NO-inducible nitrosothionein mediates NO removal in tandem with thioredoxin

Nature Chemical Biology

Volumn 9, Issue 10, 2013, Pages 657-663

  Zhou, Shengmin ^a   Narukami, Toshiaki ^a   Masuo, Shunsuke ^a   Shimizu, Motoyuki ^a   Fujita, Tomoya ^a   Doi, Yuki ^a   Kamimura, Yosuke ^a   Takaya, Naoki ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACONITATE HYDRATASE; CYSTEINE; DNA FRAGMENT; GENOMIC DNA; HEAVY METAL; METAL ION; METALLOTHIONEIN; NITRIC OXIDE; NITRIC OXIDE INDUCIBLE NITROSOTHIONEIN; OXIDOREDUCTASE; PORPHOBILINOGEN DEAMINASE; S NITROSOGLUTATHIONE; S NITROSOTHIOL; THIOREDOXIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; ASPERGILLUS NIDULANS; CELL DAMAGE; CLONING; DNA SEQUENCE; GEL FILTRATION CHROMATOGRAPHY; GENE DISRUPTION; HOMOLOGOUS RECOMBINATION; IN VITRO STUDY; IN VIVO STUDY; METAL TOLERANCE; NITROSATION; NITROSATIVE STRESS; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; SPECTROFLUOROMETRY;

ASPERGILLUS NIDULANS; FUNGAL PROTEINS; GENES, FUNGAL; NITRIC OXIDE; REACTIVE NITROGEN SPECIES; S-NITROSOGLUTATHIONE; THIOREDOXINS;

EMERICELLA NIDULANS;

EID: 84884534948     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1316     Document Type: Article

References (48)

1. Stamler, J.S. Redox signaling: Nitrosylation and related target interactions of nitric oxide. Cell 78, 931-936 (1994).
2. Goretski, J., Zafiriou, O.C. & Hollocher, T.C. Steady-state nitric oxide concentrations during denitrification. J. Biol. Chem. 265, 11535-11538 (1990).
3. Hausladen, A. & Stamler, J.S. Nitrosative stress. Methods Enzymol. 300, 389-395 (1999).
4. Forrester, M.T. & Foster, M.W. Protection from nitrosative stress: A central role for microbial flavohemoglobin. Free Radic. Biol. Med. 52, 1620-1633 (2012).
5. Gardner, A.M., Helmick, R.A. & Gardner, P.R. Flavorubredoxin, an inducible catalyst for nitric oxide reduction and detoxification in Escherichia coli. J. Biol. Chem. 277, 8172-8177 (2002).
6. Shoun, H. & Tanimoto, T. Denitrification by the fungus Fusarium oxysporum and involvement of cytochrome P-450 in the respiratory nitrite reduction. J. Biol. Chem. 266, 11078-11082 (1991).
7. St. John, G. et al. Peptide methionine sulfoxide reductase from Escherichia coli and Mycobacterium tuberculosis protects bacteria against oxidative damage from reactive nitrogen intermediates. Proc. Natl. Acad. Sci. USA 98, 9901-9906 (2001).
8. De Groote, M.A., Testerman, T., Xu, Y., Stauffer, G. & Fang, F.C. Homocysteine antagonism of nitric oxide-related cytostasis in Salmonella typhimurium. Science 272, 414-417 (1996).
9. Flatley, J. et al. Transcriptional responses of Escherichia coli to S-nitrosoglutathione under defined chemostat conditions reveal major changes in methionine biosynthesis. J. Biol. Chem. 280, 10065-10072 (2005).
10. Hromatka, B.S., Noble, S.M. & Johnson, A.D. Transcriptional response of Candida albicans to nitric oxide and the role of the YHB1 gene in nitrosative stress and virulence. Mol. Biol. Cell 16, 4814-4826 (2005).
11. Nittler, M.P., Hocking-Murray, D., Foo, C.K. & Sil, A. Identification of Histoplasma capsulatum transcripts induced in response to reactive nitrogen species. Mol. Biol. Cell 16, 4792-4813 (2005).
12. Sarver, A. & DeRisi, J. Fzf1p regulates an inducible response to nitrosative stress in Saccharomyces cerevisiae. Mol. Biol. Cell 16, 4781-4791 (2005).
13. Hess, D.T., Matsumoto, A., Kim, S.O., Marshall, H.E. & Stamler, J.S. Protein S-nitrosylation: Purview and parameters. Nat. Rev. Mol. Cell Biol. 6, 150-166 (2005).
14. Clancy, R.M., Levartovsky, D., Leszczynska-Piziak, J., Yegudin, J. & Abramson, S.B. Nitric oxide reacts with intracellular glutathione and activates the hexose monophosphate shunt in human neutrophils: Evidence for S-nitrosoglutathione as a bioactive intermediary. Proc. Natl. Acad. Sci. USA 91, 3680-3684 (1994).
15. Liu, L. et al. A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410, 490-494 (2001).
16. Benhar, M., Forrester, M.T. & Stamler, J.S. Protein denitrosylation: Enzymatic mechanisms and cellular functions. Nat. Rev. Mol. Cell Biol. 10, 721-732 (2009).
17. Foster, M.W., Liu, L., Zeng, M., Hess, D.T. & Stamler, J.S. A genetic analysis of nitrosative stress. Biochemistry 48, 792-799 (2009).
18. Wei, W. et al. S-Nitrosylation from GSNOR deficiency impairs DNA repair and promotes hepatocarcinogenesis. Sci. Transl. Med. 2, 19ra13 (2010).
19. Takasaki, K. et al. Fungal ammonia fermentation, a novel metabolic mechanism that couples the dissimilatory and assimilatory pathways of both nitrate and ethanol. Role of acetyl CoA synthetase in anaerobic ATP synthesis. J. Biol. Chem. 279, 12414-12420 (2004).
20. Shimizu, M., Fujii, T., Masuo, S., Fujita, K. & Takaya, N. Proteomic analysis of Aspergillus nidulans cultured under hypoxic conditions. Proteomics 9, 7-19 (2009).
21. Zhou, S. et al. Functional analysis and subcellular location of two flavohemoglobins from Aspergillus oryzae. Fungal Genet. Biol. 48, 200-207 (2011).
22. de Jesús-Berríos, M. et al. Enzymes that counteract nitrosative stress promote fungal virulence. Curr. Biol. 13, 1963-1968 (2003).
23. Schinko, T. et al. Transcriptome analysis of nitrate assimilation in Aspergillus nidulans reveals connections to nitric oxide metabolism. Mol. Microbiol. 78, 720-738 (2010).
24. Zhou, S. et al. Heme-biosynthetic porphobilinogen deaminase protects Aspergillus nidulans from nitrosative stress. Appl. Environ. Microbiol. 78, 103-109 (2012).
25. Wortman, J.R. et al. The 2008 update of the Aspergillus nidulans genome annotation: A community effort. Fungal Genet. Biol. 46 (suppl. 1): S2-S13 (2009).
26. Capdevila, M. & Atrian, S. Metallothionein protein evolution: A miniassay. J. Biol. Inorg. Chem. 16, 977-989 (2011).
27. de Oliveira, M.G., Shishido, S.M., Seabra, A.B. & Morgon, N.H. Thermal stability of primary S-nitrosothiols: Roles of autocatalysis and structural effects on the rate of nitric oxide release. J. Phys. Chem. A 106, 8963-8970 (2002).
28. Jaffrey, S.R. & Snyder, S.H. The biotin switch method for the detection of S-nitrosylated proteins. Sci. STKE 2001, pl1 (2001).
29. Gow, A., Doctor, A., Mannick, J. & Gaston, B. S-Nitrosothiol measurements in biological systems. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 851, 140-151 (2007).
30. Romero, J.M. & Bizzozero, O.A. Intracellular glutathione mediates the denitrosylation of protein nitrosothiols in the rat spinal cord. J. Neurosci. Res. 87, 701-709 (2009).
31. Stoyanovsky, D.A. et al. Thioredoxin and lipoic acid catalyze the denitrosation of low molecular weight and protein S-nitrosothiols. J. Am. Chem. Soc. 127, 15815-15823 (2005).
32. Thön, M., Al-Abdallah, Q., Hortschansky, P. & Brakhage, A.A. The thioredoxin system of the filamentous fungus Aspergillus nidulans: Impact on development and oxidative stress response. J. Biol. Chem. 282, 27259-27269 (2007).
33. Sengupta, R. et al. Thioredoxin catalyzes the denitrosation of low-molecular mass and protein S-nitrosothiols. Biochemistry 46, 8472-8483 (2007).
34. Benhar, M., Forrester, M.T., Hess, D.T. & Stamler, J.S. Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins. Science 320, 1050-1054 (2008).
35. Nikitovic, D. & Holmgren, A. S-nitrosoglutathione is cleaved by the thioredoxin system with liberation of glutathione and redox regulating nitric oxide. J. Biol. Chem. 271, 19180-19185 (1996).
36. Thön, M. et al. The CCAAT-binding complex coordinates the oxidative stress response in eukaryotes. Nucleic Acids Res. 38, 1098-1113 (2010).
37. Gold, B. et al. Identification of a copper-binding metallothionein in pathogenic mycobacteria. Nat. Chem. Biol. 4, 609-616 (2008).
38. Schwarz, M.A. et al. Metallothionein protects against the cytotoxic and DNA-damaging effects of nitric oxide. Proc. Natl. Acad. Sci. USA 92, 4452-4456 (1995).
39. Tucker, S.L. et al. A fungal metallothionein is required for pathogenicity of Magnaporthe grisea. Plant Cell 16, 1575-1588 (2004).
40. Münger, K., Germann, U.A. & Lerch, K. Isolation and structural organization of the Neurosporra crassa copper metallothionein gene. EMBO J. 4, 2665-2668 (1985).
41. Vašák, M. & Meloni, G. Chemistry and biology of mammalian metallothioneins. J. Biol. Inorg. Chem. 16, 1067-1078 (2011).
42. Liu, S.X. et al. Reconstitution of apo-superoxide dismutase by nitric oxide-induced copper transfer from metallothioneins. Chem. Res. Toxicol. 13, 922-931 (2000).
43. Cai, L., Koropatnick, J. & Cherian, M.G. Metallothionein protects DNA from copper-induced but not iron-induced cleavage in vitro. Chem. Biol. Interact. 96, 143-155 (1995).
44. Kröncke, K.D. Nitrosative stress and transcription. Biol. Chem. 384, 1365-1377 (2003).
45. Lushchak, O.V., Inoue, Y. & Lushchak, V.I. Regulatory protein Yap1 is involved in response of yeast Saccharomyces cerevisiae to nitrosative stress. Biochemistry (Mosc). 75, 629-664 (2010).
46. Asano, Y., Hagiwara, D., Yamashino, T. & Mizuno, T. Characterization of the bZip-type transcription factor NapA with reference to oxidative stress response in Aspergillus nidulans. Biosci. Biotechnol. Biochem. 71, 1800-1803 (2007).
47. Datta, P.K. & Lianos, E.A. Nitric oxide induces metallothionein-1 gene expression in mesangial cells. Transl. Res. 148, 180-187 (2006).
48. Liu, L. et al. Essential roles of S-nitrosothiols in vascular homeostasis and endotoxic shock. Cell 116, 617-628 (2004).