Insulin-signalling molecules in the liver of high-fat diet and fructose-induced type-2 diabetic adult male rat

Applied Physiology, Nutrition and Metabolism

Volumn 40, Issue 8, 2015, Pages 769-781

  Narasimhan, Akilavalli ^a   Chinnaiyan, Mayilvanan ^a   Karundevi, Balasubramanian ^a  

^a UNIVERSITY OF MADRAS   (India)

Author keywords

Ferulic acid; Gluconeogenesis; Glycogenesis; Glycogenolysis; Insulin resistance; Insulin signalling

Indexed keywords

ANTIDIABETIC AGENT; CHOLAGOGUE; COUMARIC ACID; FERULIC ACID; FRUCTOSE; GLUCOSE BLOOD LEVEL; INSULIN;

ANIMAL; BLOOD; DISEASE MODEL; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; GLUCONEOGENESIS; GLUCOSE BLOOD LEVEL; INSULIN RESISTANCE; LIPID DIET; LIVER; MALE; METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; RAT; SIGNAL TRANSDUCTION;

ANIMALS; BLOOD GLUCOSE; CHOLAGOGUES AND CHOLERETICS; COUMARIC ACIDS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; FRUCTOSE; GLUCONEOGENESIS; HYPOGLYCEMIC AGENTS; INSULIN; INSULIN RESISTANCE; LIVER; MALE; RATS; SIGNAL TRANSDUCTION;

EID: 84938815871     PISSN: 17155312     EISSN: 17155320     Source Type: Journal    
DOI: 10.1139/apnm-2015-0002     Document Type: Article

References (65)

1. Adisakwattana, S., Moonsan, P., and Yibchok-Anun, S. 2008. Insulin-releasing properties of a series of cinnamic acid derivatives in vitro and in vivo. J. Agric. Food Chem. 56: 7838–7844. doi:10.1021/jf801208t. PMID: 18651742.
2. Adisakwattana, S., Chantarasinlapin, P., Thammarat, H., and Yibchok-Anun, S. 2009. A series of cinnamic acid derivatives and their inhibitory activity on intestinal alpha-glucosidase. J. Enzyme Inhib. Med. Chem. 24(5): 1194–1200. doi:10.1080/14756360902779326. PMID: 19772492.
3. Adisakwattana, S., Pongsuwan, J., Wungcharoen, C., and Yibchok-anun, S. 2013. In vitro effects of cinnamic acid derivatives on protein tyrosine phosphatase 1B. J. Enzyme. Inhib. Med. Chem. 28: 1067–1072. doi:10.3109/14756366.2012. 715286. PMID: 22957721.
4. Balasubashini, M.S., Rukkumani, R., Viswanathan, P., and Menon, V.P. 2004. Ferulic acid alleviates lipid peroxidation in diabetic rats. Phytother. Res. 18: 310–314. doi:10.1002/ptr.1440. PMID: 15162367.
5. Barbour, L.A., McCurdy, C.E., Hernandez, T.L., Kirwan, J.P., Catalano, P.M., and Friedman, J.E. 2007. Cellular mechanisms for insulin resistance in normal pregnancy and gestational diabetes. Diabetes Care, 30: S112–S119. doi:10. 2337/dc07-s202. PMID: 17596458.
6. Bischoff, H. 1995. The mechanism of alpha-glucosidase inhibition in the management of diabetes. Clin. Invest. Med. 18: 303–311. PMID: 8549017.
7. Bollen, M., Keppens, S., and Stalmans, W. 1998. Specific features of glycogen metabolism in the liver. Biochem. J. 336: 19–31. PMID: 9806880.
8. Choi, R., Kim, B.H., Naowaboot, J., Lee, M.Y., Hyun, M.R., Cho, E.J., et al. 2011. Effects of ferulic acid on diabetic nephropathy in a rat model of type 2 diabetes. Exp. Mol. Med. 43: 676–683. doi:10.3858/emm.2011.43.12.078. PMID: 21975281.
9. Cohen, P., and Goedert, M. 2004. GSK3 inhibitors: development and therapeutic potential. Nat. Rev. Drug Discov. 3: 479–487. doi:10.1038/nrd1415. PMID: 15173837.
10. Cornblath, M., Randle, P.J., Parmeggiani, A., and Morgan, H.E. 1963. Regulation of glycogenolysis in muscle. Effects of glucagon and anoxia on lactate production, glycogen content, and phosphorylase activity in the perfused isolated rat heart. J. Biol. Chem. 238: 1592–1597. PMID: 14023049.
11. Dajani, R., Fraser, E., Roe, S.M., Young, N., Good, V., Dale, T.C., and Pearl, L.H. 2001. Crystal structure of glycogen synthase kinase 3 beta: structural basis for phosphate-primed substrate specificity and autoinhibition. Cell, 105: 721–732. doi:10.1016/S0092-8674(01)00374-9. PMID: 11440715.
12. Elchebly, M., Payette, P., Michaliszyn, E., Cromlish, W., Collins, S., Loy, A.L., et al. 1999. Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene. Science, 283: 1544–1548. doi:10.1126/science.283.5407.1544. PMID: 10066179.
13. Erion, D.M., and Shulman, G.I. 2010. Diacylglycerol-mediated insulin resistance. Nat. Med. 16: 400–402. doi:10.1038/nm0410-400. PMID: 20376053.
14. Fisher, S.J., and Kahn, C.R. 2003. Insulin signaling is required for insulin’s direct and indirect action on hepatic glucose production. J. Clin. Invest. 111: 463–468. doi:10.1172/JCI200316426. PMID: 12588884.
15. Fourney, R.M., Miyakoshi, J., Day, R.S., and Randall, R.J. 1988. Northern blotting: efficient RNA staining and transfer. Focus, 10: 5–7.
16. Gohil, K.J., Kshirsagar, S.B., and Sahane, R.S. 2012. Ferulic acid–a comprehensive pharmacology of an important bioflavonoid. Int. J. Pharm. Sci. Res. 3: 700–710.
17. Goward, C.R., Hartwell, R., Atkinson, T., and Scawen, M.D. 1986. The purification and characterization of glucokinase from the thermophile Bacillus stearothermophilus. Biochem. J. 237: 415–420. PMID: 3099754.
18. Graf, E. 1992. Antioxidant potential of ferulic acid. Free Radic. Biol. Med. 13: 435–448. doi:10.1016/0891-5849(92)90184-I. PMID: 1398220.
19. Guinovart, J.J., Gomez-Foix, A.M., Seoane, J., Fernandez-Novell, J.M., Bellido, D., and Vilaro, S. 1997. Bridging the gap between glucose phosphorylation and glycogen synthesis in the liver. Biochem. Soc. Trans. 25: 157–160. PMID: 9056863.
20. Hall, R.K., Yamasaki, T., Kucera, T., Waltner-Law, M., O’Brien, R., and Granner, D.K. 2000. Regulation of phosphoenolpyruvate carboxykinase and insulin-like growth factor-binding protein-1 gene expression by insulin. The role of winged helix/forkhead proteins. J. Biol. Chem. 275: 30169–30175. doi: 10.1074/jbc.M004898200. PMID: 10913147.
21. Hassid, W., and Abraham, S. 1975. Chemical procedures for analysis of polysaccharides. In Methods in Enzymology, Vol. 3. Edited by S. Colowick and N. Kaplan. Academic Press, New York, N.Y., USA. pp. 34–36.
22. Hollman, P.C., and Katan, M.B. 1998. Bioavailability and health effects of dietary flavonols in man. Arch. Toxicol. Suppl. 20: 237–248. doi:10.1007/978-3-642-46856-8_21. PMID: 9442297.
23. Hotamisligil, G.S., Peraldi, P., Budavari, A., Ellis, R., White, M.F., and Spiegelman, B.M. 1996. IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha-and obesity-induced insulin resistance. Science, 271: 665–670. doi:10.1126/science.271.5249.665. PMID:8571133.
24. International Diabetes Federation. 2013. Diabetes Atlas, 6th ed. International Diabetes Federation. pp. 29–48.
25. Jung, E.H., Kim, S.R., Hwang, I.K., and Ha, T.Y. 2007. Hypoglycemic effects of a phenolic acid fraction of rice bran and ferulic acid in C57BL/KsJ-db/db mice. J. Agric. Food Chem. 55: 9800–9804. doi:10.1021/jf0714463. PMID: 17973443.
26. Kanuri, G., Spruss, A., Wagnerberger, S., Bischoff, S.C., and Bergheim, I. 2011. Fructose-induced steatosis in mice: role of plasminogen activator inhibitor-1, microsomal triglyceride transfer protein and NKT cells. Lab. Invest. 91: 885–895. doi:10.1038/labinvest.2011.44. PMID: 21423135.
27. Katz, A., Nambi, S.S., Mather, K., Baron, A.D., Follmann, D.A., Sullivan, G., and Quon, M.J. 2000. Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. J. Clin. Endocrinol. Metab. 85: 2402–2410. doi:10.1210/jcem.85.7.6661. PMID: 10902785.
28. Kim, P., Laivenieks, M., Vieille, C., and Zeikus, J.G. 2004. Effect of overexpression of Actinobacillus succinogenes phosphoenolpyruvate carboxykinase on succinate production in Escherichia coli. Appl. Environ. Microbiol. 70: 1238–1241. doi:10.1128/AEM.70.2.1238-1241.2004. PMID: 14766613.
29. Konig, M., Bulik, S., and Holzhutter, H.G. 2012. Quantifying the contribution of the liver to glucose homeostasis: a detailed kinetic model of human hepatic glucose metabolism. PLoS Comput. Biol. 8: e1002577. doi:10.1371/journal.pcbi. 1002577. PMID: 22761565.
30. Laviola, L., Belsanti, G., Davalli, A.M., Napoli, R., Perrini, S., Weir, G.C., et al. 2001. Effects of streptozocin diabetes and diabetes treatment by islet transplantation on in vivo insulin signaling in rat heart. Diabetes, 50: 2709–2720. doi: 10.2337/diabetes.50.12.2709. PMID: 11723053.
31. Leavens, K.F., and Birnbaum, M.J. 2011. Insulin signaling to hepatic lipid metabolism in health and disease. Crit. Rev. Biochem. Mol. Biol. 46: 200–215. doi: 10.3109/10409238.2011.562481. PMID: 21599535.
32. Leloir, L.F., and Goldemberg, S.H. 1962. Glycogen synthetase from rat liver. In Methods in enzymology, Vol. 5. Edited by S.P. Colowick and N.O. Kaplan. Academic Press, New York, N.Y., USA. pp. 145–146.
33. Li, J.M., Li, Y.C., Kong, L.D., and Hu, Q.H. 2010. Curcumin inhibits hepatic protein-tyrosine phosphatase 1B and prevents hypertriglyceridemia and hepatic steatosis in fructose-fed rats. Hepatology, 51: 1555–1566. doi:10.1002/hep.23524. PMID: 20222050.
34. Lowry, O.H., Rosebrough, N.J., Farr, A.L., and Randall, R.J. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193: 265–275. PMID: 14907713.
35. Martinez, F.J., Rizza, R.A., and Romero, J.C. 1994. High-fructose feeding elicits insulin resistance, hyperinsulinism, and hypertension in normal mongrel dogs. Hypertension, 23: 456–463. doi:10.1161/01.HYP.23.4.456. PMID: 8144215.
36. Matthews, D.R., Hosker, J.P., Rudenski, A.S., Naylor, B.A., Treacher, D.F., and Turner, R.C. 1985. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia, 28: 412–419. doi:10.1007/BF00280883. PMID: 3899825.
37. Mitrakou, A., Kelley, D., Mokan, M., Veneman, T., Pangburn, T., Reilly, J., and Gerich, J. 1992. Role of reduced suppression of glucose production and diminished early insulin release in impaired glucose tolerance. N. Engl. J. Med. 326: 22–29. doi:10.1056/NEJM199201023260104. PMID: 1727062.
38. Nakae, J., Kitamura, T., Silver, D.L., and Accili, D. 2001. The forkhead transcription factor Foxo1 (Fkhr) confers insulin sensitivity onto glucose-6-phosphatase expression. J. Clin. Invest. 108: 1359–1367. doi:10.1172/JCI200112876. PMID: 11696581.
39. Nikoulina, S.E., Ciaraldi, T.P., Mudaliar, S., Mohideen, P., Carter, L., and Henry, R.R. 2000. Potential role of glycogen synthase kinase-3 in skeletal muscle insulin resistance of type 2 diabetes. Diabetes, 49: 263–271. doi:10. 2337/diabetes.49.2.263. PMID: 10868943.
40. Nomura, E., Kashiwada, A., Hosoda, A., Nakamura, K., Morishita, H., Tsuno, T., and Taniguchi, H. 2003. Synthesis of amide compounds of ferulic acid, and their stimulatory effects on insulin secretion in vitro. Bioorg. Med. Chem. 11: 3807–3813. doi:10.1016/S0968-0896(03)00280-3. PMID: 12901926.
41. Nordlie, R.C., and Arion, W.J. 1965. Liver microsomal glucose 6-phosphatase, inorganic pyrophosphatase, and pyrophosphate-glucose phosphotransferase. 3. associated nucleoside triphosphate-and nucleoside diphosphateglucose phosphotransferase activities. J. Biol. Chem. 240: 2155–2164. PMID: 14299641.
42. Norhammar, A., Tenerz, A., Nilsson, G., Hamsten, A., Efendic, S., Ryden, L., and Malmberg, K. 2002. Glucose metabolism in patients with acute myocardial infarction and no previous diagnosis of diabetes mellitus: a prospective study. Lancet, 359: 2140–2144. doi:10.1016/S0140-6736(02)09089-X. PMID: 12090978.
43. Park, J.M., Kim, T.H., Bae, J.S., Kim, M.Y., Kim, K.S., and Ahn, Y.H. 2010. Role of resveratrol in FOXO1-mediated gluconeogenic gene expression in the liver. Biochem. Biophys. Res. Commun. 403: 329–334. doi:10.1016/j.bbrc.2010.11. 028. PMID: 21078299.
44. Pearce, N.J., Arch, J.R., Clapham, J.C., Coghlan, M.P., Corcoran, S.L., Lister, C.A., et al. 2004. Development of glucose intolerance in male transgenic mice over-expressing human glycogen synthase kinase-3β on a muscle-specific promoter. Metabolism, 53: 1322–1330. doi:10.1016/j.metabol.2004.05.008. PMID: 15375789.
45. Pederson, T.M., Kramer, D.L., and Rondinone, C.M. 2001. Serine/threonine phosphorylation of IRS-1 triggers its degradation: possible regulation by tyrosine phosphorylation. Diabetes, 50: 24–31. doi:10.2337/diabetes.50.1.24. PMID: 11147790.
46. Plotkin, B., Kaidanovich, O., Talior, I., and Eldar-Finkelman, H. 2003. Insulin mimetic action of synthetic phosphorylated peptide inhibitors of glycogen synthase kinase-3. J. Pharmacol. Exp. Ther. 305: 974–980. doi:10.1124/jpet. 102.047381. PMID: 12626660.
47. Polonsky, K.S., Sturis, J., and Bell, G.I. 1996. Non-insulin-dependent diabetes mellitus-a genetically programmed failure of the beta cell to compensate for insulin resistance. N. Engl. J. Med. 334(12): 777–783. doi:10.1056/NEJM199603213341207. PMID: 8592553.
48. Prabhakar, P.K., Prasad, R., Ali, S., and Doble, M. 2013. Synergistic interaction of ferulic acid with commercial hypoglycemic drugs in streptozotocin induced diabetic rats. Phytomedicine, 20: 488–494. doi:10.1016/j.phymed.2012.12.004. PMID: 23490007.
49. Qin, B., Anderson, R.A., and Adeli, K. 2008. Tumor necrosis factor-α directly stimulates the overproduction of hepatic apolipoprotein B100-containing VLDL via impairment of hepatic insulin signaling. Am. J. Physiol. Gastrointest. Liver Physiol. 294: G1120–G1129. doi:10.1152/ajpgi.00407.2007. PMID: 18372392.
50. Roglans, N., Vila, L., Farre, M., Alegret, M., Sanchez, R.M., Vazquez-Carrera, M., and Laguna, J.C. 2007. Impairment of hepatic Stat-3 activation and reduction of PPARalpha activity in fructose-fed rats. Hepatology, 45: 778–788. doi:10. 1002/hep.21499. PMID: 17326204.
51. Rohn, S., Rawel, H.M., and Kroll, J. 2002. Inhibitory effects of plant phenols on the activity of selected enzymes. J. Agric. Food Chem. 50: 3566–3571. doi:10. 1021/jf011714b. PMID: 12033830.
52. Roy, S., Metya, S.K., Sannigrahi, S., Rahaman, N., and Ahmed, F. 2013. Treatment with ferulic acid to rats with streptozotocin-induced diabetes: effects on oxidative stress, pro-inflammatory cytokines, and apoptosis in the pancreatic β cell. Endocrine, 44: 369–379. doi:10.1007/s12020-012-9868-8. PMID: 23299178.
53. Sakai, S., Ochiai, H., Nakajima, K., and Terasawa, K. 1997. Inhibitory effect of ferulic acid on macrophage inflammatory protein-2 production in a murine macrophage cell line, RAW264. 7. Cytokine, 9: 242–248. doi:10.1006/cyto.1996. 0160. PMID: 9112332.
54. Samuel, V.T., Liu, Z.X., Wang, A., Beddow, S.A., Geisler, J.G., Kahn, M., et al. 2007. Inhibition of protein kinase C epsilon prevents hepatic insulin resistance in nonalcoholic fatty liver disease. J. Clin. Invest. 117: 739–745. doi:10.1172/JCI30400. PMID: 17318260.
55. Schmoll, D., Walker, K.S., Alessi, D.R., Grempler, R., Burchell, A., Guo, S., et al. 2000. Regulation of glucose-6-phosphatase gene expression by protein kinase Balpha and the forkhead transcription factor FKHR. Evidence for insulin response unit-dependent and-independent effects of insulin on promoter activity. J. Biol. Chem. 275: 36324–36333. PMID: 10960473.
56. Shanik, M.H., Xu, Y., Skrha, J., Dankner, R., Zick, Y., and Roth, J. 2008. Insulin resistance and hyperinsulinemia: is hyperinsulinemia the cart or the horse? Diabetes Care, 31: S262–S268. doi:10.2337/dc08-s264. PMID: 18227495.
57. Smith, S.A., Porter, L.E., Biswas, N., and Freed, M.I. 2004. Rosiglitazone, but not glyburide, reduces circulating proinsulin and proinsulin:insulin ratio in type 2 diabetes. J. Clin. Endocrinol. Metab. 89: 6048–6053. doi:10.1210/jc.2004-0705. PMID: 15579757.
58. Son, M.J., Rico, C.W., Nam, S.H., and Kang, M.Y. 2010. Influence of oryzanol and ferulic Acid on the lipid metabolism and antioxidative status in high fat-fed mice. J. Clin. Biochem. Nutr. 46: 150–156. doi:10.3164/jcbn.09-98. PMID: 20216948.
59. Son, M.J., Rico, C.W., Nam, S.H., and Kang, M.Y. 2011. Effect of oryzanol and ferulic acid on the glucose metabolism of mice fed with a high-fat diet. J. Food Sci. 76: H7–H10. doi:10.1111/j.1750-3841.2010.01907.x. PMID: 21535685.
60. Stefan, N., and Haring, H.U. 2013. The role of hepatokines in metabolism. Nat. Rev. Endocrinol. 9: 144–152. doi:10.1038/nrendo.2012.258. PMID: 23337953.
61. Yue, T.L., Bao, W., Gu, J.L., Cui, J., Tao, L., Ma, X.L., et al. 2005. Rosiglitazone treatment in Zucker diabetic fatty rats is associated with ameliorated cardiac insulin resistance and protection from ischemia/reperfusion-induced myocardial injury. Diabetes, 54: 554–562. doi:10.2337/diabetes.54.2.554. PMID: 15677515.
62. Zabolotny, J.M., Kim, Y.B., Welsh, L.A., Kershaw, E.E., Neel, B.G., and Kahn, B.B. 2008. Protein-tyrosine phosphatase 1B expression is induced by inflammation in vivo. J. Biol. Chem. 283: 14230–14241. doi:10.1074/jbc.M800061200. PMID: 18281274.
63. Zhao, Z., and Moghadasiana, M.H. 2008. Chemistry, natural sources, dietary intake and pharmacokinetic properties of ferulic acid: A review. Food Chem. 109: 691–702. doi:10.1016/j.foodchem.2008.02. 039.
64. Zhou, G., Myers, R., Li, Y., Chen, Y., Shen, X., Fenyk-Melody, J., et al. 2001. Role of AMP-activated protein kinase in mechanism of metformin action. J. Clin. Invest. 108: 1167–1174. doi:10.1172/JCI200113505. PMID: 11602624.
65. Zhu, H., Liang, Q.H., Xiong, X.G., Chen, J., Wu, D., Wang, Y., et al. 2014. Antiinflammatory effects of the bioactive compound ferulic acid contained in Oldenlandia diffusa on collagen-induced arthritis in rats. Evid. Based Complement. Alternat. Med. 2014: 573801. doi:10.1155/2014/573801. PMID:24883069.