Compound C stimulates heme oxygenase-1 gene expression via the Nrf2-ARE pathway to preserve human endothelial cell survival

Biochemical Pharmacology

Volumn 82, Issue 4, 2011, Pages 371-379

  Liu, Xiao Ming ^a   Peyton, Kelly J ^a   Shebib, Ahmad R ^a   Wang, Hong ^b   Durante, William ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b TEMPLE UNIVERSITY   (United States)

Author keywords

Compound C; Endothelial cells; Heme oxygenase 1; Oxidative stress

Indexed keywords

6 [4(2 PIPERIDIN 1 YL ETHOXY) PHENYL] 3 PYRIDIN 4 YL PYRAZOLO[1,5-A]PYRIMIDINE; ACETYLCYSTEINE; ADENYLATE KINASE; APOCYNIN; BILIRUBIN; BILIVERDIN; CARBON MONOXIDE; DACTINOMYCIN; GLUTATHIONE; HEME OXYGENASE 1; PYRIMIDINE ANTAGONIST; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CELL DEATH; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DRUG POTENTIATION; ENDOTHELIUM CELL; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; NORTHERN BLOTTING; OUTCOME ASSESSMENT; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM; WESTERN BLOTTING;

AMP-ACTIVATED PROTEIN KINASES; ANTIOXIDANTS; CELL SURVIVAL; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEME OXYGENASE-1; HUMANS; NF-E2-RELATED FACTOR 2; PYRAZOLES; PYRIMIDINES; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION;

EID: 79960353816     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2011.05.016     Document Type: Article

References (38)

1. G. Zhou, R. Myers, Y. Li, Y. Chen, X. Shen, and J. Fenyk-Melody Role of AMPK-activated protein kinase in mechanism of metformin action J Clin Invest 108 2001 1167 1174 (Pubitemid 32995375)
2. J. Bain, L. Plater, M. Elliott, N. Shpiro, C.J. Hastie, and H. McLauchlin The selectivity of protein kinase inhibitors: a further update Biochem J 408 2007 297 315
3. B.M. Emerling, B. Viollet, K.V. Tormos, and N.S. Chandel Compound C inhibits hypoxic activation of HIF-1-independent of AMPK FEBS Lett 581 2007 5727 5731 (Pubitemid 350179784)
4. P.B. Yu, C.C. Hong, C. Sachidanandan, J.L. Babitt, D.Y. Deng, and S.A. Hoyng Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism Nat Chem Biol 4 2008 33 41 (Pubitemid 350273653)
5. L. Vucicevic, M. Misirkic, K. Janjetovic, Harhaji-Trajkovic, M. Prica, and D. Stevanovic AMPK-activated protein kinase-dependent and -independent mechanisms underlying in vitro antiglioma action of compound C Biochem Pharmacol 77 2009 1684 1693
6. M. Nam, W.H. Lee, E.J. Bae, and S.G. Kim Compound C inhibits clonal expansion of preadipocytes by increasing p21 level irrespective of AMPK inhibition Arch Biochem Biophys 479 2008 74 81
7. J. Jin, T.D. Mullen, Q. Hou, J. Bielawski, A. Bielawski, and X. Zhang AMPK inhibitor compound C stimulates ceramide production and promotes Bax redistribution and apoptosis in MCF7 breast carcinoma cells J Lipid Res 50 2009 2389 2397
8. L and Mcl-1 Exp Cell Res 316 2010 2194 2203
9. X.M. Liu, K.J. Peyton, A.R. Shebib, H. Wang, R.J. Korthuis, and W. Durante Activation of AMPK stimulates heme oxygenase-1 gene expression and human endothelial cell survival Am J Physiol Heart Circ Physiol 300 2011 H84 93
10. R. Tenhunen, H.S. Marver, and R. Schmid The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase Proc Natl Acad Sci USA 61 1968 748 755
11. J. Alam, and J.L. Cook Transcriptional regulation of the heme oxygenase-1 gene via the stress response pathway Curr Pharm Des 9 2003 2499 2511 (Pubitemid 37236369)
12. T. Ishii, K. Itoh, E. Ruiz, D.S. Leake, H. Unoki, and M. Yamamoto Role of Nrf2 in the regulation of CD36 and stress protein expression in murine macrophages: activation by oxidatively modified LDL and 4-hydroxynonenal Circ Res 94 2004 609 616 (Pubitemid 38387743)
13. X.-L. Chen, S.E. Varner, A.S. Rao, J.Y. Grey, S. Thomas, and C.K. Cook Laminar flow induction antioxidant response element-mediated genes in endothelial cells; a novel anti-inflammatory mechanism J Biol Chem 278 2003 703 711 (Pubitemid 36790739)
14. X.M. Liu, K.J. Peyton, D. Ensenat, H. Wang, M. Hannink, and J. Alam Nitric oxide simulates heme oxygenase-1 gene transcription via the Nrf2/ARE complex to promote vascular smooth muscle cell survival Cardiovasc Res 75 2007 381 389 (Pubitemid 46961918)
15. X.M. Liu, K.J. Peyton, D. Ensenat, H. Wang, A.I. Schafer, and J. Alam Endoplasmic reticulum stress stimulates heme oxygenase-1 gene expression in vascular smooth muscle cells: role in cell survival J Biol Chem 280 2005 872 877
16. W. Durante Targeting heme oxygenase-1 in vascular disease Curr Drug Targets 11 2010 1504 1516
17. D. Morse, L. Lin, A.M. Choi, and S.W. Ryter Heme oxygenase-1, a critical arbitrator of cell death in lung injury and disease Free Radic Biol Med 47 2009 1 12
18. T. Takahashi, K. Morita, R. Akagi, and S. Sassa Heme oxygenase-1: a novel therapeutic target in oxidative tissue injuries Curr Med Chem 11 2004 1546 1561
19. C.C. Lin, X.M. Liu, K.J. Peyton, H. Wang, W.C. Yang, and S.J. Lin Far infrared therapy inhibits vascular endothelial inflammation via the induction of heme oxygenase-1 Arterioscler Thromb Vasc Biol 28 2008 739 745 (Pubitemid 351651343)
20. J. Alam Multiple elements within the 5′ distal enhancer of the mouse heme oxygenase-1 gene mediate induction by heavy metals J Biol Chem 269 1994 25049 25056
21. J. Alam, C. Wick, D. Stewart, P. Gong, C. Touchard, and S. Otterbein Mechanism of heme oxygenase-1 gene activation by cadmium in MCF-7 mammary epithelial cells: role of p38 kinase and Nrf2 transcription factor J Biol Chem 275 2000 27694 27702
22. X.M. Liu, D. Ensenat, H. Wang, A.I. Schafer, and W. Durante Physiologic stretch inhibits apoptosis in vascular endothelium FEBS Lett 541 2003 52 56 (Pubitemid 36428916)
23. K. Itoh, N. Wakabayashi, Y. Katoh, T. Ishii, Y. O'Connor, and M. Yamamoto Keap1 regulates both cytoplasmic-nuclear shuffling and degradation of Nrf2 in response to electrophiles Genes Cells 8 2003 379 391 (Pubitemid 36504013)
24. D.D. Zang, and M. Hannink Distinct cysteine residues in keap1 are required for keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventative agents and oxidative stress Mol Cell Biol 23 2003 8137 8151 (Pubitemid 37377505)
25. E. Schulz, J. Dopheide, S. Schuhmacher, S.R. Thomas, K. Chen, and A. Daiber Suppression of JNK pathway by induction of a metabolic stress response prevents vascular injury and dysfunction Circulation 118 2008 1347 1357
26. Z. Chen, I.-C. Peng, W. Sun, M.-I. Su, P.-H. Hsu, and Y. Fu AMP-activated protein kinase functionally phosphorylates endothelial nitric oxide synthase ser633 Circ Res 104 2009 496 505
27. A. Young, W. Wu, W. Sun, H. Benjamin Larmin, N. Wang, and Y.S. Li Flow activation of AMPK-activated protein kinase in vascular endothelium leads to Kruppel-like factor 2 expression Arterioscler Thromb Vasc Biol 29 2009 1902 1908
28. R. Motterlini, R. Foresti, M. Intaglietta, and R.M. Winslow NO-mediated activation of heme oxygenase: endogenous cytoprotection against oxidative stress to the endothelium Am J Physiol Heart Circ Physiol 270 1996 H107 H114
29. W. Durante, M.H. Kroll, N. Christodoulides, K.J. Peyton, and A.I. Schafer Nitric oxide induces heme oxygenase and carbon monoxide production in vascular smooth muscle cells Circ Res 80 1997 557 564 (Pubitemid 27137293)
30. C.X. Santos, E.I. Anjos, and O. Augusto Uric acid oxidation by peroxynitrite: multiple reactions, free radical formation, and amplification of lipid oxidation Arch Biochem Biophys 372 1999 285 294 (Pubitemid 30026778)
31. C.F. Mueller, K. Laude, J.S. McNally, and D.G. Harrison ATVB in focus: redox mechanisms in blood vessels Arterioscler Thromb Vasc Biol 25 2005 274 278 (Pubitemid 40189145)
32. J. Stolk, T.J. Hilterman, J.H. Dijkman, and A.J. Verhoeven Characteristics of the inhibition of NADPH oxidase activation in neutrophils by apocynin, a methoxy-substituted catechol Am J Respir Cell Mol Biol 11 1994 95 102
33. S. Heumuller, S. Wind, E. Barbosa-Sicard, H.H.H.W. Schmidt, R. Busse, and K. Schroder Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant Hypertension 51 2008 211 217 (Pubitemid 351159930)
34. A. Yachie, Y. Niida, T. Wada, N. Igarishi, H. Kaneda, and T. Toma Oxidative stress causes endothelial cell injury in human heme oxygenase-1-deficiency J Clin Invest 103 1999 129 135 (Pubitemid 29031171)
35. S. Chen, M. Sega, and A. Agarwal Lumen digestion" technique for isolation of aortic endothelial cells from heme oxygenase-1 knockout mice Biotechniques 37 2004 84 86
36. R. Stocker, Y. Yamamoto, A.F. McDonagh, A.N. Glazer, and B.N. Ames Bilirubin is an antioxidant of possible physiological importance Science 235 1987 1043 1046 (Pubitemid 17049750)
37. C.A. Piantodosi, M.S. Carraway, and H.B. Suliman Carbon monoxide, oxidative stress, and mitochondrial permeability pore transition Free Radic Biol Med 40 2006 1332 1339
38. C. Taille, J. El-Benna, S. Lanone, Boczkowski, and R. Motterlini Mitochondrial respiratory chain and NAD(P)H oxidase are targets for the antiproliferative effect of carbon monoxide in human airway smooth muscle J Biol Chem 280 2005 25350 25360 (Pubitemid 40962237)