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Erschienen in: European Journal of Nutrition 2/2013

01.03.2013 | Original Contribution

Low-protein diet improves blood and urinary glucose levels and renal manifestations of diabetes in C57BLKS-db/db mice

verfasst von: Emi Arimura, Masahisa Horiuchi, Hiroaki Kawaguchi, Noriaki Miyoshi, Kohji Aoyama, Toru Takeuchi

Erschienen in: European Journal of Nutrition | Ausgabe 2/2013

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Abstract

Purpose

Dietary protein content is related clinically to the development of diabetic nephropathy. Here, we investigated how dietary protein content (12–24 % energy) within the range used by humans affected renal manifestations including the expressions of genes involved in the renin-angiotensin (RA) system in control and diabetic mice. Moreover, we examined the effects of dietary protein content on HbA1c and urinary glucose.

Methods

Control (CT) and leptin receptor-deficient obese (db) mice, 5 weeks old, were fed the diets below. Under ad libitum conditions, mice were fed 12, 18, and 24 % energy from protein (L-, M-, and H-diets) for 8 weeks. Under pair-feeding conditions, db mice were supplied H-diet (db-Hp) to the equivalent energy to that consumed by db-L mice. Renal manifestations and values related to glucose and insulin were examined biochemically and pathologically.

Results

Under ad libitum conditions, db mice consumed food and water dose dependently of the dietary protein content, although they were consumed similarly by CT mice. CT-L mice showed lower urinary albumin and kidney weight, in association with lower mRNA levels of angiotensinogen and renin, than CT-H mice. Under pair-feeding conditions, db-L mice showed a lower ratio of kidney/body weight, HbA1C, and urinary glucose, and a higher β-cell distribution rate in the pancreas than db-Hp mice.

Conclusions

Low-protein intake in the range used by humans may relieve renal manifestations through the suppressed expression of genes in the renal RA system of CT mice. On the other hand, in db mice, low-protein intake improved hyperglycemia and the renal manifestations of diabetes.
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Literatur
1.
Zurück zum Zitat Zimmet P, Alberti KGMM, Shaw J (2001) Global and societal implications of the diabetes epidemic. Nature 414:782–787CrossRef Zimmet P, Alberti KGMM, Shaw J (2001) Global and societal implications of the diabetes epidemic. Nature 414:782–787CrossRef
2.
Zurück zum Zitat Magkos F, Yannakoulia M, Chan JL, Mantzoros CS (2009) Management of the metabolic syndrome and type 2 diabetes through lifestyle modification. Ann Rev Nutr 29:223–256CrossRef Magkos F, Yannakoulia M, Chan JL, Mantzoros CS (2009) Management of the metabolic syndrome and type 2 diabetes through lifestyle modification. Ann Rev Nutr 29:223–256CrossRef
3.
Zurück zum Zitat Mogensen CE (2002) Diabetic renal disease in patients with type 2 diabetes mellitus: new strategies for prevention and treatment. Treat Endocrinol 1:3–11CrossRef Mogensen CE (2002) Diabetic renal disease in patients with type 2 diabetes mellitus: new strategies for prevention and treatment. Treat Endocrinol 1:3–11CrossRef
4.
Zurück zum Zitat Adler AI, Stevens RJ, Manley SE, Manley SE, Bilous RW, Cull CA, Holman RR, on behalf of the UKPDS group (2003) Development and progression of nephropathy in type 2 diabetes: the United Kingdom prospective diabetes study (UKPDS 64). Kidney Int 63:225-232 Adler AI, Stevens RJ, Manley SE, Manley SE, Bilous RW, Cull CA, Holman RR, on behalf of the UKPDS group (2003) Development and progression of nephropathy in type 2 diabetes: the United Kingdom prospective diabetes study (UKPDS 64). Kidney Int 63:225-232
5.
Zurück zum Zitat Remuzzi G, Benigni A, Remuzzi A (2006) Mechanisms of progression and regression of renal lesions of chronic nephropathies and diabetes. J Clin Invest 116:288–296CrossRef Remuzzi G, Benigni A, Remuzzi A (2006) Mechanisms of progression and regression of renal lesions of chronic nephropathies and diabetes. J Clin Invest 116:288–296CrossRef
6.
Zurück zum Zitat Jafar-Mohammadi B, McCarthy MI (2008) Genetics of type 2 diabetes mellitus and obesity–a review. Ann Med 40:2–10CrossRef Jafar-Mohammadi B, McCarthy MI (2008) Genetics of type 2 diabetes mellitus and obesity–a review. Ann Med 40:2–10CrossRef
7.
Zurück zum Zitat Lindgren CM, McCarthy MI (2008) Mechanisms of disease: genetic insights into the etiology of type 2 diabetes and obesity. Nat Clin Pract Endocrinol Metab 4:156–163CrossRef Lindgren CM, McCarthy MI (2008) Mechanisms of disease: genetic insights into the etiology of type 2 diabetes and obesity. Nat Clin Pract Endocrinol Metab 4:156–163CrossRef
8.
Zurück zum Zitat Tsunehara CH, Leonetti DL, Fujimoto WF (1990) Diet of second-generation Japanese-American men with and without non-insulin-dependent diabetes. Am J Clin Nutr 52:731–738 Tsunehara CH, Leonetti DL, Fujimoto WF (1990) Diet of second-generation Japanese-American men with and without non-insulin-dependent diabetes. Am J Clin Nutr 52:731–738
9.
Zurück zum Zitat Nanri A, Mizoue T, Noda M, Takahashi Y, Kato M, Inoue M, Tsugane S (2010) Rice intake and type 2 diabetes in Japanese men and women: the Japan public health center-based prospective study. Am J Clin Nutr 92:1468–1477CrossRef Nanri A, Mizoue T, Noda M, Takahashi Y, Kato M, Inoue M, Tsugane S (2010) Rice intake and type 2 diabetes in Japanese men and women: the Japan public health center-based prospective study. Am J Clin Nutr 92:1468–1477CrossRef
10.
Zurück zum Zitat American Diabetes Association (1987) Nutritional recommendations and principles for individuals with diabetes mellitus: 1986. Diabetes Care 10:126–132 American Diabetes Association (1987) Nutritional recommendations and principles for individuals with diabetes mellitus: 1986. Diabetes Care 10:126–132
11.
Zurück zum Zitat Gross JL, de Azevedo MJ, Silveiro SP, Canani LH, Caramori ML, Zelmanovitz T (2005) Diabetic nephropathy: diagnosis, prevention, and treatment. Diabetes Care 28:164–176CrossRef Gross JL, de Azevedo MJ, Silveiro SP, Canani LH, Caramori ML, Zelmanovitz T (2005) Diabetic nephropathy: diagnosis, prevention, and treatment. Diabetes Care 28:164–176CrossRef
12.
Zurück zum Zitat Zatz R, Meyer TW, Rennke HG, Brenner BM (1985) Predominance of hemodynamic rather than metabolic factors in the pathogenesis of diabetic glomerulopathy. Proc Natl Acad Sci USA 82:5963–5967CrossRef Zatz R, Meyer TW, Rennke HG, Brenner BM (1985) Predominance of hemodynamic rather than metabolic factors in the pathogenesis of diabetic glomerulopathy. Proc Natl Acad Sci USA 82:5963–5967CrossRef
13.
Zurück zum Zitat Williams AJ, Baker F, Walls J (1987) Effect of varying quantity and quality of dietary protein intake in experimental renal disease in rats. Nephron 46:83–90CrossRef Williams AJ, Baker F, Walls J (1987) Effect of varying quantity and quality of dietary protein intake in experimental renal disease in rats. Nephron 46:83–90CrossRef
14.
Zurück zum Zitat Fernández-Repollet E, Tapia E, Martínez-Maldonado M (1987) Effects of angiotensin-converting enzyme inhibition on altered renal hemodynamics induced by low protein diet in the rat. J Clin Invest 80:1045–1049CrossRef Fernández-Repollet E, Tapia E, Martínez-Maldonado M (1987) Effects of angiotensin-converting enzyme inhibition on altered renal hemodynamics induced by low protein diet in the rat. J Clin Invest 80:1045–1049CrossRef
15.
Zurück zum Zitat American Diabetes Association (2010) Standards of medical care in diabetes-2010. Diabetes Care 33:S11–S61CrossRef American Diabetes Association (2010) Standards of medical care in diabetes-2010. Diabetes Care 33:S11–S61CrossRef
16.
Zurück zum Zitat Piatti PM, Monti LD, Magni F et al (1994) Hypocaloric high-protein diet improves glucose oxidation and spares lean body mass: comparison to hypocaloric high-carbohydrate diet. Metabolism 43:1481–1487CrossRef Piatti PM, Monti LD, Magni F et al (1994) Hypocaloric high-protein diet improves glucose oxidation and spares lean body mass: comparison to hypocaloric high-carbohydrate diet. Metabolism 43:1481–1487CrossRef
17.
Zurück zum Zitat Gannon MC, Nuttall FQ, Saeed A, Jordan K, Hoover H (2003) An increase in dietary protein improves the blood glucose response in persons with type 2 diabetes. Am J Clin Nutr 78:734–741 Gannon MC, Nuttall FQ, Saeed A, Jordan K, Hoover H (2003) An increase in dietary protein improves the blood glucose response in persons with type 2 diabetes. Am J Clin Nutr 78:734–741
18.
Zurück zum Zitat Berger S, Vongaraya N (1966) Insulin response to ingested protein in diabetes. Diabetes 15:303–306 Berger S, Vongaraya N (1966) Insulin response to ingested protein in diabetes. Diabetes 15:303–306
19.
Zurück zum Zitat Linn T, Geyer R, Prassek S, Laube H (1996) Effect of dietary protein intake on insulin secretion and glucose metabolism in insulin-dependent diabetes mellitus. J Clin Endocrinol Metab 81:3938–3943CrossRef Linn T, Geyer R, Prassek S, Laube H (1996) Effect of dietary protein intake on insulin secretion and glucose metabolism in insulin-dependent diabetes mellitus. J Clin Endocrinol Metab 81:3938–3943CrossRef
20.
Zurück zum Zitat Linn T, Santosa B, Grönemeyer D, Aygen S, Scholz N, Busch M, Bretzel RG (2000) Effect of long-term dietary protein intake on glucose metabolism in humans. Diabetologia 43:1257–1265CrossRef Linn T, Santosa B, Grönemeyer D, Aygen S, Scholz N, Busch M, Bretzel RG (2000) Effect of long-term dietary protein intake on glucose metabolism in humans. Diabetologia 43:1257–1265CrossRef
21.
Zurück zum Zitat Leiter EH, Coleman DL, Eisenstein AB, Strack I (1981) Dietary control of pathogenesis in C57BL/KsJ db/db diabetes mice. Metabolism 30:554–562CrossRef Leiter EH, Coleman DL, Eisenstein AB, Strack I (1981) Dietary control of pathogenesis in C57BL/KsJ db/db diabetes mice. Metabolism 30:554–562CrossRef
22.
Zurück zum Zitat Leiter EH, Coleman DL, Ingram DK, Reynolds MA (1983) Influence of dietary carbohydrate on the induction of diabetes in C57BL/KsJ-db/db diabetes mice. J Nutr 113:184–195 Leiter EH, Coleman DL, Ingram DK, Reynolds MA (1983) Influence of dietary carbohydrate on the induction of diabetes in C57BL/KsJ-db/db diabetes mice. J Nutr 113:184–195
23.
Zurück zum Zitat Brouhard BH, Rajaraman S, LaGrone LF (1987) Effect of varied protein intake on the nephropathy of the diabetic mouse (C57BL/sJ db/db). Int J Pediatr Nephrol 8:59–68 Brouhard BH, Rajaraman S, LaGrone LF (1987) Effect of varied protein intake on the nephropathy of the diabetic mouse (C57BL/sJ db/db). Int J Pediatr Nephrol 8:59–68
24.
Zurück zum Zitat Layman DK, Clifton P, Gannon MC, Krauss RM, Nuttall FQ (2008) Protein in optimal health: heart disease and type 2 diabetes. Am J Clin Nutr 87:1571S–1575S Layman DK, Clifton P, Gannon MC, Krauss RM, Nuttall FQ (2008) Protein in optimal health: heart disease and type 2 diabetes. Am J Clin Nutr 87:1571S–1575S
25.
Zurück zum Zitat Tai ES, Tan MLS, Stevens RD et al (2010) Insulin resistance is associated with a metabolic profile of altered protein metabolism in Chinese and Asian-Indian men. Diabetologia 53:757–767CrossRef Tai ES, Tan MLS, Stevens RD et al (2010) Insulin resistance is associated with a metabolic profile of altered protein metabolism in Chinese and Asian-Indian men. Diabetologia 53:757–767CrossRef
26.
Zurück zum Zitat Westerterp-Plantenga MS, Nieuwenhuizen A, Tomé D, Soenen S, Westerterp KR (2009) Dietary protein weight loss, and weight maintenance. Annu Rev Nutr 29:21–41CrossRef Westerterp-Plantenga MS, Nieuwenhuizen A, Tomé D, Soenen S, Westerterp KR (2009) Dietary protein weight loss, and weight maintenance. Annu Rev Nutr 29:21–41CrossRef
27.
Zurück zum Zitat Teixeria SR, Tappenden KA, Erdman JW Jr (2003) Altering dietary protein type and quantity reduces urinary albumin excretion without affecting plasma glucose concentrations in BKS.cg-m +Lepr db /+ Lepr db (db/db) mice. J Nutr 133:673–678 Teixeria SR, Tappenden KA, Erdman JW Jr (2003) Altering dietary protein type and quantity reduces urinary albumin excretion without affecting plasma glucose concentrations in BKS.cg-m +Lepr db /+ Lepr db (db/db) mice. J Nutr 133:673–678
28.
Zurück zum Zitat Chen H, Charlat O, Tartaglia LA et al (1996) Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice. Cell 84:491–495CrossRef Chen H, Charlat O, Tartaglia LA et al (1996) Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice. Cell 84:491–495CrossRef
29.
Zurück zum Zitat Sharma K, McCue P, Dunn SR (2003) Diabetic kidney disease in the db/db mouse. Am J Physiol Renal Physiol 284:F1138–F1144 Sharma K, McCue P, Dunn SR (2003) Diabetic kidney disease in the db/db mouse. Am J Physiol Renal Physiol 284:F1138–F1144
30.
Zurück zum Zitat Matsumoto M, Tanimoto M, Gohda T et al (2008) Effect of pitavastatin on type 2 diabetes mellitus nephropathy in KK-Ay/Ta mice. Metabolism 57:691–697CrossRef Matsumoto M, Tanimoto M, Gohda T et al (2008) Effect of pitavastatin on type 2 diabetes mellitus nephropathy in KK-Ay/Ta mice. Metabolism 57:691–697CrossRef
31.
Zurück zum Zitat Tozzo E, Ponticiello R, Swartz J et al (2007) The dual peroxisome proliferator-activated receptor α/γ activator muraglitazar prevents the natural progression of diabetes in db/db mice. J Pharm Experim Ther 321:107–115CrossRef Tozzo E, Ponticiello R, Swartz J et al (2007) The dual peroxisome proliferator-activated receptor α/γ activator muraglitazar prevents the natural progression of diabetes in db/db mice. J Pharm Experim Ther 321:107–115CrossRef
32.
Zurück zum Zitat Yajima K, Hirose H, Fujita H et al (2003) Combination therapy with PPARγ and PPARα agonists increases glucose-stimulated insulin secretion in db/db mice. Am J Physiol Endocr Metab 284:E966–E971 Yajima K, Hirose H, Fujita H et al (2003) Combination therapy with PPARγ and PPARα agonists increases glucose-stimulated insulin secretion in db/db mice. Am J Physiol Endocr Metab 284:E966–E971
33.
Zurück zum Zitat Garris DR, Garris BL (2005) Estrogenic restoration of functional pancreatic islet cytoarchitecture in diabetes (db/db) mutant C57BL/KsJ mice: relationship to estradiol localization, systemic glycemia, and persistent hyperinsulinemia. Cell Tissue Res 319:231–242CrossRef Garris DR, Garris BL (2005) Estrogenic restoration of functional pancreatic islet cytoarchitecture in diabetes (db/db) mutant C57BL/KsJ mice: relationship to estradiol localization, systemic glycemia, and persistent hyperinsulinemia. Cell Tissue Res 319:231–242CrossRef
34.
Zurück zum Zitat Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159CrossRef Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159CrossRef
35.
Zurück zum Zitat Maezawa Y, Yokote K, Sonezaki K et al (2006) Influence of C-peptide on early glomerular changes in diabetic mice. Diabetes Metab Res Rev 22:313–322CrossRef Maezawa Y, Yokote K, Sonezaki K et al (2006) Influence of C-peptide on early glomerular changes in diabetic mice. Diabetes Metab Res Rev 22:313–322CrossRef
36.
Zurück zum Zitat Reich HN, Oudit GY, Penninger JM, Scholey JW, Herzenberg AM (2008) Decreased glomerular and tubular expression of ACE2 in patients with type 2 diabetes and kidney disease. Kidney Int 74:1610–1616CrossRef Reich HN, Oudit GY, Penninger JM, Scholey JW, Herzenberg AM (2008) Decreased glomerular and tubular expression of ACE2 in patients with type 2 diabetes and kidney disease. Kidney Int 74:1610–1616CrossRef
37.
Zurück zum Zitat Juárez P, Vilchis-Landeros MM, Ponce-Coria J et al (2007) Soluble betaglycan reduces renal damage progression in db/db mice. Am J Physiol Renal Physiol 292:F321–F329CrossRef Juárez P, Vilchis-Landeros MM, Ponce-Coria J et al (2007) Soluble betaglycan reduces renal damage progression in db/db mice. Am J Physiol Renal Physiol 292:F321–F329CrossRef
38.
Zurück zum Zitat Correa-Rotter R, Hostetter TH, Rosenberg ME (1992) Effect of dietary protein on renin and angiotensinogen gene expression after renal ablation. Am J Physiol 262:F631–F638 Correa-Rotter R, Hostetter TH, Rosenberg ME (1992) Effect of dietary protein on renin and angiotensinogen gene expression after renal ablation. Am J Physiol 262:F631–F638
39.
Zurück zum Zitat Skøtt O, Briggs JP (1987) Direct demonstration of macula-mediated renin secretion. Science 237:1618–1620CrossRef Skøtt O, Briggs JP (1987) Direct demonstration of macula-mediated renin secretion. Science 237:1618–1620CrossRef
40.
Zurück zum Zitat Peters H, Border WA, Noble NA (2000) Angiotensin II blockade and low-protein diet produce additive therapeutic effects in experimental glomerulonephritis. Kidney Int 57:1493–1501CrossRef Peters H, Border WA, Noble NA (2000) Angiotensin II blockade and low-protein diet produce additive therapeutic effects in experimental glomerulonephritis. Kidney Int 57:1493–1501CrossRef
41.
Zurück zum Zitat Shafrir E, Ziv E, Mosthaf L (1999) Nutritionally induced insulin resistance and receptor defect leading to β-cell failure in animal models. Ann N Y Acad Sci 892:223–246CrossRef Shafrir E, Ziv E, Mosthaf L (1999) Nutritionally induced insulin resistance and receptor defect leading to β-cell failure in animal models. Ann N Y Acad Sci 892:223–246CrossRef
42.
Zurück zum Zitat Davis RC, Castellani LW, Hosseini M et al (2010) Early hepatic insulin resistance precedes the onset of diabetes in obese C57BLKS-db/db mice. Diabetes 59:1616–1625CrossRef Davis RC, Castellani LW, Hosseini M et al (2010) Early hepatic insulin resistance precedes the onset of diabetes in obese C57BLKS-db/db mice. Diabetes 59:1616–1625CrossRef
43.
Zurück zum Zitat Savino A, Pelliccia P, Giannini C et al (2011) Implications for kidney disease in obese children and adolescents. Pediatr Nephrol 26:749–758CrossRef Savino A, Pelliccia P, Giannini C et al (2011) Implications for kidney disease in obese children and adolescents. Pediatr Nephrol 26:749–758CrossRef
44.
Zurück zum Zitat Hems R, Ross BD, Berry MN, Krebs HA (1966) Gluconeogenesis in the perfused rat liver. Biochem J 101:284–292 Hems R, Ross BD, Berry MN, Krebs HA (1966) Gluconeogenesis in the perfused rat liver. Biochem J 101:284–292
45.
Zurück zum Zitat Bohnensack R, Fritz S (1991) Stimulation of alanine metabolism by ammonia in the perfused rat liver. Quantitative analysis by means of a mathematical model. Biochim Biophys Acta 1073:347–356CrossRef Bohnensack R, Fritz S (1991) Stimulation of alanine metabolism by ammonia in the perfused rat liver. Quantitative analysis by means of a mathematical model. Biochim Biophys Acta 1073:347–356CrossRef
Metadaten
Titel
Low-protein diet improves blood and urinary glucose levels and renal manifestations of diabetes in C57BLKS-db/db mice
verfasst von
Emi Arimura
Masahisa Horiuchi
Hiroaki Kawaguchi
Noriaki Miyoshi
Kohji Aoyama
Toru Takeuchi
Publikationsdatum
01.03.2013
Verlag
Springer-Verlag
Erschienen in
European Journal of Nutrition / Ausgabe 2/2013
Print ISSN: 1436-6207
Elektronische ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-012-0387-4

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