Tetrahydrobiopterin has a glucose-lowering effect by suppressing hepatic gluconeogenesis in an endothelial nitric oxide synthase dependent manner in diabetic mice

Diabetes

Volumn 62, Issue 9, 2013, Pages 3033-3043

  Abudukadier, Abulizi ^a   Fujita, Yoshihito ^a   Obara, Akio ^a   Ohashi, Akiko ^b   Fukushima, Toru ^a   Sato, Yuichi ^a   Ogura, Masahito ^a   Nakamura, Yasuhiko ^a   Fujimoto, Shimpei ^a   Hosokawa, Masaya ^a   Hasegawa, Hiroyuki ^b   Inagaki, Nobuya ^a  

^a KYOTO UNIVERSITY   (Japan)

^b NIHON UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE NUCLEOTIDE; ADENYLATE KINASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOSE; GLUCOSE 6 PHOSPHATASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ALPHA; INSULIN; MESSENGER RNA; N(G) NITROARGININE METHYL ESTER; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PIG INSULIN; PYRUVIC ACID; SEPIAPTERIN; SMALL INTERFERING RNA; STREPTOZOCIN; TETRAHYDROBIOPTERIN; UNCLASSIFIED DRUG; 5,6,7,8-TETRAHYDROBIOPTERIN; ANTIDIABETIC AGENT; BIOPTERIN; DRUG DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIDIABETIC ACTIVITY; ARTICLE; DIET RESTRICTION; DIMERIZATION; DRUG UPTAKE; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; GENETIC TRANSFECTION; GLUCONEOGENESIS; GLUCOSE BLOOD LEVEL; GLUCOSE INTOLERANCE; GLUCOSE METABOLISM; GLUCOSE OXIDATION; GLUCOSE TOLERANCE TEST; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; LIVER CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGLE DRUG DOSE; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; ANIMAL; C57BL MOUSE; CELL CULTURE; DRUG EFFECT; ENZYMOLOGY; EXPERIMENTAL DIABETES MELLITUS; GENETICS; IMMUNOHISTOCHEMISTRY; LIVER; METABOLISM;

ANIMALS; BIOPTERIN; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; ENDOTHELIAL CELLS; GLUCONEOGENESIS; HEPATOCYTES; HYPOGLYCEMIC AGENTS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; LIVER; MALE; MICE; MICE, INBRED C57BL; NITRIC OXIDE SYNTHASE TYPE III; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING;

EID: 84887392410     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db12-1242     Document Type: Article

References (47)

1. Triggle CR, Ding H. A review of endothelial dysfunction in diabetes: a focus on the contribution of a dysfunctional eNOS. J Am Soc Hypertens 2010;4:102-115
2. Huang PL. eNOS, metabolic syndrome and cardiovascular disease. Trends Endocrinol Metab 2009;20:295-302
3. Kim JA, Montagnani M, Koh KK, Quon MJ. Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms. Circulation 2006;113:1888-1904
4. Duplain H, Burcelin R, Sartori C, et al. Insulin resistance, hyperlipidemia, and hypertension in mice lacking endothelial nitric oxide synthase. Circulation 2001;104:342-345
5. Shankar RR, Wu Y, Shen HQ, et al. Mice with gene disruption of both endothelial and neuronal nitric oxide synthase exhibit insulin resistance. Diabetes 2000;49:684-687
6. Stuehr D, Pou S, Rosen GM. Oxygen reduction by nitric-oxide synthases. J Biol Chem 2001;276:14533-14536
7. Vásquez-Vivar J, Kalyanaraman B, Martásek P, et al. Superoxide generation by endothelial nitric oxide synthase: the influence of cofactors. Proc Natl Acad Sci USA 1998;95:9220-9225
8. Crabtree MJ, Channon KM. Synthesis and recycling of tetrahydrobiopterin in endothelial function and vascular disease. Nitric Oxide 2011;25:81-88
9. Landmesser U, Dikalov S, Price SR, et al. Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J Clin Invest 2003;111:1201-1209
10. Meininger CJ, Marinos RS, Hatakeyama K, et al. Impaired nitric oxide production in coronary endothelial cells of the spontaneously diabetic BB rat is due to tetrahydrobiopterin deficiency. Biochem J 2000;349:353-356
11. Xu J, Wu Y, Song P, et al. Proteasome-dependent degradation of guanosine 59-triphosphate cyclohydrolase I causes tetrahydrobiopterin deficiency in diabetes mellitus. Circulation 2007;116:944-953
12. Meininger CJ, Cai S, Parker JL, et al. GTP cyclohydrolase I gene transfer reverses tetrahydrobiopterin deficiency and increases nitric oxide synthesis in endothelial cells and isolated vessels from diabetic rats. FASEB J 2004;18:1900-1902
13. Ding QF, Hayashi T, Packiasamy AR, et al. The effect of high glucose on NO and O2-through endothelial GTPCH1 and NADPH oxidase. Life Sci 2004;75:3185-3194
14. Kietadisorn R, Juni RP, Moens AL. Tackling endothelial dysfunction by modulating NOS uncoupling: new insights into its pathogenesis and therapeutic possibilities. Am J Physiol Endocrinol Metab 2012;302:E481-E495
15. Katusic ZS, d'Uscio LV, Nath KA. Vascular protection by tetrahy-drobiopterin: progress and therapeutic prospects. Trends Pharmacol Sci 2009;30:48-54
16. Wajngot A, Chandramouli V, Schumann WC, et al. Quantitative contributions of gluconeogenesis to glucose production during fasting in type 2 diabetes mellitus. Metabolism 2001;50:47-52
17. Lin HV, Accili D. Hormonal regulation of hepatic glucose production in health and disease. Cell Metab 2011;14:9-19
18. Oyadomari S, Koizumi A, Takeda K, et al. Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J Clin Invest 2002;109:525-532
19. Fujita Y, Hosokawa M, Fujimoto S, et al. Metformin suppresses hepatic gluconeogenesis and lowers fasting blood glucose levels through reactive nitrogen species in mice. Diabetologia 2010;53:1472-1481
20. Fujimoto S, Mukai E, Hamamoto Y, et al. Prior exposure to high glucose augments depolarization-induced insulin release by mitigating the decline of ATP level in rat islets. Endocrinology 2002;143:213-221
21. Ogura M, Nakamura Y, Tanaka D, et al. Overexpression of SIRT5 confirms its involvement in deacetylation and activation of carbamoyl phosphate synthetase 1. Biochem Biophys Res Commun 2010;393:73-78
22. Sawabe K, Wakasugi KO, Hasegawa H. Tetrahydrobiopterin uptake in supplemental administration: elevation of tissue tetrahydrobiopterin in mice following uptake of the exogenously oxidized product 7, 8-dihydrobiopterin and subsequent reduction by an anti-folate-sensitive process. J Pharmacol Sci 2004;96:124-133
23. Sawabe K, Suetake Y, Nakanishi N, et al. Cellular accumulation of tetra-hydrobiopterin following its administration is mediated by two different processes; direct uptake and indirect uptake mediated by a methotrexate- sensitive process. Mol Genet Metab 2005;86(Suppl. 1):S133-S138
24. 14C]tetrahydrobiopterin and its developmental change in mice. J Pharmacol Exp Ther 1993;267:971-978
25. Matei V, Rodríguez-Vilarrupla A, Deulofeu R, et al. Three-day tetrahy-drobiopterin therapy increases in vivo hepatic NOS activity and reduces portal pressure in CCl4 cirrhotic rats. J Hepatol 2008;49:192-197
26. Elrod JW, Duranski MR, Langston W, et al. eNOS gene therapy exacerbates hepatic ischemia-reperfusion injury in diabetes: a role for eNOS uncoupling. Circ Res 2006;99:78-85
27. Shah V, Cao S, Hendrickson H, et al. Regulation of hepatic eNOS by caveolin and calmodulin after bile duct ligation in rats. Am J Physiol Gastrointest Liver Physiol 2001;280:G1209-G1216
28. Wei CL, Khoo HE, Lee KH, et al. Differential expression and localization of nitric oxide synthases in cirrhotic livers of bile duct-ligated rats. Nitric Oxide 2002;7:91-102
29. McNaughton L, Puttagunta L, Martinez-Cuesta MA, et al. Distribution of nitric oxide synthase in normal and cirrhotic human liver. Proc Natl Acad Sci USA 2002;99:17161-17166
30. Mei Y, Thevananther S. Endothelial nitric oxide synthase is a key mediator of hepatocyte proliferation in response to partial hepatectomy in mice. Hepatology 2011;54:1777-1789
31. Zhang BB, Zhou G, Li C. AMPK: an emerging drug target for diabetes and the metabolic syndrome. Cell Metab 2009;9:407-416
32. Hardie DG. The AMP-activated protein kinase pathway-new players upstream and downstream. J Cell Sci 2004;117:5479-5487
33. Carabaza A, Ricart MD, Mor A, et al. Role of AMP on the activation of glycogen synthase and phosphorylase by adenosine, fructose, and gluta-mine in rat hepatocytes. J Biol Chem 1990;265:2724-2732
34. Ouyang J, Parakhia RA, Ochs RS. Metformin activates AMP kinase through inhibition of AMP deaminase. J Biol Chem 2011;286:1-11
35. Fogarty S, Hardie DG. Development of protein kinase activators: AMPK as a target in metabolic disorders and cancer. Biochim Biophys Acta 2010; 1804:581-589
36. Kojima S, Ona S, Iizuka I, et al. Antioxidative activity of 5, 6, 7, 8-tetrahydrobiopterin and its inhibitory effect on paraquat-induced cell toxicity in cultured rat hepatocytes. Free Radic Res 1995;23:419-430
37. Delgado-Esteban M, Almeida A, Medina JM. Tetrahydrobiopterin deficiency increases neuronal vulnerability to hypoxia. J Neurochem 2002;82:1148-1159
38. Kang KT, Sullivan JC, Spradley FT, et al. Antihypertensive therapy increases tetrahydrobiopterin levels and NO/cGMP signaling in small arteries of angiotensin II-infused hypertensive rats. Am J Physiol Heart Circ Physiol 2011;300:H718-H724
39. Higaki Y, Hirshman MF, Fujii N, et al. Nitric oxide increases glucose uptake through a mechanism that is distinct from the insulin and contraction pathways in rat skeletal muscle. Diabetes 2001;50:241-247
40. Zhang J, Xie Z, Dong Y, et al. Identification of nitric oxide as an endogenous activator of the AMP-activated protein kinase in vascular endothelial cells. J Biol Chem 2008;283:27452-27461
41. Viollet B, Guigas B, Leclerc J, et al. AMP-activated protein kinase in the regulation of hepatic energy metabolism: from physiology to therapeutic perspectives. Acta Physiol (Oxf) 2009;196:81-98
42. Cook S, Scherrer U. Insulin resistance, a new target for nitric oxide-delivery drugs. Fundam Clin Pharmacol 2002;16:441-453
43. Shaw RJ, Lamia KA, Vasquez D, et al. The kinase LKB1 mediates glucose homeostasis in liver and therapeutic effects of metformin. Science 2005; 310:1642-1646
44. Inzucchi SE, Maggs DG, Spollett GR, et al. Efficacy and metabolic effects of metformin and troglitazone in type II diabetes mellitus. N Engl J Med 1998;338:867-872
45. Blau N. Defining tetrahydrobiopterin (BH4)-responsiveness in PKU. J Inherit Metab Dis 2008;31:2-3
46. Moens AL, Kietadisorn R, Lin JY, et al. Targeting endothelial and myocardial dysfunction with tetrahydrobiopterin. J Mol Cell Cardiol 2011;51:559-563
47. Heitzer T, Krohn K, Albers S, et al. Tetrahydrobiopterin improves endothelium-dependent vasodilation by increasing nitric oxide activity in patients with Type II diabetes mellitus. Diabetologia 2000;43:1435-1438