SRT1720 counteracts glucosamine-induced endoplasmic reticulum stress and endothelial dysfunction

Cardiovascular Research

Volumn 107, Issue 2, 2015, Pages 295-306

  Fiorentino, Teresa Vanessa ^a   Procopio, Teresa ^a   Mancuso, Elettra ^a   Arcidiacono, Gaetano Paride ^a   Andreozzi, Francesco ^a   Arturi, Franco ^a   Sciacqua, Angela ^a   Perticone, Francesco ^a   Hribal, Marta Letizia ^a   Sesti, Giorgio ^a  

^a UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

Author keywords

Endoplasmic reticulum stress; Endothelial dysfunction; Hexosamine pathway; mTOR signalling; SRT1720

Indexed keywords

BUTYRIC ACID; CELL PROTEIN; GLUCOSAMINE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; N [2 [3 (1 PIPERAZINYLMETHYL)IMIDAZO[2,1 B]THIAZOL 6 YL]PHENYL] 2 QUINOXALINECARBOXAMIDE; FUSED HETEROCYCLIC RINGS;

ACETYLATION; APOPTOSIS; ARTICLE; CAPILLARY ENDOTHELIAL CELL; CONTROLLED STUDY; CYTOKINE RELEASE; ENDOPLASMIC RETICULUM STRESS; ENDOTHELIAL DYSFUNCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; HYPERGLYCEMIA; LONG TERM EXPOSURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REAL TIME POLYMERASE CHAIN REACTION; UMBILICAL VEIN ENDOTHELIAL CELL; WESTERN BLOTTING; CELL CULTURE; DRUG EFFECTS; METABOLISM;

APOPTOSIS; CELLS, CULTURED; ENDOPLASMIC RETICULUM STRESS; GLUCOSAMINE; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYPERGLYCEMIA;

EID: 84938843413     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvv169     Document Type: Article

References (54)

1. Rask-Madsen C, King GL. Mechanisms of disease: endothelial dysfunction in insulin resistance and diabetes. Nat Clin Pract Endocrinol Metab 2007;3:46-56.
2. Selvin E, Marinopoulos S, Berkenblit G, Rami T, Brancati FL, Powe NR, Golden SH. Meta-analysis: glycosylated hemoglobin and cardiovascular disease in diabetes mellitus. Ann Intern Med 2004;141:421-431.
3. Nathan DM, Lachin J, Cleary P, Orchard T, Brillon DJ, Backlund JY, Genuth SM, Lachin JM, Orchard TJ, Raskin P, Zinman B; Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications (DCCT/EDIC) Study Research Group. Intensive diabetes therapy and carotid intima-media thickness in type 1 diabetes mellitus. N Engl J Med 2003;348:2294-2303.
4. Turner R. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). Lancet 1998;352:837-853.
5. Fiorentino TV, Prioletta A, Zuo P, Folli F. Hyperglycemia-induced oxidative stress and its role in diabetes mellitus related cardiovascular diseases. Curr Pharm Des 2013;19:5695-5703.
6. Rossetti L. Perspective: hexosamines and nutrient sensing. Endocrinology 2000;141:1922-1925.
7. Brownlee M. The pathobiology of diabetic complications. A unifying mechanism. Diabetes 2005;54:1615-1625.
8. Werstuck GH, Khan MI, Femia G, Kim AJ, Tedesco V, Trigatti B, Shi Y. Glucosamine-induced endoplasmic reticulum dysfunction is associated with accelerated atherosclerosis in a hyperglycemic mouse model. Diabetes 2006;55:93-101.
9. Laczy B, Hill BG, Wang K, Paterson AJ, White CR, Xing D, Chen YF, Darley-Usmar V, Oparil S, Chatham JC. Protein O-GlcNylation: a new signaling paradigm for the cardiovascular system. Am J Physiol Heart Circ Physiol 2009;296:H13-H28.
10. Marsh SA, Chatam JC. The paradoxical world of protein O-GlcNylation: a novel effector of cardiovascular (dys)function. Card Res 2011;89:487-488.
11. Federici M, Menghini R, Mauriello A, Hribal ML, Ferrelli F, Lauro D, Sbraccia P, Spagnoli LG, Sesti G, Lauro R. Insulin-dependent activation of endothelial nitric oxide synthase is impaired by O-linked glycosylation modification of signaling proteins in human coronary endothelial cells. Circulation 2002;106:466-472.
12. Wells L, Vosseller K, Hart GW. Glycosylation of nucleocytoplasmic proteins: signal transduction and O-GlcN. Science 2001;291:2376-2378.
13. Srinivasan V, Tatu U, Mohan V, Balasubramanyam M. Molecular convergence of hexosamine biosynthetic pathway and ER stress leading to insulin resistance in L6 skeletal muscle cells. Mol Cell Biochem 2009;328:217-224.
14. Evans-Molina C, Hatanaka M, Mirmira RG. Lost in translation: endoplasmic reticulum stress and the decline of β-cell health in diabetes mellitus. Diabetes Obes Metab 2013;15:159-169.
15. -/- mice. Atherosclerosis 2011;219:134-140.
16. Civelek M, Manduchi E, Riley RJ, Stoeckert CJ Jr, Davies PF. Chronic endoplasmic reticulum stress activates unfolded protein response in arterial endothelium in regions of susceptibility to atherosclerosis. Circ Res 2009;105:453-461.
17. Chistiakov DA, Sobenin IA, Orekhov AN, Bobryshev YV. Role of endoplasmic reticulum stress in atherosclerosis and diabetic macrovascular complications. Biomed Res Int 2014;2014:610140.
18. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007;8:519-529.
19. Hotamisligil GS. Endoplasmic reticulum stress and atherosclerosis. Nat Med 2010;16:396-399.
20. Xu C, Bailly-Maitre B, Reed JC. Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 2005;115:2656-2664.
21. Banks AS, Kon N, Knight C, Matsumoto M, Gutierrez-Juarez R, Rossetti L, Gutiérrez-Juárez R, Rossetti L, Gu W, Accili D. Sirt1 gain of function increases energy efficiency and prevents diabetes in mice. Cell Metab 2008;8:333-341.
22. Ghemrawi R, Pooya S, Lorentz S, Gauchotte G, Arnold C, Gueant JL, Battaglia-Hsu SF. Decreased vitamin B12 availability induces ER stress through impaired SIRT1-deacetylation of HSF1. Cell Death and Disease 2013;4:e553.
23. Jung TW, Lee KT, Lee MW, Ka KH. SIRT1 attenuates palmitate-induced endoplasmic reticulum stress and insulin resistance in HepG2 cells via induction of oxygen-regulated protein 150. Biochem Biophys Res Commun 2012;422:229-232.
24. Lee J, Hong SW, Park SE, Rhee EJ, Park CY, Oh KW, Park SW, Lee WY. Exendin-4 attenuates endoplasmic reticulum stress through a SIRT1-dependent mechanism. Cell Stress Chaperones 2014; doi:10.1007/s12192-013-0490-3.
25. Li Y, Xu S, Giles A, Nakamura K, Lee JW, Hou X, Donmez G, Li J, Luo Z, Walsh K, Guarente L, Zang M. Hepatic overexpression of SIRT1 in mice attenuates endoplasmic reticulum stress and insulin resistance in the liver. FASEB J 2011;25:1664-1679.
26. Milne JC, Lambert PD, Schenk S, Carney DP, Smith JJ, Gagne DJ, Jin L, Boss O, Perni RB, Vu CB, Bemis JE, Xie R, Disch JS, Ng PY, Nunes JJ, Lynch AV, Yang H, Galonek H, Israelian K, Choy W, Iffland A, Lavu S, Medvedik O, Sinclair DA, Olefsky JM, Jirousek MR, Elliott PJ, Westphal CH. Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes. Nature 2007;450:712-716.
27. Minor RK, Baur JA, Gomes AP, Ward TM, Csiszar A, Mercken EM, Abdelmohsen K, Shin YK, Canto C, Scheibye-Knudsen M, Krawczyk M, Irusta PM, Martín-Montalvo A, Hubbard BP, Zhang Y, Lehrmann E, White AA, Price NL, Swindell WR, Pearson KJ, Becker KG, Bohr VA, Gorospe M, Egan JM, Talan MI, Auwerx J, Westphal CH, Ellis JL, Ungvari Z, Vlasuk GP, Elliott PJ, Sinclair DA, de Cabo R. SRT1720 improves survival and healthspan of obese mice. Sci Rep 2011;1:70.
28. Mitchell SJ, Martin-Montalvo A, Mercken EM, Palacios HH, Ward TM, Abulwerdi G, Minor RK, Vlasuk GP, Ellis JL, Sinclair DA, Dawson J, Allison DB, Zhang Y, Becker KG, Bernier M, de Cabo R. The SIRT1 activator SRT1720 extends lifespan and improves health of mice fed a standard diet. Cell Rep 2014;6:836-843.
29. Khan MI, Pichna BA, Shi Y, Bowes AJ, Werstuck GH. Evidence supporting a role for endoplasmic reticulum stress in the development of atherosclerosis in a hyperglycaemic mouse model. Antioxid Redox Signal 2009;11:2289-2298.
30. Al-Mutairi M, Al-Harthi S, Cadalbert L, Plevin R. Over-expression of mitogen-activated protein kinase phosphatase-2 enhances adhesion molecule expression and protects against apoptosis in human endothelial cells. Br J Pharmacol 2010;161:782-798.
31. D'Alessandris C, Andreozzi F, Federici M, Cardellini M, Brunetti A, Ranalli M, Del Guerra S, Lauro D, Del Prato S, Marchetti P, Lauro R, Sesti G. Increased O-glycosylation of insulin signaling proteins results in their impaired activation and enhanced susceptibility to apoptosis in pancreatic beta-cells. FASEB J 2004;18:959-961.
32. Andreozzi F, Laratta E, Procopio C, Hribal ML, Sciacqua A, Perticone M, Miele C, Perticone F, Sesti G. Interleukin-6 impairs the insulin signaling pathway, promoting production of nitric oxide in human umbilical vein endothelial cells. Mol Cell Biol 2007;27:2372-2383.
33. Itkonen HM, Mills IG. N-linked glycosylation supports cross-talk between receptor tyrosine kinases and androgen receptor. PLoS ONE 2013;8:e65016.
34. Srinivasan S, Ohsugi M, Liu Z, Fatrai S, Bernal-Mizrachi E, Permutt MA. Endoplasmic reticulum stress-induced apoptosis is partly mediated by reduced insulin signaling through phosphatidylinositol 3-kinase/Akt and increased glycogen synthase kinase-3 beta in mouse insulinoma cells. Diabetes 2005;54:968-975.
35. Hotamisligil GS, Peraldi P, Budavari A, Ellis R, White MF, Spiegelman BM. IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance. Science 1996;271:665-668.
36. Hasegawa Y, Saito T, Ogihara T, Ishigaki Y, Yamada T, Imai J, Uno K, Gao J, Kaneko K, Shimosawa T, Asano T, Fujita T, Oka Y, Katagiri H. Blockade of the nuclear factor-κB pathway in the endothelium prevents insulin resistance and prolongs life spans. Circulation 2012;125:1122-1133.
37. Minamino T, Komuro I, Kitakaze M. Endoplasmic reticulum stress as a therapeutic target in cardiovascular disease. Circ Res 2010;107:1071-1082.
38. Erbay E, Babaev VR, Mayers JR, Makowski L, Charles KN, Snitow ME, Fazio S, Wiest MM, Watkins SM, Linton MF, Hotamisligil GS. Reducing endoplasmic reticulum stress through a macrophage lipid chaperone alleviates atherosclerosis. Nat Med 2009;15:1383-1391.
39. Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, Smith RO, Görgün CZ, Hotamisligil GS. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 2006;313:1137-1140.
40. Gao Y, Wells L, Comer FI, Parker GJ, Hart GW. Dynamic O-glycosylation of nuclear and cytosolic proteins: cloning and characterization of a neutral, cytosolic beta-N-acetylglucosaminidase from human brain. J Biol Chem 2001;276:9838-9845.
41. Bachar E, Ariav Y, Ketzinel-Gilad M, Cerasi E, Kaiser N, Leibowitz G. Glucose amplifies fatty acid-induced endoplasmic reticulum stress in pancreatic beta-cells via activation of mTORC1. PLoS ONE 2009;4:e4954.
42. Ghosh HS, McBurney M, Robbins PD. SIRT1 negatively regulates the mammalian target of rapamycin. PLoS ONE 2010;5:e9199.
43. Corradetti MN, Guan KL. Upstream of the mammalian target of rapamycin: do all roads pass through mTOR? Oncogene 2006;25:6347-6360.
44. Pacholec M, Bleasdale JE, Chrunyk B, Cunningham D, Flynn D, Garofalo RS, Griffith D, Griffor M, Loulakis P, Pabst B, Qiu X, Stockman B, Thanabal V, Varghese A, Ward J, Withka J, Ahn K. .SRT1720, SRT2183, SRT1460, and resveratrol are not direct activators of SIRT1. J Biol Chem 2010;285:8340-8351.
45. Huber JL, McBurney MW, Distefano PS, McDonagh T. SIRT1-independent mechanisms of the putative sirtuin enzyme activators SRT1720 and SRT2183. Future Med Chem 2010;2:1751-1759.
46. Werstuck GH, Lentz SR, Dayal S, Hossain GS, Sood SK, Shi YY, Zhou J, Maeda N, Krisans SK, Malinow MR, Austin RC. Homocysteine-induced endoplasmic reticulum stress causes dysregulation of the cholesterol and triglyceride biosynthetic pathways. J Clin Invest 2001;107:1263-1273.
47. Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E, Tuncman G, Görgün C, Glimcher LH, Hotamisligil GS. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 2004;306:457-461.
48. Pober JS, Sessa WC. Evolving functions of endothelial cells in inflammation. Nat Rev Immunol 2007;7:803-815.
49. Rajapakse AG, Ming XF, Carvas JM, Yang Z. O-linked beta-N-acetylglucosamine during hyperglycemia exerts both anti-inflammatory and pro-oxidative properties in the endothelial system. Oxid Med Cell Longev 2009;2:172-175.
50. Zachara NE. The roles of O-linked beta-N-acetylglucosamine in cardiovascular physiology and disease. Am J Physiol Heart Circ Physiol 2012;302:H1905-H1918.
51. Ngoh GA, Hamid T, Prabhu SD, Jones SP. O-GlcNAc signaling attenuates ER stress-induced cardiomyocyte death. Am J Physiol Heart Circ Physiol 2009;297:H1711-9.
52. Kato H, Nakajima S, Saito Y, Takahashi S, Katoh R, Kitamura M. mTORC1 serves ER stress-triggered apoptosis via selective activation of the IRE1-JNK pathway. Cell Death Differ 2012;19:310-320.
53. Glidden EJ, Gray LG, Vemuru S, Li D, Harris TE, Mayo MW. Multiple site acetylation of Rictor stimulates mammalian target of Rapamycin complex-2 (mTORC2)-dependent phosphorylation of Akt protein. J Biol Chem 2012;287:581-588.
54. Dai H, Kustigian L, Carney D, Case A, Considine T, Hubbard BP, Perni RB, Riera TV, Szczepankiewicz B, Vlasuk GP, Stein RL. SIRT1 activation by small molecules: kinetic and biophysical evidence for direct interaction of enzyme and activator. JBiolChem 2010;285:32695-32703.