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Metabolomic analysis of amino acid and energy metabolism in rats supplemented with chlorogenic acid

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Abstract

This study was conducted to investigate effects of chlorogenic acid (CGA) supplementation on serum and hepatic metabolomes in rats. Rats received daily intragastric administration of either CGA (60 mg/kg body weight) or distilled water (control) for 4 weeks. Growth performance, serum biochemical profiles, and hepatic morphology were measured. Additionally, serum and liver tissue extracts were analyzed for metabolomes by high-resolution 1H nuclear magnetic resonance-based metabolomics and multivariate statistics. CGA did not affect rat growth performance, serum biochemical profiles, or hepatic morphology. However, supplementation with CGA decreased serum concentrations of lactate, pyruvate, succinate, citrate, β-hydroxybutyrate and acetoacetate, while increasing serum concentrations of glycine and hepatic concentrations of glutathione. These results suggest that CGA supplementation results in perturbation of energy and amino acid metabolism in rats. We suggest that glycine and glutathione in serum may be useful biomarkers for biological properties of CGA on nitrogen metabolism in vivo.

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Abbreviations

CGA:

Chlorogenic acid

PC:

Principal components

PCA:

Principal component analysis

NMR:

Nuclear magnetic resonance

References

  • Algamdi N, Mullen W, Crozier A (2011) Tea prepared from Anastatica hirerochuntica seeds contains a diversity of antioxidant flavonoids, chlorogenic acids and phenolic compounds. Phytochemistry 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Cai Y, Luo Q, Sun M et al (2004) Antioxidant activity and phenolic compounds of 112 traditional Chinese medicinal plants associated with anticancer. Life Sci 74:2157–2184

    Article  CAS  PubMed  Google Scholar 

  • Cruz M, Maldonado-Bernal C, Mondragon-Gonzalez R et al (2008) Glycine treatment decreases proinflammatory cytokines and increases interferon-gamma in patients with type 2 diabetes. J Endocrinol Invest 31:694–699

    Article  CAS  PubMed  Google Scholar 

  • Dai ZL, Zhang J, Wu G et al (2010) Utilization of amino acids by bacteria from the pig small intestine. Amino Acids 39:1201–1215

    Article  CAS  PubMed  Google Scholar 

  • Dai ZL, Wu G, Zhu WY (2011) Amino acid metabolism in intestinal bacteria: links between gut ecology and host health. Front Biosci 16:1768–1786

    Article  CAS  Google Scholar 

  • Dai ZL, Li XL, Xi PB et al (2012a) Metabolism of select amino acids in bacteria from the pig small intestine. Amino Acids 42:1597–1608

    Article  CAS  PubMed  Google Scholar 

  • Dai ZL, Li XL, Xi PB et al (2012b) Regulatory role for l-arginine in the utilization of amino acids by pig small-intestinal bacteria. Amino Acids 43:233–244

    Article  CAS  PubMed  Google Scholar 

  • Dai ZL, Wu ZL, Yang Y et al (2013a) Nitric oxide and energy metabolism in mammals. BioFactors 39:383–391

    Article  CAS  PubMed  Google Scholar 

  • Dai ZL, Li XL, Xi PB et al (2013b) l-Glutamine regulates amino acid utilization by intestinal bacteria. Amino Acids 45:501–512

    Article  CAS  PubMed  Google Scholar 

  • Dai ZL, Wu ZL, Jia SC et al (2014) Analysis of amino acid composition in proteins of animal tissues and foods as pre-column o-phthaldialdehyde derivatives by HPLC with fluorescence detection. J Chromatogr B. doi:10.1016/j.jchromb.2014.03.025

    Google Scholar 

  • Díaz-Flores M, Cruz M, Duran-Reyes G et al (2013) Oral supplementation with glycine reduces oxidative stress in patients with metabolic syndrome, improving their systolic blood pressure. Can J Physiol Pharmacol 91:855–860

    Article  PubMed  Google Scholar 

  • El Hafidi M, Pérez I, Zamora J et al (2004) Glycine intake decreases plasma free fatty acids, adipose cell size, and blood pressure in sucrose-fed rats. Am J Physiol Regulatory Integrative Comp Physiol 287:1387–1393

    Article  Google Scholar 

  • Foo HL, Loh TC, Lai PW et al (2003) Effects of adding Lactobacillus plantarum I-UL4 metabolites in drinking water of rats. Pakistan J Nutr 2:283–288

    Article  Google Scholar 

  • Fu WJ, Stromberg AJ, Viele K et al (2010) Statistics and bioinformatics in nutritional sciences: analysis of complex data in the era of systems biology. J Nutr Biochem 21:561–572

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Greenberg JA, Boozer CN, Geliebter A (2006) Coffee, diabetes and weight control. Am J Clin Nutr 84:682–693

    CAS  PubMed  Google Scholar 

  • Hayes JD, McLellan LI (1999) Glutathione and glutathione-dependent enzymes represent a co-ordinately regulated defence against oxidative stress. Free Radical Res 31:273–300

    Article  CAS  Google Scholar 

  • He ML, Wang YZ, Xu ZR et al (2003) Effect of dietary rare earth elements on growth performance and blood parameters of rats. J Anim Physiol Anim Nutr 87:229–235

    Article  CAS  Google Scholar 

  • He QH, Ren PP, Kong XF et al (2011) Metabolomics and its role in amino acid nutrition research. Front Biosci 16:2451–2460

    Article  CAS  Google Scholar 

  • He QH, Ren PP, Kong XF et al (2012) Comparison of serum metabolite compositions between obese and lean growing pigs using an NMR-based metabonomic approach. J Nutr Biochem 23:133–139

    Article  CAS  PubMed  Google Scholar 

  • He LQ, Yang HS, Li TJ et al (2013) Effects of dietary l-lysine intake on the intestinal mucosa and expression of CAT genes in weaned piglets. Amino Acids 45:383–391

    Article  CAS  PubMed  Google Scholar 

  • Hou YQ, Wang L, Zhang W et al (2012) Protective effects of N-acetylcysteine on intestinal functions of piglets challenged with lipopolysaccharide. Amino Acids 43:1233–1242

    Article  CAS  PubMed  Google Scholar 

  • Hou YQ, Wang L, Yi D et al (2013) N-acetylcysteine reduces inflammation in the small intestine by regulating redox, EGF and TLR4 signaling. Amino Acids 45:513–522

    Article  CAS  PubMed  Google Scholar 

  • Huang Z, Chang C (2008) Advances of study on glucose and lipids metabolism of chlorogenic acid regulating. J Hyg Res 37:637–639

    Google Scholar 

  • Ji L, Jiang P, Lu B et al (2013) Chlorogenic acid, a dietary polyphenol, protects acetaminophen-induced liver injury and its mechanism. J Nutr Biochem 24:1911–1919

    Article  CAS  PubMed  Google Scholar 

  • Jiang CY, Yang KM, Yang L et al (2013) A 1H NMR-based metabonomic investigation of time-related metabolic trajectories of the plasma, urine and liver extracts of hyperlipidemic hamsters. PLoS One 8:e66786

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jobgen WS, Fried SK, Fu WJ et al (2006) Regulatory role for the arginine-nitric oxide pathway in metabolism of energy substrates. J Nutr Biochem 17:571–588

    Article  CAS  PubMed  Google Scholar 

  • Kasai H, Fukada S, Yamaizumi Z et al (2000) Action of chlorogenic acid in vegetables and fruits as an inhibitor of 8-hydroxydeoxyguanosine formation in vitro and in a rat carcinogenesis model. Food Chem Toxicol 38:467–471

    Article  CAS  PubMed  Google Scholar 

  • Kauppinen RA, Nicholls DG (1986) Synaptosomal bioenergetics. The role of glycolysis, pyruvate oxidation and responses to hypoglycaemia. Eur J Biochem 158:159–165

    Article  CAS  PubMed  Google Scholar 

  • Kong XF, Wu G, Yin YL (2011) Roles of phytochemicals in amino acid nutrition. Front Biosci S3:372–384

    Article  CAS  Google Scholar 

  • Krebs HA (1970) Rate control of the tricarboxylic acid cycle. Adv Enzym Regul 8:335–353

    Article  CAS  Google Scholar 

  • Krebs HA, Lowenstein JM (1960) The tricarboxylic acid cycle. Metab Pathw 1:129–203

    CAS  Google Scholar 

  • Li P, Yin YL, Li DF et al (2007) Amino acids and immune function. Br J Nutr 98:237–252

    Article  CAS  PubMed  Google Scholar 

  • Li SY, Chang CQ, Ma FY et al (2009) Modulating effects of chlorogenic acid on lipids and glucose metabolism and expression of hepatic peroxisome proliferator-activated receptor-α in golden hamsters fed on high fat diet. Biomed Environ Sci 22:122–129

    Article  CAS  PubMed  Google Scholar 

  • Li XL, Rezaei R, Li L et al (2011) Composition of amino acids in feed ingredients for animal diets. Amino Acids 40:1159–1168

    Article  CAS  PubMed  Google Scholar 

  • Liao PQ, Wei L, Zhang XY et al (2007) Metabolic profiling of serum from gadolinium chloride-treated rats by 1H NMR spectroscopy. Anal Biochem 364:112–121

    Article  CAS  PubMed  Google Scholar 

  • Lindon JC, Holmes E, Nicholson JK (2001) Pattern recognition methods and applications in biomedical magnetic resonance. Prog NMR Spectrosc 39:1–40

    Article  CAS  Google Scholar 

  • Liu G, Wang Y, Wang Z et al (2011) Nuclear magnetic resonance (NMR)-based metabolomic studies on urine and serum biochemical profiles after chronic cysteamine supplementation in rats. J Agric Food Chem 59:5572–5578

    Article  CAS  PubMed  Google Scholar 

  • Lou Z, Wang H, Zhu S (2011) Antibacterial activity and mechanism of action of chlorogenic acid. J Food Sci 76:M398–M403

    Article  CAS  PubMed  Google Scholar 

  • Mahaffey KR, Capar SG, Gladen BC et al (1981) Concurrent exposure to lead, cadmium, and arsenic. Effects on toxicity and tissue metal concentrations in the rat. J Lab Clin Med 98:463–481

    CAS  PubMed  Google Scholar 

  • Marques V, Farah A (2009) Chlorogenic acids and related compounds in medicinal plants and infusions. Food Chem 113:1370–1376

    Article  CAS  Google Scholar 

  • Matilla B, Mauriz JL, Culebras JM et al (2002) Glycine: a cell-protecting anti-oxidant nutrient. Nutrición Hospitalaria 17:2–9

    CAS  PubMed  Google Scholar 

  • Mauriz JL, Matilla B, Culebras JM et al (2001) Dietary glycine inhibits activation of nuclear factor kappa B and prevents liver injury in hemorrhagic shock in the rat. Free Radic Biol Med 31:1236–1244

    Article  CAS  PubMed  Google Scholar 

  • Meng S, Cao J, Feng Q et al (2013) Roles of chlorogenic acid on regulating glucose and lipids metabolism: a review. Evid Based Complement Alternat Med. doi:10.1155/2013/801457

    Google Scholar 

  • Mubarak A, Hodgson JM, Considine MJ et al (2013) Supplementation of a high-fat diet with chlorogenic acid is associated with insulin resistance and hepatic lipid accumulation in mice. J Agric Food Chem 61:4371–4378

    Article  CAS  PubMed  Google Scholar 

  • Park JB (2013) Isolation and quantification of major chlorogenic acids in three major instant coffee brands and their potential effects on H2O2-induced mitochondrial membrane depolarization and apoptosis in PC-12 cells. Food Funct 4:1632–1638

    Article  CAS  PubMed  Google Scholar 

  • Ren WK, Luo W, Wu MM et al (2013a) Dietary l-glutamine supplementation improves pregnancy outcome in mice infected with type-2 porcine circovirus. Amino Acids 45:479–488

    Article  CAS  PubMed  Google Scholar 

  • Ren WK, Zou LX, Ruan Z et al (2013b) Dietary l-proline supplementation confers immuno-stimulatory effects on inactivated Pasteurella multocida vaccine immunized mice. Amino Acids 45:555–561

    Article  CAS  PubMed  Google Scholar 

  • Rezaei R, Wang WW, Wu ZL et al (2013a) Biochemical and physiological bases for utilization of dietary amino acids by young pigs. J Anim Sci Biotech 4:7

    Article  CAS  Google Scholar 

  • Rezaei R, Knabe DA, Tekwe CD et al (2013b) Dietary supplementation with monosodium glutamate is safe and improves growth performance in postweaning pigs. Amino Acids 44:911–923

    Article  CAS  PubMed  Google Scholar 

  • Ruan Z, Lv Y, Fu X et al (2013) Metabolomic analysis of amino acid metabolism in colitic rats supplemented with lactosucrose. Amino Acids 45:877–887

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Ramírez A, Ortiz-Balderas E, Cardozo-Saldaña G et al (2014) Glycine restores glutathione and protects against oxidative stress in vascular tissue from sucrose-fed rats. Clin Sci (Lond) 126:19–29

    Article  Google Scholar 

  • Satterfield MC, Wu G (2011) Growth and development of brown adipose tissue: significance and nutritional regulation. Front Biosci 16:1589–1608

    Article  CAS  Google Scholar 

  • Satterfield MC, Dunlap KA, Keisler DH et al (2012) Arginine nutrition and fetal brown adipose tissue development in diet-induced obese sheep. Amino Acids 43:1593–1603

    Article  Google Scholar 

  • Satterfield MC, Dunlap KA, Keisler DH et al (2013) Arginine nutrition and fetal brown adipose tissue development in nutrient-restricted sheep. Amino Acids 45:489–499

    Article  CAS  PubMed  Google Scholar 

  • Schnackenberg L, Beger RD, Dragan Y (2005) NMR-based metabonomic evaluation of livers from rats chronically treated with tamoxifen, mestranol, and phenobarbital. Metabolomics 1:87–94

    Article  CAS  Google Scholar 

  • Schulz JB, Lindenau J, Seyfried J et al (2000) Glutathione, oxidative stress and neurodegeneration. Eur J Biochem 267:4904–4911

    Article  CAS  PubMed  Google Scholar 

  • Shi H, Dong L, Bai Y et al (2009) Chlorogenic acid against carbon tetrachloride-induced liver fibrosis in rats. Eur J Pharmacol 623:119–124

    Article  CAS  PubMed  Google Scholar 

  • Shi H, Dong L, Jiang J et al (2012) Chlorogenic acid reduces liver inflammation and fibrosis through inhibition of toll-like receptor 4 signaling pathway. Toxicology 303:107–114

    Article  PubMed  Google Scholar 

  • Shi H, Dong L, Dang X et al (2013) Effect of chlorogenic acid on LPS-induced proinflammatory signaling in hepatic stellate cells. Inflamm Res 62:581–587

    Article  CAS  PubMed  Google Scholar 

  • Tan BE, Li XG, Wu G et al (2012) Dynamic changes in blood flow and oxygen consumption in the portal-drained viscera of growing pigs receiving acute administration of l-arginine. Amino Acids 43:2481–2489

    Article  CAS  PubMed  Google Scholar 

  • Trouillas P, Calliste CA, Allais DP et al (2003) Antioxidant, anti-inflammatory and antiproliferative properties of sixteen water plant extracts used in the Limousin countryside as herbal teas. Food Chem 80:399–407

    Article  CAS  Google Scholar 

  • Wan CW, Wong CNY, Pin WK et al (2013) Chlorogenic acid exhibits cholesterol lowering and fatty liver attenuating properties by up-regulating the gene expression of PPAR-α in hypercholesterolemic rats induced with a high-cholesterol diet. Phytother Res 27:545–551

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Wu G, Zhou H et al (2009) Emerging technologies for amino acid nutrition research in the post-genome era. Amino Acids 37:177–186

    Article  PubMed  Google Scholar 

  • Wang QJ, Hou YQ, Yi D et al (2013a) Protective effects of N-acetylcysteine on alleviating acetic acid-induced colitis in a porcine model. BMC Gastroenterol 13:133

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang WW, Wu ZL, Dai ZL et al (2013b) Glycine metabolism in animals and humans: implications for nutrition and health. Amino Acids 45:463–477

    Article  PubMed  Google Scholar 

  • Wang W, Dai Z, Wu Z et al (2014) Glycine is a nutritionally essential amino acid for maximal growth of milk-fed young pigs. Amino Acids. doi:10.1007/s00726-014-1758-3

  • Wei JW, Carroll RJ, Harden KK et al (2012) Comparisons of treatment means when factors do not interact in two-factorial studies. Amino Acids 42:2031–2035

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wojtczak AB (1968) Control of acetoacetate and β-hydroxybutyrate production in rat liver mitochondria. Biochem Biophys Res Commun 31:634–640

    Article  CAS  PubMed  Google Scholar 

  • Wu G (2010) Functional amino acids in growth, reproduction and health. Adv Nutr 1:31–37

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wu G (2013a) Amino acids: biochemistry and nutrition. CRC Press, Boca Raton

    Book  Google Scholar 

  • Wu G (2013b) Functional amino acids in nutrition and health. Amino Acids 45:407–411

    Article  CAS  PubMed  Google Scholar 

  • Wu GY, Gunasekara A, Brunengraber H et al (1991) Effects of extracellular pH, CO2, and \( {\text{HCO}}_{3}^{ - } \) on ketogenesis in perfused rat liver. Am J Physiol 261:E221–E226

  • Wu GY, Fang YZ, Yang S et al (2004) Glutathione metabolism and its implications for health. J Nutr 134:489–492

    CAS  PubMed  Google Scholar 

  • Wu G, Bazer FW, Burghardt RC et al (2011) Proline and hydroxyproline metabolism: implications for animal and human nutrition. Amino Acids 40:1053–1063

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wu ZL, Satterfield MC, Bazer FW et al (2012) Regulation of brown adipose tissue development and white fat reduction by l-arginine. Curr Opin Clin Nutr Metab Care 15:529–538

    Article  CAS  PubMed  Google Scholar 

  • Wu X, Zhang YZ, Yin YL et al (2013a) Roles of heat-shock protein 70 in protecting against intestinal mucosal damage. Front Biosci 18:356–365

    Article  CAS  Google Scholar 

  • Wu G, Wu ZL, Dai ZL et al (2013b) Dietary requirements of “nutritionally nonessential amino acids” by animals and humans. Amino Acids 44:1107–1113

    Article  CAS  PubMed  Google Scholar 

  • Wu G, Bazer FW, Dai ZL et al (2014) Amino acid nutrition in animals: protein synthesis and beyond. Annu Rev Anim Biosci 2:387–417

    Article  Google Scholar 

  • Xu Y, Chen J, Yu X et al (2010) Protective effects of chlorogenic acid on acute hepatotoxicity induced by lipopolysaccharide in mice. Inflammation 59:871–877

    CAS  Google Scholar 

  • Xu XD, Zhang LH, Shao B et al (2013) Safety evaluation of meso-zeaxanthin. Food Control 32:678–686

    Article  CAS  Google Scholar 

  • Yang Y, Li C, Nie X et al (2007) Metabonomic studies of human hepatocellular carcinoma using high-resolution magic-angle spinning 1H NMR spectroscopy in conjunction with multivariate data analysis. J Proteome Res 6:2605–2614

    Article  CAS  PubMed  Google Scholar 

  • Yao K, Guan S, Li T et al (2011) Dietary l-arginine supplementation enhances intestinal development and expression of vascular endothelial growth factor in weanling piglets. Br J Nutr 105:703–709

    Article  CAS  PubMed  Google Scholar 

  • Yun N, Kang JW, Lee SM (2012) Protective effects of chlorogenic acid against ischemia/reperfusion injury in rat liver: molecular evidence of its antioxidant and anti-inflammatory properties. J Nutr Biochem 23:1249–1255

    Article  CAS  PubMed  Google Scholar 

  • Zhang LT, Chang CQ, Liu Y et al (2011) Effect of chlorogenic acid on disordered glucose and lipid metabolism in db/db mice and its mechanism. Acta Academiae Medicinae Sinicae 33:281–286

    PubMed  Google Scholar 

  • Zhao Y, Wang J, Ballevre O et al (2012) Antihypertensive effects and mechanisms of chlorogenic acids. Hypertens Res 35:370–402

    Article  CAS  PubMed  Google Scholar 

  • Zira A, Kostidis S, Theocharis S et al (2013) 1H NMR-based metabonomics approach in a rat model of acute liver injury and regeneration induced by CCl4 administration. Toxicology 303:115–124

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This research was financially supported by National Natural Science Foundation of China (Grant No. 31001014), the Research Foundation (SKLF-TS-201108 and SKLF-TS-200817) and the Open Project Program (SKLF-KF-201005 and SKLF-KF-201216) of State Key Laboratory of Food Science and Technology at Nanchang University, and Texas A&M AgriLife Research H82000. H. Assaad was supported by a postdoctoral training grant (R25T-CA090301) from the National Cancer Institute.

Conflict of interest

The authors declare that they have no conflict of interests.

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Authors and Affiliations

  1. State Key Laboratory of Food Science and Technology, College of Life Science and Food Engineering, Nanchang University, Rm325, 235 Nanjing Street, Nanchang, 330047, China

    Zheng Ruan, Yuhui Yang, Yan Zhou, Yanmei Wen, Zeyuan Deng & Yulong Yin

  2. Institute of Nutrition and Food Safety, Center for Disease Control and Prevention of Jiangxi Province, Nanchang, 330029, China

    Sheng Ding

  3. Hunan Engineering and Research Center of Animal and Poultry Science, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, 410125, China

    Gang Liu, Xin Wu, Peng Liao & Yulong Yin

  4. Hunan New Wellful Co., LTD, Changsha, 410001, China

    Peng Liao

  5. Department of Animal Science, Texas A&M University, College Station, TX, 77843-2471, USA

    Houssein Assaad & Guoyao Wu

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  1. Zheng Ruan
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  2. Yuhui Yang
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  3. Yan Zhou
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  6. Gang Liu
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  7. Xin Wu
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  8. Peng Liao
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  9. Zeyuan Deng
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  10. Houssein Assaad
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  11. Guoyao Wu
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  12. Yulong Yin
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Correspondence to Peng Liao or Yulong Yin.

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Ruan, Z., Yang, Y., Zhou, Y. et al. Metabolomic analysis of amino acid and energy metabolism in rats supplemented with chlorogenic acid. Amino Acids 46, 2219–2229 (2014). https://doi.org/10.1007/s00726-014-1762-7

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