Zinc regulates iNOS-derived nitric oxide formation in endothelial cells

Redox Biology

Volumn 2, Issue 1, 2014, Pages 945-954

  Cortese Krott, Miriam M ^a   Kulakov, Larissa ^a   Opländer, Christian ^a   Kolb Bachofen, Victoria ^a   Kröncke, Klaus D ^a   Suschek, Christoph V ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Endothelial cells; Gene expression; Inducible nitric oxide synthase; NF B; Zinc

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; ZINC; CYCLOOXYGENASE 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; MESSENGER RNA; PROSTAGLANDIN SYNTHASE; ZINC ION;

ANIMAL; AORTA; BIOSYNTHESIS; CYTOLOGY; DRUG EFFECTS; ENDOTHELIUM CELL; ENZYMOLOGY; METABOLISM; RAT; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL ISOLATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIAL DYSFUNCTION; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC TRANSCRIPTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN STABILITY; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ZINC HOMEOSTASIS;

ANIMALS; AORTA; ENDOTHELIAL CELLS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; RATS; ZINC;

EID: 84906057987     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2014.06.011     Document Type: Article

References (61)

1. Vita J.A. Endothelial function. Circulation 2011, 124:e906-e912. http://www.ncbi.nlm.nih.gov/pubmed/22184047, 10.1016/j.redox.2014.06.011.
2. Moncada S., Palmer R.M.J., Higgs E.A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacological Reviews 1991, 43:109-142. http://www.ncbi.nlm.nih.gov/pubmed/1852778.
3. Nathan C. Points of control in inflammation. Nature 2002, 420:846-852. http://www.ncbi.nlm.nih.gov/pubmed/12490957, 10.1016/j.redox.2014.06.011.
4. Kleinert H., Schwarz P.M., Förstermann U. Regulation of the expression of inducible nitric oxide synthase. Biological Chemistry 2003, 384:1343-1364. http://www.ncbi.nlm.nih.gov/pubmed/14669979, 10.1016/j.redox.2014.06.011.
5. Förstermann U., Sessa W.C. Nitric oxide synthases: regulation and function. European Heart Journal 2012, 33:829-837. http://www.ncbi.nlm.nih.gov/pubmed/21890489, 10.1016/j.redox.2014.06.011.
6. Villanueva C., Giulivi C. Subcellular and cellular locations of nitric oxide synthase isoforms as determinants of health and disease. Free Radical Biology & Medicine 2010, 49:307-316. http://www.ncbi.nlm.nih.gov/pubmed/20388537, 10.1016/j.redox.2014.06.011.
7. Hill B.G., Dranka B.P., Bailey S.M., Lancaster J.R., Darley-Usmar V.M. What part of no don't you understand? Some answers to the cardinal questions in nitric oxide biology. Journal of Biological Chemistry 2010, 285:19699-19704. http://www.ncbi.nlm.nih.gov/pubmed/20410298, 10.1016/j.redox.2014.06.011.
8. Lee M., Choy J.C. Positive feedback regulation of human inducible nitric-oxide synthase expression by Ras protein S-nitrosylation. Journal of Biological Chemistry 2013, 288:15677-15686. http://www.ncbi.nlm.nih.gov/pubmed/23599434, 10.1016/j.redox.2014.06.011.
9. Krezel A., Hao Q., Maret W. The zinc/thiolate redox biochemistry of metallothionein and the control of zinc ion fluctuations in cell signaling. Archives of Biochemistry and Biophysics 2007, 463:188-200. http://www.ncbi.nlm.nih.gov/pubmed/17391643, 10.1016/j.redox.2014.06.011.
10. Kröncke K.D. Cellular stress and intracellular zinc dyshomeostasis. Archives of Biochemistry and Biophysics 2007, 463:183-187. http://www.ncbi.nlm.nih.gov/pubmed/17442256, 10.1016/j.redox.2014.06.011.
11. Maret W. Molecular aspects of human cellular zinc homeostasis: redox control of zinc potentials and zinc signals. Biometals: An International Journal on the Role of Metal Ions in Biology, Biochemistry, and Medicine 2009, 22:149-157. http://www.ncbi.nlm.nih.gov/pubmed/19130267, 10.1016/j.redox.2014.06.011.
12. Cortese-Krott M.M., Suschek C.V., Wetzel W., Kröncke K.D., Kolb-Bachofen V. Nitric oxide-mediated protection of endothelial cells from hydrogen peroxide is mediated by intracellular zinc and glutathione. American Journal of Physiology- Cell Physiology 2009, 296:C811-C820. http://www.ncbi.nlm.nih.gov/pubmed/19193864, 10.1016/j.redox.2014.06.011.
13. Cortese M.M., Suschek C.V., Wetzel W., Kröncke K.D., Kolb-Bachofen V. Zinc protects endothelial cells from hydrogen peroxide via Nrf2-dependent stimulation of glutathione biosynthesis. Free Radical Biology & Medicine 2008, 44:2002-2012. http://www.ncbi.nlm.nih.gov/pubmed/18355458, 10.1016/j.redox.2014.06.011.
14. 2+ release. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:13952-13957. http://www.ncbi.nlm.nih.gov/pubmed/14617770, 10.1016/j.redox.2014.06.011.
15. Oteiza P.I. Zinc and the modulation of redox homeostasis. Free Radical Biology & Medicine 2012, 53:1748-1759. http://www.ncbi.nlm.nih.gov/pubmed/22960578, 10.1016/j.redox.2014.06.011.
16. Berendji D., Kolb-Bachofen V., Meyer K.L., Grapenthin O., Weber H., Wahn V., Kröncke K.D. Nitric oxide mediates intracytoplasmic and intranuclear zinc release. FEBS Letters 1997, 405:37-41. http://www.ncbi.nlm.nih.gov/pubmed/9094420, 10.1016/j.redox.2014.06.011.
17. Bernal P.J., Leelavanichkul K., Bauer E., Cao R., Wilson A., Wasserloos K.J., Watkins S.C., Pitt B.R., St Croix C.M. Nitric-oxide-mediated zinc release contributes to hypoxic regulation of pulmonary vascular tone. Circulation Research 2008, 102:1575-1583. http://www.ncbi.nlm.nih.gov/pubmed/18483408, 10.1016/j.redox.2014.06.011.
18. Pearce L.L., Wasserloos K., St Croix C.M., Gandley R., Levitan E.S., Pitt B.R. Metallothionein, nitric oxide and zinc homeostasis in vascular endothelial cells. Journal of Nutrition 2000, 130:1467S-1470S. http://www.ncbi.nlm.nih.gov/pubmed/10801961.
19. Li H., Cao R., Wasserloos K.J., Bernal P., Liu Z.Q., Pitt B.R., St Croix C.M. Nitric oxide and zinc homeostasis in pulmonary endothelium. Annals of the New York Academy of Sciences 2010, 1203:73-78. http://www.ncbi.nlm.nih.gov/pubmed/20716286, 10.1016/j.redox.2014.06.011.
20. St Croix C.M., Stitt M.S., Leelavanichkul K., Wasserloos K.J., Pitt B.R., Watkins S.C. Nitric oxide-induced modification of protein thiolate clusters as determined by spectral fluorescence resonance energy transfer in live endothelial cells. Free Radical Biology & Medicine 2004, 37:785-792. http://www.ncbi.nlm.nih.gov/pubmed/15304254, 10.1016/j.redox.2014.06.011.
21. St Croix C.M., Wasserloos K.J., Dineley K.E., Reynolds I.J., Levitan E.S., Pitt B.R. Nitric oxide-induced changes in intracellular zinc homeostasis are mediated by metallothionein/thionein. American Journal of Physiology - Lung Cellular and Molecular Physiology 2002, 282:L185-L192. http://www.ncbi.nlm.nih.gov/pubmed/11792622, 10.1016/j.redox.2014.06.011.
22. Stitt M.S., Wasserloos K.J., Tang X., Liu X., Pitt B.R., St Croix C.M. Nitric oxide-induced nuclear translocation of the metal responsive transcription factor, MTF-1 is mediated by zinc release from metallothionein. Vascular Pharmacology 2006, 44:149-155. http://www.ncbi.nlm.nih.gov/pubmed/16423564, 10.1016/j.redox.2014.06.011.
23. Li H., Raman C.S., Glaser C.B., Blasko E., Young T.A., Parkinson J.F., Whitlow M., Poulos T.L. Crystal structures of zinc-free and -bound heme domain of human inducible nitric-oxide synthase. Implications for dimer stability and comparison with endothelial nitric-oxide synthase. Journal of Biological Chemistry 1999, 274:21276-21284. http://www.ncbi.nlm.nih.gov/pubmed/10409685, 10.1016/j.redox.2014.06.011.
24. Mitchell D.A., Erwin P.A., Michel T., Marletta M.A. S-nitrosation and regulation of inducible nitric oxide synthase. Biochemistry 2005, 44:4636-4647. http://www.ncbi.nlm.nih.gov/pubmed/15779890, 10.1016/j.redox.2014.06.011.
25. Perry J.M., Marletta M.A. Effects of transition metals on nitric oxide synthase catalysis. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:11101-11106. http://www.ncbi.nlm.nih.gov/pubmed/9736696, 10.1016/j.redox.2014.06.011.
26. Stuehr D.J., Griffith O.W. Mammalian nitric oxide synthases. Advances in Enzymology and Related Areas of Molecular Biology 1992, 65:287-346. http://www.ncbi.nlm.nih.gov/pubmed/1373932.
27. Yamaoka J., Kume T., Akaike A., Miyachi Y. Suppressive effect of zinc ion on iNOS expression induced by interferon-γ or tumor necrosis factor-α in murine keratinocytes. Journal of Dermatological Science 2000, 23:27-35. http://www.ncbi.nlm.nih.gov/pubmed/10699762, 10.1016/j.redox.2014.06.011.
28. Suschek C., Rothe H., Fehsel K., Enczmann J., Kolb-Bachofen V. Induction of a macrophage-like nitric oxide synthase in cultured rat aortic endothelial cells. IL-1beta-mediated induction regulated by tumor necrosis factor-alpha and IFN-gamma. Journal of Immunology (Baltimore, MD: 1950) 1993, 151:3283-3291. http://www.ncbi.nlm.nih.gov/pubmed/7690801.
29. Kleinert H., Euchenhofer C., Ihrig-Biedert I., Förstermann U. Glucocorticoids inhibit the induction of nitric oxide synthase II by down-regulating cytokine-induced activity of transcription factor nuclear factor-kappa B. Molecular Pharmacology 1996, 49:15-21. http://www.ncbi.nlm.nih.gov/pubmed/8569701.
30. Rassaf T., Bryan N.S., Kelm M., Feelisch M. Concomitant presence of N-nitroso and S-nitroso proteins in human plasma. Free Radical Biology & Medicine 2002, 33:1590-1596. http://www.ncbi.nlm.nih.gov/pubmed/12446216, 10.1016/j.redox.2014.06.011.
31. Slater T.F., Sawyer B., Sträuli U. Studies on succinate-tetrazolium reductase systems: III. Points of coupling of four different tetrazolium salts. III. Points of coupling of four different tetrazolium salts. Biochimica et Biophysica Acta 1963, 77:383-393. http://www.ncbi.nlm.nih.gov/pubmed/14089413, 10.1016/j.redox.2014.06.011.
32. Teng X., Zhang H., Snead C., Catravas J.D. A reverse nuclear factor-kappaB element in the rat type II nitric oxide synthase promoter mediates the induction by interleukin-1beta and interferon-gamma in rat aortic smooth muscle cells. General Pharmacology 2000, 34:9-16. http://www.ncbi.nlm.nih.gov/pubmed/10793263, 10.1016/j.redox.2014.06.011.
33. Brigelius-Flohé R., Flohé L. Basic principles and emerging concepts in the redox control of transcription factors. Antioxidants & Redox Signaling 2011, 15:2335-2381. http://www.ncbi.nlm.nih.gov/pubmed/21194351, 10.1016/j.redox.2014.06.011.
34. Mukaida N., Morita M., Ishikawa Y., Rice N., Okamoto S., Kasahara T., Matsushima K. Novel mechanism of glucocorticoid-mediated gene repression. Nuclear factor-kappa B is target for glucocorticoid-mediated interleukin 8 gene repression. Journal of Biological Chemistry 1994, 269:13289-13295. http://www.ncbi.nlm.nih.gov/pubmed/8175759.
35. Liu M.J., Bao S., Gálvez-Peralta M., Pyle C.J., Rudawsky A.C., Pavlovicz R.E., Killilea D.W., Li C., Nebert D.W., Wewers M.D., Knoell D.L. ZIP8 regulates host defense through zinc-mediated inhibition of NF-kappaB. Cell Reports 2013, 3:386-400. http://www.ncbi.nlm.nih.gov/pubmed/23403290, 10.1016/j.redox.2014.06.011.
36. Jeon Y.J., Han S.H., Lee Y.W., Yea S.S., Yang K.-H. Inhibition of NF-κB/Rel nuclear translocation by dexamethasone: mechanism for the inhibition of iNOS gene expression. IUBMB Life 1998, 45:435-441. 10.1016/j.redox.2014.06.011.
37. Heyninck K., De Valck D., Vanden Berghe W., Van Criekinge W., Contreras R., Fiers W., Haegeman G., Beyaert R. The zinc finger protein A20 inhibits TNF-induced NF-κB-dependent gene expression by interfering with an RIP- or TRAF2-mediated transactivation signal and directly binds to a novel NF-κB-inhibiting protein ABIN. Journal of Cell Biology 1999, 145:1471-1482. http://www.ncbi.nlm.nih.gov/pubmed/10385526, 10.1016/j.redox.2014.06.011.
38. De Vera M.E., Taylor B.S., Wang Q., Shapiro R.A., Billiar T.R., Geller D.A. Dexamethasone suppresses iNOS gene expression by upregulating I-κBα and inhibiting NF-κB. American Journal of Physiology 1997, 273:G1290-G1296. http://www.ncbi.nlm.nih.gov/pubmed/9435553.
39. Haase H., Rink L. Zinc signals and immune function. BioFactors (Oxford, England) 2014, 40:27-40. http://www.ncbi.nlm.nih.gov/pubmed/23804522, 10.1016/j.redox.2014.06.011.
40. Jeon K.I., Jeong J.Y., Jue D.M. Thiol-reactive metal compounds inhibit NF-kappa B activation by blocking I kappa B kinase. Journal of Immunology (Baltimore, MD: 1950) 2000, 164:5981-5989. http://www.ncbi.nlm.nih.gov/pubmed/10820281, 10.1016/j.redox.2014.06.011.
41. Prasad A.S. Clinical, immunological, anti-inflammatory and antioxidant roles of zinc. Experimental Gerontology 2008, 43:370-377. http://www.ncbi.nlm.nih.gov/pubmed/18054190, 10.1016/j.redox.2014.06.011.
42. Uzzo R.G., Leavis P., Hatch W., Gabai V.L., Dulin N., Zvartau N., Kolenko V.M. Zinc inhibits nuclear factor-kappa B activation and sensitizes prostate cancer cells to cytotoxic agents. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research 2002, 8:3579-3583. http://www.ncbi.nlm.nih.gov/pubmed/12429649.
43. Kim C.H., Kim J.H., Moon S.J., Chung K.C., Hsu C.Y., Seo J.T., Ahn Y.S. Pyrithione, a zinc ionophore, inhibits NF-kappaB activation. Biochemical and Biophysical Research Communications 1999, 259:505-509. http://www.ncbi.nlm.nih.gov/pubmed/10364448, 10.1016/j.redox.2014.06.011.
44. Ho E., Quan N., Tsai Y.H., Lai W., Bray T.M. Dietary zinc supplementation inhibits NFkappaB activation and protects against chemically induced diabetes in CD1 mice. Experimental Biology and Medicine (Maywood, N.J.) 2001, 226:103-111. http://www.ncbi.nlm.nih.gov/pubmed/11446433.
45. Oteiza P.I., Clegg M.S., Keen C.L. Short-term zinc deficiency affects nuclear factor-kappab nuclear binding activity in rat testes. Journal of Nutrition 2001, 131:21-26. http://www.ncbi.nlm.nih.gov/pubmed/11208933.
46. Mackenzie G.G., Zago M.P., Keen C.L., Oteiza P.I. Low intracellular zinc impairs the translocation of activated NF-kappa B to the nuclei in human neuroblastoma IMR-32 cells. Journal of Biological Chemistry 2002, 277:34610-34617. http://www.ncbi.nlm.nih.gov/pubmed/12089148, 10.1016/j.redox.2014.06.011.
47. Brieger A., Rink L., Haase H. Differential regulation of TLR-dependent MyD88 and TRIF signaling pathways by free zinc ions. Journal of Immunology (Baltimore, MD: 1950) 2013, 191:1808-1817. http://www.ncbi.nlm.nih.gov/pubmed/23863901, 10.1016/j.redox.2014.06.011.
48. Connell P., Young V.M., Toborek M., Cohen D.A., Barve S., McClain C.J., Hennig B. Zinc attenuates tumor necrosis factor-mediated activation of transcription factors in endothelial cells. Journal of the American College of Nutrition 1997, 16:411-417. http://www.ncbi.nlm.nih.gov/pubmed/9322188, 10.1016/j.redox.2014.06.011.
49. Hennig B., Meerarani P., Toborek M., McClain C.J. Antioxidant-like properties of zinc in activated endothelial cells. Journal of the American College of Nutrition 1999, 18:152-158. http://www.ncbi.nlm.nih.gov/pubmed/10204831, 10.1016/j.redox.2014.06.011.
50. Maret W., Jacob C., Vallee B.L., Fischer E.H. Inhibitory sites in enzymes: zinc removal and reactivation by thionein. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:1936-1940. http://www.ncbi.nlm.nih.gov/pubmed/10051573, 10.1016/j.redox.2014.06.011.
51. 2+. Toxicology 1999, 133:139-145. http://www.ncbi.nlm.nih.gov/pubmed/10378480, 10.1016/j.redox.2014.06.011.
52. Ye B., Maret W., Vallee B.L. Zinc metallothionein imported into liver mitochondria modulates respiration. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:2317-2322. http://www.ncbi.nlm.nih.gov/pubmed/11226237, 10.1016/j.redox.2014.06.011.
53. Gazaryan I.G., Krasnikov B.F., Ashby G.A., Thorneley R.N., Kristal B.S., Brown A.M. Zinc is a potent inhibitor of thiol oxidoreductase activity and stimulates reactive oxygen species production by lipoamide dehydrogenase. Journal of Biological Chemistry 2002, 277:10064-10072. http://www.ncbi.nlm.nih.gov/pubmed/11744691, 10.1016/j.redox.2014.06.011.
54. Haase H., Maret W. Intracellular zinc fluctuations modulate protein tyrosine phosphatase activity in insulin/insulin-like growth factor-1 signaling. Experimental Cell Research 2003, 291:289-298. http://www.ncbi.nlm.nih.gov/pubmed/14644152, 10.1016/j.redox.2014.06.011.
55. Gerlier D., Thomasset N. Use of MTT colorimetric assay to measure cell activation. Journal of Immunological Methods 1986, 94:57-63. http://www.ncbi.nlm.nih.gov/pubmed/3782817, 10.1016/j.redox.2014.06.011.
56. Lichten L.A., Cousins R.J. Mammalian zinc transporters: nutritional and physiologic regulation. Annual Review of Nutrition 2009, 29:153-176. http://www.ncbi.nlm.nih.gov/pubmed/19400752, 10.1016/j.redox.2014.06.011.
57. Gibson R.S., Hess S.Y., Hotz C., Brown K.H. Indicators of zinc status at the population level: a review of the evidence. British Journal of Nutrition 2008, 99(Suppl. 3):S14-S23. http://www.ncbi.nlm.nih.gov/pubmed/18598584, 10.1016/j.redox.2014.06.011.
58. Bozym R.A., Chimienti F., Giblin L.J., Gross G.W., Korichneva I., Li Y., Libert S., Maret W., Parviz M., Frederickson C.J., Thompson R.B. Free zinc ions outside a narrow concentration range are toxic to a variety of cells in vitro. Experimental Biology and Medicine (Maywood, N.J.) 2010, 235:741-750. http://www.ncbi.nlm.nih.gov/pubmed/20511678, 10.1016/j.redox.2014.06.011.
59. Kröncke K.D., Fehsel K., Schmidt T., Zenke F.T., Dasting I., Wesener J.R., Bettermann H., Breunig K.D., Kolb-Bachofen V. Nitric oxide destroys zinc-sulfur clusters inducing zinc release from metallothionein and inhibition of the zinc finger-type yeast transcription activator LAC9. Biochemical and Biophysical Research Communications 1994, 200:1105-1110. http://www.ncbi.nlm.nih.gov/pubmed/8179589, 10.1016/j.redox.2014.06.011.
60. Frederickson C.J., Koh J.-Y., Bush A.I. The neurobiology of zinc in health and disease. Nature Reviews Neuroscience 2005, 6:449-462. http://www.ncbi.nlm.nih.gov/pubmed/15891778, 10.1016/j.redox.2014.06.011.
61. Shumilla J.A., Wetterhahn K.E., Barchowsky A. Inhibition of NF-[kappa]B Binding to DNA by chromium, cadmium, mercury, zinc, and arsenite in vitro: evidence of a thiol mechanism. Archives of Biochemistry and Biophysics 1998, 349:356-362. http://www.ncbi.nlm.nih.gov/pubmed/9448725, 10.1016/j.redox.2014.06.011.