning laser microscope (CLSM SPII, Leica) in a blinded protocol. The captured images were analyzed using the ImageJ program (24) to quantify the fluorescence from the antibody. The fluorescence intensity was quantified and expressed as the mean gray level per pixel of the stained area.

    Statistical analyses. Results were expressed as means ± SEM. The effects of SEB were tested by comparing the SEB and control groups by ANOVA using SPSS-10.0 software (SPSS). To analyze the effects of dietary supplementation, the SEB-SDAP and SEB-IC groups were compared with the SEB group by ANOVA followed by Scheffé’s post-hoc test. Differences were considered significant at P < 0.05.

RESULTS

    Mucosal enzyme activities. SEB treatment stimulated mucosal MPO activity compared to the control group (SEB group, 3.1 ± 0.2 UMPO/g mucosa; control group, 2.2 ± 0.2 UMPO/g mucosa; P < 0.05). Dietary supplementation with SDAP or IC did not affect the SEB-induced MPO activity (SEB-SDAP group, 2.9 ± 0.2 UMPO/g mucosa; SEB-IC group, 3.2 ± 0.4 UMPO/g mucosa). Neither SEB treatment nor dietary supplements affected the activities of the mucosal marker enzymes, sucrase and Na⁺/K⁺-ATPase (Table 1).

    Transport of D-Glu across BBMVs. SEB treatment reduced the maximal transport rate (V_max) across the apical SGLT1 by 20% (P < 0.05) and increased passive permeability (K_d) 3-fold (P < 0.05) (Table 2). The Michaelis constant (K_m) did not differ between the SEB group and the other groups (Table 2). The SDAP-supplemented diet increased the D-Glc V_max by 10% compared to the SEB group, without affecting the passive component (Table 2). The IC-supplemented diet did not affect the D-Glc kinetic constants.

    Specific phlorizin binding measurements. There was a linear correlation between D-Glc V_max and specific binding of 50 µmol/L phlorizin (Fig. 1), indicating that the changes in D-Glc V_max were due to changes in the density of SGLT1 transporters in the membrane. This linear correlation between D-Glc V_max and B₅₀ is defined by the equation y = 3.63x – 107.5 (r = 0.9468; P < 0.05). The slope of the line is the turnover number for the phlorizin binding site; that is, the number of cycles SGLT1/s. The value obtained in the present experiments (3.63 cycles/s) is in the range of values previously reported for chicken (22) and rabbit intestine (25).

View larger version (11K): [in this window] [in a new window]   FIGURE 1 Correlation between D-Glc Vmax and specific phlorizin binding to BBMVs in control, SEB, SEB-SDAP, and SEB-IC rats. Values of D-Glc Vmax are means ± SEM, n = 6; see Table 2. B50, specific phlorizin binding to BBMVs at a phlorizin concentration of 50 µmol/L; Phz, phlorizin. There is a linear correlation between D-Glc Vmax and B50, defined by the equation y = 3.63x – 107.5 (r = 0.9468; P < 0.05).

View larger version (8K): [in this window] [in a new window]   FIGURE 2 Western blot analysis of SGLT1 in BBMVs in control, SEB, SEB-SDAP, and SEB-IC rats. Representative Western blots of BBMVs of small intestine from control (lanes 1 and 5), SEB (lanes 2 and 6), SEB-SDAP (lanes 3 and 7), and SEB-IC rats (lanes 4 and 8) blotted with anti-SGLT1 antibody in the presence (lanes 1 to 4) and in the absence (lanes 5 to 8) of the antigenic peptide. Each lane contained 30 µg of protein. Molecular mass standard is shown on the left.

View larger version (113K): [in this window] [in a new window]   FIGURE 3 Immunohistochemical localization of SGLT1 in control, SEB, SEB-SDAP, and SEB-IC rats. Representative images of indirect immunofluorescence of SGLT1 in the jejunum, showing the typical localization of SGLT1 on the apical membrane of enterocytes and the differing degree of SGLT1 expression among the experimental groups.

	DISCUSSION

TOP ABSTRACT METHODS DISCUSSION LITERATURE CITED

 
We have recently characterized a rat model of intestinal inflammation induced by the i.p. administration of SEB. The model shows increased MPO activity, increased water content in feces, and activation of lymphoid populations of Peyer’s patches, without affecting blood variables, food intake, or body weight (14). In the present study, we demonstrated that administration of SEB also affects the intestinal absorption of nutrients by reducing the capacity of the jejunum to transport D-Glc through the apical SGLT1, without changing the affinity constant of the transporter for the substrate. The hypothesis that this effect of SEB is due to a reduction in the number of D-Glc transporters in the brush border membrane was further supported by Western blot results and by immunohistochemical localization of SGLT1 along the villus. Sundaram et al. (26) also observed a specific reduction of Na⁺-glucose cotransport during chronic ileitis due to inhibition of SGLT1 expression in the apical membrane, in a model based on the administration of Eimeria magna oocytes to rabbits; Sekikawa et al. (27) observed a strong reduction in SGLT1 expression in the jejunum without changes in SGLT1 mRNA transcription in rats infected with the nematode Nippostrongylus brasiliensis. The recent demonstration that IFN downregulates Na⁺-coupled D-Glc transport in T84 cells (28) and that TNF inhibits D-fructose uptake in rabbit intestine (29) supports the view that cytokines produced during inflammatory processes may be involved in the control of nutrient transporter expression.

Our results from immune staining SGLT1 showed that the protein is present in absorptive epithelial cells along the crypt-villus axis, with higher expression in the upper villous region than in the mid and basal regions, confirming the results of Ferraris et al. (30). The findings that the integrity of the mucosa and the size of the villi were not affected by SEB administration support the view that the effects of SEB on mucosal morphology are small, if any. Therefore, the changes in D-Glc transport kinetics observed in rats challenged with SEB are due to specific effects on the function of SGLT1. The kinetic analysis of D-Glc transport also showed that SEB increased D-Glc K_d 3-fold. This observation raised the possibility that SEB affected the passive flux of D-Glc across a low affinity GLUT-type facilitated mechanism located in the apical membrane (31). However, the use of specific inhibitors demonstrated that our brush border vesicles lacked any facilitated D-Glc transport and confirmed that the rise in the transmembrane D-Glc flux during the enterotoxin-induced mucosal inflammation was the result of increased D-Glc simple diffusion.

SEB administration had no observable effect on amino acid uptake rates in the present study. This differs from the results of Topouchian et al. (20), who reported a marked decrease in leucine and glutamate fluxes across the mucosa of rats infected with C. parvum, an effect that was attributed to a decrease in the Na⁺ electrochemical gradient (18). We observed no effect of SEB administration on Na⁺/K⁺-ATPase in the mucosal homogenates either, indicating that the absorption of nutrients whose uptake depends on the maintenance of Na⁺ and electrical gradients across the membrane will not be affected.

In rats challenged with SEB, SDAP increased SGLT1 maximal transport capacity. No changes occurred in the SEB-IC group. This effect of SDAP was confirmed by Western and immunohistochemistry analyses of the mucosa. SDAP, a complex mixture of serum proteins used as food additives in farm animal production, improves growth and performance in pigs (8) and has been suggested as an alternative to antimicrobial medication (11). Although the mechanism of action of SDAP is still controversial, there is evidence that it prevents pathogen infectivity by improving immunocompetence and reducing bacterial adhesion to the mucosa (32). Recently, Bosi et al. (9) showed that SDAP can also reduce proinflammatory cytokine expression in the gut of early-weaned piglets challenged with enterotoxigenic Escherichia coli K88, and Pérez-Bosque et al. (14) have observed that SDAP brings SEB-induced cytotoxic populations back to values close to those in healthy rats. These findings agree with the lower intravillous lamina propria cell density observed by Jiang et al. (33) and are consistent with the view that SDAP can limit the production of cytokines by modulating the immune response.

The nutritional consequences of increased passive permeability and reduced mediated uptake on total D-Glc absorption are difficult to predict. After a meal, the luminal concentration of D-Glc is expected to be high, and in this condition absorption of D-Glc in vivo by apical transporters and by simple diffusion will also be high. The effects of SEB on passive permeability would enhance D-Glc absorption by the nonmediated transcellular pathway, fully compensating for the small reduction in SGLT1 V_max. We calculated that in control rats, at a luminal D-Glc concentration of 50 mmol/L, 25% of total uptake would take place by the mediated mechanism and 75% by simple diffusion, whereas in SEB rats, these figures would be 6 and 94%, respectively. At low luminal D-Glc concentrations, however, the contribution of enhanced K_d would be low, while the mediated pathway would contribute substantially. We estimated that at a luminal D-Glc concentration of 0.2 mmol/L, a level typically found during interdigestive periods (34), SDAP would increase the intestinal capacity to absorb D-Glc by 8–9%. This small but significant effect may contribute to the increase in growth and performance observed in farm animals fed SDAP supplements (8,9).

	ACKNOWLEDGMENTS

 
The rabbit polyclonal antibody raised against the synthetic peptide corresponding to amino acids 564–575 of the rabbit intestinal SGLT1 sequence and the antigenic peptide were generously provided by Prof. M. Kasahara. The authors gratefully acknowledge the technical assistance of Ms. Sandra Rubio.

	FOOTNOTES

 
¹ Presented in part at the 19th Meeting of the European Intestinal Transport Group, Guilford, UK, 2004 [Garriga, C., Pérez-Bosque, A., Amat, C., Campbell, J. M., Quigley, J. D., Polo, J. & Moretó, M. (2004) Effects of diets supplemented with animal plasma and immunoglobulin concentrate on intestinal transport of glucose and amino acids in rats challenged with the Staphylococcus aureus enterotoxin B. J. Physiol. Biochem. 60:164 (abs.)].

² Supported by the programs PROFIT (FIT-010000–2003-164) and Eureka Euroagri (E!2452) and by grant 2001SGR0142 (Generalitat de Catalunya, Spain).

⁴ Abbreviations used: BBMV, brush border membrane vesicle; D-Glc, D-glucose; GLUT2, glucose transporter type 2; IC, immunoglobulin concentrate; i.p., intraperitoneal; K_d, diffusion constant; K_m, Michaelis constant; MPO, myeloperoxidase; SDAP, spray-dried animal plasma; SEB, Staphylococcus aureus enterotoxin B; SEB-IC, Staphylococcus aureus enterotoxin B plus immunoglobulin concentrate; SEB-SDAP, Staphylococcus aureus enterotoxin B plus spray-dried animal plasma; SGLT1, sodium glucose transporter 1; UMPO, unit of myeloperoxidase activity; V_max, maximal transport rate.

Manuscript received 8 February 2005. Initial review completed 4 March 2005. Revision accepted 27 April 2005.

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