CpG methylation attenuates Sp1 and Sp3 binding to the human extracellular superoxide dismutase promoter and regulates its cell-specific expression

Free Radical Biology and Medicine

Volumn 48, Issue 7, 2010, Pages 895-904

  Zelko, Igor N ^a   Mueller, Michael R ^a   Folz, Rodney J ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

Chromatin organization; DNA methylation; Epigenetic regulation; Free radicals; Lung; Methyl binding proteins; Reactive oxygen species; Transcription

Indexed keywords

AZACITIDINE; CYTOSINE; DNA METHYLTRANSFERASE; METHYL CPG BINDING PROTEIN 2; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR SP1; TRANSCRIPTION FACTOR SP3;

ANIMAL CELL; ARTICLE; ATTENUATION; BINDING KINETICS; CHROMATIN STRUCTURE; CONTROLLED STUDY; CPG ISLAND; DEMETHYLATION; DNA METHYLATION; EMBRYO; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REPRESSION; EPIGENETICS; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG ALVEOLUS CELL; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

ANIMALS; CELL LINE, TUMOR; CHROMATIN ASSEMBLY AND DISASSEMBLY; CPG ISLANDS; DNA METHYLATION; DROSOPHILA; EPIGENESIS, GENETIC; EPITHELIAL CELLS; EXTRACELLULAR SPACE; HUMANS; LUNG; METHYL-CPG-BINDING PROTEIN 2; METHYLTRANSFERASES; ORGAN SPECIFICITY; OXIDATION-REDUCTION; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SP1 TRANSCRIPTION FACTOR; SP3 TRANSCRIPTION FACTOR; SUPEROXIDE DISMUTASE;

HEXAPODA; MAMMALIA;

EID: 77249099223     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.01.007     Document Type: Article

References (39)

1. Zelko I.N., Mariani T.J., and Folz R.J. Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic. Biol. Med. 33 (2002) 337-349
2. Noor R., Mittal S., and Iqbal J. Superoxide dismutase-applications and relevance to human diseases. Med. Sci. Monit. 8 (2002) RA210-RA215
3. Fattman C.L., Schaefer L.M., and Oury T.D. Extracellular superoxide dismutase in biology and medicine. Free Radic. Biol. Med. 35 (2003) 236-256
4. Folz R.J., Abushamaa A.M., and Suliman H.B. Extracellular superoxide dismutase in the airways of transgenic mice reduces inflammation and attenuates lung toxicity following hyperoxia. J. Clin. Invest. 103 (1999) 1055-1066
5. Ahmed M.N., Suliman H.B., Folz R.J., Nozik-Grayck E., Golson M.L., Mason S.N., and Auten R.L. Extracellular superoxide dismutase protects lung development in hyperoxia-exposed newborn mice. Am. J. Respir. Crit. Care Med. 167 (2003) 400-405
6. Rabbani Z.N., Anscher M.S., Folz R.J., Archer E., Huang H., Chen L., Golson M.L., Samulski T.S., Dewhirst M.W., and Vujaskovic Z. Overexpression of extracellular superoxide dismutase reduces acute radiation induced lung toxicity. BMC Cancer 5 (2005) 59
7. Bowler R.P., Nicks M., Warnick K., and Crapo J.D. Role of extracellular superoxide dismutase in bleomycin-induced pulmonary fibrosis. Am. J. Physiol. Lung Cell Mol. Physiol. 282 (2002) L719-L726
8. Fattman C.L., Chang L.Y., Termin T.A., Petersen L., Enghild J.J., and Oury T.D. Enhanced bleomycin-induced pulmonary damage in mice lacking extracellular superoxide dismutase. Free Radic. Biol. Med. 35 (2003) 763-771
9. Gongora M.C., Lob H.E., Landmesser U., Guzik T.J., Martin W.D., Ozumi K., Wall S.M., Wilson D.S., Murthy N., Gravanis M., Fukai T., and Harrison D.G. Loss of extracellular superoxide dismutase leads to acute lung damage in the presence of ambient air: a potential mechanism underlying adult respiratory distress syndrome. Am. J. Pathol. 173 (2008) 915-926
10. Zelko I.N., and Folz R.J. Sp1 and Sp3 transcription factors mediate trichostatin A-induced and basal expression of extracellular superoxide dismutase. Free Radic. Biol. Med. 37 (2004) 1256-1271
11. Zelko I.N., and Folz R.J. Myeloid zinc finger (MZF)-like, Kruppel-like and Ets families of transcription factors determine the cell-specific expression of mouse extracellular superoxide dismutase. Biochem. J. 369 (2003) 375-386
12. Zelko I.N., Mueller M.R., and Folz R.J. Transcription factors Sp1 and Sp3 regulate expression of human extracellular superoxide dismutase in lung fibroblasts. Am. J. Respir. Cell Mol. Biol. 39 (2008) 243-251
13. Ordway J.M., and Curran T. Methylation matters: modeling a manageable genome. Cell Growth Differ. 13 (2002) 149-162
14. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 16 (2002) 6-21
15. Luoma J.S., Stralin P., Marklund S.L., Hiltunen T.P., Sarkioja T., and Yla-Herttuala S. Expression of extracellular SOD and iNOS in macrophages and smooth muscle cells in human and rabbit atherosclerotic lesions: colocalization with epitopes characteristic of oxidized LDL and peroxynitrite-modified proteins. Arterioscler. Thromb. Vasc. Biol. 18 (1998) 157-167
16. Laukkanen M.O., Mannermaa S., Hiltunen M.O., Aittomaki S., Airenne K., Janne J., and Yla-Herttuala S. Local hypomethylation in atherosclerosis found in rabbit EC-SOD gene. Arterioscler. Thromb. Vasc. Biol. 19 (1999) 2171-2178
17. Li L.C., and Dahiya R. MethPrimer: designing primers for methylation PCRs. Bioinformatics 18 (2002) 1427-1431
18. Zhu B., Chen Z., Cheng X., and Wu Y. Induction of TRAG-3 expression in A549 lung adenocarcinoma cell line by 5-aza-2′ deoxyazacytidine. Lung Cancer 38 (2002) 321-322
19. Bakker J., Lin X., and Nelson W.G. Methyl-CpG binding domain protein 2 represses transcription from hypermethylated Pi-class glutathione S-transferase gene promoters in hepatocellular carcinoma cells. J. Biol. Chem. 277 (2002) 22573-22580
20. Tada Y., Brena R.M., Hackanson B., Morrison C., Otterson G.A., and Plass C. Epigenetic modulation of tumor suppressor CCAAT/enhancer binding protein alpha activity in lung cancer. J. Natl. Cancer Inst. 98 (2006) 396-406
21. Bouchard C., Dittrich O., Kiermaier A., Dohmann K., Menkel A., Eilers M., and Luscher B. Regulation of cyclin D2 gene expression by the Myc/Max/Mad network: Myc-dependent TRRAP recruitment and histone acetylation at the cyclin D2 promoter. Genes Dev. 15 (2001) 2042-2047
22. Oury T.D., Chang L.Y., Marklund S.L., Day B.J., and Crapo J.D. Immunocytochemical localization of extracellular superoxide dismutase in human lung. Lab. Invest. 70 (1994) 889-898
23. Su W.Y., Folz R., Chen J.S., Crapo J.D., and Chang L.Y. Extracellular superoxide dismutase mRNA expressions in the human lung by in situ hybridization. Am. J. Respir. Cell Mol. Biol. 16 (1997) 162-170
24. Zelko I.N., Mueller M.R., and Folz R.J. Transcription factors sp1 and sp3 regulate expression of human extracellular superoxide dismutase in lung fibroblasts. Am. J. Respir. Cell Mol. Biol. 39 (2008) 243-251
25. Bouwman P., and Philipsen S. Regulation of the activity of Sp1-related transcription factors. Mol. Cell. Endocrinol. 195 (2002) 27-38
26. Marin M., Karis A., Visser P., Grosveld F., and Philipsen S. Transcription factor Sp1 is essential for early embryonic development but dispensable for cell growth and differentiation. Cell 89 (1997) 619-628
27. Bouwman P., Gollner H., Elsasser H.P., Eckhoff G., Karis A., Grosveld F., Philipsen S., and Suske G. Transcription factor Sp3 is essential for post-natal survival and late tooth development. EMBO J. 19 (2000) 655-661
28. Kennett S.B., Udvadia A.J., and Horowitz J.M. Sp3 encodes multiple proteins that differ in their capacity to stimulate or repress transcription. Nucleic Acids Res. 25 (1997) 3110-3117
29. Majello B., De Luca P., and Lania L. Sp3 is a bifunctional transcription regulator with modular independent activation and repression domains. J. Biol. Chem. 272 (1997) 4021-4026
30. Dennig J., Beato M., and Suske G. An inhibitor domain in Sp3 regulates its glutamine-rich activation domains. EMBO J. 15 (1996) 5659-5667
31. Chan Y., Fish J.E., D'Abreo C., Lin S., Robb G.B., Teichert A.M., Karantzoulis-Fegaras F., Keightley A., Steer B.M., and Marsden P.A. The cell-specific expression of endothelial nitric-oxide synthase: a role for DNA methylation. J. Biol. Chem. 279 (2004) 35087-35100
32. Lee L.T., Tan-Un K.C., Pang R.T., Lam D.T., and Chow B.K. Regulation of the human secretin gene is controlled by the combined effects of CpG methylation, Sp1/Sp3 ratio, and the E-box element. Mol. Endocrinol. 18 (2004) 1740-1755
33. Pang R.T., Lee L.T., Ng S.S., Yung W.H., and Chow B.K. CpG methylation and transcription factors Sp1 and Sp3 regulate the expression of the human secretin receptor gene. Mol. Endocrinol. 18 (2004) 471-483
34. Zhu W.G., Srinivasan K., Dai Z., Duan W., Druhan L.J., Ding H., Yee L., Villalona-Calero M.A., Plass C., and Otterson G.A. Methylation of adjacent CpG sites affects Sp1/Sp3 binding and activity in the p21(Cip1) promoter. Mol. Cell. Biol. 23 (2003) 4056-4065
35. Jones P.L., Veenstra G.J., Wade P.A., Vermaak D., Kass S.U., Landsberger N., Strouboulis J., and Wolffe A.P. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat. Genet. 19 (1998) 187-191
36. Ng H.H., Zhang Y., Hendrich B., Johnson C.A., Turner B.M., Erdjument-Bromage H., Tempst P., Reinberg D., and Bird A. MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nat. Genet. 23 (1999) 58-61
37. Nan X., Ng H.H., Johnson C.A., Laherty C.D., Turner B.M., Eisenman R.N., and Bird A. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393 (1998) 386-389
38. Chahrour M., Jung S.Y., Shaw C., Zhou X., Wong S.T., Qin J., and Zoghbi H.Y. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320 (2008) 1224-1229
39. Yasui D.H., Peddada S., Bieda M.C., Vallero R.O., Hogart A., Nagarajan R.P., Thatcher K.N., Farnham P.J., and Lasalle J.M. Integrated epigenomic analyses of neuronal MeCP2 reveal a role for long-range interaction with active genes. Proc. Natl. Acad. Sci. USA 104 (2007) 19416-19421