Nε-carboxymethyllysine-mediated endoplasmic reticulum stress promotes endothelial cell injury through Nox4/MKP-3 interaction

Free Radical Biology and Medicine

Volumn 74, Issue , 2014, Pages 294-306

  Lee, Wen Jane ^a,b   Huey Herng Sheu, Wayne ^a,c   Liu, Shing Hwa ^d   Yi, Yu Chiao ^a   Chen, Wei Chih ^a   Lin, Shih Yi ^a   Liang, Kae Woei ^a   Shen, Chin Chang ^e   Yeh, Hsiang Yu ^f   Lin, Li Yun ^f   Tsai, Yi Ching ^a,c   Tien, Hsing Ru ^c   Lee, Maw Rong ^c   Yang, Tzung Jie ^c   Sheu, Meei Ling ^a,c  

^a TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^b TUNGHAI UNIVERSITY   (Taiwan)

^c NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^e INSTITUTE OF NUCLEAR ENERGY RESEARCH   (Taiwan)

^f HUNGKUANG UNIVERSITY   (Taiwan)

Author keywords

AGEs; CML; ERK; Free radicals; Human endothelial cells; MKP 3; Nox4

Indexed keywords

6 N CARBOXYMETHYLLYSINE; ACETYLCYSTEINE; APOCYNIN; DUAL SPECIFICITY PHOSPHATASE 6; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SMALL INTERFERING RNA; THAPSIGARGIN; LYSINE; N(6)-CARBOXYMETHYLLYSINE; NOX4 PROTEIN, HUMAN; PROTEIN BINDING; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL DAMAGE; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENDOTHELIUM CELL; ENDOTHELIUM INJURY; ENZYME ACTIVATION; FEMALE; GENE SILENCING; HUMAN; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; LIPID DIET; MALE; MICROVASCULAR ENDOTHELIAL CELL; MIDDLE AGED; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; TANDEM MASS SPECTROMETRY; UMBILICAL VEIN ENDOTHELIAL CELL; ANALOGS AND DERIVATIVES; ANIMAL; BLOOD; C57BL MOUSE; CHEMICALLY INDUCED; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULARLY TARGETED THERAPY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSFORMED CELL LINE;

ANIMALS; APOPTOSIS; CELL LINE, TRANSFORMED; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; DIET, HIGH-FAT; DUAL SPECIFICITY PHOSPHATASE 6; ENDOPLASMIC RETICULUM STRESS; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; LYSINE; MALE; MICE; MICE, INBRED C57BL; MOLECULAR TARGETED THERAPY; NADPH OXIDASE; PROTEIN BINDING; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84907367024     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.06.015     Document Type: Article

References (27)

1. M.M. Anderson, and J.W. Heinecke Production of N(epsilon)-(carboxymethyl) lysine is impaired in mice deficient in NADPH oxidase: a role for phagocyte-derived oxidants in the formation of advanced glycation end products during inflammation Diabetes 52 2003 2137 2143 (Pubitemid 36919809)
2. J. Ni, X. Yuan, J. Gu, X. Yue, X. Gu, and R.H. Nagaraj et al. Plasma protein pentosidine and carboxymethyllysine, biomarkers for age-related macular degeneration Mol. Cell. Proteomics 8 2009 1921 1933
3. J.S. Hwang, C.H. Shin, and S.W. Yang Clinical implications of N epsilon-(carboxymethyl)lysine, advanced glycation end product, in children and adolescents with type 1 diabetes Diabetes Obes. Metab. 7 2005 263 267 (Pubitemid 40542817)
4. S. Drinda, S. Franke, C.C. Canet, P. Petrow, R. Brauer, and C. Huttich et al. Identification of the advanced glycation end products N(epsilon)- carboxymethyllysine in the synovial tissue of patients with rheumatoid arthritis Ann. Rheum. Dis. 61 2002 488 492 (Pubitemid 34539089)
5. R. Bucala, K.J. Tracey, and A. Cerami Advanced glycosylation products quench nitric oxide and mediate defective endothelium-dependent vasodilatation in experimental diabetes J. Clin. Invest. 87 1991 432 438
6. S.H. Liu, W.H. Sheu, M.R. Lee, W.J. Lee, Y.C. Yi, and T.J. Yang et al. Advanced glycation end product N(epsilon)-carboxymethyllysine induces endothelial cell injury: the involvement of SHP-1-regulated VEGFR-2 dephosphorylation J. Pathol. 230 2013 215 227
7. M. Brownlee The pathobiology of diabetic complications: a unifying mechanism Diabetes 54 2005 1615 1625 (Pubitemid 40770750)
8. D. Versari, E. Daghini, A. Virdis, L. Ghiadoni, and S. Taddei Endothelial dysfunction as a target for prevention of cardiovascular disease Diabetes Care 32 Suppl. 2 2009 S314 S321
9. 2+ release modulates endothelial nitric-oxide synthase via extracellular signal-regulated kinase (ERK) 1/2-mediated serine 635 phosphorylation J. Biol. Chem. 286 2011 20100 20108
10. J. Zhang, and H. Cai Netrin-1 prevents ischemia/reperfusion-induced myocardial infarction via a DCC/ERK1/2/eNOS s1177/NO/DCC feed-forward mechanism J. Mol. Cell. Cardiol. 48 2010 1060 1070
11. I. Tabas The role of endoplasmic reticulum stress in the progression of atherosclerosis Circ. Res. 107 2010 839 850
12. H. Xu, Q. Yang, M. Shen, X. Huang, M. Dembski, and R. Gimeno et al. Dual specificity MAPK phosphatase 3 activates PEPCK gene transcription and increases gluconeogenesis in rat hepatoma cells J. Biol. Chem. 280 2005 36013 36018 (Pubitemid 41633871)
13. Z. Wu, P. Jiao, X. Huang, B. Feng, Y. Feng, and S. Yang et al. MAPK phosphatase-3 promotes hepatic gluconeogenesis through dephosphorylation of forkhead box O1 in mice J. Clin. Invest. 120 2010 3901 3911
14. D.W. Chan, V.W. Liu, G.S. Tsao, K.M. Yao, T. Furukawa, and K.K. Chan et al. Loss of MKP3 mediated by oxidative stress enhances tumorigenicity and chemoresistance of ovarian cancer cells Carcinogenesis 29 2008 1742 1750
15. M.L. Sheu, C.K. Chiang, K.S. Tsai, F.M. Ho, T.I. Weng, and H.Y. Wu et al. Inhibition of NADPH oxidase-related oxidative stress-triggered signaling by honokiol suppresses high glucose-induced human endothelial cell apoptosis Free Radic. Biol. Med. 44 2008 2043 2050
16. M.L. Sheu, F.M. Ho, R.S. Yang, K.F. Chao, W.W. Lin, and S.Y. Lin-Shiau et al. High glucose induces human endothelial cell apoptosis through a phosphoinositide 3-kinase-regulated cyclooxygenase-2 pathway Arterioscler. Thromb. Vasc. Biol. 25 2005 539 545 (Pubitemid 40315675)
17. S.H. Liu, C.N. Yang, H.C. Pan, Y.J. Sung, K.K. Liao, and W.B. Chen et al. IL-13 downregulates PPAR-gamma/heme oxygenase-1 via ER stress-stimulated calpain activation: aggravation of activated microglia death Cell. Mol. Life Sci. 67 2010 1465 1476
18. S.H. Liu, K.B. Wang, K.H. Lan, W.J. Lee, H.C. Pan, and S.M. Wu et al. Calpain/SHP-1 interaction by honokiol dampening peritoneal dissemination of gastric cancer in nu/nu mice PLoS One 7 2012 e43711
19. K. Chen, M.T. Kirber, H. Xiao, Y. Yang, and J.F. Keaney Jr. Regulation of ROS signal transduction by NADPH oxidase 4 localization J. Cell Biol. 181 2008 1129 1139 (Pubitemid 351915488)
20. P.S. Gargalovic, N.M. Gharavi, M.J. Clark, J. Pagnon, W.P. Yang, and A. He et al. The unfolded protein response is an important regulator of inflammatory genes in endothelial cells Arterioscler. Thromb. Vasc. Biol. 26 2006 2490 2496 (Pubitemid 44607470)
21. M.I. Khan, B.A. Pichna, Y. Shi, A.J. Bowes, and G.H. Werstuck Evidence supporting a role for endoplasmic reticulum stress in the development of atherosclerosis in a hyperglycaemic mouse model Antioxid. Redox Signaling 11 2009 2289 2298
22. P.A. Outinen, S.K. Sood, S.I. Pfeifer, S. Pamidi, T.J. Podor, and J. Li et al. Homocysteine-induced endoplasmic reticulum stress and growth arrest leads to specific changes in gene expression in human vascular endothelial cells Blood 94 1999 959 967 (Pubitemid 29361827)
23. L. Rossig, J. Haendeler, C. Hermann, P. Malchow, C. Urbich, and A.M. Zeiher et al. Nitric oxide down-regulates MKP-3 mRNA levels: involvement in endothelial cell protection from apoptosis J. Biol. Chem. 275 2000 25502 25507
24. P.A. Kern, S. Ranganathan, C. Li, L. Wood, and G. Ranganathan Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance Am. J. Physiol. Endocrinol. Metab. 280 2001 E745 E751
25. J. Kuroda, T. Ago, S. Matsushima, P. Zhai, M.D. Schneider, and J. Sadoshima NADPH oxidase 4 (Nox4) is a major source of oxidative stress in the failing heart Proc. Natl. Acad. Sci. USA 107 2010 15565 15570
26. M. Sedeek, G. Callera, A. Montezano, A. Gutsol, F. Heitz, and C. Szyndralewiez et al. Critical role of Nox4-based NADPH oxidase in glucose-induced oxidative stress in the kidney: implications in type 2 diabetic nephropathy Am. J. Physiol. Renal Physiol 299 2010 F1348 F1358
27. J. Li, J.J. Wang, Q. Yu, K. Chen, K. Mahadev, and S.X. Zhang Inhibition of reactive oxygen species by Lovastatin downregulates vascular endothelial growth factor expression and ameliorates blood-retinal barrier breakdown in db/db mice: role of NADPH oxidase 4 Diabetes 59 2010 1528 1538