Hawthorn leaf flavonoids alleviate nonalcoholic fatty liver disease by enhancing the adiponectin/AMPK pathway

International Journal of Clinical and Experimental Medicine

Volumn 8, Issue 10, 2015, Pages 17295-17307

  Li, Zhongping ^a   Xu, Jiaoya ^a   Zheng, Peiyong ^a   Xing, Lianjun ^a   Shen, Hongyi ^a   Yang, Lili ^a   Zhang, Li ^a   Ji, Guang ^a  

^a SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

Author keywords

Adenosine monophosphate activated protein kinase; Adiponectin; Hawthorn leaf flavonoids; Nonalcoholic fatty liver disease

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ACYL COENZYME A DESATURASE 1; ACYL COENZYME A OXIDASE; ADENOSINE MONOPHOSPHATE ACTIVATED PROTEIN KINASE; ADENOSINE PHOSPHATE; ADIPONECTIN; ADIPONECTIN RECEPTOR; ADIPONECTIN RECEPTOR 2; ALANINE AMINOTRANSFERASE; ALKALINE PHOSPHATASE; ASPARTATE AMINOTRANSFERASE; CARNITINE PALMITOYLTRANSFERASE I; CD36 ANTIGEN; CHOLESTEROL; CRATAEGUS EXTRACT; FATTY ACID; FATTY ACID SYNTHASE; GLUCOSE; HAWTHORN LEAF FLAVONOID; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; HYPERIN; LACTATE DEHYDROGENASE; LIVER X RECEPTOR ALPHA; LOW DENSITY LIPOPROTEIN CHOLESTEROL; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; QUERCETIN; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; VITEXIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; CRATAEGUS; DISORDERS OF CARBOHYDRATE METABOLISM; DYSLIPIDEMIA; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIPID DIET; LIPID LIVER LEVEL; LIVER DYSFUNCTION; LIVER STRUCTURE; LIVER WEIGHT; MALE; NONALCOHOLIC FATTY LIVER; NONHUMAN; PLANT LEAF; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ULTRAVIOLET SPECTROPHOTOMETRY; UPREGULATION; WESTERN BLOTTING;

EID: 84949682950     PISSN: None     EISSN: 19405901     Source Type: Journal    
DOI: None     Document Type: Article

References (40)

1. Angulo P. Nonalcoholic fatty liver disease. Rev Gastroenterol Mex 2005; 70 Suppl 3: 52-56.
2. Lazo M and Clark JM. The epidemiology of nonalcoholic fatty liver disease: a global perspective. Semin Liver Dis 2008; 28: 339-350.
3. Hui E, Xu A, Bo Yang H and Lam KS. Obesity as the common soil of non-alcoholic fatty liver disease and diabetes: Role of adipokines. J Diabetes Investig 2013; 4: 413-425.
4. Marinangeli CP and Jones PJ. Functional food ingredients as adjunctive therapies to pharmacotherapy for treating disorders of metabolic syndrome. Ann Med 2010; 42: 317-333.
5. Naito Y and Yoshikawa T. Oxidative stress-induced posttranslational modification of proteins as a target of functional food. Forum Nutr 2009; 61: 39-54.
6. Fan C, Yan J, Qian Y, Wo X and Gao L. Regulation of lipoprotein lipase expression by effect of hawthorn flavonoids on peroxisome proliferator response element pathway. J Pharmacol Sci 2006; 100: 51-58.
7. Herbst M, Roberts JM, Rosier PT and Gowing DJ. Seasonal and interannual variability of canopy transpiration of a hedgerow in southern England. Tree Physiol 2007; 27: 321-333.
8. Wang T, An Y, Zhao C, Han L, Boakye-Yiadom M, Wang W and Zhang Y. Regulation effects of Crataegus pinnatifida leaf on glucose and lipids metabolism. J Agric Food Chem 2011; 59: 4987-4994.
9. Wu J, Peng W, Qin R and Zhou H. Crataegus pinnatifida: chemical constituents, pharmacology, and potential applications. Molecules 2014; 19: 1685-1712.
10. Fasshauer M and Paschke R. Regulation of adipocytokines and insulin resistance. Dia-betologia 2003; 46: 1594-1603.
11. Abenavoli L, Luigiano C, Guzzi PH, Milic N, Morace C, Stelitano L, Consolo P, Miraglia S, Fagoonee S, Virgilio C, Luzza F, De Lorenzo A and Pellicano R. Serum adipokine levels in overweight patients and their relationship with non-alcoholic fatty liver disease. Panminerva Med 2014; 56: 189-193.
12. Makimura H, Mizuno TM, Bergen H and Mobbs CV. Adiponectin is stimulated by adrenalectomy in ob/ob mice and is highly correlated with resistin mRNA. Am J Physiol Endocrinol Metab 2002; 283: E1266-1271.
13. Xu A, Wang Y, Keshaw H, Xu LY, Lam KS and Cooper GJ. The fat-derived hormone adiponectin alleviates alcoholic and nonalcoholic fatty liver diseases in mice. J Clin Invest 2003; 112: 91-100.
14. Kantartzis K, Staiger H, Machann J, Schick F, Claussen CD, Machicao F, Fritsche A, Haring HU and Stefan N. Adiponectin oligomers and ectopic fat in liver and skeletal muscle in humans. Obesity (Silver Spring) 2009; 17: 390-392.
15. Chen H, Zhang L, Li X, Li X, Sun G, Yuan X, Lei L, Liu J, Yin L, Deng Q, Wang J, Liu Z, Yang W, Wang Z, Zhang H and Liu G. Adiponectin activates the AMPK signaling pathway to regulate lipid metabolism in bovine hepatocytes. J Steroid Biochem Mol Biol 2013; 138: 445-454.
16. Ahn KS, Hahm MS, Park EJ, Lee HK and Kim IH. Corosolic acid isolated from the fruit of Crataegus pinnatifida var. psilosa is a protein kinase C inhibitor as well as a cytotoxic agent. Planta Med 1998; 64: 468-470.
17. Niu C, Chen C, Chen L, Cheng K, Yeh C and Cheng J. Decrease of blood lipids induced by Shan-Zha (fruit of Crataegus pinnatifida) is mainly related to an increase of PPARalpha in liver of mice fed high-fat diet. Horm Metab Res 2011; 43: 625-630.
18. Zhang PC and Xu SX. Flavonoid ketohexosefuranosides from the leaves of Crataegus pinnatifida Bge. var. major N.E.Br. Phytochemistry 2001; 57: 1249-1253.
19. Liu RH and Yu BY. [Study on the chemical constituents of the leaves from Crataegus pinnatifida Bge. var. major N. E. Br]. Zhong Yao Cai 2006; 29: 1169-1173.
20. Zhang PC, Zhou YJ and Xu SX. Two novel flavonoid glycosides from Crataegus pinnatifida Bge.var.major N. E. Br. J Asian Nat Prod Res 2001; 3: 77-82.
21. Shetty S, Kusminski CM and Scherer PE. Adiponectin in health and disease: evaluation of adiponectin-targeted drug development strategies. Trends Pharmacol Sci 2009; 30: 234-239.
22. Stojsavljevic S, Gomercic Palcic M, Virovic Jukic L, Smircic Duvnjak L and Duvnjak M. Adipokines and proinflammatory cytokines, the key mediators in the pathogenesis of nonalcoholic fatty liver disease. World J Ga-stroenterol 2014; 20: 18070-18091.
23. Woo YC, Tso AW, Xu A, Law LS, Fong CH, Lam TH, Lo SV, Wat NM, Cheung BM and Lam KS. Combined use of serum adiponectin and tumor necrosis factor-alpha receptor 2 levels was comparable to 2-hour post-load glucose in diabetes prediction. PLoS One 2012; 7: e36868.
24. Yamauchi T, Kamon J, Ito Y, Tsuchida A, Yokomizo T, Kita S, Sugiyama T, Miyagishi M, Hara K, Tsunoda M, Murakami K, Ohteki T, Uchida S, Takekawa S, Waki H, Tsuno NH, Shibata Y, Terauchi Y, Froguel P, Tobe K, Koyasu S, Taira K, Kitamura T, Shimizu T, Nagai R and Kadowaki T. Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 2003; 423: 762-769.
25. Liu Y, Michael MD, Kash S, Bensch WR, Monia BP, Murray SF, Otto KA, Syed SK, Bhanot S, Sloop KW, Sullivan JM and Reifel-Miller A. Deficiency of adiponectin receptor 2 reduces diet-induced insulin resistance but promotes type 2 diabetes. Endocrinology 2007; 148: 683-692.
26. Yamauchi T, Nio Y, Maki T, Kobayashi M, Ta-kazawa T, Iwabu M, Okada-Iwabu M, Kawamoto S, Kubota N, Kubota T, Ito Y, Kamon J, Tsuchida A, Kumagai K, Kozono H, Hada Y, Ogata H, Tokuyama K, Tsunoda M, Ide T, Murakami K, Awazawa M, Takamoto I, Froguel P, Hara K, Tobe K, Nagai R, Ueki K and Kadowaki T. Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat Med 2007; 13: 332-339.
27. Kotronen A, Yki-Jarvinen H, Aminoff A, Berg-holm R, Pietilainen KH, Westerbacka J, Talmud PJ, Humphries SE, Hamsten A, Isomaa B, Groop L, Orho-Melander M, Ehrenborg E and Fisher RM. Genetic variation in the ADIPOR2 gene is associated with liver fat content and its surrogate markers in three independent cohorts. Eur J Endocrinol 2009; 160: 593-602.
28. Asano T, Watanabe K, Kubota N, Gunji T, Omata M, Kadowaki T and Ohnishi S. Adi-ponectin knockout mice on high fat diet develop fibrosing steatohepatitis. J Gastroenterol Hepatol 2009; 24: 1669-1676.
29. Lin HV, Kim JY, Pocai A, Rossetti L, Shapiro L, Scherer PE and Accili D. Adiponectin resistance exacerbates insulin resistance in insulin receptor transgenic/knockout mice. Diabetes 2007; 56: 1969-1976.
30. Kadowaki T and Yamauchi T. Adiponectin receptor signaling: a new layer to the current model. Cell Metab 2011; 13: 123-124.
31. Dzamko NL and Steinberg GR. AMPK-de-pendent hormonal regulation of whole-body energy metabolism. Acta Physiol (Oxf) 2009; 196: 115-127.
32. Yamauchi T, Kamon J, Minokoshi Y, Ito Y, Waki H, Uchida S, Yamashita S, Noda M, Kita S, Ueki K, Eto K, Akanuma Y, Froguel P, Foufelle F, Ferre P, Carling D, Kimura S, Nagai R, Kahn BB and Kadowaki T. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat Med 2002; 8: 1288-1295.
33. Li X, Li X, Chen H, Lei L, Liu J, Guan Y, Liu Z, Zhang L, Yang W, Zhao C, Fu S, Li P, Liu G and Wang Z. Non-esterified fatty acids activate the AMP-activated protein kinase signaling pathway to regulate lipid metabolism in bovine hepatocytes. Cell Biochem Biophys 2013; 67: 1157-1169.
34. Jeong HW, Lee JW, Kim WS, Choe SS, Kim KH, Park HS, Shin HJ, Lee GY, Shin D, Lee H, Lee JH, Choi EB, Lee HK, Chung H, Park SB, Park KS, Kim HS, Ro S and Kim JB. A newly identified CG301269 improves lipid and glucose metabolism without body weight gain through activation of peroxisome proliferator-activated receptor alpha and gamma. Diabetes 2011; 60: 496-506.
35. Keller H, Mahfoudi A, Dreyer C, Hihi AK, Medin J, Ozato K and Wahli W. Peroxisome proliferator-activated receptors and lipid metabolism. Ann N Y Acad Sci 1993; 684: 157-173.
36. Bonnefont JP, Djouadi F, Prip-Buus C, Gobin S, Munnich A and Bastin J. Carnitine palmitoyltransferases 1 and 2: biochemical, molecular and medical aspects. Mol Aspects Med 2004; 25: 495-520.
37. Green S, Tugwood JD and Issemann I. The molecular mechanism of peroxisome proliferator action: a model for species differences and mechanistic risk assessment. Toxicol Lett 1992; 64-65 Spec No: 131-139.
38. Poirier Y, Antonenkov VD, Glumoff T and Hil-tunen JK. Peroxisomal beta-oxidation--a metabolic pathway with multiple functions. Biochim Biophys Acta 2006; 1763: 1413-1426.
39. Dentin R, Pegorier JP, Benhamed F, Foufelle F, Ferre P, Fauveau V, Magnuson MA, Girard J and Postic C. Hepatic glucokinase is required for the synergistic action of ChREBP and SREBP-1c on glycolytic and lipogenic gene expression. J Biol Chem 2004; 279: 20314-20326.
40. Stoeckman AK and Towle HC. The role of SREBP-1c in nutritional regulation of lipogenic enzyme gene expression. J Biol Chem 2002; 277: 27029-27035.