Effect of citrus flavonoids on lipid metabolism and glucose-regulating enzyme mRNA levels in type-2 diabetic mice

International Journal of Biochemistry and Cell Biology

Volumn 38, Issue 7, 2006, Pages 1134-1145

  Jung, Un Ju ^a   Lee, Mi Kyung ^a   Park, Yong Bok ^a   Kang, Mi Ae ^a   Choi, Myung Sook ^a  

^a Kyungpook National University   (South Korea)

Author keywords

C57BL KsJ db db mice; Hesperidin; Hypoglycemic; Hypolipidemic; Naringin

Indexed keywords

ACYL COENZYME A; AURANTIIN; BIOFLAVONOID; CARNITINE PALMITOYLTRANSFERASE; CHOLESTEROL; CHOLESTEROL ACYLTRANSFERASE; FATTY ACID; FATTY ACID SYNTHASE; GLUCOKINASE; GLUCOSE 6 PHOSPHATASE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUCOSE REGULATED PROTEIN; GLUCOSE TRANSPORTER 2; GLUCOSE TRANSPORTER 4; HESPERIDIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; LIPID; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHATIDATE PHOSPHATASE; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLESTEROL METABOLISM; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVITY; FATTY ACID OXIDATION; LIPID METABOLISM; LIVER; MALE; MOUSE; MOUSE STRAIN; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION;

ANIMALS; CITRUS; DIABETES MELLITUS, TYPE 2; FLAVANONES; GLUCOKINASE; HESPERIDIN; LIPID METABOLISM; MALE; MICE; MICE, INBRED C57BL; PHYTOTHERAPY; RNA, MESSENGER;

ANIMALIA; CITRUS;

EID: 33645892889     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2005.12.002     Document Type: Article

References (71)

1. Abel E.D., Peronl O., Kim J.K., Kim Y.B., Boss O., Hadro E., et al. Adipose-selective targeting of the GLUT4 gene impairs insulin action in muscle and liver. Nature 409 (2001) 729-733
2. American Institute of Nutrition. Report of the American Institute of Nutrition ad hoc Committee on Standards for Nutritional Studies. The Journal of Nutrition 107 (1977) 1340-1348
3. Bhathena S.J., and Velasquez M.T. Beneficial role of dietary phytoestrogens in obesity and diabetes. The American Journal of Clinical Nutrition 76 (2002) 1191-1201
4. Borradaile N.M., de Dreu L.E., and Huff M.W. Inhibition of net HepG2 cell apolipoprotein B secretion by the citrus flavonoid naringenin involves activation of phosphatidylinositol 3-kinase, independent of insulin receptor substrate-1 phosphorylation. Diabetes 52 (2003) 2554-2561
5. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72 (1976) 248-254
6. Brichard S., Henquin J.C., and Girard J. Phlorizin treatment of diabetic rats partially reverses the abnormal expression of genes involved in hepatic glucose metabolism. Diabetologia 36 (1993) 292-298
7. Brown M.S., Ho Y.K., and Goldstein J.L. The cholesteryl ester cycle in macrophage foam cells. Continual hydrolysis and re-esterification of cytoplasmic cholesteryl esters. The Journal of Biological Chemistry 255 (1980) 9344-9352
8. Burcelin R., Eddouks M., Kandé J., Assan R., and Girard J. Evidence that GLUT-2 mRNA and protein concentrations are decreased by hyperinsulinaemia and increased by hyperglycaemia in liver of diabetic rats. The Biochemical Journal 288 (1992) 675-679
9. Carl M.N., Lakshmanan M.R., and Porter J.W. Fatty acid synthase from rat liver. Methods in Enzymology 35 (1975) 37-44
10. Cha J.Y., Cho Y.S., Kim I., Anno T., Rahman S.M., and Yanagita T. Effect of hesperetin, a citrus flavonoid, on the liver triacylglycerol content and phosphatidate phosphohydrolase activity in orotic acid-fed rats. Plant Foods for Human Nutrition 56 (2001) 349-358
11. Choe S.C., Kim H.S., Jeong T.S., Bok S.H., and Park Y.B. Naringin has an antiatherogenic effect with the inhibition of intercellular adhesion molecule-1 in hypercholesterolemic rabbits. Journal of Cardiovascular Pharmacology 38 (2001) 947-955
12. Choi J.S., Yokozawa T., and Oura H. Improvement of hyperglycemia and hyperlipidemia in streptozotocin-diabetic rats by a methanolic extract of prunus davidiana stems and its main component, pruning. Planta Medica 57 (1991) 208-211
13. Chomzynski P., and Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Annual review of Biochemistry 162 (1987) 156-159
14. Costa L.G., Cole T.B., Jarvik G.P., and Furlong C.E. Functional genomics of the paraoxonase (PON1) polymorphisms: Effects on pesticide sensitivity, cardiovascular disease, and drug metabolism. Annual Review of Medicine 54 (2003) 371-392
15. Durrington P.N., Mackness B., and Mackness M.I. The hunt for nutritional and pharmacological modulators of paraoxonase. Arteriosclerosis, Thrombosis, and Vascular Biology 22 (2002) 1248-1250
16. Erickson S.K., Schrewsbery M.A., Brooks C., and Meyer D.J. Rat liver acyl-coenzyme A: Cholesterol acyltransferase: Its regulation in vivo and some of properties in vitro. Journal of Lipid Research 21 (1980) 930-941
17. Erlund I., Merririnne E., Alfthan G., and Aro A. Plasma kinetics and urinary excretion of the flavanones naringenin and hesperetin in human after ingestion of orange juice and grapefruit juice. The Journal of Nutrition 131 (2001) 235-241
18. Ferre T., Pujol A., Riu E., Bosch F., and Valera A. Correction of diabetic alterations by glucokinase. Proceedings of the National Academy of Sciences of the United States of America 93 (1996) 7225-7230
19. Folch J., Lees M., and Sloan-Stanley G.H. A simple method for isolation and purification of total lipids from animal tissues. The Journal of Biological Chemistry 226 (1956) 497-509
20. Foley J.E. Rationale and application of fatty acid oxidation inhibitors in treatment of diabetes mellitus. Diabetes Care 15 (1992) 773-784
21. Friedman J.E., Sun Y., Ishizuka T., Farrell C.J., McCormack S.E., Herron L.M., et al. Phosphoenolpyruvate carboxykinase (GTP) gene transcription and hyperglycemia are regulated by glucocorticoids in genetically obese db/db transgenic mice. The Journal of Biological Chemistry 272 (1997) 31475-31481
22. Fritz I.B. Factors influencing the rates of long chain fatty acid oxidation and synthesis in mammalian systems. Physiological Reviews 41 (1961) 52-129
23. Fuhrman B., and Aviram M. Preservation of paraoxonase activity by wine flavonoids: Possible role in protection of LDL from lipid peroxidation. Annals of the New York Academy of Sciences 957 (2002) 321-324
24. Fulgencio J.P., Kohl C., Girard J., and Pegorier J.P. Troglitazone inhibits fatty acid oxidation and esterification, and gluconeogenesis in isolated hepatocytes from starved rats. Diabetes 45 (1995) 1556-1562
25. Gibbs E.M., Stock J.L., McCoid S.C., Stukenbrok H.A., Pessin J.E., Stevenson R.W., et al. Glycemic improvement in diabetic db/db mice by overexpression of the human insulin-regulatable glucose transporter (GLUT4). The Journal of Clinical Investigation 95 (1995) 1512-1518
26. Groop L.C., Bonadonna R.C., DelPrato S., Ratheiser K., and Zyck K. Glucose and free fatty acid metabolism in non-insulin-dependent diabetes mellitus. Journal of Clinical Investigation 84 (1989) 205-213
27. Halminski M.A., Marsh J.B., and Harrison E.H. Differential effects of fish oil, safflower oil and palm oil on fatty acid oxidation and glycerolipid synthesis in rat liver. The Journal of Nutrition 121 (1991) 1554-1561
28. Hawkins M., Tonelli J., Kishore P., Stein D., Ragucci E., Gitig A., et al. Contribution of elevated free fatty acid levels to the lack of glucose effectiveness in type 2 diabetes. Diabetes 52 (2003) 2748-2758
29. Hulcher F.H., and Oleson W.H. Simplified spectrophotometric assay for microsomal 3-hydroxy-3-methylglutaryl CoA reductase by measurement of coenzyme A. Journal of Lipid Research 14 (1973) 625-631
30. Hummel K.P., Dickie M.W., and Coleman D.L. Diabetes, new mutation in the mouse. Science 153 (1966) 1127-1128
31. Iynedjian P.B., Gjinovci A., and Renold A.E. Stimulation by insulin of glucokinase gene transcription in liver of diabetic rats. The Journal of Biology Chemistry 263 (1988) 740-744
32. Jung U.J., Kim H.J., Lee J.S., Lee M.K., Kim H.O., Park E.J., et al. Naringin supplementation lowers plasma lipids and enhances erythrocyte antioxidant enzyme activities in hypercholesterolemic subjects. Clinical Nutrition 22 (2003) 561-568
33. Jung U.J., Lee M.K., Jeong K.S., and Choi M.S. The hypoglycemic effects of hesperidin and naringin are partly mediated by hepatic glucose-regulating enzymes in C57BL/KsJ-db/db mice. The Journal of Nutrition 134 (2004) 2499-2503
34. Kahn A. Transcriptional regulation by glucose in the liver. Biochimie 79 (1997) 113-118
35. Kim J.K., Gavrilova O., Chen Y., Reitman M.L., and Shulman G.I. Mechanism of insulin resistance in A-ZIP/F-1 fatless mice. The Journal Biological Chemistry 275 (2000) 8456-8460
36. Kim S.Y., Kim H.I., Park S.K., Im S.S., Li T., Cheon H.G., et al. Liver glucokinase can be activated by peroxisome proliferators-activated receptor-γ. Diabetes 53 (2004) S66-S70
37. Kodama H., Fujita H., and Yamaguchi I. Development of hyperglycaemia and insulin resistance in conscious genetically diabetes (C57BL/KsJ-db/db) mice. Diabetologia 37 (1994) 739-744
38. Kuhnau J. The flavonoids A class of semi-essential food components: Their role in human nutrition. World Review of Nutrition and Dietetics 24 (1976) 117-191
39. Lazarow P.B. Assay of peroxisomal β-oxidation of fatty acids. Methods in Enzymology 72 (1981) 315-319
40. Liang Y.C., Tsai S.H., Tsai D.C., Lin-Shiau S.Y., and Lin J.K. Suppression of inducible cyclooxygenas and nitric oxide synthase through activation of peroxisome proliferators-activated receptor-γ by flavonoids in mouse macrophages. FEBS Letters 496 (2001) 12-18
41. Liu X., Kim J.K., Li Y., Li J., Liu F., and Chen X. Tannic acid stimulates glucose transport and inhibits adipocyte differentiation in 3T3-L1 cells. The Journal of Nutrition 135 (2005) 165-171
42. Mackness B., Durrington P., McElduff P., Yarnell J., Azam N., Watt M., et al. Paraoxonase and susceptibility to organophosphorus poisoning in farmers dipping sheep. Pharmacogenetics 13 (2003) 81-88
43. Mackness M.I., Harty D., Bhatnagar D., Winocour P.H., Arrol S., Ishola M., et al. Serum paraoxonase activity in familial hypercholesterolaemia and insulin-dependent diabetes mellitus. Atherosclerosis 86 (1991) 193-199
44. Markwell M.A.K., McGroarty E.J., Bieber L.L., and Tolbert N.E. The subcellular distribution of carnitine acyltransferases in mammalian liver and kidney. The Journal of Biological Chemistry 248 (1973) 3426-3432
45. McGarry J.D. Disordered metabolism in diabetes: Have we underemphasized the fat component?. Journal of cellular biochemistry 55 Suppl. (1994) 29-38
46. McGarry J.D., and Foster D.W. Regulation of hepatic fatty acid oxidation and ketone body production. Annual Review of Biochemistry 49 (1980) 395-420
47. Memon R.A., Grunfeld C., Moser A.H., and Feingold K.R. Fatty acid synthesis in obese insulin resistant diabetic mice. Hormone and Metabolic Research 26 (1994) 85-87
48. Misra P., Chakrabarti R., Vikramadithyan R.K., Bolusu G., Juluri S., Hiriyan J., et al. PAT5A: A partial agonist of peroxisome proliferators-activated receptor γ is a potent antidiabetic thiazolidinedione yet weakly adipogenic. The Journal of Pharmacology and Experimental Therapeutics 306 (2003) 763-771
49. Muñoz M.C., Barberà A., Domínguez J., Fernàndez-Alvarez J., Gomis R., and Guinovart J.J. Effects of tungstate, a new potential oral antidiabetic agent, in Zucker diabetic fatty rats. Diabetes 50 (2001) 131-138
50. Nathan J.D., Zdankiewicz P.D., Wang J., Spector S.A., Aspelund G., Jena B.P., et al. Impaired hepatocyte glucose transport protein (GLUT2) internalization in chronic pancreatitis. Pancreas 22 (2001) 172-178
51. Oka Y., Assano T., Shibasaki Y., Lin J.L., Tsukuda K., Akanuma Y., et al. Increased liver glucose-transporter protein and mRNA in streptozotocin-induced diabeteic rats. Diabetes 39 (1990) 441-446
52. Kris-Etherton P.M., and Keen C.L. Evidence that the antioxidant flavonoids in tea and cocoa are beneficial for cardiovascular health. Current Opinion Lipidology 13 (2002) 41-44
53. Pitkanen E., Pitkanen O., and Uotila L. Enzymatic determination of unbound d-mannose in serum. European Journal of Clinical Chemistry and Clinical Biochemistry 35 (1997) 761-766
54. Pinent M., Blay M., Blade M.C., Salvado M.J., Arola L., and Ardevol A. Grape seed-derived procyanidins have an antihyperglycemic effect in streptozotocin-induced diabetic rats and insulinomimetic activity in insulin-sensitive cell lines. Endocrinology 145 (2004) 4985-4990
55. Postic C., Shiota M., Niswender K.D., Jetton T.L., Chen Y., Moates J.M., et al. Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic β-cell-specific gene knock-outs using Cre recombinase. The Journal of Biological Chemistry 274 (1999) 305-315
56. Randle P.J., Kerbey A.L., and Espinal J. Mechanisms decreasing glucose oxidation in diabetes and starvation: Role of lipid fuels and hormones. Diabetes Metabolism Reviews 4 (1988) 623-638
57. Raz I., Eldor R., Cernea S., and Shafrir E. Diabetes, insulin resistance and derangements in lipid metabolism. Cure through intervention in fat transport and storage. Diabetes Metabolism Research Reviews 21 (2005) 3-14
58. Rencurel F., Waeber G., Antoine B., Rocchiccioli F., Maulard P., Girard J., et al. Requirement of glucose metabolism for regulation of glucose transporter type 2 (GLUT2) gene expression in liver. The Biochemical Journal 314 (1996) 903-909
59. Sandouk T., Reda D., and Hofmann C. Antidiabetic agent pioglitazone enhances adipocyte differentiation of 3T3-F442A cells. The American Journal of Physiology 264 (1993) C1600-C1608
60. Santomauro A.T., Boden G., Silva M.E., Rocha D.M., Santos R.F., Ursich M.J., et al. Overnight lowering of free fatty acids with Acipimox improves insulin resistance and glucose tolerance in obese diabetic and nondiabetic subjects. Diabetes 48 (1999) 1836-1841
61. Shah P., Vella A., Basu A., Basu R., Adkins A., Schwenk W.F., et al. Elevated free fatty acids impair glucose metabolism in women: Decreased stimulation of muscle glucose uptake and suppression of splanchnic glucose production during combined hyperinsulinemia and hyperglycemia. Diabetes 52 (2003) 38-42
62. Shapiro D.J., Nordstrom J.L., Mitschelen J.J., Rodwell V.W., and Schimke R.T. Micro assay for 3-hydroxy-3-methylglutaryl-CoA reductase in rat liver and in L-cell fibroblasts. Biochimica et Biophysica Acta 370 (1974) 369-377
63. Shiomi M., Ito T., Tsukada T., Tsujita Y., and Horikoshi H. Combination treatment with troglitazone, an insulin action enhancer, and pravastatin an inhibitor of HMG-CoA reductase, shows a synergistic effect on atherosclerosis on WHHL rabbits. Atherosclerosis 142 (1999) 345-353
64. Shisheva A., and Shechter Y. Quercetin selectively inhibits insulin receptor function in vitro and the bioresponses of insulin and insulinomimetic agents in rat adipocytes. Biochemistry 31 (1992) 8059-8063
65. Song J., Kwon O., Chen S., Daruwala R., Eck P., Park J.B., et al. Flavonoid inhibition of sodium-dependent Vitamin C transporter 1 (SVCT1) and glucose transporter isoform 2 (GLUT2), intestinal transporters for Vitamin C and glucose. The Journal of Biological Chemistry 277 (2002) 15252-15260
66. Suckling K.E., and Stange E.F. Role of acyl-CoA, cholesterol acyl-transferase in cellular cholesterol metabolism. Journal of Lipid Research 26 (1985) 647-671
67. Waltner-Law M.E., Wang X.L., Law W.B., Hall L.R., Nawano M., and Granner D.K. Epigallocatechin gallate, a constituent of green tea, represses hepatic glucose production. The Journal of Biological Chemistry 277 (2002) 34933-34940
68. 2+-dependent phosphatidate phosphohydrolase in pulmonary glycerolipid biosynthesis. Biochimica et Biophysica Acta 796 (1984) 346-372
69. Windmueller H.G., and Spaeth A.E. De novo synthesis of fatty acid in perfused rat liver as a determinant of plasma lipoprotein production. Archives of Biochemistry and Biophysics 122 (1967) 362-369
70. Yamauchi T., Kamon J., Waki H., Murakami K., Motojima K., Komeda K., et al. The mechanisms by which both heterozygous peroxisome proliferators-activated receptor γ (PPAR γ) deficiency and PPAR γ agonist improve insulin resistance. The Journal of Biological Chemistry 276 (2001) 41245-41254
71. Zhou Y.P., Berggren P.O., and Grill V. A fatty acid-induced decrease in pyruvate dehydrogenase activity is an important determinant of beta-cell dysfunction in the obese diabetic db/db mouse. Diabetes 45 (1996) 580-586