A thioredoxin reductase and/or thioredoxin system-based mechanism for antioxidant effects of ambroxol

Biochimie

Volumn 97, Issue 1, 2014, Pages 92-103

  Huang, Jin ^a   Xu, Jianying ^b   Tian, Lin ^c   Zhong, Liangwei ^a  

^a UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^b SHANXI MEDICAL UNIVERSITY   (China)

^c CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

Ambroxol; Reactive oxidative species; Thioredoxin; Thioredoxin reductase

Indexed keywords

AMBROXOL; HYDROGEN PEROXIDE; INSULIN; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; THIOREDOXIN; THIOREDOXIN REDUCTASE;

ANTIOXIDANT ACTIVITY; ARTICLE; BRONCHUS MUCOSA; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HUMAN TISSUE; KINETICS; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION;

2′,7′-DICHLOROFLUORESCIN; 2′-7′-DICHLORODIHYDROFLUORESCEIN DIACETATE; 3-(4,5-DIMETHYLTHIAZOL-2-YL)-2,5-DIPHENYLTETRAZOLIUM BROMIDE; 5,5′-DITHIOBIS-(2-NITROBENZOIC ACID); 5-(IODOACETAMIDO)FLUORESCEIN; 5-IAF; ABX; AMBROXOL; DCF; DCFH-DA; DITHIOTHREITOL; DTNB; DTT; GUA HCL; GUANIDINE HYDROCHLORIDE; MTT; PHENYLMETHANESULFONYL FLUORIDE; PMSF; RADICAL OXIDATIVE SPECIES; REACTIVE OXIDATIVE SPECIES; ROS; THIOREDOXIN; THIOREDOXIN REDUCTASE; TRANS-4-(2-AMINO-3,5-DIBROMOBENZYLAMINO)-CYCLOHEXANOL, AMBROXOL; TRX; TRXR;

AMBROXOL; ANIMALS; ANTIOXIDANTS; BRONCHI; CATTLE; CELL LINE; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIAL CELLS; HUMANS; HYDROGEN PEROXIDE; OXIDATIVE STRESS; PROTEIN BINDING; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; THIOREDOXIN-DISULFIDE REDUCTASE; THIOREDOXINS;

EID: 84891856235     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2013.09.024     Document Type: Article

References (60)

1. B.G. Disse The pharmacology of ambroxol-review and new results Eur. J. Respir. Dis. Suppl. 153 1987 255 262
2. J.S. Hong, H.H. Ko, E.S. Han, and C.S. Lee Inhibition of bleomycin-induced cell death in rat alveolar macrophages and human lung epithelial cells by ambroxol Biochem. Pharmacol. 66 2003 1297 1306
3. A. Gillissen, and D. Nowak Characterization of N-acetylcysteine and ambroxol in anti-oxidant therapy Respir. Med. 92 1998 609 623
4. A. Gillissen, A. Bartling, S. Schoen, and G. Schultze-Werninghaus Antioxidant function of ambroxol in mononuclear and polymorphonuclear cells in vitro Lung 175 1997 235 242
5. A. Gillissen, B. Scharling, M. Jaworska, A. Bartling, K. Rasche, and G. Schultze-Werninghaus Oxidant scavenger function of ambroxol in vitro: a comparison with N-acetylcysteine Res. Exp. Med. (Berl.) 196 1997 389 398
6. M. Malerba, and B. Ragnoli Ambroxol in the 21st century: pharmacological and clinical update Expert Opin. Drug Metab. Toxicol. 4 2008 1119 1129
7. D. Nowak, A. Antczak, M. Krol, P. Bialasiewicz, and T. Pietras Antioxidant properties of ambroxol Free Radic. Biol. Med. 16 1994 517 522
8. D. Nowak, A. Antczak, T. Pietras, P. Bialasiewicz, and M. Krol Protective effect of ambroxol against heat- and hydrogen peroxide-induced damage to lung lipids in mice Eur. Respir. J. 7 1994 1629 1634
9. S.P. Zhao, Q.L. Guo, R.K. Wang, and E. Wang Oxidative and anti-oxidative effects of ambroxol on acute hydrochloric acid-induced lung injury in rats Zhong Nan Da Xue Xue Bao Yi Xue Ban 29 2004 586 588
10. J.A. Wiktorska, A. Lewinski, M. Stuss, D. Nowak, T. Pietras, and E. Sewerynek Effects of certain antioxidants on lipid peroxidation process in lung homogenates of l-thyroxine-receiving rats Neuro Endocrinol. Lett. 31 2010 137 146
11. M. Malerba, A. Ponticiello, A. Radaeli, G. Bensi, and V. Grassi Effect of twelve-months therapy with oral ambroxol in preventing exacerbations in patients with COPD. Double-blind, randomized, multicenter, placebo-controlled study (the AMETHIST trial) Pulm. Pharmacol. Ther. 17 2004 27 34
12. E. Puscinska, L. Radwan, and J. Zielinski Effect of intravenous ambroxol hydrochloride on lung function and exercise capacity in patients with severe chronic obstructive pulmonary disease Pneumonol. Alergol. Pol. 62 1994 246 249
13. J.E. Repine, A. Bast, and I. Lankhorst Oxidative stress in chronic obstructive pulmonary disease. Oxidative stress study group Am. J. Respir. Crit. Care Med. 156 1997 341 357
14. P.N. Dekhuijzen, K.K. Aben, I. Dekker, L.P. Aarts, P.L. Wielders, C.L. van Herwaarden, and A. Bast Increased exhalation of hydrogen peroxide in patients with stable and unstable chronic obstructive pulmonary disease Am. J. Respir. Crit. Care Med. 154 1996 813 816
15. J. Huang, J. Xu, H. Liu, L. Zhong, Thioredoxin reductase/thioredoxin: insights from their interaction with 4-hydroxy-2-nonenal for their implications in acute exacerbation of chronic obstructive pulmonary disease (2013) in press.
16. E.S. Arner, L. Zhong, and A. Holmgren Preparation and assay of mammalian thioredoxin and thioredoxin reductase Methods Enzymol. 300 1999 226 239
17. E.S. Arner, and A. Holmgren Physiological functions of thioredoxin and thioredoxin reductase Eur. J. Biochem. 267 2000 6102 6109
18. L. Zhong, E.S. Arner, and A. Holmgren Structure and mechanism of mammalian thioredoxin reductase: the active site is a redox-active selenolthiol/selenenylsulfide formed from the conserved cysteine-selenocysteine sequence Proc. Natl. Acad. Sci. U. S. A. 97 2000 5854 5859
19. K. Fritz-Wolf, S. Kehr, M. Stumpf, S. Rahlfs, and K. Becker Crystal structure of the human thioredoxin reductase-thioredoxin complex Nat. Commun. 2 2011 383
20. S.R. Lee, S. Bar-Noy, J. Kwon, R.L. Levine, T.C. Stadtman, and S.G. Rhee Mammalian thioredoxin reductase: oxidation of the C-terminal cysteine/selenocysteine active site forms a thioselenide, and replacement of selenium with sulfur markedly reduces catalytic activity Proc. Natl. Acad. Sci. U. S. A. 97 2000 2521 2526
21. A. Holmgren Thioredoxin Annu. Rev. Biochem. 54 1985 237 271
22. S. Kumar, M. Bjornstedt, and A. Holmgren Selenite is a substrate for calf thymus thioredoxin reductase and thioredoxin and elicits a large non-stoichiometric oxidation of NADPH in the presence of oxygen Eur. J. Biochem. 207 1992 435 439
23. M. Bjornstedt, M. Hamberg, S. Kumar, J. Xue, and A. Holmgren Human thioredoxin reductase directly reduces lipid hydroperoxides by NADPH and selenocystine strongly stimulates the reaction via catalytically generated selenols J. Biol. Chem. 270 1995 11761 11764
24. S. Mendiratta, Z.C. Qu, and J.M. May Enzyme-dependent ascorbate recycling in human erythrocytes: role of thioredoxin reductase Free Radic. Biol. Med. 25 1998 221 228
25. W.H. Watson, J. Pohl, W.R. Montfort, O. Stuchlik, M.S. Reed, G. Powis, and D.P. Jones Redox potential of human thioredoxin 1 and identification of a second dithiol/disulfide motif J. Biol. Chem. 278 2003 33408 33415
26. K.T. Barglow, C.G. Knutson, J.S. Wishnok, S.R. Tannenbaum, and M.A. Marletta Site-specific and redox-controlled S-nitrosation of thioredoxin Proc. Natl. Acad. Sci. U. S. A. 108 2011 E600 E606
27. S. Casagrande, V. Bonetto, M. Fratelli, E. Gianazza, I. Eberini, T. Massignan, M. Salmona, G. Chang, A. Holmgren, and P. Ghezzi Glutathionylation of human thioredoxin: a possible crosstalk between the glutathione and thioredoxin systems Proc. Natl. Acad. Sci. U. S. A. 99 2002 9745 9749
28. P. Wang, Y. Wu, X. Li, X. Ma, and L. Zhong Thioredoxin and thioredoxin reductase control tissue factor activity by thiol redox-dependent mechanism J. Biol. Chem. 288 2013 3346 3358
29. X. Ren, M. Bjornstedt, B. Shen, M.L. Ericson, and A. Holmgren Mutagenesis of structural half-cystine residues in human thioredoxin and effects on the regulation of activity by selenodiglutathione Biochemistry 32 1993 9701 9708
30. G.M. Kuster, D.A. Siwik, D.R. Pimentel, and W.S. Colucci Role of reversible, thioredoxin-sensitive oxidative protein modifications in cardiac myocytes Antioxid. Redox Signal. 8 2006 2153 2159
31. S.T. Lehtonen, S. Ohlmeier, R. Kaarteenaho-Wiik, T. Harju, P. Paakko, Y. Soini, and V.L. Kinnula Does the oxidative stress in chronic obstructive pulmonary disease cause thioredoxin/peroxiredoxin oxidation? Antioxid. Redox Signal. 10 2008 813 819
32. L. Zhong, E.S. Arner, J. Ljung, F. Aslund, and A. Holmgren Rat and calf thioredoxin reductase are homologous to glutathione reductase with a carboxyl-terminal elongation containing a conserved catalytically active penultimate selenocysteine residue J. Biol. Chem. 273 1998 8581 8591
33. G. Zhai, and L. Zhong N-Terminal affinity tags may lead to increased sensitivity of human thioredoxin-1 to oxidants Chin. J. Biochem. Mol. Biol. 26 2010 243 253
34. Y. Du, H. Zhang, J. Lu, and A. Holmgren Glutathione and glutaredoxin act as a backup of human thioredoxin reductase 1 to reduce thioredoxin 1 preventing cell death by aurothioglucose J. Biol. Chem. 287 2012 38210 38219
35. N.A. Bersani, J.R. Merwin, N.I. Lopez, G.D. Pearson, and G.F. Merrill Protein electrophoretic mobility shift assay to monitor redox state of thioredoxin in cells Methods Enzymol. 347 2002 317 326
36. Y. Wu, L. Yang, and L. Zhong Decreased serum levels of thioredoxin in patients with coronary artery disease plus hyperhomocysteinemia is strongly associated with the disease severity Atherosclerosis 212 2010 351 355
37. M.W. Pfaffl A new mathematical model for relative quantification in real-time RT-PCR Nucleic Acids Res. 29 2001 e45
38. I. Rahman, A.A. van Schadewijk, A.J. Crowther, P.S. Hiemstra, J. Stolk, W. MacNee, and W.I. De Boer 4-Hydroxy-2-nonenal, a specific lipid peroxidation product, is elevated in lungs of patients with chronic obstructive pulmonary disease Am. J. Respir. Crit. Care Med. 166 2002 490 495
39. N. Kondo, H. Nakamura, H. Masutani, and J. Yodoi Redox regulation of human thioredoxin network Antioxid. Redox Signal. 8 2006 1881 1890
40. L. Zhong, and A. Holmgren Essential role of selenium in the catalytic activities of mammalian thioredoxin reductase revealed by characterization of recombinant enzymes with selenocysteine mutations J. Biol. Chem. 275 2000 18121 18128
41. M. Meloun, T. Syrovy, and A. Vrana The thermodynamic dissociation constants of ambroxol, antazoline, naphazoline, oxymetazoline and ranitidine by the regression analysis of spectrophotometric data Talanta 62 2004 511 522
42. S. Gromer, S. Urig, and K. Becker The thioredoxin system-from science to clinic Med. Res. Rev. 24 2004 40 89
43. A. Holmgren Tryptophan fluorescence study of conformational transitions of the oxidized and reduced form of thioredoxin J. Biol. Chem. 247 1972 1992 1998
44. J. Qin, G.M. Clore, W.P. Kennedy, J. Kuszewski, and A.M. Gronenborn The solution structure of human thioredoxin complexed with its target from Ref-1 reveals peptide chain reversal Structure 4 1996 613 620
45. A. Holmgren Thioredoxin and glutaredoxin systems J. Biol. Chem. 264 1989 13963 13966
46. M. Refai, A. Brunelli, F. Xiume, M. Salati, V. Sciarra, L. Socci, L. Di Nunzio, and A. Sabbatini Short-term perioperative treatment with ambroxol reduces pulmonary complications and hospital costs after pulmonary lobectomy: a randomized trial Eur. J. Cardiothorac. Surg. 35 2009 469 473
47. A. Jekell, A. Hossain, U. Alehagen, U. Dahlstrom, and A. Rosen Elevated circulating levels of thioredoxin and stress in chronic heart failure Eur. J. Heart Fail. 6 2004 883 890
48. H. Nakamura, J. Vaage, G. Valen, C.A. Padilla, M. Bjornstedt, and A. Holmgren Measurements of plasma glutaredoxin and thioredoxin in healthy volunteers and during open-heart surgery Free Radic. Biol. Med. 24 1998 1176 1186
49. M. Mezzetti, L. Colombo, M. Marini, V. Crusi, P. Pierfedirici, and E. Mussini A pharmacokinetics study on pulmonary tropism of ambroxol on patients under thoracic surgery Surg. Intensive Care 13 1990 179 185
50. O. Rackham, A.M. Shearwood, R. Thyer, E. McNamara, S.M. Davies, B.A. Callus, A. Miranda-Vizuete, S.J. Berners-Price, Q. Cheng, E.S. Arner, and A. Filipovska Substrate and inhibitor specificities differ between human cytosolic and mitochondrial thioredoxin reductases: implications for development of specific inhibitors Free Radic. Biol. Med. 50 2011 689 699
51. J. Bodenstein, and H. Follmann Characterization of two thioredoxins in pig heart including a new mitochondrial protein Z. Naturforsch. C 46 1991 270 279
52. K. Hirasaka, C.U. Lago, M.A. Kenaston, K. Fathe, S.M. Nowinski, T. Nikawa, and E.M. Mills Identification of a redox-modulatory interaction between uncoupling protein 3 and thioredoxin 2 in the mitochondrial intermembrane space Antioxid. Redox Signal. 15 2011 2645 2661
53. J. Hu, L. Dong, and C.E. Outten The redox environment in the mitochondrial intermembrane space is maintained separately from the cytosol and matrix J. Biol. Chem. 283 2008 29126 29134
54. M.R. Fernando, H. Nanri, S. Yoshitake, K. Nagata-Kuno, and S. Minakami Thioredoxin regenerates proteins inactivated by oxidative stress in endothelial cells Eur. J. Biochem. 209 1992 917 922
55. C. Gitler, B. Zarmi, E. Kalef, R. Meller, U. Zor, and R. Goldman Calcium-dependent oxidation of thioredoxin during cellular growth initiation Biochem. Biophys. Res. Commun. 290 2002 624 628
56. J.R. Gasdaska, D.L. Kirkpatrick, W. Montfort, M. Kuperus, S.R. Hill, M. Berggren, and G. Powis Oxidative inactivation of thioredoxin as a cellular growth factor and protection by a Cys73 - >Ser mutation Biochem. Pharmacol. 52 1996 1741 1747
57. A. Weichsel, J.R. Gasdaska, G. Powis, and W.R. Montfort Crystal structures of reduced, oxidized, and mutated human thioredoxins: evidence for a regulatory homodimer Structure 4 1996 735 751
58. A. Levent, and Z. Senturk Colorimetric and atomic absorption spectrometric determination of mucolytic drug ambroxol through ion-pair formation with iron and thiocyanate Comb. Chem. High Throughput Screen. 13 2010 675 682
59. 2, a necessary evil for cell signaling Science 312 2006 1882 1883
60. R. Tkacova, Z. Kluchova, P. Joppa, D. Petrasova, and A. Molcanyiova Systemic inflammation and systemic oxidative stress in patients with acute exacerbations of COPD Respir. Med. 101 2007 1670 1676