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Published in: European Journal of Nutrition 1/2017

01-02-2017 | Original Contribution

Deteriorated glucose metabolism with a high-protein, low-carbohydrate diet in db mice, an animal model of type 2 diabetes, might be caused by insufficient insulin secretion

Authors: Emi Arimura, Wijang Pralampita Pulong, Ancah Caesarina Novi Marchianti, Miwa Nakakuma, Masaharu Abe, Miharu Ushikai, Masahisa Horiuchi

Published in: European Journal of Nutrition | Issue 1/2017

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Abstract

Purpose

We previously showed the deleterious effects of increased dietary protein on renal manifestations and glucose metabolism in leptin receptor-deficient (db) mice. Here, we further examined its effects on glucose metabolism, including urinary C-peptide. We also orally administered mixtures corresponding to low- or high-protein diets to diabetic mice.

Methods

In diet experiments, under pair-feeding (equivalent energy and fat) conditions using a metabolic cage, mice were fed diets with different protein content (L diet: 12 % protein, 71 % carbohydrate, 17 % fat; H diet: 24 % protein, 59 % carbohydrate, 17 % fat) for 15 days. In oral administration experiments, the respective mixtures (L mixture: 12 % proline, 71 % maltose or starch, 17 % linoleic acid; H mixture: 24 % proline, 59 % maltose or starch, 17 % linoleic acid) were supplied to mice. Biochemical parameters related to glucose metabolism were measured.

Results

The db–H diet mice showed significantly higher water intake, urinary volume, and glucose levels than db–L diet mice but similar levels of excreted urinary C-peptide. In contrast, control-H diet mice showed significantly higher C-peptide excretion than control-L diet mice. Both types of mice fed H diet excreted high levels of urinary albumin. When maltose mixtures were administered, db–L mixture mice showed significantly higher blood glucose after 30 min than db–H mixture mice. However, db mice administered starch–H mixture showed significantly higher blood glucose 120–300 min post-administration than db–L mixture mice, although both groups exhibited similar insulin levels.

Conclusions

High-protein, low-carbohydrate diets deteriorated diabetic conditions and were associated with insufficient insulin secretion in db mice. Our findings may have implications for dietary management of diabetic symptoms in human patients.
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Literature
1.
go back to reference 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.
go back to reference 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
3.
go back to reference 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
4.
go back to reference 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
5.
go back to reference Pan Y, Guo LL, Jin HM (2008) Low-protein diet for diabetic nephropathy: a meta-analysis of randomized controlled trials. Am J Clin Nutr 88:660–666 Pan Y, Guo LL, Jin HM (2008) Low-protein diet for diabetic nephropathy: a meta-analysis of randomized controlled trials. Am J Clin Nutr 88:660–666
6.
go back to reference Rietman A, Schwarz J, Tomé D, Kok FJ, Mensink M (2014) High dietary protein intake, reducing or eliciting insulin resistance? Eur J Clin Nutr 68:973–979CrossRef Rietman A, Schwarz J, Tomé D, Kok FJ, Mensink M (2014) High dietary protein intake, reducing or eliciting insulin resistance? Eur J Clin Nutr 68:973–979CrossRef
7.
go back to reference 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
8.
go back to reference Metges CC, Barth CA (2000) Metabolic consequences of a high dietary-protein intake in adulthood: assessment of the available evidence. J Nutr 130:886–889 Metges CC, Barth CA (2000) Metabolic consequences of a high dietary-protein intake in adulthood: assessment of the available evidence. J Nutr 130:886–889
9.
go back to reference Kuroe A, Fukushima M, Usami M et al (2003) Impaired β-cell function and insulin sensitivity in Japanese subjects with normal glucose tolerance. Diabetes Res Clin Pract 59:71–77CrossRef Kuroe A, Fukushima M, Usami M et al (2003) Impaired β-cell function and insulin sensitivity in Japanese subjects with normal glucose tolerance. Diabetes Res Clin Pract 59:71–77CrossRef
10.
go back to reference 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
11.
go back to reference 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
12.
go back to reference Arimura E, Horiuchi M, Kawaguchi H, Miyoshi N, Aoyama K, Takeuchi T (2013) Low-protein diet improves blood and urinary glucose levels and renal manifestations of diabetes in C57BLKS-db/db mice. Eur J Nutr 52:813–824CrossRef Arimura E, Horiuchi M, Kawaguchi H, Miyoshi N, Aoyama K, Takeuchi T (2013) Low-protein diet improves blood and urinary glucose levels and renal manifestations of diabetes in C57BLKS-db/db mice. Eur J Nutr 52:813–824CrossRef
13.
go back to reference Goldberg T, Weijing C, Peppa M et al (2004) Advanced glycoxidation end products in commonly consumed foods. J Am Diet Assoc 104:1287–1291CrossRef Goldberg T, Weijing C, Peppa M et al (2004) Advanced glycoxidation end products in commonly consumed foods. J Am Diet Assoc 104:1287–1291CrossRef
14.
go back to reference 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
15.
go back to reference 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 84:491495 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 84:491495
16.
go back to reference Stechman MJ, Ahmad BN, Loh NY et al (2010) Establishing normal plasma and 24-hour urinary biochemistry ranges in C3H, BALB/c and C57BL/6 J mice following acclimatization in metabolic cage. Lab Anim 44:218–225CrossRef Stechman MJ, Ahmad BN, Loh NY et al (2010) Establishing normal plasma and 24-hour urinary biochemistry ranges in C3H, BALB/c and C57BL/6 J mice following acclimatization in metabolic cage. Lab Anim 44:218–225CrossRef
17.
go back to reference Burke BJ, Hartog M, Heaton KW, Hooper S (1982) Assessment of the metabolic effects of dietary carbohydrate and fibre by measuring urinary excretion of C-peptide. Hum Nutr Clin Nutr 36:373–380 Burke BJ, Hartog M, Heaton KW, Hooper S (1982) Assessment of the metabolic effects of dietary carbohydrate and fibre by measuring urinary excretion of C-peptide. Hum Nutr Clin Nutr 36:373–380
18.
go back to reference Linn T, Strate C, Schneider K (1999) Diet promotes β-cell loss by apoptosis in prediabetic nonobese diabetic mice. Endocrinology 140:3767–3773 Linn T, Strate C, Schneider K (1999) Diet promotes β-cell loss by apoptosis in prediabetic nonobese diabetic mice. Endocrinology 140:3767–3773
19.
go back to reference 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
20.
go back to reference Teixeira 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 +Leprdb/+ Leprdb (db/db) mice. J Nutr 133:673–678 Teixeira 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 +Leprdb/+ Leprdb (db/db) mice. J Nutr 133:673–678
21.
go back to reference Nordquist L, Lai EY, Sjöquist M, Patzak A, Persson AEG (2008) Proinsulin C-peptide constricts glomerular afferent arterioles in diabetic mice. A potential renoprotective mechanism. Am J Physiol Regul Integr Comp Physiol 294:R836–R841CrossRef Nordquist L, Lai EY, Sjöquist M, Patzak A, Persson AEG (2008) Proinsulin C-peptide constricts glomerular afferent arterioles in diabetic mice. A potential renoprotective mechanism. Am J Physiol Regul Integr Comp Physiol 294:R836–R841CrossRef
22.
go back to reference 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
23.
go back to reference Aguilera A, Reis de Souza TC, Mariscal-Landín G, Escobar K, Montaño S, Bernal MG (2015) Standardized ileal digestibility of proteins and amino acids in sesame expeller and soya bean meal in weaning piglets. J Anim Physiol Anim Nutr 99:728–736CrossRef Aguilera A, Reis de Souza TC, Mariscal-Landín G, Escobar K, Montaño S, Bernal MG (2015) Standardized ileal digestibility of proteins and amino acids in sesame expeller and soya bean meal in weaning piglets. J Anim Physiol Anim Nutr 99:728–736CrossRef
24.
go back to reference Jensen KT, Löbmann K, Rades T, Grohganz H (2014) Involving co-amorphous drug formulations by the addition of the highly water soluble amino acid, proline. Pharmaceutics 6:416–435CrossRef Jensen KT, Löbmann K, Rades T, Grohganz H (2014) Involving co-amorphous drug formulations by the addition of the highly water soluble amino acid, proline. Pharmaceutics 6:416–435CrossRef
25.
go back to reference Krebs HA, Notton BM, Hems R (1966) Gluconeogenesis in mouse-liver slices. Biochem J 101:607–617CrossRef Krebs HA, Notton BM, Hems R (1966) Gluconeogenesis in mouse-liver slices. Biochem J 101:607–617CrossRef
26.
go back to reference Chen Y, Cao Y, Zhao L, Kong X, Hua Y (2014) Macronutrients and micronutrients of soybean oil bodies extracted at different pH. J Food Sci 79:C1285–C1291CrossRef Chen Y, Cao Y, Zhao L, Kong X, Hua Y (2014) Macronutrients and micronutrients of soybean oil bodies extracted at different pH. J Food Sci 79:C1285–C1291CrossRef
27.
go back to reference Bois-Joyeux B, Chanez M, Azzout B, Peret J (1986) Studies on the early changes in rat hepatic fructose 2,6-bisphosphate and enzymes in response to a high protein diet. J Nutr 116:446–454 Bois-Joyeux B, Chanez M, Azzout B, Peret J (1986) Studies on the early changes in rat hepatic fructose 2,6-bisphosphate and enzymes in response to a high protein diet. J Nutr 116:446–454
28.
go back to reference Li H, Lee J, He C, Zou M-H, Xie Z (2014) Suppression of the mTORC1/STAT3/Notch1 pathway by activated AMPK prevents hepatic insulin resistance induced by excess amino acids. Am J Physiol Endocrinol Metab 306:E197–E209CrossRef Li H, Lee J, He C, Zou M-H, Xie Z (2014) Suppression of the mTORC1/STAT3/Notch1 pathway by activated AMPK prevents hepatic insulin resistance induced by excess amino acids. Am J Physiol Endocrinol Metab 306:E197–E209CrossRef
29.
go back to reference Peters AL, Davidson MB (1993) Protein and fat effects on glucose responses and insulin requirements in subjects with insulin-dependent diabetes mellitus. Am J Clin Nutr 58:555–560 Peters AL, Davidson MB (1993) Protein and fat effects on glucose responses and insulin requirements in subjects with insulin-dependent diabetes mellitus. Am J Clin Nutr 58:555–560
30.
go back to reference Kiehm TG, Anderson JW, Ward K (1976) Beneficial effects of a high carbohydrate, high fiber diet on hyperglycemic diabetic men. Am J Clin Nutr 29:895–899 Kiehm TG, Anderson JW, Ward K (1976) Beneficial effects of a high carbohydrate, high fiber diet on hyperglycemic diabetic men. Am J Clin Nutr 29:895–899
31.
go back to reference Chandalia M, Garg A, Lutjohann D et al (2000) Beneficial effects of high dietary fiber intake in patients with type 2 diabetes mellitus. N Engl J Med 342:1392–1398CrossRef Chandalia M, Garg A, Lutjohann D et al (2000) Beneficial effects of high dietary fiber intake in patients with type 2 diabetes mellitus. N Engl J Med 342:1392–1398CrossRef
32.
go back to reference The Council for Science and Technology, Ministry of Education, Culture, Sports, Science and Technology, JAPAN (2010) Amino acid composition of foods in 2010, Standard tables of food composition in Japan. Official Gazette Co-operation of Japan, Tokyo The Council for Science and Technology, Ministry of Education, Culture, Sports, Science and Technology, JAPAN (2010) Amino acid composition of foods in 2010, Standard tables of food composition in Japan. Official Gazette Co-operation of Japan, Tokyo
Metadata
Title
Deteriorated glucose metabolism with a high-protein, low-carbohydrate diet in db mice, an animal model of type 2 diabetes, might be caused by insufficient insulin secretion
Authors
Emi Arimura
Wijang Pralampita Pulong
Ancah Caesarina Novi Marchianti
Miwa Nakakuma
Masaharu Abe
Miharu Ushikai
Masahisa Horiuchi
Publication date
01-02-2017
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 1/2017
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-015-1075-y

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