Low-Carbohydrate Diet Inhibits Different Advanced Glycation End Products in Kidney Depending on Lipid Composition but Causes Adverse Morphological Changes in a Non-Obese Model Mice
Abstract
:1. Introduction
2. Materials and Methods
2.1. Materials
2.2. Animals and Diet
2.3. Serum and Tissue Sampling
2.4. Western Blot Analysis
2.5. Morphological Analysis
2.6. Biochemical Measurements
2.7. N(epsilon)-(carboxymethyl)lysine (CML) and N(epsilon)-(carboxyethyl) (CEL) Levels in Kidney and Serum
2.8. Statistical Analysis
3. Results
3.1. Body Weight and Weights of Liver and Kidney
3.2. Weights of EATs and Adipocyte Area.
3.3. Morphological Analysis of Kidney
3.4. CEL and CML Levels in Serum and Kidney
3.5. Biochemical Analysis
3.6. Hepatic Glycogen Accumulation
3.7. AMP-Activated Protein Kinase (AMPK) Activation in Kidney and Liver
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
- Astrup, A.; Meinert Larsen, T.; Harper, A. Atkins and other low-carbohydrate diets: Hoax or an effective tool for weight loss? Lancet 2004, 364, 897–899. [Google Scholar] [CrossRef]
- Bravata, D.M.; Sanders, L.; Huang, J.; Krumholz, H.M.; Olkin, I.; Gardner, C.D.; Bravata, D.M. Efficacy and safety of low-carbohydrate diets: A systematic review. JAMA 2003, 289, 1837–1850. [Google Scholar] [CrossRef] [PubMed]
- Fields, H.; Ruddy, B.; Wallace, M.R.; Shah, A.; Millstine, D. Are Low-Carbohydrate Diets Safe and Effective? J. Am. Osteopath. Assoc. 2016, 116, 788–793. [Google Scholar] [CrossRef] [PubMed]
- Halton, T.L.; Hu, F.B. The effects of high protein diets on thermogenesis, satiety and weight loss: A critical review. J. Am. Coll. Nutr. 2004, 23, 373–385. [Google Scholar] [CrossRef]
- Pawlak, R. Low-carbohydrate, high-protein diets for management of type 2 diabetes. Am. J. Clin. Nutr. 2013, 98, 247–248. [Google Scholar] [CrossRef]
- Shai, I.; Schwarzfuchs, D.; Henkin, Y.; Shahar, D.R.; Witkow, S.; Greenberg, I.; Golan, R.; Fraser, D.; Bolotin, A.; Vardi, H.; et al. Weight loss with a low-carbohydrate, Mediterranean, or low-fat diet. N. Engl. J. Med. 2008, 359, 229–241. [Google Scholar] [CrossRef]
- Pesta, D.H.; Samuel, V.T. A high-protein diet for reducing body fat: Mechanisms and possible caveats. Nutr. Metab. 2014, 11, 53. [Google Scholar] [CrossRef]
- Layman, D.K.; Boileau, R.A.; Erickson, D.J.; Painter, J.E.; Shiue, H.; Sather, C.; Christou, D.D. A reduced ratio of dietary carbohydrate to protein improves body composition and blood lipid profiles during weight loss in adult women. J. Nutr. 2003, 133, 411–417. [Google Scholar] [CrossRef]
- Rolland, C.; Hession, M.; Murray, S.; Wise, A.; Broom, I. Randomized clinical trial of standard dietary treatment versus a low-carbohydrate/high-protein diet or the LighterLife Programme in the management of obesity. J. Diabetes 2009, 1, 207–217. [Google Scholar] [CrossRef]
- Kadowaki, S.; Kaburagi, T. Low Carbohydrate-High Protein Diet in Non-obese Mice. Jpn. J. Nut. Diet. 2016, 74, 51–59. [Google Scholar] [CrossRef]
- Axen, K.V.; Axen, K. Very low-carbohydrate versus isocaloric high-carbohydrate diet in dietary obese rats. Obesity (Silver Spring) 2006, 14, 1344–1352. [Google Scholar] [CrossRef] [PubMed]
- Lagiou, P.; Sandin, S.; Lof, M.; Trichopoulos, D.; Adami, H.O.; Weiderpass, E. Low carbohydrate-high protein diet and incidence of cardiovascular diseases in Swedish women: Prospective cohort study. BMJ 2012, 344, e4026. [Google Scholar] [CrossRef] [PubMed]
- Noto, H.; Goto, A.; Tsujimoto, T.; Noda, M. Low-carbohydrate diets and all-cause mortality: A systematic review and meta-analysis of observational studies. PLoS ONE 2013, 8, e55030. [Google Scholar] [CrossRef] [PubMed]
- Fontana, L.; Eagon, J.C.; Trujillo, M.E.; Scherer, P.E.; Klein, S. Visceral fat adipokine secretion is associated with systemic inflammation in obese humans. Diabetes 2007, 56, 1010–1013. [Google Scholar] [CrossRef]
- Kim, J.Y.; van de Wall, E.; Laplante, M.; Azzara, A.; Trujillo, M.E.; Hofmann, S.M.; Schraw, T.; Durand, J.L.; Li, H.; Li, G.; et al. Obesity-associated improvements in metabolic profile through expansion of adipose tissue. J. Clin. Invest. 2007, 117, 2621–2637. [Google Scholar] [CrossRef]
- De Konig, L.; Fung, T.T.; Liao, X.; Chiuve, S.E.; Rimm, E.B.; Willett, W.C.; Spiegelman, D.; Hu, F.B. Low carbohydrate diet scores and risk of type 2 diabetes in men. Am. J. Clin. Nutr. 2011, 93, 844–850. [Google Scholar] [CrossRef]
- Kadowaki, S.; Kaburagi, T. Different Effects on Hepatic Lipid Metabolism of Low Carbohydrate Diet on Obese and Non-Obese Mice. Diabetes Obes. Int. J. 2017, 2, 1–10. [Google Scholar]
- Wang, Q.; Afshin, A.; Yakoob, M.Y.; Singh, G.M.; Rehm, C.D.; Khatibzadeh, S.; Micha, R.; Shi, P.; Mozaffarian, D.; Ezzati, M.; et al. Impact of nonoptimal intakes of saturated, polyunsaturated, and trans fat on global burdens of coronary heart disease. J. Am. Heart Assoc. 2016, 5, e002891. [Google Scholar] [CrossRef]
- Taylor, M.K.; Sullivan, D.K.; Mahnken, J.D.; Burns, J.F.; Swerdlow, R.H. Feasibility and efficacy data from a ketogenic diet intervention in Alzheimer’s disease. Alzheimers Dement. 2018, 4, 28–36. [Google Scholar] [CrossRef]
- Zupec-Kania, B.; Spellman, E. An overview of the ketogenic diet for pediatric epilepsy. Nutr. Clin. Pract. 2018, 23, 589–596. [Google Scholar] [CrossRef]
- Aminzadeh-Gohari, S.; Feichtinger, R.G.; Vidali, S.; Locker, F.; Rutherford, T.; O’Donnel, M.; Stoger-Kleiber, A.; Mayr, J.A.; Sperl, W.; Kofler, B. A ketogenic diet supplemented with medium-chain triglycerides enhances the anti-tumor and anti-angiogenic efficacy of chemotherapy on neuroblastoma xenografts in a CD1-nu mouse model. Oncotarget 2017, 8, 64728–64744. [Google Scholar] [CrossRef] [PubMed]
- Wood, T.R.; Kelly, C. Insulin, glucose and beta-hydroxybutyrate responses to medium-chain triglyceride-based sports supplement: A pilot study. J. Insul. Resist. 2017, 2, 1–9. [Google Scholar] [CrossRef]
- Clegg, M.E. They say coconut oil can aid weight loss, but can it really? Eur. J. Clin. Nutr. 2017, 71, 1139–1143. [Google Scholar] [CrossRef] [PubMed]
- Mumme, K. Effects of medium-chain triglycerides on weight loss and body composition: A meta-analysis of randomized controlled trials. J. Acad. Nutr. Diet. 2015, 115, 249–263. [Google Scholar] [CrossRef] [PubMed]
- Kanikarla-Marie, P.; Jain, S.K. Hyperketonemia (acetoacetate) upregulates NADPH oxidase 4 and elevates oxidative stress, ICAM-1, and monocyte adhesivity in endothelial cells. Cell. Physiol. Biochem. 2015, 35, 364–373. [Google Scholar] [CrossRef] [PubMed]
- Nagai, R.; Nagai, M.; Shimasaki, S.; Baynes, J.W.; Fujiwara, Y. Citric acid inhibits development of cataracts, proteinuria and ketosis in streptozotocin (type 1) diabetic rats. Biochem. Biophys. Res. Commun. 2010, 393, 118–122. [Google Scholar] [CrossRef]
- Decleves, A.E.; Zolkipli, Z.; Satriano, J.; Wang, L.; Nakayama, T.; Rogac, M.; Le, T.P.; Nortier, J.L.; Farquhar, M.G.; Naviaux, R.K.; et al. Regulation of lipid accumulation by AMP-activated kinase [corrected] in high fat diet-induced kidney injury. Kidney Int. 2014, 85, 611–623. [Google Scholar] [CrossRef]
- Weinberg, J.M. Lipotoxicity. Kidney Int. 2006, 70, 1560–1566. [Google Scholar] [CrossRef]
- Kuwahara, S.; Hosojima, M.; Kaneko, R.; Aoki, H.; Nakano, D.; Sasagawa, T.; Kabasawa, H.; Kaseda, R.; Yasukawa, R.; Ishikawa, T.; et al. Megalin-mediated tubuloglomerular alterations in high-fat diet-induced kidney disease. J. Am. Soc. Nephrol. 2016, 27, 1996–2008. [Google Scholar] [CrossRef]
- Yamamoto, T.; Takabatake, Y.; Takahashi, A.; Kimura, T.; Namba, T.; Matsuda, J.; Minami, S.; Kaimori, J.Y.; Matsui, I.; Matsusaka, T.; et al. High-fat diet-induced lysosomal dysfunction and impaired autophagic flux contribute lipotoxicity in the kidney. J. Am. Soc. Nephrol. 2017, 28, 1534–1551. [Google Scholar] [CrossRef]
- Friedman, A.N. High-protein diets: Potential effects on the kidney in renal health and disease. Am. J. Kidney Dis. 2004, 44, 950–962. [Google Scholar] [CrossRef] [PubMed]
- Xie, Y.; Bowe, B.; Li, T.; Xian, H.; Yan, Y.; Al-Aly, Z. Higher blood urea nitrogen is associated with increased risk of incident diabetes mellitus. Kidney Int. 2018, 93, 741–752. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Miyata, T.; Ueda, Y.; Horie, K.; Nangaku, M.; Tanaka, S.; van Ypersele de Strihou, C.; Kurokawa, K. Renal catabolism of advanced glycation end products: The fate of pentosidine. Kidney Int. 1998, 53, 416–422. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gugliucci, A.; Bendayan, M. Renal fate of circulating advanced glycated end products (AGE): Evidence for reabsorption and catabolism of AGE-peptides by renal proximal tubular cells. Diabetologia 1996, 39, 149–160. [Google Scholar] [CrossRef] [Green Version]
- Kuro-o, M.; Moe, O.W. Klotho and kidney disease. J. Nephrol. 2010, 23, S136–S144. [Google Scholar]
- Handa, K.; Inukai, K.; Onuma, H.; Kudo, A.; Tsugawa, K.; Kitahara, A.; Moriya, R.; Takahashi, K.; Sumitani, Y.; Hosaka, T.; et al. Long-term low carbohydrate diet leads to deleterious metabolic manifestations in diabetic mice. PLoS ONE 2014, 9, e10498. [Google Scholar] [CrossRef] [Green Version]
- Lihn, A.S.; Pedersen, S.B.; Richelsen, B. Adiponectin: Action, regulation, and association to insulin sensitivity. Obes. Rev. 2005, 6, 13–21. [Google Scholar] [CrossRef]
- Coppari R and Bjorbaek, C. Leptin revisited: Its mechanism of action and potential for treating diabetes. Nat. Rev. Drug Discov. 2012, 11, 692–708. [Google Scholar] [CrossRef] [Green Version]
- Lamont, B.J.; Waters, M.F.; Andrikopoulos, S. A low-carbohydrate high-fat diet increases weight gain and does not improve glucose tolerance, insulin secretion, or β-cell mass in NZO mice. Nutr. Diabetes 2016, 6, e194. [Google Scholar] [CrossRef]
- Chan, P.; Hsieh, P. The role of adipocyte hypertrophy and hypoxia in the development of obesity-associated adipose tissue inflammation and insulin resistance. In Adiposity: Omics and Molecular Understanding; Gordeladze, J.O., Ed.; IntechOpen: London, UK, 2017. [Google Scholar]
- Hammarstedt, A.; Graham, T.E.; Kahn, B.B. Adipose tissue dysregulation and reduced insulin sensitivity in non-obese individuals with enlarged abdominal adipose cells. Diabetol. Metab. Syndr. 2012, 4, 42. [Google Scholar] [CrossRef] [Green Version]
Casual Serum | Fasting Serum | |||
---|---|---|---|---|
Glucose (mg/dL) | β-Hydroxybutyrate (mmol/L) | Glucose (mg/dL) | β-Hydroxybutyrate (mmol/L) | |
Control | 300.5 ± 9.15 | 0.08 ± 0.01 | 185.5 ± 25.50 | 1.48 ± 0.08 |
LC | 333.8 ± 23.80 | 0.31 ± 0.03 | 204.2 ± 21.85 | 1.65 ± 0.17 |
MCT-LC | 264.9 ± 37.74 | 0.45± 0.12 * | 141.2 ± 7.09 | 1.72 ± 0.18 |
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Kaburagi, T.; Kanaki, K.; Otsuka, Y.; Hino, R. Low-Carbohydrate Diet Inhibits Different Advanced Glycation End Products in Kidney Depending on Lipid Composition but Causes Adverse Morphological Changes in a Non-Obese Model Mice. Nutrients 2019, 11, 2801. https://doi.org/10.3390/nu11112801
Kaburagi T, Kanaki K, Otsuka Y, Hino R. Low-Carbohydrate Diet Inhibits Different Advanced Glycation End Products in Kidney Depending on Lipid Composition but Causes Adverse Morphological Changes in a Non-Obese Model Mice. Nutrients. 2019; 11(11):2801. https://doi.org/10.3390/nu11112801
Chicago/Turabian StyleKaburagi, Tomoko, Kazuma Kanaki, Yuko Otsuka, and Rumi Hino. 2019. "Low-Carbohydrate Diet Inhibits Different Advanced Glycation End Products in Kidney Depending on Lipid Composition but Causes Adverse Morphological Changes in a Non-Obese Model Mice" Nutrients 11, no. 11: 2801. https://doi.org/10.3390/nu11112801