Hepatic FoxO1 acetylation is involved in oleanolic acid-induced memory of glycemic control: Novel findings from study 2

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Zhou, Xiu ^a   Zeng, Xiao Yi ^a   Wang, Hao ^a   Li, Songpei ^a   Jo, Eunjung ^a   Xue, Charlie C L ^a   Tan, Minjia ^b   Molero, Juan C ^a   Ye, Ji Ming ^a  

^a RMIT UNIVERSITY   (Australia)

^b SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; GLUCOSE 6 PHOSPHATASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCOGEN SYNTHASE KINASE 3BETA; HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE 1; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 4; HISTONE DEACETYLASE 5; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INSULIN; MESSENGER RNA; OLEANOLIC ACID; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PROTEIN KINASE B; SIRTUIN 1; TRANSCRIPTION FACTOR FKHR; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; FORKHEAD TRANSCRIPTION FACTOR; FOXO1 PROTEIN, MOUSE; GLUCOSE BLOOD LEVEL; HISTONE ACETYLTRANSFERASE TYPE B COMPLEX; SIRT1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AREA UNDER THE CURVE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GLUCONEOGENESIS; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE TEST; GLYCEMIC CONTROL; HYPERGLYCEMIA; IN VIVO STUDY; INSULIN BLOOD LEVEL; LIVER LEVEL; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PROTEIN ACETYLATION; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; TREATMENT DURATION; ACETYLATION; ANIMAL; C57BL MOUSE; DIABETES MELLITUS, TYPE 2; DRUG EFFECTS; GENETICS; LIVER; METABOLISM; PHOSPHORYLATION;

ACETYLATION; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BLOOD GLUCOSE; DIABETES MELLITUS, TYPE 2; FORKHEAD TRANSCRIPTION FACTORS; HISTONE ACETYLTRANSFERASES; LIVER; MALE; MICE; MICE, INBRED C57BL; OLEANOLIC ACID; PHOSPHORYLATION; SIRTUIN 1;

EID: 84907270584     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0107231     Document Type: Article

References (48)

1. Danaei G, Finucane MM, Lu Y, Singh GM, Cowan MJ, et al. (2011) National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2.7 million participants. Lancet 378: 31-40.
2. American Diabetes Association (2013) Diabetes Guidelines.
3. Castellano JM, Guinda A, Delgado T, Rada M, Cayuela JA (2013) Biochemical basis of the antidiabetic activity of oleanolic acid and related pentacyclic triterpenes. Diabetes 62: 1791-1799.
4. Tan MJ, Ye JM, Turner N, Hohnen-Behrens C, Ke CQ, et al. (2008) Antidiabetic activities of triterpenoids isolated from bitter melon associated with activation of the AMPK pathway. Chem Biol 15: 263-273.
5. Pergola PE, Raskin P, Toto RD, Meyer CJ, Huff JW, et al. (2011) Bardoxolone methyl and kidney function in CKD with type 2 diabetes. N Engl J Med 365: 327-336.
6. Gray SP, Cooper ME (2011) Diabetic nephropathy in 2010: Alleviating the burden of diabetic nephropathy. Nat Rev Nephrol 7: 71-73.
7. Zhou G, Myers R, Li Y, Chen Y, Shen X, et al. (2001) Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 108: 1167-1174.
8. Saha AK, Avilucea PR, Ye JM, Assifi MM, Kraegen EW, et al. (2004) Pioglitazone treatment activates AMP-activated protein kinase in rat liver and adipose tissue in vivo. Biochem Biophys Res Commun 314: 580-585.
9. Turner N, Li JY, Gosby A, To SW, Cheng Z, et al. (2008) Berberine and its more biologically available derivative, dihydroberberine, inhibit mitochondrial respiratory complex I: a mechanism for the action of berberine to activate AMP-activated protein kinase and improve insulin action. Diabetes 57: 1414-1418.
10. Iseli TJ, Turner N, Zeng XY, Cooney GJ, Kraegen EW, et al. (2013) Activation of AMPK by bitter melon triterpenoids involves CaMKKbeta. PLoS One 8: e62309.
11. Wang X, Liu R, Zhang W, Zhang X, Liao N, et al. (2013) Oleanolic acid improves hepatic insulin resistance via antioxidant, hypolipidemic and anti-inflammatory effects. Mol Cell Endocrinol 376: 70-80.
12. Liby KT, Yore MM, Sporn MB (2007) Triterpenoids and rexinoids as multifunctional agents for the prevention and treatment of cancer. Nat Rev Cancer 7: 357-369.
13. Zeng XY, Wang YP, Cantley J, Iseli TJ, Molero JC, et al. (2012) Oleanolic acid reduces hyperglycemia beyond treatment period with Akt/FoxO1-induced suppression of hepatic gluconeogenesis in type-2 diabetic mice. PLoS One 7: e42115.
14. Mihaylova MM, Vasquez DS, Ravnskjaer K, Denechaud PD, Yu RT, et al. (2011) Class IIa histone deacetylases are hormone-activated regulators of FOXO and mammalian glucose homeostasis. Cell 145: 607-621.
15. Siebel AL, Fernandez AZ, El-Osta A (2010) Glycemic memory associated epigenetic changes. Biochem Pharmacol 80: 1853-1859.
16. Ren LP, Chan SM, Zeng XY, Laybutt DR, Iseli TJ, et al. (2012) Differing endoplasmic reticulum stress response to excess lipogenesis versus lipid oversupply in relation to hepatic steatosis and insulin resistance. PLoS One 7: e30816.
17. Mu J, Woods J, Zhou YP, Roy RS, Li Z, et al. (2006) Chronic inhibition of dipeptidyl peptidase-4 with a sitagliptin analog preserves pancreatic beta-cell mass and function in a rodent model of type 2 diabetes. Diabetes 55: 1695-1704.
18. Kusakabe T, Tanioka H, Ebihara K, Hirata M, Miyamoto L, et al. (2009) Beneficial effects of leptin on glycaemic and lipid control in a mouse model of type 2 diabetes with increased adiposity induced by streptozotocin and a high-fat diet. Diabetologia 52: 675-683.
19. Ye JM, Tid-Ang J, Turner N, Zeng XY, Li HY, et al. (2011) PPARdelta agonists have opposing effects on insulin resistance in high fat-fed rats and mice due to different metabolic responses in muscle. Br J Pharmacol 163: 556-566.
20. Nakae J, Kitamura T, Silver DL, Accili D (2001) The forkhead transcription factor Foxo1 (Fkhr) confers insulin sensitivity onto glucose-6-phosphatase expression. J Clin Invest 108: 1359-1367.
21. McArdle J, Moorman NJ, Munger J (2012) HCMV targets the metabolic stress response through activation of AMPK whose activity is important for viral replication. PLoS Pathog 8: e1002502.
22. Mihaylova MM, Shaw RJ (2013) Metabolic reprogramming by class I and II histone deacetylases. Trends Endocrinol Metab 24: 48-57.
23. Zhang BB, Zhou G, Li C (2009) AMPK: an emerging drug target for diabetes and the metabolic syndrome. Cell Metab 9: 407-416.
24. Canto C, Auwerx J (2010) AMP-activated protein kinase and its downstream transcriptional pathways. Cell Mol Life Sci 67: 3407-3423.
25. Miller RA, Chu Q, Xie J, Foretz M, Viollet B, et al. (2013) Biguanides suppress hepatic glucagon signalling by decreasing production of cyclic AMP. Nature 494: 256-260.
26. Foretz M, Hebrard S, Leclerc J, Zarrinpashneh E, Soty M, et al. (2010) Metformin inhibits hepatic gluconeogenesis in mice independently of the LKB1/AMPK pathway via a decrease in hepatic energy state. J Clin Invest 120: 2355-2369.
27. Jager S, Trojan H, Kopp T, Laszczyk MN, Scheffler A (2009) Pentacyclic triterpene distribution in various plants - rich sources for a new group of multi-potent plant extracts. Molecules 14: 2016-2031.
28. Saha PK, Reddy VT, Konopleva M, Andreeff M, Chan L (2010) The triterpenoid 2-cyano-3,12-dioxooleana-1,9-dien-28-oic-acid methyl ester has potent anti-diabetic effects in diet-induced diabetic mice and Lepr(db/db) mice. J Biol Chem 285: 40581-40592.
29. Nathan DM, Buse JB, Davidson MB, Ferrannini E, Holman RR, et al. (2009) Medical management of hyperglycemia in type 2 diabetes: a consensus algorithm for the initiation and adjustment of therapy: a consensus statement of the American Diabetes Association and the European Association for the Study of Diabetes. Diabetes Care 32: 193-203.
30. Hutton JC, O'Brien RM (2009) Glucose-6-phosphatase catalytic subunit gene family. J Biol Chem 284: 29241-29245.
31. Gross DN, van den Heuvel AP, Birnbaum MJ (2008) The role of FoxO in the regulation of metabolism. Oncogene 27: 2320-2336.
32. Zhao Y, Wang Y, Zhu WG (2011) Applications of post-translational modifications of FoxO family proteins in biological functions. J Mol Cell Biol 3: 276-282.
33. Zhang X, Gan L, Pan H, Guo S, He X, et al. (2002) Phosphorylation of serine 256 suppresses transactivation by FKHR (FOXO1) by multiple mechanisms. Direct and indirect effects on nuclear/cytoplasmic shuttling and DNA binding. J Biol Chem 277: 45276-45284.
34. Matsuzaki H, Daitoku H, Hatta M, Aoyama H, Yoshimochi K, et al. (2005) Acetylation of Foxo1 alters its DNA-binding ability and sensitivity to phosphorylation. Proc Natl Acad Sci U S A 102: 11278-11283.
35. Qiang L, Banks AS, Accili D (2010) Uncoupling of acetylation from phosphorylation regulates FoxO1 function independent of its subcellular localization. J Biol Chem 285: 27396-27401.
36. Huang H, Regan KM, Wang F, Wang D, Smith DI, et al. (2005) Skp2 inhibits FOXO1 in tumor suppression through ubiquitin-mediated degradation. Proc Natl Acad Sci U S A 102: 1649-1654.
37. Clayton AL, Hazzalin CA, Mahadevan LC (2006) Enhanced histone acetylation and transcription: a dynamic perspective. Mol Cell 23: 289-296.
38. Calnan DR, Brunet A (2008) The FoxO code. Oncogene 27: 2276-2288.
39. Grozinger CM, Schreiber SL (2000) Regulation of histone deacetylase 4 and 5 and transcriptional activity by 14-3-3-dependent cellular localization. Proc Natl Acad Sci U S A 97: 7835-7840.
40. Wang AH, Kruhlak MJ, Wu J, Bertos NR, Vezmar M, et al. (2000) Regulation of histone deacetylase 4 by binding of 14-3-3 proteins. Mol Cell Biol 20: 6904-6912.
41. Senf SM, Sandesara PB, Reed SA, Judge AR (2011) p300 Acetyltransferase activity differentially regulates the localization and activity of the FOXO homologues in skeletal muscle. Am J Physiol Cell Physiol 300: C1490-1501.
42. Takigawa-Imamura H, Sekine T, Murata M, Takayama K, Nakazawa K, et al. (2003) Stimulation of glucose uptake in muscle cells by prolonged treatment with scriptide, a histone deacetylase inhibitor. Biosci Biotechnol Biochem 67: 1499-1506.
43. McGee SL, Hargreaves M (2010) Histone modifications and skeletal muscle metabolic gene expression. Clin Exp Pharmacol Physiol 37: 392-396.
44. Kaiser C, James SR (2004) Acetylation of insulin receptor substrate-1 is permissive for tyrosine phosphorylation. BMC Biol 2: 23.
45. Wang B, Moya N, Niessen S, Hoover H, Mihaylova MM, et al. (2011) A hormone-dependent module regulating energy balance. Cell 145: 596-606.
46. Matsumoto M, Han S, Kitamura T, Accili D (2006) Dual role of transcription factor FoxO1 in controlling hepatic insulin sensitivity and lipid metabolism. J Clin Invest 116: 2464-2472.
47. Zhang L, Qin X, Zhao Y, Fast L, Zhuang S, et al. (2012) Inhibition of histone deacetylases preserves myocardial performance and prevents cardiac remodeling through stimulation of endogenous angiomyogenesis. J Pharmacol Exp Ther 341: 285-293.
48. Juengel E, Makarevic J, Tsaur I, Bartsch G, Nelson K, et al. (2013) Resistance after chronic application of the HDAC-inhibitor valproic acid is associated with elevated Akt activation in renal cell carcinoma in vivo. PLoS One 8: e53100.