Transcriptional regulation of Nox4 by histone deacetylases in human endothelial cells

Basic Research in Cardiology

Volumn 107, Issue 5, 2012, Pages

  Siuda, Daniel ^a   Zechner, Ulrich ^a   Hajj, Nady El ^a   Prawitt, Dirk ^a   Langer, David ^a   Xia, Ning ^a   Horke, Sven ^a   Pautz, Andrea ^a   Kleinert, Hartmut ^a   Rstermann, Ulrich Fö ^a   Li, Huige ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Endothelial cells; Gene regulation; Histone deacetylase; NADPH oxidase; Nox4

Indexed keywords

HISTONE DEACETYLASE 3; MESSENGER RNA; PROTEIN C JUN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; RNA POLYMERASE II; SMALL INTERFERING RNA; TRICHOSTATIN A; VORINOSTAT; HISTONE; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; NOX4 PROTEIN, HUMAN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ARTICLE; CHROMATIN STRUCTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA METHYLATION; ENDOTHELIUM CELL; ENZYME INHIBITION; GENE; GENE EXPRESSION REGULATION; GENE SILENCING; HISTONE ACETYLATION; HUMAN; HUMAN CELL; NOX4 GENE; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; CELL CULTURE; DRUG EFFECT; ENZYMOLOGY; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY;

BASE SEQUENCE; CELLS, CULTURED; DNA METHYLATION; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HISTONES; HUMANS; MOLECULAR SEQUENCE DATA; NADPH OXIDASE; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-JUN; TRANSCRIPTION, GENETIC;

EID: 84863650832     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-012-0283-3     Document Type: Article

References (54)

1. Ago T, Kitazono T, Ooboshi H, Iyama T, Han YH, Takada J, Wakisaka M, Ibayashi S, Utsumi H, IidaM(2004)Nox4 as the major catalytic component of an endothelial NAD(P)H oxidase. Circulation 109:227-233. doi:10.1161/01.CIR. 0000105680.92873.70
2. Alam S, Li H, Margariti A, Martin D, Zampetaki A, Habi O, Cockerill G, Hu Y, Xu Q, Zeng L (2011) Galectin-9 protein expression in endothelial cells is positively regulated by histone deacetylase 3. J Biol Chem 286:44211-44217. doi:10.1074/jbc. M111.242289
3. Ballestar E (2011) An introduction to epigenetics. Adv Exp Med Biol 711:1-11
4. Bedard K, Krause KH (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87:245-313. doi:10.1152/physrev.00044.2005
5. Blackwell L, Norris J, Suto CM, Janzen WP (2008) The use of diversity profiling to characterize chemical modulators of the histone deacetylases. Life Sci 82:1050-1058. doi:10.1016/j.lfs. 2008.03.004
6. Brandes RP, Kreuzer J (2005) Vascular NADPH oxidases: molecular mechanisms of activation. Cardiovasc Res 65:16-27. doi:10.1016/j.cardiores.2004. 08.007
7. Diebold I, Petry A, Hess J, Gorlach A (2010) The NADPH oxidase subunit NOX4 is a new target gene of the hypoxia-inducible factor-1. Mol Biol Cell 21:2087-2096. doi:10.1091/mbc.E09-12-1003
8. Dokmanovic M, Clarke C, Marks PA (2007) Histone deacetylase inhibitors: overview and perspectives. Mol Cancer Res 5:981-989. doi:10.1158/1541-7786.MCR- 07-0324
9. Drummond GR, Selemidis S, Griendling KK, Sobey CG (2011) Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nat Rev Drug Discov 10:453-471. doi: 10.1038/nrd3403
10. Edgell CJ, McDonald CC, Graham JB (1983) Permanent cell line expressing human factor VIII-related antigen established by hybridization. Proc Natl Acad Sci USA 80:3734-3737
11. Eferl R, Wagner EF (2003) AP-1: a double-edged sword in tumorigenesis. Nat Rev Cancer 3:859-868. doi:10.1038/nrc1209
12. Ellmark SH, Dusting GJ, Fui MN, Guzzo-Pernell N, Drummond GR (2005) The contribution of Nox4 to NADPH oxidase activity in mouse vascular smooth muscle. Cardiovasc Res 65:495-504. doi:10.1016/j.cardiores.2004.10.026
13. Farre D, Roset R, Huerta M, Adsuara JE, Rosello L, Alba MM, Messeguer X (2003) Identification of patterns in biological sequences at the ALGGEN server: PROMO and MALGEN. Nucleic Acids Res 31:3651-3653
14. Forstermann U (2008) Oxidative stress in vascular disease: causes, defense mechanisms and potential therapies. Nat Clin Pract Cardiovasc Med 5:338-349. doi:10.1038/ncpcardio1211
15. Fu Y, Zhang Y, Wang Z, Wang L, Wei X, Zhang B, Wen Z, Fang H, Pang Q, Yi F (2010) Regulation of NADPH oxidase activity is associated with miRNA-25-mediated NOX4 expression in experimental diabetic nephropathy. Am J Nephrol 32:581-589. doi:10.1159/000322105
16. Fuks F, Burgers WA, Godin N, Kasai M, Kouzarides T (2001) Dnmt3a binds deacetylases and is recruited by a sequence-specific repressor to silence transcription. EMBO J 20:2536-2544. doi:10.1093/emboj/20.10.2536
17. Goettsch C, Goettsch W, Brux M, Haschke C, Brunssen C, Muller G, Bornstein SR, Duerrschmidt N, Wagner AH, Morawietz H (2011) Arterial flow reduces oxidative stress via an antioxidant response element and Oct-1 binding site within the NADPH oxidase 4 promoter in endothelial cells. Basic Res Cardiol 106:551-561. doi:10.1007/s00395-011-0170-3
18. Granger A, Abdullah I, Huebner F, Stout A, Wang T, Huebner T, Epstein JA, Gruber PJ (2008) Histone deacetylase inhibition reduces myocardial ischemia-reperfusion injury in mice. FASEB journal : official publication of the Federation of American Societies for Experimental Biology 22:3549-3560. doi:10.1096/ fj.08-108548 19. Griendling KK (2004) Novel NAD(P)H oxidases in the cardiovascular system. Heart 90:491-493
19. Guzik TJ, Sadowski J, Guzik B, Jopek A, Kapelak B, Przybylowski P, Wierzbicki K, Korbut R, Harrison DG, Channon KM (2006) Coronary artery superoxide production and nox isoform expression in human coronary artery disease. Arterioscler Thromb Vasc Biol 26:333-339. doi:10.1161/01.ATV. 0000196651.64776.51
20. Harrison D, Griendling KK, Landmesser U, Hornig B, Drexler H (2003) Role of oxidative stress in atherosclerosis. Am J Cardiol 91:7A-11A
21. Hwang J, Kleinhenz DJ, Lassegue B, Griendling KK, Dikalov S, Hart CM (2005) Peroxisome proliferator-activated receptorgamma ligands regulate endothelial membrane superoxide production. Am J Physiol Cell Physiol 288:C899-C905. doi: 10.1152/ajpcell.00474.2004
22. Im YB, Jee MK, Jung JS, Choi JI, Jang JH, Kang SK (2012) miR23b ameliorates neuropathic pain in spinal cord by silencing NADPH oxidase 4. Antioxid Redox Signal 16:1046-1060. doi: 10.1089/ars.2011.4224
23. Jung SB, Kim CS, Naqvi A, Yamamori T, Mattagajasingh I, Hoffman TA, Cole MP, Kumar A, Dericco JS, Jeon BH, Irani K (2010) Histone deacetylase 3 antagonizes aspirin-stimulated endothelial nitric oxide production by reversing aspirin-induced lysine acetylation of endothelial nitric oxide synthase. Circ Res 107:877-887. doi:10.1161/CIRCRESAHA.110.222968
24. Katsuyama M, Hirai H, Iwata K, Ibi M, Matsuno K, Matsumoto M, Yabe-Nishimura C (2011) Sp3 transcription factor is crucial for transcriptional activation of the human NOX4 gene. FEBS J 278:964-972. doi:10.1111/j.1742-4658. 2011.08018.x
25. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D (2002) The human genome browser at UCSC. Genome Res 12:996-1006. doi:10.1101/gr.229102 Article published online before print in May 2002
26. Klose RJ, Bird AP (2006) Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci 31:89-97. doi:10.1016/ j.tibs.2005.12.008
27. Kroller-Schon S, Schulz E, Wenzel P, Kleschyov AL, Hortmann M, Torzewski M, Oelze M, Renne T, Daiber A, Munzel T (2011) Differential effects of heart rate reduction with ivabradine in two models of endothelial dysfunction and oxidative stress. Basic Res Cardiol 106:1147-1158. doi:10.1007/s00395-011-0227- 0233
28. LaBonte MJ, Wilson PM, Fazzone W, Groshen S, Lenz HJ, Ladner RD (2009) DNA microarray profiling of genes differentially regulated by the histone deacetylase inhibitors vorinostat and LBH589 in colon cancer cell lines. BMC Med Genomics 2:67. doi:10.1186/1755-8794-2-67
29. Lassegue B, Clempus RE (2003) Vascular NAD(P)H oxidases: specific features, expression, and regulation. Am J Physiol Regul Integr Comp Physiol 285:R277-R297. doi:10.1152/ajpregu. 00758.2002
30. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402-408. doi:10.1006/meth. 2001.1262
31. Manea A, Tanase LI, Raicu M, Simionescu M (2010) Jak/STAT signaling pathway regulates nox1 and nox4-based NADPH oxidase in human aortic smooth muscle cells. Arterioscler Thromb Vasc Biol 30:105-112. doi:10.1161/ATVBAHA.109. 193896
32. Manea A, Tanase LI, Raicu M, Simionescu M (2010) Transcriptional regulation of NADPH oxidase isoforms, Nox1 and Nox4, by nuclear factor-kappaB in human aortic smooth muscle cells. Biochem Biophys Res Commun 396:901-907. doi:10.1016/ j.bbrc.2010.05.019
33. Matouk CC, Marsden PA (2008) Epigenetic regulation of vascular endothelial gene expression. Circ Res 102:873-887. doi: 10.1161/CIRCRESAHA.107. 171025
34. Messeguer X, Escudero R, Farre D, Nunez O, Martinez J, Alba MM (2002) PROMO: detection of known transcription regulatory elements using species-tailored searches. Bioinformatics 18: 333-334
35. Miyano K, Ueno N, Takeya R, Sumimoto H (2006) Direct involvement of the small GTPase Rac in activation of the superoxide-producing NADPH oxidase Nox1. J Biol Chem 281:21857-21868. doi:10.1074/jbc.M513665200
36. Morawietz H (2011) Endothelial NADPH oxidases: friends or foes? Basic Res Cardiol 106:521-525. doi:10.1007/s00395-011-0188-6
37. Murdoch CE, Alom-Ruiz SP, Wang MS, Zhang M, Walker S, Yu B, Brewer A, Shah AM (2011) Role of endothelial Nox2 NADPH oxidase in angiotensin II-induced hypertension and vasomotor dysfunction. Basic Res Cardiol 106:527-538. doi:10.1007/ s00395-011-0179-7
38. Park Y, Yang JY, Zhang HR, Chen XN, Zhang CH (2011) Effect of PAR2 in regulating TNF-alpha and NAD(P)H oxidase in coronary arterioles in type 2 diabetic mice. Basic Res Cardiol 106:111-123. doi:10.1007/s00395-010-0129-9
39. Pendyala S, Moitra J, Kalari S, Kleeberger SR, Zhao Y, Reddy SP, Garcia JG, Natarajan V (2011) Nrf2 regulates hyperoxiainduced Nox4 expression in human lung endothelium: identification of functional antioxidant response elements on the Nox4 promoter. Free Radic Biol Med 50:1749-1759. doi:10.1016/ j.freeradbiomed.2011.03.022
40. Rossig L, Li H, Fisslthaler B, Urbich C, Fleming I, Forstermann U, Zeiher AM, Dimmeler S (2002) Inhibitors of histone deacetylation downregulate the expression of endothelial nitric oxide synthase and compromise endothelial cell function in vasorelaxation and angiogenesis. Circ Res 91:837-844
41. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386
42. Ruf N, Bahring S, Galetzka D, Pliushch G, Luft FC, Nurnberg P, Haaf T, Kelsey G, Zechner U (2007) Sequence-based bioinformatic prediction and QUASEP identify genomic imprinting of the KCNK9 potassium channel gene in mouse and human. Hum Mol Genet 16:2591-2599. doi:10.1093/hmg/ddm216
43. Sirker A, Zhang M, Shah AM (2011) NADPH oxidases in cardiovascular disease: insights from in vivo models and clinical studies. Basic Res Cardiol 106:735-747. doi:10.1007/s00395-011-0190-z
44. Smith CL (2008) A shifting paradigm: histone deacetylases and transcriptional activation. BioEssays 30:15-24. doi:10.1002/ bies.20687
45. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403:41-45. doi:10.1038/47412
46. Sturrock A, Cahill B, Norman K, Huecksteadt TP, Hill K, Sanders K, Karwande SV, Stringham JC, Bull DA, Gleich M, Kennedy TP, Hoidal JR (2006) Transforming growth factor-beta1 induces Nox4 NAD(P)H oxidase and reactive oxygen speciesdependent proliferation in human pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 290:L661-L673. doi:10.1152/ajplung. 00269.2005
47. Takac I, Schroder K, Zhang L, Lardy B, Anilkumar N, Lambeth JD, Shah AM, Morel F, Brandes RP (2011) The E-loop is involved in hydrogen peroxide formation by the NADPH oxidase Nox4. J Biol Chem 286:13304-13313. doi:10.1074/jbc.M110. 192138
48. Vasa-Nicotera M, Chen H, Tucci P, Yang AL, Saintigny G, Menghini R, Mahe C, Agostini M, Knight RA, Melino G, Federici M (2011) miR-146a is modulated in human endothelial cell with aging. Atherosclerosis 217:326-330. doi:10.1016/ j.atherosclerosis.2011.03.034
49. Xia N, Daiber A, Habermeier A, Closs EI, Thum T, Spanier G, Lu Q, Oelze M, Torzewski M, Lackner KJ, Munzel T, Forstermann U, Li H (2010) Resveratrol reverses endothelial nitricoxide synthase uncoupling in apolipoprotein E knockout mice. J Pharmacol Exp Ther 335:149-154. doi:10.1124/jpet.110. 168724
50. Xu H, Czerwinski P, Hortmann M, Sohn HY, Forstermann U, Li H (2008) Protein kinase C alpha promotes angiogenic activity of human endothelial cells via induction of vascular endothelial growth factor. Cardiovasc Res 78:349-355. doi:10.1093/cvr/cvm085
51. Xu H, Goettsch C, Xia N, Horke S, Morawietz H, Forstermann U, Li H (2008) Differential roles of PKCalpha and PKCepsilon in controlling the gene expression of Nox4 in human endothelial cells. Free Radic Biol Med 44:1656-1667. doi:10.1016/ j.freeradbiomed.2008.01.023
52. Zampetaki A, Zeng L, Margariti A, Xiao Q, Li H, Zhang Z, Pepe AE, Wang G, Habi O, deFalco E, Cockerill G, Mason JC, Hu Y, Xu Q (2010) Histone deacetylase 3 is critical in endothelial survival and atherosclerosis development in response to disturbed flow. Circulation 121:132-142. doi:10.1161/CIRCULATIONAHA. 109. 890491
53. Zhang L, Sheppard OR, Shah AM, Brewer AC (2008) Positive regulation of the NADPH oxidase NOX4 promoter in vascular smooth muscle cells by E2F. Free Radic Biol Med 45:679-685. doi:10.1016/j.freeradbiomed.2008.05.019
54. Zhang YS, He L, Liu B, Li NS, Luo XJ, Hu CP, Ma QL, Zhang GG, Li YJ, Peng J (2012) A novel pathway of NADPH oxidase/ vascular peroxidase 1 in mediating oxidative injury following ischemia-reperfusion. Basic Res Cardiol 107:266. doi:10.1007/ s00395-012-0266-4