Protein nitration promotes inducible nitric oxide synthase transcription mediated by NF-κB in high glucose-stimulated human lens epithelial cells

Molecular and Cellular Endocrinology

Volumn 370, Issue 1-2, 2013, Pages 78-86

  Li, Yanning ^a   Liu, Demei ^a   Liu, Yuan ^a   Li, En ^a   Wang, Hui ^a   Liu, Kun ^a   Qi, Jinsheng ^a  

^a HEBEI MEDICAL UNIVERSITY   (China)

Author keywords

Inducible nitric oxide synthase; NF B; P300; Protein nitration; Transcriptional control

Indexed keywords

E1A ASSOCIATED P300 PROTEIN; GLUCOSE; INDUCIBLE NITRIC OXIDE SYNTHASE; PEROXYNITRITE; TRANSCRIPTION FACTOR RELA;

ARTICLE; BINDING SITE; CELL STIMULATION; CONTROLLED STUDY; GENE ACTIVATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HYPERGLYCEMIA; INDUCIBLE NITRIC OXIDE SYNTHASE GENE; LENS EPITHELIUM; NUCLEOTIDE SEQUENCE; PREDICTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN NITRATION; PROTEIN PROTEIN INTERACTION; RNA SEQUENCE;

BINDING SITES; CELL LINE; DIABETES COMPLICATIONS; EPITHELIAL CELLS; GLUCOSE; HUMANS; LENS, CRYSTALLINE; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; P300-CBP TRANSCRIPTION FACTORS; PEROXYNITROUS ACID; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 84876394623     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2013.02.015     Document Type: Article

References (41)

1. Ashall L., Horton C.A., Nelson D.E., Paszek P., Harper C.V., Sillitoe K., Ryan S., Spiller D.G., Unitt J.F., Broomhead D.S., Kell D.B., Rand D.A., Sée V., White M.R. Pulsatile stimulation determines timing and specificity of NF-kappaB-dependent transcription. Science 2009, 324:242-246.
2. Azevedo-Martins A.K., Lortz S., Lenzen S., Curi R., Eizirik D.L., Tiedge M. Improvement of the mitochondrial antioxidant defense status prevents cytokine-induced nuclear factor-kappaB activation in insulin-producing cells. Diabetes 2003, 52:93-101.
3. Bar-Shai M., Reznick A.Z. Peroxynitrite induces an alternative NF-kappaB activation pathway in L8 rat myoblasts. Antioxid. Redox Signal. 2006, 8:639-652.
4. Chew J., Biswas S., Shreeram S., Humaidi M., Wong E.T., Dhillion M.K., Teo H., Hazra A., Fang C.C., López-Collazo E., Bulavin D.V., Tergaonkar V. WIP1 phosphatase is a negative regulator of NF-kappaB signalling. Nat. Cell Biol. 2009, 11:659-666.
5. Cooke C.L., Davidge S.T. Peroxynitrite increases iNOS through NF-kappaB and decreases prostacyclin synthase in endothelial cells. Am. J. Physiol. Cell Physiol. 2002, 282:C395-C402.
6. Das C., Lucia M.S., Hansen K.C., Tyler J.K. CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature 2009, 459:113-117.
7. Deng W.G., Wu K.K. Regulation of inducible nitric oxide synthase expression by p300 and p50 acetylation. J. Immunol. 2003, 171:6581-6588.
8. DeRubertis F.R., Craven P.A., Melhem M.F., Salah E.M. Attenuation of renal injury in db/db mice overexpressing superoxide dismutase: evidence for reduced superoxide-nitric oxide interaction. Diabetes 2004, 53:762-768.
9. Duplain H., Sartori C., Dessen P., Jayet P.Y., Schwab M., Bloch J., Nicod P., Scherrer U. Stimulation of peroxynitrite catalysis improves insulin sensitivity in high fat diet-fed mice. J. Physiol. 2008, 586:4011-4016.
10. El-Osta A., Brasacchio D., Yao D., Pocai A., Jones P.L., Roeder R.G., Cooper M.E., Brownlee M. Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia. J. Exp. Med. 2008, 205:2409-2417.
11. Feng X., Guo Z., Nourbakhsh M., Hauser H., Ganster R., Shao L., Geller D.A. Identification of a negative response element in the human inducible nitric-oxide synthase (hiNOS) promoter: the role of NF-kappa B-repressing factor (NRF) in basal repression of the hiNOS gene. Proc. Natl. Acad. Sci. USA 2002, 99:14212-14217.
12. Fontana M., Pinnen F., Lucente G., Pecci L. Prevention of peroxynitrite-dependent damage by carnosine and related sulphonamido pseudodipeptides. Cell. Mol. Life Sci. 2002, 59:546-551.
13. Ganster R.W., Taylor B.S., Shao L., Geller D.A. Complex regulation of human inducible nitric oxide synthase gene transcription by Stat 1 and NF-kappa B. Proc. Natl. Acad. Sci. USA 2001, 98:8638-8643.
14. Gautier M., Zhang H., Fearon I.M. Peroxynitrite formation mediates LPC-induced augmentation of cardiac late sodium currents. J. Mol. Cell. Cardiol. 2008, 44:241-251.
15. Granja A.G., Sabina P., Salas M.L., Fresno M., Revilla Y. Regulation of inducible nitric oxide synthase expression by viral A238L-mediated inhibition of p65/RelA acetylation and p300 transactivation. J. Virol. 2006, 80:10487-10496.
16. Guo H., Mi Z., Kuo P.C. Characterization of short range DNA looping in endotoxin-mediated transcription of the murine inducible nitric-oxide synthase (iNOS) gene. J. Biol. Chem. 2008, 283:25209-25217.
17. Jiang Q., Liu P., Wu X., Liu W., Shen X., Lan T., Xu S., Peng J., Xie X., Huang H. Berberine attenuates lipopolysaccharide-induced extracelluar matrix accumulation and inflammation in rat mesangial cells: involvement of NF-κB signaling pathway. Mol. Cell. Endocrinol. 2011, 331:34-40.
18. Karamouzis M.V., Konstantinopoulos P.A., Papavassiliou A.G. Roles of CREB-binding protein (CBP)/p300 in respiratory epithelium tumorigenesis. Cell Res. 2007, 17:324-332.
19. Kaur H., Chen S., Xin X., Chiu J., Khan Z.A., Chakrabarti S. Diabetes-induced extracellular matrix protein expression is mediated by transcription coactivator p300. Diabetes 2006, 55:3104-3111.
20. Kohr M.J., Wang H., Wheeler D.G., Velayutham M., Zweier J.L., Ziolo M.T. Targeting of phospholamban by peroxynitrite decreases beta-adrenergic stimulation in cardiomyocytes. Cardiovasc. Res. 2008, 77:353-361.
21. Kubo E., Singh D.P., Akagi Y. Gene expression profiling of diabetic and galactosaemic cataractous rat lens by microarray analysis. Diabetologia 2005, 48:790-798.
22. Levrand S., Pesse B., Feihl F., Waeber B., Pacher P., Rolli J., Schaller M.D., Liaudet L. Peroxynitrite is a potent inhibitor of NF-{kappa}B activation triggered by inflammatory stimuli in cardiac and endothelial cell lines. J. Biol. Chem. 2005, 280:34878-34887.
23. Li Y., Qi J., Liu K., Li B., Wang H., Jia J. Peroxynitrite-induced nitration of cyclooxygenase-2 and inducible nitric oxide synthase promotes their binding in diabetic angiopathy. Mol. Med. 2010, 16:335-342.
24. Nambu H., Kubo E., Takamura Y., Tsuzuki S., Tamura M., Akagi Y. Attenuation of aldose reductase gene suppresses high-glucose-induced apoptosis and oxidative stress in rat lens epithelial cells. Diabetes Res. Clin. Pract. 2008, 82:18-24.
25. Nelson J.D., Denisenko O., Bomsztyk K. Protocol for the fast chromatin immunoprecipitation (ChIP) method. Nat. Protoc. 2006, 1:179-185.
26. Niedick I., Froese N., Oumard A., Mueller P.P., Nourbakhsh M., Hauser H., Köster M. Nucleolar localization and mobility analysis of the NF-kappaB repressing factor NRF. J. Cell. Sci. 2004, 117:3447-3458.
27. Osada H., Yoshitake Y., Ikeda T., Ishigaki Y., Takata T., Tomosugi N., Sasaki H., Yonekura H. Ultraviolet B-induced expression of amphiregulin and growth differentiation factor 15 in human lens epithelial cells. Mol. Vis. 2011, 17:159-169.
28. Park S.W., Huq M.D., Hu X., Wei L.N. Tyrosine nitration on p65: a novel mechanism to rapidly inactivate nuclear factor-kappaB. Mol. Cell Proteomics 2005, 4:300-309.
29. Porasuphatana S., Weaver J., Rosen G.M. Inducible nitric oxide synthase catalyzes ethanol oxidation to alpha-hydroxyethyl radical and acetaldehyde. Toxicology 2006, 223:167-174.
30. Randazzo J., Zhang P., Makita J., Blessing K., Kador P.F. Orally active multi-functional antioxidants delay cataract formation in streptozotocin (type 1) diabetic and gamma-irradiated rats. PLoS ONE 2011, 6:e18980.
31. Romagnoli M., Gomez-Cabrera M.C., Perrelli M.G., Biasi F., Pallardo F.V., Sastre J., Poli G., Vina J. Xanthine oxidase-induced oxidative stress causes activation of NF-kappaB and inflammation in the liver of type I diabetic rats. Free Radic. Biol. Med. 2010, 49:171-177.
32. Ruberte J., Ayuso E., Navarro M., Carretero A., Nacher V., Haurigot V., George M., Llombart C., Casellas A., Costa C., Bosch A., Bosch F. Increased ocular levels of IGF-1 in transgenic mice lead to diabetes-like eye disease. J. Clin. Invest. 2004, 113:1149-1157.
33. Samikkannu T., Thomas J.J., Bhat G.J., Wittman V., Thekkumkara T.J. Acute effect of high glucose on long-term cell growth: a role for transient glucose increase in proximal tubule cell injury. Am. J. Physiol. Renal Physiol. 2006, 291:F162-F175.
34. Schildknecht S., Daiber A., Ghisla S., Cohen R.A., Bachschmid M.M. Acetaminophen inhibits prostanoid synthesis by scavenging the PGHS-activator peroxynitrite. FASEB J. 2008, 22:215-224.
35. Tao L., Jiao X., Gao E., Lau W.B., Yuan Y., Lopez B., Christopher T., RamachandraRao S.P., Williams W., Southan G., Sharma K., Koch W., Ma X.L. Nitrative inactivation of thioredoxin-1 and its role in postischemic myocardial apoptosis. Circulation 2006, 114:1395-1402.
36. Tay S., Hughey J.J., Lee T.K., Lipniacki T., Quake S.R., Covert M.W. Single-cell NF-kappaB dynamics reveal digital activation and analogue information processing. Nature 2010, 466:267-271.
37. Taylor B.S., de Vera M.E., Ganster R.W., Wang Q., Shapiro R.A., Morris S.M., Billiar T.R., Geller D.A. Multiple NF-kappaB enhancer elements regulate cytokine induction of the human inducible nitric oxide synthase gene. J. Biol. Chem. 1998, 273:15148-15156.
38. Teng X., Zhang H., Snead C., Catravas J.D. Molecular mechanisms of iNOS induction by IL-1 beta and IFN-gamma in rat aortic smooth muscle cells. Am. J. Physiol. Cell Physiol. 2002, 282:C144-C152.
39. Vareniuk I., Pavlov I.A., Obrosova I.G. Inducible nitric oxide synthase gene deficiency counteracts multiple manifestations of peripheral neuropathy in a streptozotocin-induced mouse model of diabetes. Diabetologia 2008, 51:2126-2133.
40. Wu F., Wilson J.X. Peroxynitrite-dependent activation of protein phosphatase type 2A mediates microvascular endothelial barrier dysfunction. Cardiovasc. Res. 2009, 81:38-45.
41. Zhang Z., Yuan W., Sun L., Szeto F.L., Wong K.E., Li X., Kong J., Li Y.C. 1,25-Dihydroxyvitamin D3 targeting of NF-kappaB suppresses high glucose-induced MCP-1 expression in mesangial cells. Kidney Int. 2007, 72:193-201.