Simvastatin-dependent up-regulation of heme oxygenase-1 via mRNA stabilization in human endothelial cells

European Journal of Pharmaceutical Sciences

Volumn 41, Issue 1, 2010, Pages 118-124

  Hinkelmann, Urte ^a   Grosser, Nina ^a   Erdmann, Kati ^a   Schröder, Henning ^a,b   Immenschuh, Stephan ^c  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b UNIVERSITY OF MINNESOTA   (United States)

^c HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Endothelial cells; Gene regulation; Heme oxygenase 1; Signaling; Statins

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; DACTINOMYCIN; HEME OXYGENASE 1; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SIMVASTATIN; HEME OXYGENASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DRUG ACTIVITY; DRUG HALF LIFE; DRUG MECHANISM; ENDOTHELIUM CELL; ENZYME INDUCTION; ENZYME INHIBITION; ENZYME REGULATION; GENE ACTIVATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; RAT; RNA STABILITY; UPREGULATION; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; ENZYMOLOGY; GENETICS; VASCULAR ENDOTHELIUM;

CELLS, CULTURED; ENDOTHELIUM, VASCULAR; HEME OXYGENASE (DECYCLIZING); HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; RNA, MESSENGER; SIMVASTATIN; UP-REGULATION;

EID: 77954761548     PISSN: 09280987     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejps.2010.05.021     Document Type: Article

References (53)

1. Abraham N.G., Asija A., Drummond G., Peterson S. Heme oxygenase-1 gene therapy: recent advances and therapeutic applications. Curr. Gene Ther. 2007, 7:89-108.
2. Alam J., Cook J.L. How many transcription factors does it take to turn on the heme oxygenase-1 gene?. Am. J. Respir. Cell Mol. Biol. 2007, 36:166-174.
3. Alam J., Igarashi K., Immenschuh S., Shibahara S., Tyrrell R.M. Regulation of heme oxygenase-1 gene transcription: recent advances and highlights from the International Conference (Uppsala, 2003) on Heme Oxygenase. Antioxid. Redox Signal. 2004, 6:924-933.
4. Ali F., Hamdulay S.S., Kinderlerer A.R., Boyle J.J., Lidington E.A., Yamaguchi T., Soares M.P., Haskard D.O., Randi A.M., Mason J.C. Statin-mediated cytoprotection of human vascular endothelial cells: a role for Kruppel-like factor 2-dependent induction of heme oxygenase-1. J. Thromb. Haemost. 2007, 5:2537-2546.
5. Ali F., Zakkar M., Karu K., Lidington E.A., Hamdulay S.S., Boyle J.J., Zloh M., Bauer A., Haskard D.O., Evans P.C., Mason J.C. Induction of the cytoprotective enzyme heme oxygenase-1 by statins is enhanced in vascular endothelium exposed to laminar shear stress and impaired by disturbed flow. J. Biol. Chem. 2009, 284:18882-18892.
6. Ali F., Ali N.S., Bauer A., Boyle J.J., Hamdulay S.S., Haskard D.O., Randi A.M., Mason J.C. PPARdelta and PGC1alpha act cooperatively to induce haem oxygenase-1 and enhance vascular endothelial cell resistance to stress. Cardiovasc. Res. 2010, 85:701-710.
7. Applegate L.A., Luscher P., Tyrrell R.M. Induction of heme oxygenase: a general response to oxidant stress in cultured mammalian cells. Cancer Res. 1991, 51:974-978.
8. Bhattacharjee R., Kaneda M., Nakahama K., Morita I. The steady-state expression of connexin43 is maintained by the PI3K/Akt in osteoblasts. Biochem. Biophys. Res. Commun. 2009, 382:440-444.
9. Bouton C., Demple B. Nitric oxide-inducible expression of heme oxygenase-1 in human cells. Translation-independent stabilization of the mRNA and evidence for direct action of nitric oxide. J. Biol. Chem. 2000, 275:32688-32693.
10. 2-induced apoptosis through functional codependence between HO-1 and AKT. Arterioscler. Thromb. Vasc. Biol. 2006, 26:2027-2034.
11. Cerezo-Guisado M.I., Garcia-Roman N., Garcia-Marin L.J., Alvarez-Barrientos A., Bragado M.J., Lorenzo M.J. Lovastatin inhibits the extracellular-signal-regulated kinase pathway in immortalized rat brain neuroblasts. Biochem. J. 2007, 401:175-183.
12. Chen J.C., Huang K.C., Lin W.W. HMG-CoA reductase inhibitors upregulate heme oxygenase-1 expression in murine RAW264.7 macrophages via ERK, p38 MAPK and protein kinase G pathways. Cell Signal. 2006, 18:32-39.
13. Chung S.W., Chen Y.H., Perrella M.A. Role of Ets-2 in the regulation of heme oxygenase-1 by endotoxin. J. Biol. Chem. 2005, 280:4578-4584.
14. Gozzelino R., Jeney V., Soares M.P. Mechanisms of cell protection by heme oxygenase-1. Annu. Rev. Pharmacol. Toxicol. 2010, 50:323-354.
15. Greenwood J., Mason J.C. Statins and the vascular endothelial inflammatory response. Trends Immunol. 2007, 28:88-98.
16. Grosser N., Erdmann K., Hemmerle A., Berndt G., Hinkelmann U., Smith G., Schroder H. Rosuvastatin upregulates the antioxidant defense protein heme oxygenase-1. Biochem. Biophys. Res. Commun. 2004, 325:871-876.
17. Grosser N., Hemmerle A., Berndt G., Erdmann K., Hinkelmann U., Schurgerc S., Wijayanti N., Immenschuh S., Schroder H. The antioxidant defense protein heme oxygenase 1 is a novel target for statins in endothelial cells. Free Radic. Biol. Med. 2004, 37:2064-2071.
18. Habara K., Hamada Y., Yamada M., Tokuhara K., Tanaka H., Kaibori M., Kamiyama Y., Nishizawa M., Ito S., Okumura T. Pitavastatin up-regulates the induction of iNOS through enhanced stabilization of its mRNA in pro-inflammatory cytokine-stimulated hepatocytes. Nitric Oxide 2008, 18:19-27.
19. Heeba G., Moselhy M.E., Hassan M., Khalifa M., Gryglewski R., Malinski T. Anti-atherogenic effect of statins: role of nitric oxide, peroxynitrite and haem oxygenase-1. Br. J. Pharmacol. 2009, 156:1256-1266.
20. Hsu M., Muchova L., Morioka I., Wong R.J., Schroder H., Stevenson D.K. Tissue-specific effects of statins on the expression of heme oxygenase-1 in vivo. Biochem. Biophys. Res. Commun. 2006, 343:738-744.
21. Hu H., Sung A., Zhao G., Shi L., Qiu D., Nishimura T., Kao P.N. Simvastatin enhances bone morphogenetic protein receptor type II expression. Biochem. Biophys. Res. Commun. 2006, 339:59-64.
22. Immenschuh S., Ramadori G. Gene regulation of heme oxygenase-1 as a therapeutic target. Biochem. Pharmacol. 2000, 60:1121-1128.
23. Immenschuh S., Schroder H. Heme oxygenase-1 and cardiovascular disease. Histol. Histopathol. 2006, 21:679-685.
24. Ishikawa K., Sugawara D., Goto J., Watanabe Y., Kawamura K., Shiomi M., Itabe H., Maruyama Y. Heme oxygenase-1 inhibits atherogenesis in Watanabe heritable hyperlipidemic rabbits. Circulation 2001, 104:1831-1836.
25. Kang M.J., Ryu B.K., Lee M.G., Han J., Lee J.H., Ha T.K., Byun D.S., Chae K.S., Lee B.H., Chun H.S., Lee K.Y., Kim H.J., Chi S.G. NF-kappaB activates transcription of the RNA-binding factor HuR, via PI3K-AKT signaling, to promote gastric tumorigenesis. Gastroenterology 2008, 135:2030-2042.
26. Keum Y.S., Yu S., Chang P.P., Yuan X., Kim J.H., Xu C., Han J., Agarwal A., Kong A.N. Mechanism of action of sulforaphane: inhibition of p38 mitogen-activated protein kinase isoforms contributing to the induction of antioxidant response element-mediated heme oxygenase-1 in human hepatoma HepG2 cells. Cancer Res. 2006, 66:8804-8813.
27. Keyse S.M., Tyrrell R.M. Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc. Natl. Acad. Sci. U.S.A. 1989, 86:99-103.
28. Kronke G., Bochkov V.N., Huber J., Gruber F., Bluml S., Furnkranz A., Kadl A., Binder B.R., Leitinger N. Oxidized phospholipids induce expression of human heme oxygenase-1 involving activation of cAMP-responsive element-binding protein. J. Biol. Chem. 2003, 278:51006-51014.
29. Kuwano Y., Rabinovic A., Srikantan S., Gorospe M., Demple B. Analysis of nitric oxide-stabilized mRNAs in human fibroblasts reveals HuR-dependent heme oxygenase 1 upregulation. Mol. Cell Biol. 2009, 29:2622-2635.
30. Kyriakis J.M., Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 2001, 81:807-869.
31. Laufs U., Liao J.K. Post-transcriptional regulation of endothelial nitric oxide synthase mRNA stability by Rho GTPase. J. Biol. Chem. 1998, 273:24266-24271.
32. Leautaud V., Demple B. Regulation of heme oxygenase-1 mRNA deadenylation and turnover in NIH3T3 cells by nitrosative or alkylation stress. BMC Mol. Biol. 2007, 8:116.
33. Lee T.S., Chang C.C., Zhu Y., Shyy J.Y. Simvastatin induces heme oxygenase-1: a novel mechanism of vessel protection. Circulation 2004, 110:1296-1302. (Epub August 30, 2004).
34. Liao J.K., Laufs U. Pleiotropic effects of statins. Annu. Rev. Pharmacol. Toxicol. 2005, 45:89-118.
35. Maines M.D. The heme oxygenase system: a regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 1997, 37:517-554.
36. Maron D.J., Fazio S., Linton M.F. Current perspectives on statins. Circulation 2000, 101:207-213.
37. Martin D., Rojo A.I., Salinas M., Diaz R., Gallardo G., Alam J., De Galarreta C.M., Cuadrado A. Regulation of heme oxygenase-1 expression through the phosphatidylinositol 3-kinase/Akt pathway and the Nrf2 transcription factor in response to the antioxidant phytochemical carnosol. J. Biol. Chem. 2004, 279:8919-8929.
38. Masuya Y., Hioki K., Tokunaga R., Taketani S. Involvement of the tyrosine phosphorylation pathway in induction of human heme oxygenase-1 by hemin, sodium arsenite, and cadmium chloride. J. Biochem. (Tokyo) 1998, 124:628-633.
39. Naidu S., Vijayan V., Santoso S., Kietzmann T., Immenschuh S. Inhibition and genetic deficiency of p38 MAPK up-regulates heme oxygenase-1 gene expression via Nrf2. J. Immunol. 2009, 182:7048-7057.
40. Nebreda A.R., Porras A. p38 MAP kinases: beyond the stress response. Trends Biochem. Sci. 2000, 25:257-260.
41. Pachori A.S., Smith A., McDonald P., Zhang L., Dzau V.J., Melo L.G. Heme-oxygenase-1-induced protection against hypoxia/reoxygenation is dependent on biliverdin reductase and its interaction with PI3K/Akt pathway. J. Mol. Cell Cardiol. 2007, 43:580-592.
42. Poss K.D., Tonegawa S. Reduced stress defense in heme oxygenase 1-deficient cells. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:10925-10930.
43. Ruperez M., Rodrigues-Diez R., Blanco-Colio L.M., Sanchez-Lopez E., Rodriguez-Vita J., Esteban V., Carvajal G., Plaza J.J., Egido J., Ruiz-Ortega M. HMG-CoA reductase inhibitors decrease angiotensin II-induced vascular fibrosis: role of RhoA/ROCK and MAPK pathways. Hypertension 2007, 50:377-383.
44. Ryter S.W., Alam J., Choi A.M. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol. Rev. 2006, 86:583-650.
45. Soares M.P., Seldon M.P., Gregoire I.P., Vassilevskaia T., Berberat P.O., Yu J., Tsui T.Y., Bach F.H. Heme oxygenase-1 modulates the expression of adhesion molecules associated with endothelial cell activation. J. Immunol. 2004, 172:3553-3563.
46. Soares M.P., Usheva A., Brouard S., Berberat P.O., Gunther L., Tobiasch E., Bach F.H. Modulation of endothelial cell apoptosis by heme oxygenase-1-derived carbon monoxide. Antioxid. Redox Signal. 2002, 4:321-329.
47. Stocker R., Perrella M.A. Heme oxygenase-1: a novel drug target for atherosclerotic diseases?. Circulation 2006, 114:2178-2189.
48. Tenhunen R., Marver H.S., Schmid R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc. Natl. Acad. Sci. U.S.A. 1968, 61:748-755.
49. True A.L., Olive M., Boehm M., San H., Westrick R.J., Raghavachari N., Xu X., Lynn E.G., Sack M.N., Munson P.J., Gladwin M.T., Nabel E.G. Heme oxygenase-1 deficiency accelerates formation of arterial thrombosis through oxidative damage to the endothelium, which is rescued by inhaled carbon monoxide. Circ. Res. 2007, 101:893-901.
50. Wagener F.A., Volk H.D., Willis D., Abraham N.G., Soares M.P., Adema G.J., Figdor C.G. Different faces of the heme-heme oxygenase system in inflammation. Pharmacol. Rev. 2003, 55:551-571.
51. Wijayanti N., Huber S., Samoylenko A., Kietzmann T., Immenschuh S. Role of NF-kappaB and p38 MAP kinase signaling pathways in the lipopolysaccharide-dependent activation of heme oxygenase-1 gene expression. Antioxid. Redox Signal. 2004, 6:802-810.
52. Wijayanti N., Kietzmann T., Immenschuh S. Heme oxygenase-1 gene activation by the NAD(P)H oxidase inhibitor 4-(2-aminoethyl) benzenesulfonyl fluoride via a protein kinase B, p38-dependent signaling pathway in monocytes. J. Biol. Chem. 2005, 280:21820-21829.
53. Yachie A., Niida Y., Wada T., Igarashi N., Kaneda H., Toma T., Ohta K., Kasahara Y., Koizumi S. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-deficiency. J. Clin. Invest. 1999, 103:129-135.