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The Journal of Nutrition Vol. 127 No. 6 June 1997, pp. 1077-1083
Copyright ©1997 by the American Society for Nutritional Sciences

Dietary Soybean Protein Increases Insulin Receptor Gene Expression in Wistar Fatty Rats when Dietary Polyunsaturated Fatty Acid Level Is Low1,2

Nobuko Iritani3, Tomomi Sugimoto, Hitomi Fukuda, Masumi Komiya, and Hitoshi Ikeda*

Tezukayama Gakuin College, Sakai, Osaka 590-01, Japan and * Pharmaceutical Research Division, Takeda Chemical Industries, Osaka 532, Japan

ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
FOOTNOTES
LITERATURE CITED

ABSTRACT

To investigate the effects of different dietary fatty acids and proteins on glucose tolerance and insulin receptor gene expression, Wistar fatty rats (genetically obese, noninsulin-dependent diabetes mellitus) and their lean littermates (8 wk old) were fed a casein or soybean protein diet containing 9% partially saturated beef tallow (plus 1% corn oil), 10% corn oil or 10% fish oil for 3 wk. In glucose tolerance tests, plasma insulin concentrations were significantly higher in obese rats fed corn oil or fish oil than in those fed partially saturated beef tallow, particularly in the soybean protein groups. However, plasma glucose concentrations were not significantly affected by dietary protein or fat. The insulin receptor mRNA concentrations in livers and adipose tissues were higher in rats fed soybean protein/partially saturated beef tallow than in those fed any other protein/fat combination. Dietary soybean protein may help to reduce the insulin resistance, but only when a diet low in polyunsaturated fatty acids is consumed. On the other hand, the insulin receptor mRNA concentrations in adipose tissue were generally lower in the obese rats of all dietary groups than in the lean rats, suggesting that insulin resistance may be due to a defect of insulin receptor gene expression.

KEY WORDS: noninsulin-dependent diabetes mellitus · insulin receptor mRNA · insulin · soybean protein · polyunsaturated fatty acids · rats

INTRODUCTION

The Wistar fatty rat with noninsulin-dependent diabetes mellitus (NIDDM) was produced by combining the insulin resistance of the Wistar Kyoto strain with the fa gene of the Zucker strain for obesity (Ikeda et al. 1981). Wistar rats are obese, hyperphagic, hyperinsulinemic and hypertriglyceridemic. They also show impaired glucose tolerance (Ikeda et al. 1981) and glycemic response to exogenous insulin (Matsuo et al. 1984a). Moreover, Wistar fatty rats have elevated levels of hepatic glycolytic and lipogenic enzymes (Ikeda et al. 1981, Matsuo et al. 1984b, Sugiyama et al. 1989, Taketomi et al. 1975).

We previously found that hepatic lipogenic enzyme gene expression was similar in obese and lean rats fed a diet without polyunsaturated fatty acids (Iritani et al. 1995). When a corn oil diet was fed to the rats, however, the gene expression was reduced in the lean rats, but not in the obese rats. Consequently, when the rats were fed corn oil, lipogenic enzyme gene expression was higher in the obese rats than in the lean rats. Thus, it appeared that the higher gene expression in the obese rats can be ascribed to defects in polyunsaturated fatty acid-induced suppression. Moreover, polyunsaturated fatty acids suppress insulin's stimulation of lipogenic enzyme gene expression (Iritani and Fukuda 1995). Thus, to clarify the relationship between dietary polyunsaturated fatty acids and insulin resistance, we have investigated the effects of different dietary fatty acids on glucose tolerance and insulin receptor gene expression in obese rats with NIDDM. Moreover, because proteins may influence insulin-dependent gene expression (Iritani et al. 1996), the effects of two different dietary proteins were also investigated.

MATERIALS AND METHODS

Materials. [alpha -32P]dCTP (111 TBq/mmol) was purchased from ICN Pharmaceuticals, (Costa Mesa, CA). Nylon filter (Hybond N) was purchased from Amersham (Buckinghamshire, U.K.). Insulin assay kit was obtained from Eiken Chemical (Tokyo, Japan). Most other reagents were obtained from Sigma (St. Louis, MO) and Wako (Osaka, Japan).

Animals. Female Wistar fatty rats (fa/fa, fa/Fa) and their lean littermates (Fa/Fa) (Ikeda et al. 1981), 8 wk old, obtained from Takeda Chemical (Osaka, Japan), were fed synthetic diets for 3 wk. Table 1 shows the diet compositions and the fatty acid compositions of partially saturated beef tallow (saturated fat), corn oil and cod liver oil (fish oil). Rats were individually housed in wire-bottomed cages kept in a temperature-controlled room (24°C) under an automatic lighting schedule (0800-2000 h). The rats had free access to water and were given equal amounts of diet/rat every day within each phenotype. The amount of diet consumed by a rat was measured at 1700 h every day and the amount of diet expected to be consumed was given for the following day.

Table 1. Composition of diet

[View Table]

Fig. 1. Effects of dietary protein and fat types on plasma glucose and insulin concentrations in portal vein (Panels A, C) and inferior vena cava (Panels B, D) of obese and lean rats. Wistar fatty rats (8 wk old) were fed the casein or soybean protein diets (containing 9% saturated fat +1% corn oil, 10% corn or 10% fish oil) for 3 wk and then killed at age 11 wk. Panels A and B show the plasma glucose concentrations of portal vein and inferior vena cava, respectively, and Panels C and D, the corresponding insulin concentrations, respectively. Means with different letters are significantly different (P < 0.05) in each panel. Means with asterisks are significantly different from the corresponding results of portal vein (Student's t test). Values are means ± SD (n = 9).
[View Larger Version of this Image (43K GIF file)]

Table 2. Effect of arginine addition to casein diet on plasma insulin concentrations in obese rats1,2

[View Table]

The oral glucose tolerance test was done 10-12 d after feeding the experimental diets to the rats. Rats were given a 400 g/L glucose solution (3 g glucose/kg body wt) by a stomach tube after being deprived of food for 20 h. Blood was withdrawn with a heparinized syringe from the tail vein.

The rats (11 wk old) were decapitated after blood was withdrawn with a heparinized syringe from the portal vein and then the inferior vena cava while under diethyl ether anesthesia. The rats were not deprived of diet and were killed between 900 and 1000 h in the morning. Plasma was obtained by centrifugation of heparinized blood at 1200 × g at 4°C for 20 min. Liver, white adipose tissue and pancreas were immediately removed and frozen in liquid nitrogen and stored at -80°C. Care and treatment of experimental animals were in accordance with the Guide for the Care and Use of Laboratory Animals (NRC 1985).

In another experiment (Table 2), the obese rats were fed the 10% corn oil/18% soybean protein or casein diet (with or without 0.5% arginine) for 1 wk and then blood was withdrawn from the tail vein. Casein and soybean protein contained 3.51 and 7.73 % arginine (0.63 and 1.39 g/100 g diet), respectively.

Slot-blot hybridization assay. Human insulin receptor cDNA (Ebina et al. 1985) was a generous gift from Y. Ebina (Institute for Enzyme Research, University of Tokushima, Japan). The genomic clone of rat rRNA was obtained from the Japanese Cancer Research Resources Bank (Mishima, Japan). A BamH1/EcoR1 fragment (~1 kb) of this clone was isolated and used as a probe for 18S rRNA. Total RNA was isolated from liver or white adipose tissue by the method of acid guanidium thiocyanate-phenol-chloroform extraction (Chomczynski and Sacchi 1987). To measure the mRNA concentrations of insulin receptors, the total RNA (20-50 µg) was denatured with formamide, spotted on nylon filter and then radiated with ultraviolet light for 5 min. The filter was prehybridized and then hybridized with 32P-labeled cDNA as described previously (Katsurada et al. 1990). Relative densities of the hybridization signals were determined by scanning the autoradiograms at 525 nm and normalized to the values of 18S rRNA.
Fig. 2. Effects of dietary protein and fat types on plasma glucose and insulin concentrations of obese and lean rats in glucose tolerance test. In the oral glucose tolerance test, rats received a 400 g/L glucose solution (3g/kg) after being deprived of food for 20 h. Panels A, B and C show the plasma glucose concentrations in rats fed saturated fat, corn oil and fish oil, respectively, and Panels D, E and F show the insulin concentrations in the rats, respectively. Means with different letters are significantly different (P < 0.05) in the glucose concentration (A, B, C) or insulin concentration (D, E, F). Values are means ± SD (n = 5-9).
[View Larger Version of this Image (32K GIF file)]

Table 3. Effects of dietary protein and fat types on increment values of plasma glucose and insulin concentrations in glucose tolerances test in obese and lean rats1

[View Table]

Table 4. Effects of dietary protein and fat types on pancreas insulin concentrations in obese and lean rats1

[View Table]

Fig. 3. Slot-blot hybridization analyses of hepatic insulin receptor mRNAs in obese and lean rats fed saturated fat/soybean protein or casein. Arbitrary units of the hybridization signals are shown under the bands of insulin receptor mRNA.
[View Larger Version of this Image (21K GIF file)]

Fig. 4. Effects of dietary protein and fat types on insulin receptor mRNA concentrations in livers (Panel A) and adipose tissue (Panel B) of obese and lean rats. The mRNA concentrations were normalized to those in lean rats fed the casein/saturated fat diet. Means with different letters are significantly different (P < 0.05). Values are means ± SD (n = 9).
[View Larger Version of this Image (44K GIF file)]

Preparation of partially purified insulin receptors. Insulin receptors were purified from livers essentially according to the method of Kadowaki et al. (1984). The livers were homogenized in 3 volumes of 50 mmol/L HEPES buffer (pH 7.6) containing 0.25 mol/L sucrose, 1 mg/L aprotinin, and 1 mmol/L phenylmethylsulfonyl fluoride. The homogenate was centrifuged at 10,000 × g for 20 min, followed by centrifugation of the supernatant at 100,000 × g for 90 min. The pellet was suspended in 50 mmol/L HEPES washing buffer (pH 7.6) containing 1 mg/L aprotinin and 1 mmol/L phenylmethylsulfonyl fluoride and was centrifuged at 100,000 × g for 60 min. The washing was repeated twice. The pellet was stored at -70°C for further purification. For experiments, samples were thawed and solubilized for 60 min in the presence of 2% Triton X-100. The insulin receptors were purified using a Wheat Germ-agarose column (Kadowaki et al. 1984). The procedures were conducted at 4°C.

Insulin binding to receptors. Lectin-purified insulin receptors were incubated with 125I-labeled insulin at 4°C for 16 h in the presence of various concentrations of unlabeled insulin in 200 µL of 25 mmol/L HEPES (pH 7.6) containing 0.05% Triton X-100, 20 mmol/L NaCl, 0.05 g/L bovine serum albumin and 150 µmol/L N-acetyl-D-glucosamine, essentially according to Hedo et al. (1981). With human gamma -globulin as carrier protein, receptor-bound insulin was precipitated with polyethylene glycol. Nonspecific binding was defined as the radioactivity precipitated in the presence of 3.1 µmol/L unlabeled insulin.

Analyses. Plasma glucose concentrations were determined by the glucose-oxidase method (Werner et al. 1970). Plasma and pancreas insulin concentrations were measured by a two-antibody system RIA according to the method of Morgan and Razarow (1963). Pancreas was homogenized and insulin was extracted with a cold solution of ethanol/2 mol/L HCl/water (75:1.5:23.5 v/v/v).

Statistical analysis. Three-way ANOVA was followed by inspection of all differences between pairs of means by using the least significant difference test (Snedecor and Cochram 1967). Portal vein vs. inferior vena cava comparisons in plasma glucose and insulin concentrations in Figure 1 were evaluated by Student's t test. Differences were considered significant at P < 0.05.

RESULTS

Plasma glucose and insulin concentrations. Wistar fatty rats were fed the experimental diets for 3 wk before they were killed at age 11 wk. The body weights of obese rats and their lean littermates were 317 ± 24.7 and 217 ± 12.2 g, respectively, at age 11 wk and showed no significant difference due to diet. Plasma glucose concentrations were not significantly affected by dietary protein or fat in lean rats (Fig. 1A, B). In obese rats fed casein, however, the glucose concentrations in the inferior vena cava (Fig. 1B) were higher in those fed fish oil than in those fed saturated fat or corn oil. Glucose concentrations were higher in obese rats than in lean rats in the fish oil group, but not in the saturated fat group. Glucose concentrations were higher in obese rats than in lean rats fed corn oil/casein, but not in those fed corn oil/soybean protein. In obese rats, the glucose concentrations in the inferior vena cava (Fig. 1B) were significantly higher than those in the portal vein (Fig. 1A).

Plasma insulin concentrations of both hepatic portal vein and inferior vena cava were significantly higher in the obese rats than in the lean rats (Fig. 1C, D). In obese rats, insulin concentrations were significantly higher in rats fed corn oil or fish oil than in those fed saturated fat, particularly in the soybean protein groups. In obese rats fed polyunsaturated fats, but not in those fed saturated fat, the concentrations were significantly higher in the soybean protein groups than in the casein groups. Insulin concentrations in the obese rats fed casein were higher in rats fed fish oil than in those fed saturated fat. Insulin concentrations were significantly higher in the portal vein than in the inferior vena cava in all dietary groups of obese rats, with the magnitude of the difference greatest in the rats fed soybean protein/polyunsaturated fat (Fig. 1C, D). These differences were not present in lean rats.

In the second experiment, the obese rats were fed the corn oil/soybean protein or casein diet (with or without 0.5% arginine) for 1 wk and then blood was withdrawn from the tail vein. The plasma insulin concentrations in the obese rats were significantly increased by the addition of 0.5% arginine to the 10% corn oil/casein diet for 1 wk (Table 2).

Glucose tolerance test. The obese rats showed glucose intolerance and hypersecretion of insulin in response to an oral glucose load (Fig. 2). The comparable increments of glucose and insulin concentrations (0-90 min after glucose intubation) were calculated from the increment values and are shown in Table 3. In the obese rats, the increment values of insulin concentrations were significantly higher in the following order: fish oil>corn oil>saturated fat in each protein group, and were higher in the soybean protein groups than in the casein groups fed both polyunsaturated fats.
Fig. 5. Effects of dietary protein and fat types on insulin binding to partially purified insulin receptors from livers of obese and lean rats. The experiments were performed using 4-7 rats per group and the Scatchard plots were calculated from the insulin binding data. A typical Scatchard plot for the insulin binding is shown.
[View Larger Version of this Image (13K GIF file)]

Insulin concentration in pancreas. Insulin concentrations in the pancreata of lean rats were not significantly affected by the diet. In both the protein groups fed saturated fat or corn oil diets, the pancreas insulin concentrations were significantly higher in the obese rats than in the lean rats (Table 4). In the obese rats fed soybean protein, the insulin concentration was lower in rats fed fish oil than in those fed saturated fat or corn oil; however, plasma insulin concentrations were considerably higher in the rats fed corn oil or fish oil (Fig. 1). The pancreas weight was not significantly affected by the diet or phenotype.

Insulin receptor mRNA concentrations in livers and adipose tissues. Figure 3 shows an example of slot-blot hybridization analysis of insulin receptors of rat livers. Relative densities normalized to the values of 18S rRNA were higher in rats fed soybean protein/saturated fat than in those fed casein/saturated fat in each phenotype. The insulin receptor mRNA concentrations in liver (Fig. 4A) and adipose tissue (Fig. 4B) were not significantly affected by the kind of dietary fatty acid in the casein groups in either obese or lean rats. However, in both obese and lean rats fed soybean protein/saturated fat, the insulin receptor mRNA concentrations were significantly higher than in those fed any other protein/fat combinations. Thus, dietary soybean protein stimulated insulin receptor gene expression in comparison with casein. Dietary polyunsaturated fatty acids suppressed the gene expression in comparison with saturated fat. The insulin receptor mRNA concentrations in adipose tissues were lower in the obese rats of all dietary groups than in the lean rats, whereas those in livers were not significantly different due to phenotype.

Insulin binding to receptors. A typical Scatchard plot for insulin binding to partially purified insulin receptors from livers of obese and lean rats is shown in Figure 5. The mean values of the insulin binding capacity and affinity constant are shown in Table 5. The insulin binding of the lean rats was lower in rats fed corn oil than in those fed saturated fat (regardless of dietary protein type) and was higher in rats fed soybean protein than in those fed casein. In the obese rats, however, the insulin binding capacities were not different in any dietary groups. The binding capacities were lower in the obese rats than in the lean. On the other hand, the insulin binding affinity to receptors was not altered by phenotype, or type of dietary fat or protein.

Table 5. Effects of dietary protein and fat types on binding capacity and affinity constant (high affinity sites) of purified insulin receptors in livers of obese and lean rats1

[View Table]

DISCUSSION

The plasma glucose concentrations were not significantly affected by the type of dietary protein or fat in lean rats, but tended to be higher in obese rats fed fish oil than in those fed saturated fat. However, plasma insulin concentrations were greatly affected by the type of dietary protein and fat. In the obese rats fed soybean protein, the plasma insulin concentrations were significantly higher in rats fed corn oil or fish oil than in those fed saturated fat.

In glucose tolerance tests, the increment values in plasma glucose concentrations were not significantly affected by dietary protein or fat type, but were higher in the obese rats than in the lean rats. However, the increment values in insulin concentrations were higher in the following order: fish oil>corn oil>saturated fat in both the protein groups of obese rats. The increment values in insulin concentrations of the obese rats fed corn oil or fish oil were higher in the soybean protein groups than in the casein groups. Unsaturated fats in combination with soybean protein may induce insulin resistance because insulin concentrations increased significantly, whereas plasma glucose concentrations remained almost stable. Even in the lean rats, the insulin concentrations were higher in the fish oil group than in the other groups. Therefore, polyunsaturated fat, particularly fish oil, appeared to stimulate insulin resistance.

In contrast, the insulin concentrations in the pancreas were significantly lower in the obese rats fed soybean protein/polyunsaturated fat than in those fed casein. Therefore, it appeared that the insulin secretion from pancreas was stimulated by dietary polyunsaturated fatty acids in the obese rats fed soybean protein, but not in those fed casein.

Soybean protein contains more arginine than casein. The plasma insulin concentrations in obese rats fed a casein/corn oil diet were significantly increased by addition of 0.5% arginine to the diet for 1 wk. It has been reported that arginine administration induced insulin secretion in in vivo studies (Levin et al. 1971, Rossetti et al. 1987). Insulin secretion appeared to be stimulated in the soybean protein/corn oil or fish oil groups as a result of greater intake of arginine from soybean protein (in combination with polyunsaturated fatty acids).

The insulin receptor mRNA concentrations in the liver and adipose tissue were significantly higher in obese and lean rats fed soybean protein/saturated fat than in those fed casein/saturated fat. The insulin receptor gene expression should be stimulated by dietary soybean protein in combination with saturated fat. However, the expression of this gene was suppressed by dietary polyunsaturated fatty acids. Moreover, the insulin receptor mRNA concentrations in adipose tissue were lower in the obese rats of all dietary groups than in the lean rats, whereas those in liver were not significantly different due to phenotype. Because the regulation of glucose transport is more complicated in liver than in adipose tissue, the insulin receptor activities would be more dependent on the insulin receptor gene expression in adipose tissue than in liver. Therefore, the insulin resistance in obese rats may be due to a defect of insulin receptor gene expression.

On the other hand, we reported previously that the insulin binding capacity of receptors in the liver of rats fed casein was lower in obese rats than in lean rats and was reduced by dietary corn oil in the lean rats but not in the obese rats (Iritani et al. 1995). Insulin receptor autophosphorylation and kinase activity toward the exogenous substrate was altered by dietary corn oil in a manner similar to the changes in insulin binding capacity. In the present experiment, in the lean rats, the insulin binding capacity of receptors was higher in the soybean protein group than in the casein group. In the obese rats, however, the insulin binding capacity was not affected by dietary protein or fat type and was lower than in the lean rats. The effects of polyunsaturated fatty acids on the insulin binding capacity of receptors were similar to the results of the previous study (Iritani et al. 1995). Thus, the effects of soybean protein and/or polyunsaturated fatty acids on the insulin receptor activities did not always coincide with the effects on gene expression. However, because the gene expression of inulin receptors was higher in the obese and lean rats fed soybean protein than in those fed casein, dietary soybean protein may help to improve insulin resistance, but only when rats are fed a diet low in polyunsaturated fatty acids.

FOOTNOTES

1   Supported by Tezukayama Gakuin College and Japan Private School Promotion Funds (Japan).
2   The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 USC section 1734 solely to indicate this fact.
3   To whom correspondence should be addressed.

Manuscript received 11 July 1996. Initial reviews completed 3 September 1996. Revision accepted 11 February 1997.

LITERATURE CITED

0022-3166/97 $3.00 ©1997 American Society for Nutritional Sciences



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