TRPV1-mediated UCP2 upregulation ameliorates hyperglycemia-induced endothelial dysfunction

Cardiovascular Diabetology

Volumn 12, Issue 1, 2013, Pages

  Sun, Jing ^a   Pu, Yunfei ^a   Wang, Peijian ^a   Chen, Sijiao ^b   Zhao, Yu ^a   Liu, Chan ^c   Shang, Qianhui ^c   Zhu, Zhiming ^a   Liu, Daoyan ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b CHINA MEDICAL UNIVERSITY   (China)

^c ZUNYI MEDICAL UNIVERSITY   (China)

Author keywords

Capsaicin; Diabetes; Endothelium; Oxidative stress; TRPV1; UCP2

Indexed keywords

CAPSAICIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; HYDROETHIDINE; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; UNCOUPLING PROTEIN 2; VANILLOID RECEPTOR 1; GLUCOSE; ION CHANNEL; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL UNCOUPLING PROTEIN 2; TRPV1 PROTEIN, MOUSE; VANILLOID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; FLUORESCENCE; HYPERGLYCEMIA; IMMUNOHISTOLOGY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UPREGULATION; VASODILATATION; ANIMAL; ARTERY; CELL CULTURE; DIABETIC ANGIOPATHY; DRUG EFFECTS; GENETICS; IN VITRO STUDY; KNOCKOUT MOUSE; METABOLISM; PHOSPHORYLATION; VASCULAR ENDOTHELIUM;

ANIMALS; ARTERIES; CAPSAICIN; CELLS, CULTURED; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DIABETIC ANGIOPATHIES; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GLUCOSE; IN VITRO TECHNIQUES; ION CHANNELS; MICE; MICE, KNOCKOUT; MITOCHONDRIAL PROTEINS; NITRIC OXIDE; OXIDATIVE STRESS; PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; TRPV CATION CHANNELS; UP-REGULATION; VASODILATION;

EID: 84876726039     PISSN: None     EISSN: 14752840     Source Type: Journal    
DOI: 10.1186/1475-2840-12-69     Document Type: Article

References (45)

1. Zou MH, Shi C, Cohen RA. High glucose via peroxynitrite causes tyrosine nitration and inactivation of prostacyclin synthase that is associated with thromboxane/prostaglandin H(2) receptor-mediated apoptosis and adhesion molecule expression in cultured human aortic endothelial cells. Diabetes 2002, 51(1):198-203.
2. Jay D, Hitomi H, Griendling KK. Oxidative stress and diabetic cardiovascular complications. Free Radic Biol Med 2006, 40(2):183-192. 10.1016/j.freeradbiomed.2005.06.018, 16413400.
3. Victor VM, Rocha M, Herance R, Hernandez-Mijares A. Oxidative stress and mitochondrial dysfunction in type 2 diabetes. Current pharmaceutical design 2011, 17(36):3947-3958. 10.2174/138161211798764915, 22188447.
4. Kaneto H, Katakami N, Matsuhisa M, Matsuoka TA. Role of reactive oxygen species in the progression of type 2 diabetes and atherosclerosis. Mediators Inflamm 2010, 2010:1-11.
5. Roe ND, Thomas DP, Ren J. Inhibition of NADPH oxidase alleviates experimental diabetes-induced myocardial contractile dysfunction. Diabetes, obesity & metabolism 2011, 13(5):465-473. 10.1111/j.1463-1326.2011.01369.x, 23638485.
6. Dong YF, Liu L, Kataoka K, Nakamura T, Fukuda M, Tokutomi Y, Nako H, Ogawa H, Kim-Mitsuyama S. Aliskiren prevents cardiovascular complications and pancreatic injury in a mouse model of obesity and type 2 diabetes. Diabetologia 2010, 53(1):180-191. 10.1007/s00125-009-1575-5, 19894030.
7. Chu KY, Leung PS. Angiotensin II Type 1 receptor antagonism mediates uncoupling protein 2-driven oxidative stress and ameliorates pancreatic islet beta-cell function in young Type 2 diabetic mice. Antioxid Redox Signal 2007, 9(7):869-878. 10.1089/ars.2007.1590, 17508912.
8. Marwick TH, Hordern MD, Miller T, Chyun DA, Bertoni AG, Blumenthal RS, Philippides G, Rocchini A. Exercise training for type 2 diabetes mellitus: impact on cardiovascular risk: a scientific statement from the American Heart Association. Circulation 2009, 119(25):3244-3262. 10.1161/CIRCULATIONAHA.109.192521, 19506108.
9. Berardi MJ, Shih WM, Harrison SC, Chou JJ. Mitochondrial uncoupling protein 2 structure determined by NMR molecular fragment searching. Nature 2011, 476(7358):109-113. 10.1038/nature10257, 3150631, 21785437.
10. Moukdar F, Robidoux J, Lyght O, Pi J, Daniel KW, Collins S. Reduced antioxidant capacity and diet-induced atherosclerosis in uncoupling protein-2-deficient mice. Journal of lipid research 2009, 50(1):59-70.
11. Tian XY, Wong WT, Xu A, Lu Y, Zhang Y, Wang L, Cheang WS, Wang Y, Yao X, Huang Y. Uncoupling protein-2 protects endothelial function in diet-induced obese mice. Circ Res 2012, 110(9):1211-1216. 10.1161/CIRCRESAHA.111.262170, 22461387.
12. Ma S, Ma L, Yang D, Luo Z, Hao X, Liu D, Zhu Z. Uncoupling protein 2 ablation exacerbates high-salt intake-induced vascular dysfunction. Am J Hypertens 2010, 23(8):822-828. 10.1038/ajh.2010.73, 20395942.
13. Li L, Chen J, Ni Y, Feng X, Zhao Z, Wang P, Sun J, Yu H, Yan Z, Liu D. TRPV1 activation prevents nonalcoholic fatty liver through UCP2 upregulation in mice. Pflugers Archiv : European journal of physiology 2012, 463(5):727-732. 10.1007/s00424-012-1078-y, 22395410.
14. Lee MS, Kim CT, Kim IH, Kim Y. Effects of capsaicin on lipid catabolism in 3T3-L1 adipocytes. Phytotherapy research : PTR 2011, 25(6):935-939. 10.1002/ptr.3339, 21626599.
15. Tu N, Chen H, Winnikes U, Reinert I, Marmann G, Pirke KM, Lentes KU. Molecular cloning and functional characterization of the promoter region of the human uncoupling protein-2 gene. Biochemical and biophysical research communications 1999, 265(2):326-334. 10.1006/bbrc.1999.1663, 10558866.
16. Ouedraogo R, Wu X, Xu SQ, Fuchsel L, Motoshima H, Mahadev K, Hough K, Scalia R, Goldstein BJ. Adiponectin suppression of high-glucose-induced reactive oxygen species in vascular endothelial cells: evidence for involvement of a cAMP signaling pathway. Diabetes 2006, 55(6):1840-1846. 10.2337/db05-1174, 16731851.
17. Nilius B. TRP channels in disease. Biochimica et Biophysica Acta (BBA)-Molecular Basis of Disease 2007, 1772(8):805-812.
18. Ma L, Zhong J, Zhao Z, Luo Z, Ma S, Sun J, He H, Zhu T, Liu D, Zhu Z. Activation of TRPV1 reduces vascular lipid accumulation and attenuates atherosclerosis. Cardiovascular research 2011, 92(3):504-513. 10.1093/cvr/cvr245, 21908651.
19. Wang P, Yan Z, Zhong J, Chen J, Ni Y, Li L, Ma L, Zhao Z, Liu D, Zhu Z. Transient receptor potential vanilloid 1 activation enhances gut glucagon-like peptide-1 secretion and improves glucose homeostasis. Diabetes 2012, 61(8):2155-2165. 10.2337/db11-1503, 22664955.
20. Yang D, Luo Z, Ma S, Wong WT, Ma L, Zhong J, He H, Zhao Z, Cao T, Yan Z. Activation of TRPV1 by dietary capsaicin improves endothelium-dependent vasorelaxation and prevents hypertension. Cell Metab 2010, 12(2):130-141. 10.1016/j.cmet.2010.05.015, 20674858.
21. Zhang LL, Liu DY, Ma LQ, Luo ZD, Cao TB, Zhong J, Yan ZC, Wang LJ, Zhao ZG, Zhu SJ. Activation of transient receptor potential vanilloid type-1 channel prevents adipogenesis and obesity. Circulation research 2007, 100(7):1063-1070. 10.1161/01.RES.0000262653.84850.8b, 17347480.
22. Xu X, Wang P, Zhao Z, Cao T, He H, Luo Z, Zhong J, Gao F, Zhu Z, Li L. Activation of transient receptor potential vanilloid 1 by dietary capsaicin delays the onset of stroke in stroke-prone spontaneously hypertensive rats. Stroke; a journal of cerebral circulation 2011, 42(11):3245-3251. 10.1161/STROKEAHA.111.618306, 23638491.
23. Liu L, Liu J, Wong WT, Tian XY, Lau CW, Wang YX, Xu G, Pu Y, Zhu Z, Xu A. Dipeptidyl peptidase 4 inhibitor sitagliptin protects endothelial function in hypertension through a glucagon-like peptide 1-dependent mechanism. Hypertension 2012, 60(3):833-841. 10.1161/HYPERTENSIONAHA.112.195115, 22868389.
24. Zhao Z, Luo Z, Wang P, Sun J, Yu H, Cao T, Ni Y, Chen J, Yan Z, Liu D. Rosiglitazone restores endothelial dysfunction in a rat model of metabolic syndrome through PPARgamma- and PPARdelta-dependent phosphorylation of Akt and eNOS. PPAR research 2011, 2011:291656. 3236323, 22190906.
25. Hao X, Chen J, Luo Z, He H, Yu H, Ma L, Ma S, Zhu T, Liu D, Zhu Z. TRPV1 activation prevents high-salt diet-induced nocturnal hypertension in mice. Pflugers Archiv : European journal of physiology 2011, 461(3):345-353. 10.1007/s00424-011-0921-x, 21246380.
26. Inoguchi T, Sonta T, Tsubouchi H, Etoh T, Kakimoto M, Sonoda N, Sato N, Sekiguchi N, Kobayashi K, Sumimoto H. Protein kinase C-dependent increase in reactive oxygen species (ROS) production in vascular tissues of diabetes: role of vascular NAD(P)H oxidase. J Am Soc Nephrol 2003, 14:S227-S232. 10.1097/01.ASN.0000077407.90309.65, 12874436.
27. Akiba Y, Kato S, Katsube K, Nakamura M, Takeuchi K, Ishii H, Hibi T. Transient receptor potential vanilloid subfamily 1 expressed in pancreatic islet beta cells modulates insulin secretion in rats. Biochemical and biophysical research communications 2004, 321(1):219-225. 10.1016/j.bbrc.2004.06.149, 15358238.
28. Van Buren JJ, Bhat S, Rotello R, Pauza ME, Premkumar LS. Sensitization and translocation of TRPV1 by insulin and IGF-I. Mol Pain 2005, 1(1):17. 10.1186/1744-8069-1-17, 1142339, 15857517.
29. J-a K, Montagnani M, Koh KK, Quon MJ. Reciprocal relationships between insulin resistance and endothelial dysfunction molecular and pathophysiological mechanisms. Circulation 2006, 113(15):1888-1904. 10.1161/CIRCULATIONAHA.105.563213, 16618833.
30. Muniyappa R, Montagnani M, Koh KK, Quon MJ. Cardiovascular actions of insulin. Endocrine Reviews 2007, 28(5):463-491. 10.1210/er.2007-0006, 17525361.
31. Vicent D, Ilany J, Kondo T, Naruse K, Fisher SJ, Kisanuki YY, Bursell S, Yanagisawa M, King GL, Kahn CR. The role of endothelial insulin signaling in the regulation of vascular tone and insulin resistance. Journal of Clinical Investigation 2003, 111(9):1373-1380. 154437, 12727929.
32. Oktavianthi S, Trimarsanto H, Febinia CA, Suastika K, Saraswati MR, Dwipayana P, Arindrarto W, Sudoyo H, Malik SG. Uncoupling protein 2 gene polymorphisms are associated with obesity. Cardiovasc Diabetol 2012, 11:41. 10.1186/1475-2840-11-41, 3412711, 22533685.
33. Snitker S, Fujishima Y, Shen H, Ott S, Pi-Sunyer X, Furuhata Y, Sato H, Takahashi M. Effects of novel capsinoid treatment on fatness and energy metabolism in humans: possible pharmacogenetic implications. The American journal of clinical nutrition 2009, 89(1):45-50. 3151435, 19056576.
34. Guarini G, Ohanyan VA, Kmetz JG, DelloStritto DJ, Thoppil RJ, Thodeti CK, Meszaros JG, Damron DS, Bratz IN. Disruption of TRPV1-mediated coupling of coronary blood flow to cardiac metabolism in diabetic mice: role of nitric oxide and BK channels. Am J Physiol Heart Circ Physiol 2012, 303(2):H216-H223. 10.1152/ajpheart.00011.2012, 22610171.
35. Ohanyan VA, Guarini G, Thodeti CK, Talasila PK, Raman P, Haney RM, Meszaros JG, Damron DS, Bratz IN. Endothelin-mediated in vivo pressor responses following TRPV1 activation. Am J Physiol Heart Circ Physiol 2011, 301(3):H1135-H1142. 10.1152/ajpheart.00082.2011, 21705674.
36. Song JX, Wang LH, Yao L, Xu C, Wei ZH, Zheng LR. Impaired transient receptor potential vanilloid 1 in streptozotocin-induced diabetic hearts. Int J Cardiol 2009, 134(2):290-292. 10.1016/j.ijcard.2007.12.081, 18378339.
37. Lei H, Venkatakrishnan A, Yu S, Kazlauskas A. Protein kinase A-dependent translocation of Hsp90α impairs endothelial nitric-oxide synthase activity in high glucose and diabetes. Journal of Biological Chemistry 2007, 282(13):9364-9371. 10.1074/jbc.M608985200, 17202141.
38. Kassis N, Bernard C, Pusterla A, Casteilla L, Pétnicaud L, Richard D, Ricquier D, Ktorza A. Correlation between pancreatic islet uncoupling protein-2 (UCP2) mRNA concentration and insulin status in rats. Experimental Diabetes Research 2000, 1(3):185-193. 10.1155/EDR.2000.185, 2477730, 11467409.
39. Rolo AP, Palmeira CM. Diabetes and mitochondrial function: role of hyperglycemia and oxidative stress. Toxicology and applied pharmacology 2006, 212(2):167-178. 10.1016/j.taap.2006.01.003, 16490224.
40. Dhamrait SS, Stephens JW, Cooper JA, Acharya J, Mani AR, Moore K, Miller GJ, Humphries SE, Hurel SJ, Montgomery HE. Cardiovascular risk in healthy men and markers of oxidative stress in diabetic men are associated with common variation in the gene for uncoupling protein 2. European heart journal 2004, 25(6):468-475. 10.1016/j.ehj.2004.01.007, 15039126.
41. Chan SH, Wu CA, Wu KL, Ho YH, Chang AY, Chan JY. Transcriptional upregulation of mitochondrial uncoupling protein 2 protects against oxidative stress-associated neurogenic hypertension. Circ Res 2009, 105(9):886-896. 10.1161/CIRCRESAHA.109.199018, 19762685.
42. Oniki H, Goto K, Fujii K, Kansui Y, Murakami N, Ohtsubo T, Matsumura K, Kitazono T. Effects of the Superoxide Dismutase Mimetic Tempol on Impaired Endothelium-Dependent and Endothelium-Independent Relaxations in Type II Diabetic Rats. Clin Exp Hypertens 2012, 35(2):112-119.
43. Simonsen U, Christensen FH, Buus NH. The effect of tempol on endothelium-dependent vasodilatation and blood pressure. Pharmacology & therapeutics 2009, 122(2):109-124. 10.1016/j.pharmthera.2009.02.002, 23638295.
44. Inoguchi T, Li P, Umeda F, Yu HY, Kakimoto M, Imamura M, Aoki T, Etoh T, Hashimoto T, Naruse M. High glucose level and free fatty acid stimulate reactive oxygen species production through protein kinase C-dependent activation of NAD(P)H oxidase in cultured vascular cells. Diabetes 2000, 49(11):1939-1945. 10.2337/diabetes.49.11.1939, 11078463.
45. Wang Y, Nishi M, Doi A, Shono T, Furukawa Y, Shimada T, Furuta H, Sasaki H, Nanjo K. Ghrelin inhibits insulin secretion through the AMPK-UCP2 pathway in beta cells. FEBS Lett 2010, 584(8):1503-1508. 10.1016/j.febslet.2010.02.069, 20206170.