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http://dx.doi.org/10.4014/jmb.1512.12009

Cloning and Characterization of Filamentous Fungal S-Nitrosoglutathione Reductase from Aspergillus nidulans  

Zhou, Yao (State Key Laboratory of Bioreactor Engineering, Biomedical Nanotechnology Center, School of Biotechnology, East China University of Science and Technology)
Zhou, Shengmin (State Key Laboratory of Bioreactor Engineering, Biomedical Nanotechnology Center, School of Biotechnology, East China University of Science and Technology)
Yu, Haijun (State Key Laboratory of Bioreactor Engineering, Biomedical Nanotechnology Center, School of Biotechnology, East China University of Science and Technology)
Li, Jingyi (State Key Laboratory of Bioreactor Engineering, Biomedical Nanotechnology Center, School of Biotechnology, East China University of Science and Technology)
Xia, Yang (State Key Laboratory of Bioreactor Engineering, Biomedical Nanotechnology Center, School of Biotechnology, East China University of Science and Technology)
Li, Baoyi (State Key Laboratory of Bioreactor Engineering, Biomedical Nanotechnology Center, School of Biotechnology, East China University of Science and Technology)
Wang, Xiaoli (State Key Laboratory of Bioreactor Engineering, Biomedical Nanotechnology Center, School of Biotechnology, East China University of Science and Technology)
Wang, Ping (State Key Laboratory of Bioreactor Engineering, Biomedical Nanotechnology Center, School of Biotechnology, East China University of Science and Technology)
Publication Information
Journal of Microbiology and Biotechnology / v.26, no.5, 2016 , pp. 928-937 More about this Journal
Abstract
S-Nitrosoglutathione reductase (GSNOR) metabolizes S-nitrosoglutathione (GSNO) and has been shown to play important roles in regulating cellular signaling and formulating host defense by modulating intracellular nitric oxide levels. The enzyme has been found in bacterial, yeast, mushroom, plant, and mammalian cells. However, to date, there is still no evidence of its occurrence in filamentous fungi. In this study, we cloned and investigated a GSNOR-like enzyme from the filamentous fungus Aspergillus nidulans. The enzyme occurred in native form as a homodimer and exhibited low thermal stability. GSNO was an ideal substrate for the enzyme. The apparent Km and kcat values were 0.55 mM and 34,100 min-1, respectively. Substrate binding sites and catalytic center amino acid residues based on those from known GSNORs were conserved in this enzyme, and the corresponding roles were verified using site-directed mutagenesis. Therefore, we demonstrated the presence of GSNOR in a filamentous fungus for the first time.
Keywords
S-Nitrosoglutathione reductase; nitrosation; denitrosation; nitric oxide; Aspergillus nidulans;
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1 Arasimowicz-Jelonek M, Floryszak-Wieczorek J. 2014. Nitric oxide: an effective weapon of the plant or the pathogen? Mol. Plant Pathol. 15: 406-416.   DOI
2 Attarian R, Bennie C, Bach H, Av-Gay Y. 2009. Glutathione disulfide and S-nitrosoglutathione detoxification by Mycobacterium tuberculosis thioredoxin system. FEBS Lett. 583: 3215-3220.   DOI
3 Bateman RL, Rauh D, Tavshanjian B, Shokat KM. 2008. Human carbonyl reductase 1 is an S-nitrosoglutathione reductase. J. Biol. Chem. 283: 35756-35762.   DOI
4 Benhar M, Forrester MT, Hess DT, Stamler JS. 2008. Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins. Science 320: 1050-1054.   DOI
5 Benhar M, Forrester MT, Stamler JS. 2009. Protein denitrosylation: enzymatic mechanisms and cellular functions. Nat. Rev. Mol. Cell Biol. 10: 721-732.   DOI
6 Burney S, Caulfield JL, Niles JC, Wishnok JS, Tannenbaum SR. 1999. The chemistry of DNA damage from nitric oxide and peroxynitrite. Mutat. Res. 424: 37-49.   DOI
7 Comtois SL, Gidley MD, Kelly DJ. 2003. Role of the thioredoxin system and the thiol-peroxidases Tpx and Bcp in mediating resistance to oxidative and nitrosative stress in Helicobacter pylori. Microbiology 149: 121-129.   DOI
8 Crotty JW. 2009. Crystal structures and kinetics of S-nitrosoglutathione reductase from Arabidopsis thaliana and Homo sapiens. PhD Dissertation, The University of Arizona, Tuscon, AZ.
9 Fernandez MR, Biosca JA, Pares X. 2003. S-Nitrosoglutathione reductase activity of human and yeast glutathione-dependent formaldehyde dehydrogenase and its nuclear and cytoplasmic localisation. Cell. Mol. Life Sci. 60: 1013-1018.   DOI
10 Foster MW, Liu L, Zeng M, Hess DT, Stamler JS. 2009. A genetic analysis of nitrosative stress. Biochemistry 48: 792-799.   DOI
11 Goretski J, Zafiriou OC, Hollocher TC. 1990. Steady-state nitric oxide concentrations during denitrification. J. Biol. Chem. 265: 11535-11538.
12 Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS. 2005. Protein S-nitrosylation: purview and parameters. Nat. Rev. Mol. Cell Biol. 6: 150-166.   DOI
13 Hou Y, Guo Z, Li J, Wang PG. 1996. Seleno compounds and glutathione peroxidase catalyzed decomposition of S-nitrosothiols. Biochem. Biophys. Res. Commun. 228: 88-93.   DOI
14 Hromatka BS, Noble SM, Johnson AD. 2005. 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.   DOI
15 Ken CF, Huang CY, Wen L, Huang JK, Lin CT. 2014. Modulation of nitrosative stress via glutathione-dependent formaldehyde dehydrogenase and S-nitrosoglutathione reductase. Int. J. Mol. Sci. 15: 14166-14179.   DOI
16 Jensen DE, Belka GK, Du Bois GC. 1998. S-Nitrosoglutathione is a substrate for rat alcohol dehydrogenase class III isoenzyme. Biochem. J. 331: 659-668.   DOI
17 Jourd’heuil D, Laroux FS, Miles AM, Wink DA, Grisham MB. 1999. Effect of superoxide dismutase on the stability of S-nitrosothiols. Arch. Biochem. Biophys. 361: 323-330.   DOI
18 Justino MC, Parente MR, Boneca IG, Saraiva LM. 2014. FrxA is an S-nitrosoglutathione reductase enzyme that contributes to Helicobacter pylori pathogenicity. FEBS J. 281: 4495-4505.   DOI
19 Kubienova L, Kopecny D, Tylichova M, Briozzo P, Skopalova J, Sebela M, et al. 2013. Structural and functional characterization of a plant S-nitrosoglutathione reductase from Solanum lycopersicum. Biochimie 95: 889-902.   DOI
20 Liu L, Hausladen A, Zeng M, Que L, Heitman J, Stamler JS. 2001. A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410: 490-494.   DOI
21 Marletta MA. 1993. Nitric oxide synthase: function and mechanism. Adv. Exp. Med. Biol. 338: 281-284.
22 Moncada S, Palmer RM, Higgs EA. 1991. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43: 109-142.
23 Myers PR, Minor RL Jr, Guerra R Jr, Bates JN, Harrison DG. 1990. Vasorelaxant properties of the endothelium-derived relaxing factor more closely resemble S-nitrosocysteine than nitric oxide. Nature 345: 161-163.   DOI
24 Sengupta R, Ryter SW, Zuckerbraun BS, Tzeng E, Billiar TR, Stoyanovsky DA. 2007. Thioredoxin catalyzes the denitrosation of low-molecular mass and protein S-nitrosothiols. Biochemistry 46: 8472-8483.   DOI
25 Peng XM, Cai GX, Zhou CH. 2013. Recent developments in azole compounds as antibacterial and antifungal agents. Curr. Top. Med. Chem. 13: 1963-2010.   DOI
26 Sakamoto A, Ueda M, Morikawa H. 2002. Arabidopsis glutathione-dependent formaldehyde dehydrogenase is an S-nitrosoglutathione reductase. FEBS Lett. 515: 20-24.   DOI
27 Sanghani PC, Robinson H, Bosron WF, Hurley TD. 2002. Human glutathione-dependent formaldehyde dehydrogenase. Structures of apo, binary, and inhibitory ternary complexes. Biochemistry 41: 10778-10786.   DOI
28 Sliskovic I, Raturi A, Mutus B. 2005. Characterization of the S-denitrosation activity of protein disulfide isomerase. J. Biol. Chem. 280: 8733-8741.   DOI
29 Staab CA, Alander J, Brandt M, Lengqvist J, Morgenstern R, Grafstrom RC, Hoog JO. 2008. Reduction of S-nitrosoglutathione by alcohol dehydrogenase 3 is facilitated by substrate alcohols via direct cofactor recycling and leads to GSH-controlled formation of glutathione transferase inhibitors. Biochem. J. 413: 493-504.   DOI
30 Stamler JS. 1994. Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell 78: 931-936.   DOI
31 Stoyanovsky DA, Tyurina YY, Tyurin VA, Anand D, Mandavia DN, Gius D, et al. 2005. Thioredoxin and lipoic acid catalyze the denitrosation of low molecular weight and protein S-nitrosothiols. J. Am. Chem. Soc. 127: 15815-15823.   DOI
32 Sudhamsu J, Crane BR. 2009. Bacterial nitric oxide synthases: what are they good for? Trends Microbiol. 17: 212-218.   DOI
33 Xu S, Guerra D, Lee U, Vierling E. 2013. S-Nitrosoglutathione reductases are low-copy number, cysteine-rich proteins in plants that control multiple developmental and defense responses in Arabidopsis. Front. Plant Sci. 4: 430.   DOI
34 Trujillo M, Alvarez MN, Peluffo G, Freeman BA, Radi R. 1998. Xanthine oxidase-mediated decomposition of S-nitrosothiols. J. Biol. Chem. 273: 7828-7834.   DOI
35 Veech RL, Guynn R, Veloso D. 1972. The time-course of the effects of ethanol on the redox and phosphorylation states of rat liver. Biochem. J. 127: 387-397.   DOI
36 Wink DA, Mitchell JB. 1998. Chemical biology of nitric oxide: insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radic. Biol. Med. 25: 434-456.   DOI
37 Zhou S, Narukami T, Masuo S, Shimizu M, Fujita T, Doi Y, et al. 2013. NO-inducible nitrosothionein mediates NO removal in tandem with thioredoxin. Nat. Chem. Biol. 9: 657-663.   DOI
38 Zhou S, Narukami T, Nameki M, Ozawa T, Kamimura Y, Hoshino T, Takaya N. 2012. Heme-biosynthetic porphobilinogen deaminase protects Aspergillus nidulans from nitrosative stress. Appl. Environ. Microbiol. 78: 103-109.   DOI
39 Zhou S, Fushinobu S, Kim SW, Nakanishi Y, Maruyama JI, Kitamoto K, et al. 2011. Functional analysis and subcellular location of two flavohemoglobins from Aspergillus oryzae. Fungal Genet. Biol. 48: 200-207.   DOI
40 Zhou S, Fushinobu S, Nakanishi Y, Kim SW, Wakagi T, Shoun H. 2009. Cloning and characterization of two flavohemoglobins from Aspergillus oryzae. Biochem. Biophys. Res. Commun. 381: 7-11.   DOI