![[Feedback]](/icons/banner/feedbackACT.gif){kind=icon}
![[For Subscribers]](/icons/banner/subscriberACT.gif){kind=icon}
![[Archive]](/icons/banner/archiveACT.gif){kind=icon}
![[Search]](/icons/banner/searchACT.gif){kind=icon}
![[Contents]](/icons/banner/tocACT.gif){kind=icon}
|
|
|
|
|
||
Departments of
*
Fisiología de la Nutrición,
Nefrología y Metabolismo Mineral,
**
Patología Experimental,
Diabetes y Metabolismo de Lípidos, Instituto Nacional de Ciencias Médicas y Nutrición "Salvador Zubirán," y
Department of Biología, Facultad de Química, Universidad Nacional Autónoma de México, México, D.F, México
2To whom correspondence should be addressed. E-mail: nimbet{at}quetzal.innsz.mx.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
KEY WORDS: • nephrotic syndrome • lipid metabolism • rats • soy protein • sterol regulatory element binding protein-1
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
). Hyperlipidemia promotes mesangial damage, glomerular sclerosis and an increment in the permeability of the glomerular capillary wall. Taken together, these lipid abnormalities are dangerous and may accelerate the atherogenic process.
Restriction of protein intake ameliorates proteinuria in nephrotic patients and rats. Low protein diets improve not only proteinuria but also cholesterolemia and blood urea nitrogen (2
). However, despite their beneficial effects, low protein diets retard growth in young individuals and reduce tissue protein in adults (3
–5
). It has been proposed that consumption of diets containing vegetable protein may retard kidney damage by lowering the glomerular filtration rate and urinary albumin excretion (6
). Soy protein is a vegetable protein that sustains adequate growth rate in rats and infants. It has an amino acid profile that meets the requirement for each amino acid in humans and rats for growth and maintenance. Therefore, soy protein is considered to be a complete protein, with a protein digestibility–corrected amino acid score of 1 (7
,8
); it also has a high arginine/lysine ratio, which is associated with lower insulin secretion compared with protein of animal origin. Soy protein also contains isoflavones, which act as weak estrogens, inhibiting tyrosine kinase–dependent signal transduction processes and functioning as cellular antioxidants (9
). Epidemiologic evidence indicates that consumption of at least 25 g of soy protein daily has a hypocholesterolemic effect (10
). Anderson and colleagues (11
) in their meta-analysis, showed that the consumption of soy protein significantly decreased serum concentrations of total cholesterol, LDL cholesterol and triglycerides (TG), with a larger decrease in subjects with moderate or severe hypercholesterolemia. Thus, individuals with renal diseases may improve their abnormal lipid profile and reduce kidney damage by consuming soy protein.
The aim of the present study was to determine whether a 20% soy protein diet that meets the protein requirement of rats improves hypercholesterolemia and decreases proteinuria in rats with persistent severe urinary loss of proteins due to chronic glomerular disease compared with a 20% casein diet. We also examined the effect of a soy protein diet on the expression of some genes that regulate lipid metabolism to elucidate the possible mechanism by which soy protein decreases total cholesterol and TG concentrations.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Male Wistar rats (100 g) were obtained from the Experimental Research Department and Animal Care Facilities at the Instituto Nacional de Ciencias Médicas y Nutrición, México City. All were maintained in individual metabolic cages during the study and had free access to water. The rooms were lighted from 0700 to 1900 h and darkened from 1900 to 0700 h. Body weight and food consumption were registered every other day. Chronic experimental NS was induced by subcutaneous injection of puromycin aminonucleoside (PAN) (Sigma Chemical, St. Louis, MO), 50, 40, 40, and 25 mg/kg body on d 0, 14, 21 and 42, respectively. Control groups were injected with 9 g/L saline. Rats were killed on d 64 by decapitation after being anesthetized with CO2. Blood was collected from the neck, and was centrifuged at 1000 x g for 10 min. Serum was separated and stored at -20°C until analysis. At the end of the experiment, serum TG, cholesterol and creatinine (Cr) concentrations and TG and cholesterol contents of the main lipoprotein subclasses were measured. Urine was collected to measure Cr and total urinary protein. A liver sample from each rat was removed rapidly and immediately frozen and stored at -80°C for extraction of total RNA. A kidney sample was used for histological and immunohistochemical studies.
The protocol of the present study was approved by the Animal Ethics Committee of the Instituto Nacional de Ciencias Médicas y Nutrición. Experimental groups (n = 10) were classified as follows: 1) control rats fed 20% casein diet; 2) nephrotic rats fed 20% casein diet, 3) control rats fed 20% soy diet, and 4) nephrotic rats fed 20% soy diet. During the experimental period, rats had free access to the appropriate experimental diet (Table 1
). The isoflavone analysis of the soy protein (SUPRO 710) was performed by Protein Technologies International, St. Louis, MO. Soy protein isolated contained 1.38, 0.71 and 0.1 9 mg/g protein of genistein, daidzein and glycitein, respectively.
|
Renal function was evaluated by determining the Cr clearance. Serum and urine Cr were measured with a Cr analyzer model 2, (Beckman Instruments, Fullerton, CA). Urinary total protein was analyzed by the Lowry method (12
). Serum cholesterol and TG were measured enzymatically according to the instructions of the kit manufacturer (Lakeside Diagnostics, México, D.F.).
Insulin radioimmunoassay.
Serum insulin was determined by RIA using a rat insulin kit (Linco Research, St. Charles, MO). The sensitivity for the rat insulin assay was 50 pmol/L, and the intra- and interassay CV were <5%. Immune complexes were counted with a Cobra II gamma counter (Packard Instruments, Meriden, CT).
Density gradient ultracentrifugation (DGUC).
To characterize the density distributions and compositions of the apoB-containing lipoproteins, 3 mL of serum was fractionated by isopycnic DGUC using a Beckman SW 40 Ti rotor at 202,000 x g for 40 h at 15°C (13
). Briefly, serum density was increased to 1.063 kg/L by the addition of dry, solid KBr. A 0.5-mL cushion of 1.210 kg/L solution was placed at the bottom of the tube followed in order by 2 mL of the density-adjusted serum sample, 1 mL of 1.0464 kg/L solution, 1 mL of 1.0336 kg/L solution, 2 mL of 1.0271 kg/L solution, 2 mL of 1.0197 kg/L solution, 2 mL of 1.0117 kg/L solution, and 2 mL of 1.006 kg/L solution. After centrifuging, the gradient was eluted from the top using a peristaltic pump operating at a flow rate of 0.5 mL/min. Cholesterol and TG were measured in each 0.5-mL fraction as described above. VLDL, intermediate density lipoprotein (IDL) and LDL cholesterol were measured by ultracentrifugation using a sequential procedure (14
)
Extraction of total RNA and hybridization.
Total RNA was isolated from tissues according to Chomczynski and Sacchi (15
). For Northern blot analysis, 20 µg of RNA were electrophoresed in a 0.8% agarose gel containing 37% formaldehyde, transferred onto a nylon membrane filter (Hybond-N+, Amersham, Buckinghamshire, UK), and cross-linked with a UV crosslinker (Amersham). cDNA probes for the rat hepatic fatty acid synthase, LDL receptor, malic enzyme, ß-hydroxy-ß-methylglutaryl-CoA (HMG-CoA) synthase, HMG-CoA reductase and SREBP-1 were prepared by reverse transcriptase-polymerase chain reaction with the primers shown in Table 2
. Probes were labeled with deoxycytidine 5'[
-32P] triphosphate (110 TBq/mmol, Amersham) by using the rediprime DNA labeling system (Amersham). Filters were prehybridized with rapid-hyb buffer at 65°C for 30 min, and then hybridized with the labeled probe for 2.5 h at 65°C. Membranes were washed once with 2X citrate saline solution (SSC)/0.1% SDS at room temperature for 20 min and then washed twice with 0.1X SSC/0.1% SDS at 65°C for 15 min each time. Image digitization and quantitation of radioactive bands (cpm) in the membranes was done with an Instant Imager electronic autoradiography system (Amersham). Membranes were also exposed to X-ray film at -70°C with an intensifying screen.
|
Kidney tissue was fixed by immersion in buffered formalin (pH 7.4) and embedded in paraffin. Sections (3 µm) were stained with hematoxylin/eosin, Schiff’s periodic acid and Masson trichromic stain. Glomerular sclerosis was defined as glomerular capillary collapse, with increased mesangial matrix and capillary fibrotic adhesion to Bowman’s capsule. Glomeruli from each kidney (n = 100) were examined for evidence of glomerular sclerosis, and the incidence of sclerotic glomeruli was estimated by dividing the number of sclerotic glomeruli by the total number of glomeruli examined. In the same glomeruli, the percentage of sclerosis affecting the whole area of capillary loops and mesangium was determined by automated image analysis (Qwin Leica, Milton Keynes, UK).
For immunohistochemistry, kidney sections were mounted in silane-covered slides and deparaffinized; the endogenous activity of peroxidase was quenched with 0.03% H2O2 in absolute methanol. Kidney sections were incubated for 3 h at room temperature with biotin-labeled rabbit or goat polyclonal antibodies against interleukin-1 (IL-1), tumor necrosis factor- (TNF-) and transforming growth factor-ß (TGF-ß)(R&D System, Minneapolis, MN) diluted 1/150 or 1/250 in PBS. Bound antibodies were detected with the system avidin-biotin peroxidase (Vector, Burlingame, CA) and counterstained with hematoxylin.
Reagents and chemicals.
Nylon membrane filters (Hybond-N+), rediprime DNA labeling system and deoxycytidine 5' [-32P] triphosphate (110 TBq/mmol) were purchased from Amersham. The vitamin-free casein and the rest of the ingredients were obtained from Teklad (Madison, WI). Isolated soy protein (Supro 710) was kindly donated by Protein Technologies International, S.A. de C.V. (México).
Statistics.
Results are presented as means ± SEM. Statistical analysis was done by two-way ANOVA. Significant differences among groups were determined by Fisher’s protected least square difference test. When the error variance in the groups was heterogeneous, a logarithmic transformation of data was carried out before ANOVA. Differences were considered significant at P < 0.05 (Statview statistical analysis program, V.4.5, Abacus Concepts, Berkeley, CA).
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Soy protein– and casein-fed control rats consumed similar amounts of food during the 64-d study (Fig. 1A
). The induction of NS with PAN did not affect food intake except on d 28–35, when nephrotic rats consumed less food than controls (P < 0.05). Casein-fed control rats grew at the fastest rate, 
4.4 ± 0.9 g/d, whereas control rats fed soy protein grew at a rate of 3.6 ± 1.1 g/d (Fig. 1
B). Growth rates differed between the casein- and soy protein–fed groups from d 21 until the end of the study. During the first 30 d of the study, nephrotic rats had growth rates that did not differ from their diet controls (4.5 ± 1.0 and 3.6 ± 1.1 g/d, respectively). However, after d 40, nephrotic rats grew more slowly than controls (P < 0.05). At the end of the study, nephrotic rats fed the soy protein diet had gained less weight than nephrotic rats fed the casein diet, Fig. 1
B, (P < 0.05).
|
Total urinary protein excretion did not differ between the casein and soy protein–fed control groups (Table 3
). On d 64 of the study, urinary protein was 21-fold higher in nephrotic rats fed casein than in the control group (P < 0.05), whereas nephrotic rats fed soy protein excreted 12-fold more protein than the control group (P < 0.05). Thus, nephrotic rats fed soy protein excreted 53% less urinary protein than nephrotic rats fed casein.
|
. At the end of the study, nephrotic rats had a lower Cr clearance than the control groups (P < 0.05) and the reduction in Cr clearance in nephrotic rats fed soy protein (24%) was less than in nephrotic rats fed casein (67%). Serum insulin.
Control rats fed casein had the highest serum insulin concentration and it was 60% higher than in control rats fed soy protein (Table 3)
. NS rats fed casein or soy protein did not differ from one another but had 86 and 70% lower serum insulin concentrations than their respective control groups.
Serum lipids.
Serum TG and cholesterol concentrations did not differ between casein- and soy protein–fed control rats (Table 3)
. On d 64, nephrotic rats fed soy protein had 50 and 58% lower serum TG and cholesterol, respectively, than nephrotic rats fed casein. Serum TG were 5.2-fold higher in nephrotic rats fed casein than in their controls (P < 0.001), whereas levels in nephrotic rats fed soy protein were 2.7-fold higher than control rats fed soy protein (P < 0.01). The serum cholesterol concentration was 4.8- and 1.3-fold higher in nephrotic rats fed casein or soy protein compared with their respective controls (P < 0.01).
Lipoproteins.
Lipoprotein-TG concentrations did not differ between the control rats (Table 4
). Nephrotic rats fed casein had the highest TG concentrations in the VLDL, LDL and HDL fractions (P < 0.05); TG were found mainly in VLDL. Thus, nephrotic rats fed casein had 3.4-, 0.78- and 0.8-fold higher VLDL-, LDL-, and HDL-TG concentrations, respectively, than nephrotic rats fed soy protein.
|
). Nephrotic rats fed casein had 1.9-, 2.9- and 0.57-fold higher VLDL, LDL and HDL cholesterol concentrations, respectively, than nephrotic rats fed soy protein (P < 0.05). Cholesterol was found mainly in the LDL fraction. The DGUC showed that the main reduction in lipoproteins of nephrotic rats fed soy protein occurred in the dense LDL and light HDL fractions (Fig. 2
). It is important to point out that the sequential ultracentrifugation methods do not provide a clear-cut separation between LDL and HDL particles as has been previously reported (16
). However, the complementary use of lipoprotein analysis with the assessment of the lipoprotein distribution using the DGUC procedure indicated that soy protein ingestion affected lipoprotein distribution.
|
|
Nephrotic rats fed the casein diet developed segmental mesangial proliferation with matrix expansion, obliteration of capillary lumens and fibrosis with adhesion between the glomerular tuft and Bowman’s capsule. The interstitium showed patches of mononuclear cell inflammation with fibrosis, and many cortical tubules showed epithelial atrophy and hyaline cylinders in their lumens (Fig. 3A
). The incidence of glomeruli with sclerotic lesions in nephrotic rats fed casein was 76.6 ± 7.6%, and the percentage of fibrotic area in these glomeruli was 37.3 ± 9%. In contrast, nephrotic rats fed soy protein had a lower incidence of sclerotic glomeruli (17.8 ± 5.9%, P < 0.05), and a smaller fibrotic area affecting mesangial matrix and glomerular capillary loops (7.8 ± 9%, P < 0.05), with minimal interstitial fibrosis and tubular damage (Fig. 3
B). The immunohistochemistry study showed strong immunostaining to IL-1, TNF- and TGF-ß in mesangial cells, mesangial inflammatory cell infiltrate (Fig. 3
C, E, G) and tubular epithelial cells in nephrotic rats fed casein. In contrast, nephrotic rats fed soy protein had fewer glomerular cells with immunostaining to IL-1, TNF- and TGF-ß (Fig. 3
D, F, H). No histological abnormalities were observed in kidney of control rats fed casein or soy (not shown).
|
Control rats fed soy protein had lower (P < 0.05) gene expression of FAS, malic enzyme and the transcription factor SREBP-1 by 44, 47 and 54%, respectively, than control rats fed casein and greater (P < 0.05) expression of HMG-CoA synthase, HMG-CoA reductase and the LDL receptor by 94, 23 and 68%, respectively, (Figs. 4
and 5
). NS rats fed casein had lower expression of FAS, malic enzyme and SREBP-1 (51, 39 and 33%, respectively) but greater expression of HMG-CoA reductase (1.5-fold) than their diet controls (P < 0.05). NS rats fed soy protein had 27, 33 and 50% lower HMG-CoA synthase, HMG-CoA reductase and LDL receptor gene expression, respectively, compared with their diet controls.
|
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
). This process increases with time as the number of glomeruli damaged increases, resulting in a life-threatening condition. Therefore, prevention of further deterioration of the kidney will benefit individuals with this renal disease.
This study provides evidence that the consumption of soy protein reduces kidney damage in rats with NS induced with PAN compared with rats fed casein. Nephrotic rats fed soy protein had lower total urinary protein excretion than NS rats fed casein, as well as an improvement in Cr clearance. The possibility that the reduced urinary loss of plasma proteins was a direct consequence of lipid intake as suggested by D’Amico (18
) was ruled out because the concentration and type of fat were the same in the groups fed casein and soy protein diets.
The correction of the biochemical abnormalities in casein-fed nephrotic rats by the soy protein diet was also reflected in the histological studies. Administration of repeated doses of PAN to rats produced a kidney disease very similar to focal segmental glomerulosclerosis in humans (19
). The glomerular endothelium, mesangial cells and intraglomerular-infiltrated macrophages entrap lipoproteins, increasing the glomerular fibrotic lesion (20
–22
). These cells phagocytize and oxidize LDL, which contain cholesterol. Oxidized lipoproteins impair endothelial function and induce inflammation, evoking higher productions of IL-1, TNF- and TGF-ß, as in nephrotic rats fed casein (23
,24
). Nephrotic rats fed soy protein had less fibrotic damage and lower concentrations of IL-1, TNF- and TGFß (Fig. 3)
.
Several potential mechanisms can be proposed to explain the beneficial effect of soy. First, the liver increases the synthesis of plasma proteins to compensate for urinary protein losses during NS (25
,26
). Due to the mobilization of several proteins from the liver to the plasma, there is also an increase in VLDL particles. The signal to the liver to increase lipoprotein synthesis probably involves the sensing of decreased plasma oncotic pressure. This is supported by the normalization of plasma lipid and lipoprotein levels in nephrotic patients and rats infused with albumin or dextran (1
). Furthermore, decreases in VLDL, IDL and LDL catabolic pathways have been reported during NS. These abnormalities are related to a decreased activity and amount of lipoprotein lipase (27
), increased hepatic lipase activity, and decreased activity and number of LDL receptors (28
). We demonstrated that nephrotic rats fed casein had 6.9- and 11.3-fold higher plasma VLDL-TG and LDL cholesterol concentrations, respectively, than their diet controls, whereas nephrotic rats fed soy protein had 1.3- and 1.9-fold higher VLDL-TG and LDL cholesterol than their controls. As a consequence, nephrotic rats fed soy protein had lower serum total cholesterol and TG than nephrotic rats fed casein. It appears that the consumption of a soy protein diet prevents glomerular injury because less development of glomerular sclerosis and reduced production of the proinflammatory cytokines were observed in nephrotic rats fed soy protein. As a consequence of the reduction in kidney damage, lipid abnormalities were reduced.
In addition to its hypocholesterolemic properties, soy protein may reduce kidney damage by a second mechanism involving soy isoflavones. Isolated soy protein provides 2 mg isoflavones/g. The main isoflavones present in the soy protein, genistein and daidzein, may reduce glomerular damage during nephrosis by protecting LDL particles from oxidation (29
), although their antioxidant capacity is limited (9
). Also, isoflavones can react with reactive oxygen species. These species are produced by neutrophils as part of the inflammatory response in kidney during NS. The main reactive oxygen species are hydrogen peroxide and superoxide anion, which react with chloride and nitric oxide, leading to the formation of hypochlorous acid and peroxynitrite. Both compounds react with tyrosine residues on proteins, producing chlorinated and nitrated proteins with abnormal function. Because isoflavones have a phenolic ring, they can react competitively with the hypochlorous acid and peroxynitrate, reducing the chlorination and nitration of proteins (9
,30
) and preventing glomeruli damage. Therefore, soy protein may reduce kidney damage during NS by reducing circulating concentrations of cholesterol and by preventing the production of abnormal proteins as a consequence of the inflammatory response.
An interesting finding was that despite the increase in the VLDL-TG fraction in NS rats, there was no increase in the concentration of the mRNA of genes involved in fatty acid synthesis. The transcription factor SREBP-1 was induced in control rats fed casein, whereas it was almost not expressed in the control rats fed soy protein or in the NS rats. SREBP-1 is an important factor for the transactivation of genes involved in fatty acid synthesis (31
). It was established recently that SREBP-1 is up-regulated by insulin (32
,33
). The consumption of casein by control rats for 64 d produced hyperinsulinemia, which was associated with an increased expression of SREBP-1, whereas ingestion of soy protein by control rats produced less than half of the serum insulin concentrations of control rats fed casein. However, in nephrotic rats fed casein or soy protein, there was almost no induction of SREBP-1 mRNA, perhaps because of their low insulin concentration (Table 3)
, which resulted in no stimulation of the SREBP-1 gene. Low insulin levels can in part be the result of the urinary excretion of this hormone during NS (34
). The reduction of the SREBP-1 mRNA concentration in nephrotic rats fed casein was associated with a concomitant reduction of FAS and malic enzyme mRNA concentrations compared with their diet controls. It is important to point out that mRNA levels alone do not necessarily indicate enzyme/protein activity or metabolic events; we are conducting studies, therefore, to assess the concentration of the mature form of SREBP-1 in nuclei of control and NS rats fed soy protein or casein to further support the evidence of the present work. Nonetheless, these data suggest that the elevated concentrations of TG present in the VLDL particles are mainly the result of a lipoprotein lipase alteration affecting the clearance of this lipoprotein, rather than an increased synthesis of TG by the liver.
However, we observed almost no expression of hepatic LDL receptor mRNA in nephrotic rats fed casein or soy protein diets. However, nephrotic rats fed casein had greater HMG-CoA reductase mRNA abundance than nephrotic rats fed soy protein. The difference in the expression of the two genes in nephrotic rats fed casein and those fed soy protein could be due in part to the different set of transcription factors required for the activation of HMG-CoA reductase and LDL receptor genes (35
,36
). Thus, the low activity of the LDL receptor in NS rats observed previously (37
) is due in part to a reduction in the abundance of its mRNA. The increase in hepatic HMG-CoA reductase in nephrotic rats fed casein may indicate an increase in the rate of cholesterol biosynthesis, as has been observed by others (38
,39
).
Soy protein has additional nutritional advantages over animal protein. As little as 25 g of soy protein is all that is required to reduce cholesterol in hypercholesterolemic subjects (10
). Thus, soy protein represents a safe, viable and practical nonpharmacologic approach to lowering cholesterol. It has been suggested that high protein intake may have deleterious effects on the kidney, particularly in preexistent kidney disease (40
). However, our results suggest that a 20% protein diet of vegetable origin given to NS rats reduces proteinuria, renal damage and the inflammatory response, as well as LDL cholesterol, VLDL-TG, and serum total cholesterol and TG concentrations compared with NS rats that consumed the casein diet. Studies in humans with NS consuming a soy diet have found decreases in plasma total cholesterol and LDL cholesterol concentrations; however, these individuals lost weight, in part due to the low concentration of soy protein in the diet (41
). Soy protein may have a role in the prevention and treatment of kidney disease. It has been shown in normal subjects that vegetable proteins induce renal changes comparable with those obtained by reducing the total amount of protein in the diet and prevent the vasodilatory and proteinuric effects of protein from meat. These effects appear to be mediated also by hormonal changes involving glucagon secretion and renal prostaglandin production (6
). Therefore, an adequate amount of soy protein that meets the protein requirement, rather than protein-restricted diets, may be beneficial in the long-term treatment of chronic renal diseases, thereby avoiding the deterioration of the nutritional status of individuals. However, further assessment of the chronic effects of high vegetable protein diet on renal function is required before its adoption in humans (42
). Furthermore, the hypocholesterolemic effect of soy protein may be of particular benefit to this type of patient because elevated levels of cholesterol can exacerbate the disease progression.
|
FOOTNOTES |
|---|
3 Abbreviations used: apo, apolipoprotein; Cr, creatinine; DGUC, density gradient ultracentrifugation; FAS, fatty acid synthase; HMG-CoA, ß-hydroxy-ß-methylglutaryl-CoA; IDL, intermediate density lipoprotein; IL-1, interleukin-1; NS, nephrotic syndrome; PAN, puromycin aminonucleoside; SREBP, sterol regulatory element binding protein; SSC, citrate saline solution; TG, triglycerides; TGF-ß, transforming growth factor-ß; TNF-, tumor necrosis factor-.
Manuscript received 18 April 2002. Initial review completed 8 May 2002. Revision accepted 13 June 2002.
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
1. Wheeler, D. C. & Bernard, D. B. (1994) Lipid abnormalities in the nephrotic syndrome: causes, consequences, and treatment. Am. J. Kidney Dis. 23:331-346.[Medline]
2. Ascencio, C., Torres, N., Sandoval, R. L., Cruz, C., Pedraza-Chavarri, J. & Tovar, A. R. (1997) Reduced kidney branched chain aminotransferase expression in puromycin aminonucleoside-induced nephrotic syndrome. Life Sci. 61:2407-2415.[Medline]
3. Harper, A. E. (1984) Biological factors influencing the utilization of amino acids. Velazquez, A. Bourges, H. eds. Genetic Factors in Nutrition 1984 Academic Press Orlando, FL. .
4. Torres, N., Martinez, L., Alemán, G., Bourges, H. & Tovar, A. R. (1998) Histidase expression is regulated by dietary protein at pretranslational level in rat liver. J. Nutr. 128:818-824.
5. Tovar, A. R., Santos, A., Halhali, A., Bourges, H. & Torres, N. (1998) Hepatic histidase gene expression responds to protein rehabilitation in undernourished growing rats. J. Nutr. 128:1631-1635.
6. Kontessis, P., Jones, S., Dodds, R., Trevisan, R., Nosadini, R., Fioretto, P., Borsato, M., Sacerdoti, D. & Viberti, G. (1990) Renal, metabolic and hormonal responses to ingestion of animal and vegetable proteins. Kidney Int. 38:136-144.[Medline]
7. Anderson, J. W., Smith, B. M. & Washnock, C. S. (1999) Cardiovascular and renal benefits of dry bean and soybean intake. Am. J. Clin. Nutr. 70:464S-474S.
8. Messina, M. J. (1999) Legumes and soybeans: overview of their nutritional profiles and health effects. Am. J. Clin. Nutr. 70:439S-450S.
9. Barnes, S., Boersma, B., Kim, H., Xu, J., Patel, R., Darley-Usmar, V. M. & Kirk, M. (2000) Isoflavonoids and chronic disease: mechanisms of action. Biofactor 12:209-214.[Medline]
10. Bakhit, R. M., Klein, B. P., Essex-Sorlie, D., Ham, J. O., Erdman, J. W. & Potter, S. M. (1994) Intake of 25 g of soybean protein with or without soybean fiber alters plasma lipids in men with elevated cholesterol concentrations. J. Nutr. 124:213-222.
11. Anderson, J. W., Johnstone, B. M. & Cook-Newell, M. E. (1995) Meta-analysis of the effects of soy protein intake on serum lipids. N. Engl. J. Med. 333:276-282.
12. Lowry, O. H., Rosebrough, N. J., Farr, A. L. & Randal, R. J. (1951) Protein measurements with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
13. Aguilar-Salinas, C. A., Barrett, P. H., Kelber, J., Delmez, J. & Schonfeld, G. (1995) Physiologic mechanisms of action of lovastatin in nephrotic syndrome. J. Lipid Res. 36:188-199.[Abstract]
14. Anonymous (1974) Lipid and lipoprotein analysis. Manual of Laboratory Operations 1974 U.S. Department of Health, Education and Welfare Washington, DC. .
15. Chomczynski, P. & Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.[Medline]
16. Lusk, L. T., Walker, W. F., DuBien, L. H. & Getz, G. S. (1979) Isolation and partial characterization of high-density lipoprotein HDL1 from rat plasma by gradient centrifugation. Biochem. J. 183:83-90.[Medline]
17. Moorhead, J. F., Chan, M. K., El-Nahas, M. & Varghese, Z. (1982) Lipid nephrotoxicity in chronic progressive glomerular and tubulo-interstitial disease. Lancet 2:1309-1312.[Medline]
18. D’Amico, G. & Gentile, M. G. (1993) Influence of diet on lipid abnormalities in human renal disease. Am. J. Kidney Dis. 22:151-157.[Medline]
19. Glasser, R. J., Velosa, J. A. & Michael, A. F. (1977) Experimental model of focal sclerosis. Relationship to protein excretion in aminonucleoside nephrosis. Lab. Invest. 36:516-519.
20. Keane, W. F. (1994) Lipids and the kidney. Kidney Int 46:910-920.[Medline]
21. Soon, L. H., Yong, J. J., Cho, K. B., Sook, K. Y., Zheng, Z. Y. & Keun, C. H. (1997) Dietary antioxidant inhibits lipoproteins oxidation and renal injury in experimental focal segmental glomerulosclerosis. Kidney Int. 51:1151-1159.[Medline]
22. Wanner, C., Greiber, S., Krämer-Guth, A., Heinloth, A. & Galle, J. (1997) Lipids and progression of renal disease: role of modified low density lipoprotein and lipoprotein(a). Kidney Int. 63(Suppl.):S102-S106.
23. Boerder, W. A. & Noble, N. A. (1993) Cytokines in kidney disease: the role of transforming growth factor-ß. Am. J. Kidney Dis. 22:105-113.[Medline]
24. Kovacs, E. J. (1991) Fibrogenic cytokines: the role of immune mediators in the development of scar tissue. Immunol. Today 12:17-23.[Medline]
25. Lewandowsky, A. E., Liao, W. S., Stinson-Fisher, C. A., Kent, J. D. & Jefferson, L. S. (1988) Effects of experimentally induced nephrosis on protein synthesis in rat liver. Am. J. Physiol. 254:C634-C642.
26. Pedraza-Chaverri, J. & Huberman, A. (1991) Actinomycin D blocks the hepatic functional albumin mRNA increase in aminonucleoside-nephrotic rats. Nephron 59:648-650.[Medline]
27. Eckel, R. H. (1989) Lipoprotein lipase. A multifunctional enzyme relevant to common metabolic diseases. N. Engl. J. Med. 320:1060-1068.[Abstract]
28. Joven, J., Villabona, C., Vilella, E., Masana, L., Alberti, R. & Valles, M. (1990) Abnormalities of lipoprotein metabolism in patients with the nephrotic syndrome. N. Engl. J. Med. 323:579-584.[Abstract]
29. Wiseman, H., O’Reilly, J. D., Adlercreutz, H., Mallet, A. I., Bowey, E. A., Rowland, I. R. & Sanders, T. A. (2000) Isoflavone phytoestrogens consumed in soy decrease F2-isoprostane concentrations and increase resistance of low-density lipoprotein to oxidation in humans. Am. J. Clin. Nutr. 72:395-400.
30. Boersma, B. J., Patel, R. P., Kirk, M., Jackson, P. L., Muccio, D., Darley-Usmar, V. M. & Barnes, S. (1999) Chlorination and nitration of soy isoflavones. Arch. Biochem. Biophys. 368:265-275.[Medline]
31. Shimano, H., Horton, J. D., Hammer, R. E., Shimomura, I., Brown, M. S. & Goldstein, J. L. (1996) Overproduction of cholesterol and fatty acid causes massive liver enlargement in transgenic mice expressing truncated SREBP-1a. J. Clin. Invest. 98:1575-1584.[Medline]
32. Shimomura, I., Bashmakov, Y., Ikemoto, S., Horton, J. D., Brown, M. S. & Goldstein, J. L. (1999) Insulin selectively increases SREBP-1c mRNA in livers of rats with streptozocin-induced diabetes. Proc. Natl. Acad. Sci. USA 96:13656-13661.
33. Shimomura, I., Matsuda, M., Hammer, R. E., Bashmakov, Y., Brown, M. S. & Goldstein, J. L. (2000) Decreased IRS-2 and increased SREBP-1c lead to mixed insulin resistance and sensitivity in livers of lipodystrophic and ob/ob mice. Mol. Cell 6:77-86.[Medline]
34. Rabkin, R., Ryan, M. P. & Duckworth, W. C. (1984) The renal metabolism of insulin. Diabetologia 27:351-357.[Medline]
35. Bennet, M. K. & Osborne, T. F. (2000) Nutrient regulation of gene expression by the sterol regulatory element binding proteins: increased recruitment of gene-specific coregulatory factors and selective hyperacetylation of histone H3 in vivo. Proc. Natl. Acad. Sci. USA 97:6340-6344.
36. Shimano, H., Shimomura, I., Hammer, R. E., Hero, J., Goldstein, J. L., Brown, M. S. & Horton, J. D. (1997) Elevated levels of SREBP-2 and cholesterol synthesis in livers of mice homozygous for a targeted disruption of the SREBP-1 gene. J. Clin. Invest. 100:2115-2124.[Medline]
37. Vaziri, N. D. & Liang, K. H. (1996) Down-regulation of hepatic LDL receptor expression in experimental nephrosis. Kidney Int. 50:887-893.[Medline]
38. Gheradi, E., Vecchia, L. & Calandra, S. (1980) Experimental nephrotic syndrome in the rat induced by puromycin aminonucleoside. Exp. Mol. Pathol. 32:128-135.[Medline]
39. Marsh, J. B. & Sparks, C. E. (1979) Hepatic secretion of lipoproteins in the rat and the effect of experimental nephrosis. J. Clin. Invest. 64:1229-1237.
40. Brenner, B. M., Meyer, T. W. & Hostetter, T. H. (1982) Dietary protein intake and the progressive nature of kidney disease: the role of hemodynamically mediated glomerular injury in the pathogenesis of progressive glomerular sclerosis in aging, renal ablation, and intrinsic renal disease. N. Engl. J. Med. 307:652-659.[Medline]
41. D’Amico, G., Gentile, M. G., Manna, G., Fellin, G., Ciceri, R., Cofano, F., Petrini, C., Lavarda, F., Perolini, S. & Porrini, M. (1992) Effect of vegetarian soy diet on hyperlipidaemia in nephrotic syndrome. Lancet 339:1131-1134.[Medline]
42. Jenkins, D. J., Kendall, C. W., Vidgen, E., Augustin, L. S., Van Erk, M., Geelen, A., Parker, T., Faulkner, D., Vuksan, V., Josse, R. G., Leiter, L. A. & Connelly, P. W. (2001) High-protein diets in hyperlipidemia: effect of wheat gluten on serum lipids, uric acid, and renal function. Am. J. Clin. Nutr. 74:57-63.
This article has been cited by other articles:
|
|
 |
|
  A. R. Tovar, I. Torre-Villalvazo, M. Ochoa, A. L. Elias, V. Ortiz, C. A. Aguilar-Salinas, and N. Torres Soy protein reduces hepatic lipotoxicity in hyperinsulinemic obese Zucker fa/fa rats J. Lipid Res., September 1, 2005; 46(9): 1823 - 1832. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Zhan and S. C Ho Meta-analysis of the effects of soy protein containing isoflavones on the lipid profile Am. J. Clinical Nutrition, February 1, 2005; 81(2): 397 - 408. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Trujillo, V. Ramirez, J. Perez, I. Torre-Villalvazo, N. Torres, A. R. Tovar, R. M. Munoz, N. Uribe, G. Gamba, and N. A. Bobadilla Renal protection by a soy diet in obese Zucker rats is associated with restoration of nitric oxide generation Am J Physiol Renal Physiol, January 1, 2005; 288(1): F108 - F116. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. E. Fair, M. R. Ogborn, H. A. Weiler, N. Bankovic-Calic, E. P. Nitschmann, S. C. Fitzpatrick-Wong, and H. M. Aukema Dietary Soy Protein Attenuates Renal Disease Progression After 1 and 3 Weeks in Han:SPRD-cy Weanling Rats J. Nutr., June 1, 2004; 134(6): 1504 - 1507. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Ascencio, N. Torres, F. Isoard-Acosta, F. J. Gomez-Perez, R. Hernandez-Pando, and A. R. Tovar Soy Protein Affects Serum Insulin and Hepatic SREBP-1 mRNA and Reduces Fatty Liver in Rats J. Nutr., March 1, 2004; 134(3): 522 - 529. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. W. Anderson Diet First, Then Medication for Hypercholesterolemia JAMA, July 23, 2003; 290(4): 531 - 533. [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
