Hydrogen peroxide decreases endothelial nitric oxide synthase promoter activity through the inhibition of Sp1 activity

DNA and Cell Biology

Volumn 28, Issue 3, 2009, Pages 119-129

  Kumar, Sanjiv ^a   Sun, Xutong ^a   Wiseman, Dean A ^a   Tian, Jing ^a   Umapathy, Nagavedi S ^a   Verin, Alexander D ^a   Black, Stephen M ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; DEFEROXAMINE MESYLATE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYDROGEN PEROXIDE; HYDROXYL RADICAL; MACROGOL; MESSENGER RNA; SCAVENGER; TRANSCRIPTION FACTOR SP1; ZINC;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; ENZYME ACTIVITY; FETUS; GEL MOBILITY SHIFT ASSAY; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PULMONARY ARTERY;

ANIMALS; CELLS, CULTURED; DOWN-REGULATION; ENDOTHELIAL CELLS; HUMANS; HYDROGEN PEROXIDE; HYDROXYL RADICAL; NITRIC OXIDE SYNTHASE TYPE III; PROMOTER REGIONS, GENETIC; PULMONARY ARTERY; REGULATORY SEQUENCES, NUCLEIC ACID; SHEEP; SP1 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP-1; ZINC;

OVIS;

EID: 62249194860     PISSN: 10445498     EISSN: None     Source Type: Journal    
DOI: 10.1089/dna.2008.0775     Document Type: Article

References (64)

1. Abman, S.H., Shanley, P.F., and Accurso, F.J. (1989). Failure of postnatal adaptation of the pulmonary circulation after chronic intrauterine pulmonary hypertension in fetal lambs. J Clin Invest 83, 1849-1858.
2. Ammendola, R., Mesuraca, M., Russo, T., and Cimino, F. (1994). The DNA-binding efficiency of Sp1 is affected by redox changes. Eur J Biochem 225, 483-489.
3. Berg, J.M. (1992). Sp1 and the subfamily of zinc finger proteins with guanine-rich binding sites. Proc Natl Acad Sci USA 89, 11109-11110.
4. Black, S.M., and Fineman, J.R. (2006). Oxidative and nitrosative stress in pediatric pulmonary hypertension: roles of endothelin-1 and nitric oxide. Vascul Pharmacol 45, 308-316.
5. Black, S.M., Johengen, M.J., and Soifer, S.J. (1998). Coordinated regulation of genes of the nitric oxide and endothelin pathways during the development of pulmonary hypertension in fetal lambs. Pediatr Res 44, 821-830.
6. Bohmann, D., Bos, T.J., Admon, A., Nishimura, T., Vogt, P.K., and Tjian, R. (1987). Human proto-oncogene c-jun encodes a DNA binding protein with structural and functional properties of transcription factor AP-1. Science 238, 1386-1392.
7. Brandes, R.P., and Kreuzer, J. (2005). Vascular NADPH oxidases: molecular mechanisms of activation. Cardiovasc Res 65, 16-27.
8. Braunstein, M., Rose, A.B., Holmes, S.G., Allis, C.D., and Broach, J.R. (1993). Transcriptional silencing in yeast is associated with reduced nucleosome acetylation. Genes Dev 7, 592-604.
9. Brennan, L.A., Steinhorn, R.H., Wedgwood, S., Mata-Greenwood, E., Roark, E.A., Russell, J.A., and Black, S.M. (2003). Increased superoxide generation is associated with pulmonary hypertension in fetal lambs: a role for NADPH oxidase. Circ Res 92, 683-691.
10. Briggs, M.R., Kadonaga, J.T., Bell, S.P., and Tjian, R. (1986). Purification and biochemical characterization of the promoter-specific transcription factor, Sp1. Science 234, 47-52.
11. Cai, H. (2005). NAD(P)H oxidase-dependent self-propagation of hydrogen peroxide and vascular disease. Circ Res 96, 818-822.
12. Cai, H., Davis, M.E., Drummond, G.R., and Harrison, D.G. (2001). Induction of endothelial NO synthase by hydrogen peroxide via a Ca(2+)/calmodulin-dependent protein kinase II/janus kinase 2-dependent pathway. Arterioscler Thromb Vasc Biol 21, 1571-1576.
13. Cieslik, K., Zembowicz, A., Tang, J.L., and Wu, K.K. (1998). Transcriptional regulation of endothelial nitric-oxide synthase by lysophosphatidylcholine. J Biol Chem 273, 14885-14890.
14. Cortese, M.M., Suschek, C.V., Wetzel, W., Kroncke, K.D., and Kolb-Bachofen, V. (2008). Zinc protects endothelial cells from hydrogen peroxide via Nrf2-dependent stimulation of glutathione biosynthesis. Free Radic Biol Med 44, 2002-2012.
15. Courey, A.J., Holtzman, D.A., Jackson, S.P., and Tjian, R. (1989). Synergistic activation by the glutamine-rich domains of human transcription factor Sp1. Cell 59, 827-836.
16. Coyle, P., Zalewski, P.D., Philcox, J.C., Forbes, I.J., Ward, A.D., Lincoln, S.F., Mahadevan, I., and Rofe, A.M. (1994). Measurement of zinc in hepatocytes by using a fluorescent probe, zinquin: relationship to metallothionein and intracellular zinc. Biochem J 303 (Pt 3), 781-786.
17. Desjarlais, J.R., and Berg, J.M. (1992). Toward rules relating zinc finger protein sequences and DNA binding site preferences. Proc Natl Acad Sci USA 89, 7345-7349.
18. Drummond, G.R., Cai, H., Davis, M.E., Ramasamy, S., and Harrison, D.G. (2000). Transcriptional and posttranscriptional regulation of endothelial nitric oxide synthase expression by hydrogen peroxide. Circ Res 86, 347-354.
19. Dynan, W.S., and Tjian, R. (1983). The promoter-specific transcription factor Sp1 binds to upstream sequences in the SV40 early promoter. Cell 35, 79-87.
20. Dynan, W.S., and Tjian, R. (1985). Control of eukaryotic messenger RNA synthesis by sequence-specific DNA-binding proteins. Nature 316, 774-778.
21. Fisslthaler, B., Benzing, T., Busse, R., and Fleming, I. (2003). Insulin enhances the expression of the endothelial nitric oxide synthase in native endothelial cells: a dual role for Akt and AP-1. Nitric Oxide 8, 253-261.
22. Floyd, R.A., Watson, J.J., and Wong, P.K. (1984). Sensitive assay of hydroxyl free radical formation utilizing high pressure liquid chromatography with electrochemical detection of phenol and salicylate hydroxylation products. J Biochem Biophys Methods 10, 221-235.
23. Forman, H.J., and Torres, M. (2002). Reactive oxygen species and cell signaling: respiratory burst in macrophage signaling. Am J Respir Crit Care Med 166, S4-S8.
24. Freedman, J.E., Sauter, R., Battinelli, E.M., Ault, K., Knowles, C., Huang, P.L., and Loscalzo, J. (1999). Deficient platelet-derived nitric oxide and enhanced hemostasis in mice lacking the NOSIII gene. Circ Res 84, 1416-1421.
25. Fridovich, I. (1995). Superoxide radical and superoxide dismutases. Annu Rev Biochem 64, 97-112.
26. Giaid, A., and Saleh, D. (1995). Reduced expression of endothelial nitric oxide synthase in the lungs of patients with pulmonary hypertension. N Engl J Med 333, 214-221.
27. Grinstein, E., Jundt, F., Weinert, I., Wernet, P., and Royer, H.D. (2002). Sp1 as G1 cell cycle phase specific transcription factor in epithelial cells. Oncogene 21, 1485-1492.
28. Grumbach, I.M., Chen, W., Mertens, S.A., and Harrison, D.G. (2005). A negative feedback mechanism involving nitric oxide and nuclear factor kappa-B modulates endothelial nitric oxide synthase transcription. J Mol Cell Cardiol 39, 595-603.
29. Guzik, T.J., and Harrison, D.G. (2006). Vascular NADPH oxidases as drug targets for novel antioxidant strategies. Drug Discov Today 11, 524-533.
30. Haworth, S.G., and Reid, L. (1976). Persistent fetal circulation: newly recognized structural features. J Pediatr 88, 614-620.
31. Huang, P.L., Huang, Z., Mashimo, H., Bloch, K.D., Moskowitz, M.A., Bevan, J.A., and Fishman, M.C. (1995). Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature 377, 239-242.
32. Josko, J., and Mazurek, M. (2004). Transcription factors having impact on vascular endothelial growth factor (VEGF) gene expression in angiogenesis. Med Sci Monit 10, RA89-RA98.
33. Kaluzova, M., Pastorekova, S., Svastova, E., Pastorek, J., Stanbridge, E.J., and Kaluz, S. (2001). Characterization of the MN/CA 9 promoter proximal region: a role for specificity protein (SP) and activator protein 1 (AP1) factors. Biochem J 359, 669-677.
34. Kavurma, M.M., and Khachigian, L.M. (2003). Sp1 inhibits proliferation and induces apoptosis in vascular smooth muscle cells by repressing p21WAF1/Cip1 transcription and cyclin D1-Cdk4-p21WAF1/Cip1 complex formation. J Biol Chem 278, 32537-32543.
35. Knoepfel, L., Steinkuhler, C., Carri, M.T., and Rotilio, G. (1994). Role of zinc-coordination and of the glutathione redox couple in the redox susceptibility of human transcription factor Sp1. Biochem Biophys Res Commun 201, 871-877.
36. Krezel, A., Hao, Q., and Maret, W. (2007). The zinc/thiolate redox biochemistry of metallothionein and the control of zinc ion fluctuations in cell signaling. Arch Biochem Biophys 463, 188-200.
37. Kumar, S., Sun, X., Wedgwood, S., and Black, S.M. (2008). Hydrogen peroxide decreases endothelial nitric oxide synthase promoter activity through the inhibition of AP-1 activity. Am J Physiol Lung Cell Mol Physiol (In press).
38. Kumar, S., Wedgwood, S., and Black, S.M. (2007). Nordihydroguaiaretic acid increases endothelial nitric oxide synthase expression via the transcription factor AP-1. DNA Cell Biol 26, 853-862.
39. Lee, P.C., Salyapongse, A.N., Bragdon, G.A., Shears, L.L., 2nd, Watkins, S.C., Edington, H.D., and Billiar, T.R. (1999). Impaired wound healing and angiogenesis in eNOS-deficient mice. Am J Physiol 277, H1600-H1608.
40. Li, J.M., and Shah, A.M. (2004). Endothelial cell superoxide generation: regulation and relevance for cardiovascular pathophysiology. Am J Physiol Regul Integr Comp Physiol 287, R1014-R1030.
41. Marsden, P.A., Heng, H.H., Scherer, S.W., Stewart, R.J., Hall, A.V., Shi, X.M., Tsui, L.C., and Schappert, K.T. (1993). Structure and chromosomal localization of the human constitutive endothelial nitric oxide synthase gene. J Biol Chem 268, 17478-17488.
42. McCabe, D.R., Maher, T.J., and Acworth, I.N. (1997). Improved method for the estimation of hydroxyl free radical levels in vivo based on liquid chromatography with electrochemical detection. J Chromatogr B Biomed Sci Appl 691, 23-32.
43. Meyer, M., Pahl, H.L., and Baeuerle, P.A. (1994). Regulation of the transcription factors NF-kappa B and AP-1 by redox changes. Chem Biol Interact 91, 91-100.
44. 2 and antioxidants have opposite effects on activation of NF-kappa B and AP-1 in intact cells: AP-1 as secondary antioxidant-responsive factor. EMBO J 12, 2005-2015.
45. Rana, U., Kothinti, R., Meeusen, J., Tabatabai, N.M., Krezoski, S., and Petering, D.H. (2008). Zinc binding ligands and cellular zinc trafficking: apo-metallothionein, glutathione, TPEN, proteomic zinc, and Zn-Sp1. J Inorg Biochem 102, 489-499.
46. Rubanyi, G.M., Romero, J.C., and Vanhoutte, P.M. (1986). Flow-induced release of endothelium-derived relaxing factor. Am J Physiol 250, H1145-H1149.
47. Rudic, R.D., Shesely, E.G., Maeda, N., Smithies, O., Segal, S.S., and Sessa, W.C. (1998). Direct evidence for the importance of endothelium-derived nitric oxide in vascular remodeling. J Clin Invest 101, 731-736.
48. Shi, J., Wang, X., Qiu, J., Si, Q., Sun, R., Guo, H., and Wu, Q. (2004). Roles of NF-kappaB and SP-1 in oxidative stress-mediated induction of platelet-derived growth factor-B by TNFalpha in human endothelial cells. J Cardiovasc Pharmacol 44, 26-34.
49. Steinhorn, R.H., Millard, S.L., and Morin, F.C., 3rd. (1995). Persistent pulmonary hypertension of the newborn. Role of nitric oxide and endothelin in pathophysiology and treatment. Clin Perinatol 22, 405-428.
50. Suvorava, T., Lauer, N., Kumpf, S., Jacob, R., Meyer, W., and Kojda, G. (2005). Endogenous vascular hydrogen peroxide regulates arteriolar tension in vivo. Circulation 112, 2487-2495.
51. Tang, J.L., Zembowicz, A., Xu, X.M., and Wu, K.K. (1995). Role of Sp1 in transcriptional activation of human nitric oxide synthase type III gene. Biochem Biophys Res Commun 213, 673-680.
52. Thomas, S.R., Chen, K., and Keaney, J.F., Jr. (2002). Hydrogen peroxide activates endothelial nitric-oxide synthase through coordinated phosphorylation and dephosphorylation via a phosphoinositide 3-kinase-dependent signaling pathway. J Biol Chem 277, 6017-6024.
53. Touyz, R.M., and Schiffrin, E.L. (2004). Reactive oxygen species in vascular biology: implications in hypertension. Histochem Cell Biol 122, 339-352.
54. Wardman, P., and Candeias, L.P. (1996). Fenton chemistry: an introduction. Radiat Res 145, 523-531.
55. Wedgwood, S., and Black, S.M. (2005). Endothelin-1 decreases endothelial NOS expression and activity through ETA receptor-mediated generation of hydrogen peroxide. Am J Physiol Lung Cell Mol Physiol 288, L480-L487.
56. Wedgwood, S., Mitchell, C.J., Fineman, J.R., and Black, S.M. (2003). Developmental differences in the shear stress-induced expression of endothelial NO synthase: changing role of AP-1. Am J Physiol Lung Cell Mol Physiol 284, L650-L662.
57. Wedgwood, S., Steinhorn, R.H., Bunderson, M., Wilham, J., Lakshminrusimha, S., Brennan, L.A., and Black, S.M. (2005). Increased hydrogen peroxide downregulates soluble guanylate cyclase in the lungs of lambs with persistent pulmonary hypertension of the newborn. Am J Physiol Lung Cell Mol Physiol 289, L660-L666.
58. Wild, L.M., Nickerson, P.A., and Morin, F.C., 3rd. (1989). Ligating the ductus arteriosus before birth remodels the pulmonary vasculature of the lamb. Pediatr Res 25, 251-257.
59. Wiseman, D.A., Wells, S.M., Hubbard, M., Welker, J.E., and Black, S.M. (2007). Alterations in zinc homeostasis underlie endothelial cell death induced by oxidative stress from acute exposure to hydrogen peroxide. Am J Physiol Lung Cell Mol Physiol 292, L165-L177.
60. Xing, F., Jiang, Y., Liu, J., Zhao, K., Mo, Y., Qin, Q., Wang, J., Ouyang, J., and Zeng, Y. (2006). Role of AP1 element in the activation of human eNOS promoter by lysophosphatidylcholine. J Cell Biochem 98, 872-884.
61. Xu, J.W., Ikeda, K., and Yamori, Y. (2004). Upregulation of endothelial nitric oxide synthase by cyanidin-3-glucoside, a typical anthocyanin pigment. Hypertension 44, 217-222.
62. Zalewski, P.D., Forbes, I.J., and Betts, W.H. (1993). Correlation of apoptosis with change in intracellular labile Zn(II) using zinquin [(2-methyl-8-p-toluenesulphonamido-6-quinolyloxy)acetic acid], a new specific fluorescent probe for Zn(II). Biochem J 296 (Pt 2), 403-408.
63. Zhang, R., Min, W., and Sessa, W.C. (1995). Functional analysis of the human endothelial nitric oxide synthase promoter. Sp1 and GATA factors are necessary for basal transcription in endothelial cells. J Biol Chem 270, 15320-15326.
64. Zhang, J., Patel, J.M., and Block, E.R. (1997). Molecular cloning, characterization and expression of a nitric oxide synthase from porcine pulmonary artery endothelial cells. Comp Biochem Physiol B Biochem Mol Biol 116, 485-491.