Effect of Acylated and Nonacylated Anthocyanins on Urine Metabolic Profile during the Development of Type 2 Diabetes in Zucker Diabetic Fatty Rats

The effect of nonacylated and acylated anthocyanins on urinary metabolites in diabetic rats was investigated. Nonacylated anthocyanins extract from bilberries (NAAB) or acylated anthocyanins extract from purple potatoes (AAPP) was given to Zucker diabetic fatty (ZDF) rats for 8 weeks at daily doses of 25 and 50 mg/kg body weight. 1H NMR metabolomics was applied to study alterations in urinary metabolites from three time points (weeks 1, 4, and 8). Both types of anthocyanins modulated the metabolites associated with the tricarboxylic acid cycle, gut microbiota metabolism, and renal function at weeks 1 and 4, such as 2-oxoglutarate, fumarate, alanine, trigonelline, and hippurate. In addition, only a high dose of AAPP decreased monosaccharides, formate, lactate, and glucose levels at week 4, suggesting improvement in energy production in mitochondria, glucose homeostasis, and oxidative stress. This study suggested different impacts of AAPP and NAAB on the metabolic profile of urine in diabetes.

[1]  Wei Chen,et al.  Anti-aging effects and mechanisms of anthocyanins and their intestinal microflora metabolites. , 2022, Critical reviews in food science and nutrition.

[2]  A. Marette,et al.  Gut Microbial Signatures of Distinct Trimethylamine N-Oxide Response to Raspberry Consumption , 2022, Nutrients.

[3]  Baoru Yang,et al.  Effects of acylated and nonacylated anthocyanins extracts on gut metabolites and microbiota in diabetic Zucker rats: A metabolomic and metagenomic study. , 2022, Food research international.

[4]  Mak-Soon Lee,et al.  Mulberry (Morus alba L.) Fruit Extract Ameliorates Inflammation via Regulating MicroRNA-21/132/143 Expression and Increases the Skeletal Muscle Mitochondrial Content and AMPK/SIRT Activities , 2021, Antioxidants.

[5]  Yumei Zhang,et al.  1H NMR Metabolomics and Full-Length RNA-Seq Reveal Effects of Acylated and Nonacylated Anthocyanins on Hepatic Metabolites and Gene Expression in Zucker Diabetic Fatty Rats , 2021, Journal of agricultural and food chemistry.

[6]  A. Abdel-Hamid,et al.  Time‐based investigation of urinary metabolic markers for Type 2 diabetes: Metabolomics approach for diabetes management , 2021, BioFactors.

[7]  Baoru Yang,et al.  Phenolic metabolites in the urine and plasma of healthy men after acute intake of purple potato extract rich in methoxysubstituted monoacylated anthocyanins. , 2021, Molecular nutrition & food research.

[8]  G. Hwang,et al.  Urinary Metabolomic Profiling in Streptozotocin-Induced Diabetic Mice after Treatment with Losartan , 2020, International journal of molecular sciences.

[9]  Yumei Zhang,et al.  Effects of Anthocyanin Extracts from Bilberry (Vaccinium myrtillus L.) and Purple Potato (Solanum tuberosum L. var. ‘Synkeä Sakari’) on the Plasma Metabolomic Profile of Zucker Diabetic Fatty Rats , 2020, Journal of agricultural and food chemistry.

[10]  M. Motilva,et al.  Berry fruits modulate kidney dysfunction and urine metabolome in Dahl salt-sensitive rats. , 2020, Free radical biology & medicine.

[11]  R. Rodrigues,et al.  Role of gut microbiota in type 2 diabetes pathophysiology , 2020, EBioMedicine.

[12]  M. Viitanen,et al.  Anthocyanin-rich extract from purple potatoes decreases postprandial glycemic response and affects inflammation markers in healthy men. , 2019, Food chemistry.

[13]  Sandrine P Claus,et al.  NMR metabolomics identifies over 60 biomarkers associated with Type II Diabetes impairment in db/db mice , 2019, Metabolomics.

[14]  J. Shaw,et al.  IDF Diabetes Atlas: Global estimates of diabetes prevalence for 2017 and projections for 2045. , 2018, Diabetes research and clinical practice.

[15]  Baoru Yang,et al.  Improved analysis of anthocyanins and vitamin C in blue-purple potato cultivars. , 2018, Food chemistry.

[16]  Huiru Tang,et al.  Metabolomics Reveals that Dietary Ferulic Acid and Quercetin Modulate Metabolic Homeostasis in Rats. , 2018, Journal of agricultural and food chemistry.

[17]  Maulidiani,et al.  Effect of Ipomoea aquatica ethanolic extract in streptozotocin (STZ) induced diabetic rats via1H NMR-based metabolomics approach. , 2017, Phytomedicine : international journal of phytotherapy and phytopharmacology.

[18]  Wei Chen,et al.  Anthocyanins as promising molecules and dietary bioactive components against diabetes – A review of recent advances , 2017 .

[19]  J. Klenk,et al.  Metabolite profiling in identifying metabolic biomarkers in older people with late-onset type 2 diabetes mellitus , 2017, Scientific Reports.

[20]  Maulidiani,et al.  Metabolite Variation in Lean and Obese Streptozotocin (STZ)-Induced Diabetic Rats via 1H NMR-Based Metabolomics Approach , 2017, Applied Biochemistry and Biotechnology.

[21]  Xiaodong Zheng,et al.  Mulberry anthocyanin extract ameliorates insulin resistance by regulating PI3K/AKT pathway in HepG2 cells and db/db mice. , 2016, The Journal of nutritional biochemistry.

[22]  Anamika Gaur,et al.  The complex metabolism of trimethylamine in humans: endogenous and exogenous sources , 2016, Expert Reviews in Molecular Medicine.

[23]  Fariba Tayyari,et al.  1H NMR‐Based Metabolomics Reveals Urinary Metabolome Modifications in Female Sprague‐Dawley Rats by Cranberry Procyanidins , 2016, The Journal of nutritional biochemistry.

[24]  M. Mahomoodally,et al.  An Investigation into the Antiobesity Effects of Morinda citrifolia L. Leaf Extract in High Fat Diet Induced Obese Rats Using a 1H NMR Metabolomics Approach , 2015, Journal of diabetes research.

[25]  J. Tomich,et al.  Characterisation and stability of anthocyanins in purple-fleshed sweet potato P40. , 2015, Food chemistry.

[26]  Sungjin Chung,et al.  Anthocyanin-rich Seoritae extract ameliorates renal lipotoxicity via activation of AMP-activated protein kinase in diabetic mice , 2015, Journal of Translational Medicine.

[27]  S. Meier,et al.  Strategy for Nuclear-Magnetic-Resonance-Based Metabolomics of Human Feces. , 2015, Analytical chemistry.

[28]  I. Kozone,et al.  New acylated anthocyanins from purple yam and their antioxidant activity , 2015, Bioscience, biotechnology, and biochemistry.

[29]  Fariba Tayyari,et al.  A 1H NMR-based approach to investigate metabolomic differences in the plasma and urine of young women after cranberry juice or apple juice consumption , 2015 .

[30]  Baoru Yang,et al.  NMR metabolomics of ripened and developing oilseed rape (Brassica napus) and turnip rape (Brassica rapa). , 2015, Food chemistry.

[31]  D. Wishart,et al.  Standardizing the experimental conditions for using urine in NMR-based metabolomic studies with a particular focus on diagnostic studies: a review , 2014, Metabolomics.

[32]  Xiaodong Zheng,et al.  Dietary supplementation with purified mulberry (Morus australis Poir) anthocyanins suppresses body weight gain in high-fat diet fed C57BL/6 mice. , 2013, Food chemistry.

[33]  Zerihun T. Dame,et al.  The Human Urine Metabolome , 2013, PloS one.

[34]  Takashi Ito,et al.  Preventive effects of Morus alba L. anthocyanins on diabetes in Zucker diabetic fatty rats , 2013, Experimental and therapeutic medicine.

[35]  Guangji Wang,et al.  GC/TOFMS analysis of metabolites in serum and urine reveals metabolic perturbation of TCA cycle in db/db mice involved in diabetic nephropathy. , 2013, American journal of physiology. Renal physiology.

[36]  Juei-Tang Cheng,et al.  Decrease of Obesity by Allantoin via Imidazoline I1-Receptor Activation in High Fat Diet-Fed Mice , 2013, Evidence-based complementary and alternative medicine : eCAM.

[37]  I. Wilson,et al.  Hippurate: the natural history of a mammalian-microbial cometabolite. , 2013, Journal of proteome research.

[38]  Qiang Feng,et al.  A metagenome-wide association study of gut microbiota in type 2 diabetes , 2012, Nature.

[39]  J. Zhou,et al.  Trigonelline: a plant alkaloid with therapeutic potential for diabetes and central nervous system disease. , 2012, Current medicinal chemistry.

[40]  Hans J. Vogel,et al.  Quantitative Metabolomic Profiling of Serum, Plasma, and Urine by 1H NMR Spectroscopy Discriminates between Patients with Inflammatory Bowel Disease and Healthy Individuals , 2012, Journal of proteome research.

[41]  L. Jaakola,et al.  Phenolic compounds in berries and flowers of a natural hybrid between bilberry and lingonberry (Vaccinium × intermedium Ruthe). , 2011, Phytochemistry.

[42]  Xian-Zhong Yan,et al.  Comparison of metabolic profiling of cyanidin-3-O-galactoside and extracts from blueberry in aged mice. , 2011, Journal of agricultural and food chemistry.

[43]  Liang Zhao,et al.  A Metabonomic Comparison of Urinary Changes in Zucker and GK Rats , 2010, Journal of biomedicine & biotechnology.

[44]  G. Mingrone,et al.  Gut microbiome-derived metabolites characterize a peculiar obese urinary metabotype , 2010, International Journal of Obesity.

[45]  Jae Heun Lee,et al.  The anti-diabetic effect of anthocyanins in streptozotocin-induced diabetic rats through glucose transporter 4 regulation and prevention of insulin resistance and pancreatic apoptosis. , 2009, Molecular nutrition & food research.

[46]  C. Mølgaard,et al.  Nuclear magnetic resonance-based metabonomics reveals strong sex effect on plasma metabolism in 17-year-old Scandinavians and correlation to retrospective infant plasma parameters. , 2009, Metabolism: clinical and experimental.

[47]  Hideyo Sato,et al.  Anti-Diabetic Effects of Pumpkin and Its Components, Trigonelline and Nicotinic Acid, on Goto-Kakizaki Rats , 2009, Bioscience, biotechnology, and biochemistry.

[48]  R. Heine,et al.  Acute Effects of Decaffeinated Coffee and the Major Coffee Components Chlorogenic Acid and Trigonelline on Glucose Tolerance , 2009, Diabetes Care.

[49]  M. K. C. Hesselink,et al.  Reduced tricarboxylic acid cycle flux in type 2 diabetes mellitus? , 2008, Diabetologia.

[50]  Lanhai Lü,et al.  Oxidative stress on the astrocytes in culture derived from a senescence accelerated mouse strain , 2008, Neurochemistry International.

[51]  R. Cox,et al.  A metabolomic comparison of urinary changes in type 2 diabetes in mouse, rat, and human. , 2007, Physiological genomics.

[52]  H. Senn,et al.  Probabilistic quotient normalization as robust method to account for dilution of complex biological mixtures. Application in 1H NMR metabonomics. , 2006, Analytical chemistry.

[53]  M. Rantalainen,et al.  The comparative metabonomics of age-related changes in the urinary composition of male Wistar-derived and Zucker (fa/fa) obese rats. , 2006, Molecular bioSystems.

[54]  M. Elisaf,et al.  Rhabdomyolysis-related renal tubular damage studied by proton nuclear magnetic resonance spectroscopy of urine. , 2002, Clinical chemistry.

[55]  I. Messana,et al.  Proton nuclear magnetic resonance spectral profiles of urine in type II diabetic patients. , 1998, Clinical chemistry.

[56]  B. Jeanrenaud,et al.  In vivo hepatic and peripheral insulin resistance in genetically obese (fa/fa) rats. , 1983, Endocrinology.