A novel persulfide detection method reveals protein persulfide- and polysulfide-reducing functions of thioredoxin and glutathione systems

Science Advances

Volumn 2, Issue 1, 2016, Pages

  Dóka, Éva ^a   Pader, Irina ^b   Bíró, Adrienn ^a   Johansson, Katarina ^b   Cheng, Qing ^b   Ballagó, Krisztina ^a   Prigge, Justin R ^c   Pastor Flores, Daniel ^d   Dick, Tobias P ^d   Schmidt, Edward E ^c   Arnér, Elias S J ^b   Nagy, Péter ^a  

^a NATIONAL INSTITUTE OF ONCOLOGY   (Hungary)

^b KAROLINSKA INSTITUTE   (Sweden)

^c MONTANA STATE UNIVERSITY   (United States)

^d GERMAN CANCER RESEARCH CENTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CYTOLOGY; ENZYMES; MAMMALS; PEPTIDES; POLYSULFIDES; SULFUR COMPOUNDS;

DETECTION PROTOCOLS; DISULFIDE REDUCTION; GLUTATHIONE REDUCTASE; HUMAN EMBRYONIC KIDNEYS; REGENERATION MECHANISMS; REGENERATION SYSTEM; SIGNALING PATHWAYS; THIOREDOXIN REDUCTASE;

PROTEINS;

CYSTATHIONINE BETA SYNTHASE; CYSTATHIONINE GAMMA LYASE; GLUTATHIONE; GLUTATHIONE REDUCTASE; PERSULFIDES; POLYSULFIDE; SULFIDE; THIOREDOXIN; THIOREDOXIN REDUCTASE 1;

ANIMAL; HEK293 CELL LINE; HUMAN; LIVER; LIVER CELL; MALE; METABOLISM; MOUSE; RAT;

ANIMALS; CYSTATHIONINE BETA-SYNTHASE; CYSTATHIONINE GAMMA-LYASE; GLUTATHIONE; GLUTATHIONE REDUCTASE; HEK293 CELLS; HEPATOCYTES; HUMANS; LIVER; MALE; MICE; RATS; SULFIDES; THIOREDOXIN REDUCTASE 1; THIOREDOXINS;

EID: 84967084322     PISSN: None     EISSN: 23752548     Source Type: Journal    
DOI: 10.1126/sciadv.1500968     Document Type: Article

References (59)

1. K. Abe, H. Kimura, The possible role of hydrogen sulfide as an endogenous neuromodulator. J. Neurosci. 16, 1066-1071 (1996).
2. R. Wang, Physiological implications of hydrogen sulfide: A whiff exploration that blossomed. Physiol. Rev. 92, 791-896 (2012).
3. C. Szabo, Gaseotransmitters: New frontiers for translational science. Sci. Transl. Med. 2, 59ps54 (2010).
4. J. L. Wallace, R. Wang, Hydrogen sulfide-based therapeutics: Exploiting a unique but ubiquitous gasotransmitter. Nat. Rev. Drug Discov. 14, 329-345 (2015).
5. P. Nagy, Chapter one-Mechanistic chemical perspective of hydrogen sulfide signaling. Methods Enzymol. 554, 3-29 (2015).
6. B. D. Paul, S. H. Snyder, H2S signalling through protein sulfhydration and beyond. Nat. Rev. Mol. Cell Biol. 13, 499-507 (2012).
7. T. Ida, T. Sawa, H. Ihara, Y. Tsuchiya, Y. Watanabe, Y. Kumagai, M. Suematsu, H. Motohashi, S. Fujii, T. Matsunaga, M. Yamamoto, K. Ono, N. O. Devarie-Baez, M. Xian, J. M. Fukuto, T. Akaike, Reactive cysteine persulfides and S-polythiolation regulate oxidative stress and redox signaling. Proc. Natl. Acad. Sci. U.S.A. 111, 7606-7611 (2014).
8. O. Kabil, R. Banerjee, Redox biochemistry of hydrogen sulfide. J. Biol. Chem. 285, 21903-21907 (2010).
9. C. Coletta, A. Papapetropoulos, K. Erdelyi, G. Olah, K. Módis, P. Panopoulos, A. Asimakopoulou, D. Gerö, I. Sharina, E. Martin, C. Szabo, Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation. Proc. Natl. Acad. Sci. U.S.A. 109, 9161-9166 (2012).
10. M. M. Cortese-Krott, B. O. Fernandez, J. L. T. Santos, E. Mergia, M. Grman, P. Nagy, M. Kelm, A. Butler, M. Feelisch, Nitrosopersulfide (SSNO-) accounts for sustained NO bioactivity of S-nitrosothiols following reaction with sulfide. Redox Biol. 2, 234-244 (2014).
11. M. M. Cortese-Krott, G. G. C. Kuhnle, A. Dyson, B. O. Fernandez, M. Grman, J. F. DuMond, M. P. Barrow, G. McLeod, H. Nakagawa, K. Ondrias, P. Nagy, S. B. King, J. E. Saavedra, L. K. Keefer, M. Singer, M. Kelm, A. R. Butler, M. Feelisch, The key bioactive reaction products of the NO/H2S interaction are S/N-hybrid species, polysulfides, and nitroxyl. Proc. Natl. Acad. Sci. U.S.A. 112, E4651-E4660 (2015).
12. G. K. Kolluru, X. Shen, C. G. Kevil, A tale of two gases: NO and H2S, foes or friends for life? Redox Biol. 1, 313-318 (2013).
13. H. Kimura, Signaling molecules: Hydrogen sulfide and polysulfide. Antioxid. Redox Signal. 22, 362-376 (2015).
14. K. Ono, T. Akaike, T. Sawa, Y. Kumagai, D. A. Wink, D. J. Tantillo, A. J. Hobbs, P. Nagy, M. Xian, J. Lin, J. M. Fukuto, Redox chemistry and chemical biology of H2S, hydropersulfides, and derived species: Implications of their possible biological activity and utility. Free Radic. Biol. Med. 77, 82-94 (2014).
15. V. S. Lin, W. Chen, M. Xian, C. J. Chang, Chemical probes for molecular imaging and detection of hydrogen sulfide and reactive sulfur species in biological systems. Chem. Soc. Rev. 44, 4596-4618 (2014).
16. C.-M. Park, I. Macinkovic, M. R. Filipovic, M. Xian, Chapter three-Use of the "tag-switch" method for the detection of protein S-sulfhydration. Methods Enzymol. 555, 39-56 (2015).
17. J. I. Toohey, Sulfur signaling: Is the agent sulfide or sulfane? Anal. Biochem. 413, 1-7 (2011).
18. T. V. Mishanina, M. Libiad, R. Banerjee, Biogenesis of reactive sulfur species for signaling by hydrogen sulfide oxidation pathways. Nat. Chem. Biol. 11, 457-464 (2015).
19. Y. Mikami, N. Shibuya, Y. Kimura, N. Nagahara, Y. Ogasawara, H. Kimura, Thioredoxin and dihydrolipoic acid are required for 3-mercaptopyruvate sulfurtransferase to produce hydrogen sulfide. Biochem. J. 439, 479-485 (2011).
20. N. Krishnan, C. Fu, D. J. Pappin, N. K. Tonks, H2S-induced sulfhydration of the phosphatase PTP1B and its role in the endoplasmic reticulum stress response. Sci. Signal. 4, ra86 (2011).
21. W. Jeong, H. W. Yoon, S.-R. Lee, S. G. Rhee, Identification and characterization of TRP14, a thioredoxin-related protein of 14 kDa. New insights into the specificity of thioredoxin function. J. Biol. Chem. 279, 3142-3150 (2004).
22. I. Pader, R. Sengupta, M. Cebula, J. Xu, J. O. Lundberg, A. Holmgren, K. Johansson, E. S. J. Arnér, Thioredoxin-related protein of 14 kDa is an efficient L-cystine reductase and S-denitrosylase. Proc. Natl. Acad. Sci. U.S.A. 111, 6964-6969 (2014).
23. R. Greiner, Z. Pálinkás, K. Bäsell, D. Becher, H. Antelmann, P. Nagy, T. P. Dick, Polysulfides link H2S to protein thiol oxidation. Antioxid. Redox Signal. 19, 1749-1765 (2013).
24. P. Nagy, Z. Pálinkás, A. Nagy, B. Budai, I. Tóth, A. Vasas, Chemical aspects of hydrogen sulfide measurements in physiological samples. Biochim. Biophys. Acta 1840, 876-891 (2014).
25. A. Vasas, É. Dóka, I. Fábián, P. Nagy, Kinetic and thermodynamic studies on the disulfidebond reducing potential of hydrogen sulfide. Nitric Oxide 46, 93-101 (2015).
26. E. A. Wintner, T. L. Deckwerth, W. Langston, A. Bengtsson, D. Leviten, P. Hill, M. A. Insko, R. Dumpit, E. VandenEkart, C. F. Toombs, C. Szabo, A monobromobimane-based assay to measure the pharmacokinetic profile of reactive sulphide species in blood. Br. J. Pharmacol. 160, 941-957 (2010).
27. X. Shen, E. A. Peter, S. Bir, R. Wang, C. G. Kevil, Analytical measurement of discrete hydrogen sulfide pools in biological specimens. Free Radic. Biol. Med. 52, 2276-2283 (2012).
28. E. S. J. Arnér, Focus on mammalian thioredoxin reductases-Important selenoproteins with versatile functions. Biochim. Biophys. Acta 1790, 495-526 (2009).
29. Q. Cheng, T. Sandalova, Y. Lindqvist, E. S. J. Arnér, Crystal structure and catalysis of the selenoprotein thioredoxin reductase 1. J. Biol. Chem. 284, 3998-4008 (2009).
30. S. Kumar, M. Björnstedt, 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, 435-439 (1992).
31. A. K. Mustafa, M. M. Gadalla, N. Sen, S. Kim, W. Mu, S. K. Gazi, R. K. Barrow, G. Yang, R. Wang, S. H. Snyder, H2S signals through protein S-sulfhydration. Sci. Signal. 2, ra72 (2009).
32. O. Kabil, R. Banerjee, Enzymology of H2S biogenesis, decay and signaling. Antioxid. Redox Signal. 20, 770-782 (2014).
33. C. H. Lillig, C. Berndt, A. Holmgren, Glutaredoxin systems. Biochim. Biophys. Acta 1780, 1304-1317 (2008).
34. S. Eriksson, J. R. Prigge, E. A. Talago, E. S. J. Arnér, E. E. Schmidt, Dietary methionine can sustain cytosolic redox homeostasis in the mouse liver. Nat. Commun. 6, 6479 (2015).
35. N. Sen, B. D. Paul, M. M. Gadalla, A. K. Mustafa, T. Sen, R. Xu, S. Kim, S. H. Snyder, Hydrogen sulfide-linked sulfhydration of NF-kB mediates its antiapoptotic actions. Mol. Cell 45, 13-24 (2012).
36. K. Zhao, Y. Ju, S. Li, Z. Altaany, R. Wang, G. Yang, S-sulfhydration of MEK1 leads to PARP-1 activation and DNA damage repair. EMBO Rep. 15, 792-800 (2014).
37. A. K. Mustafa, G. Sikka, S. K. Gazi, J. Steppan, S. M. Jung, A. K. Bhunia, V. M. Barodka, F. K. Gazi, R. K. Barrow, R.Wang, L. M. Amzel,D. E. Berkowitz, S. H. Snyder,Hydrogen sulfide as endotheliumderived hyperpolarizing factor sulfhydrates potassium channels. Circ. Res. 109, 1259-1268 (2011).
38. D. Zhang, I. Macinkovic, N. O. Devarie-Baez, J. Pan, C.-M. Park, K. S. Carroll, M. R. Filipovic, M. Xian, Detection of protein S-sulfhydration by a tag-switch technique. Angew. Chem. Int. Ed. Engl. 53, 575-581 (2014).
39. J. Pan, K. S. Carroll, Persulfide reactivity in the detection of protein S-sulfhydration. ACS Chem. Biol. 8, 1110-1116 (2013).
40. P. Nagy, Kinetics and mechanisms of thiol-disulfide exchange covering direct substitution and thiol oxidation-mediated pathways. Antioxid. Redox Signal. 18, 1623-1641 (2013).
41. Y.-M. Go, J. D. Chandler, D. P. Jones, The cysteine proteome. Free Radic. Biol. Med. 84, 227-245 (2015).
42. R. E. Hansen, D. Roth, J. R. Winther, Quantifying the global cellular thiol-disulfide status. Proc. Natl. Acad. Sci. U.S.A. 106, 422-427 (2009).
43. A. Miseta, P. Csutora, Relationship between the occurrence of cysteine in proteins and the complexity of organisms. Mol. Biol. Evol. 17, 1232-1239 (2000).
44. M. Dagnell, J. Frijhoff, I. Pader, M. Augsten, B. Boivin, J. Xu, P. K. Mandal, N. K. Tonks, C. Hellberg, M. Conrad, E. S. J. Arnér, A. Östman, Selective activation of oxidized PTP1B by the thioredoxin system modulates PDGF-b receptor tyrosine kinase signaling. Proc. Natl. Acad. Sci. U.S.A. 110, 13398-13403 (2013).
45. J. Lu, A. Holmgren, The thioredoxin antioxidant system. Free Radic. Biol. Med. 66, 75-87 (2014).
46. F. Zahedi Avval, A. Holmgren, Molecular mechanisms of thioredoxin and glutaredoxin as hydrogen donors for Mammalian s phase ribonucleotide reductase. J. Biol. Chem. 284, 8233-8240 (2009).
47. P. Nagy, C. C. Winterbourn, Rapid reaction of hydrogen sulfide with the neutrophil oxidant hypochlorous acid to generate polysulfides. Chem. Res. Toxicol. 23, 1541-1543 (2010).
48. E. S. J. Arnér, H. Sarioglu, F. Lottspeich, A. Holmgren, A. Böck, High-level expression in Escherichia coli of selenocysteine-containing rat thioredoxin reductase utilizing gene fusions with engineered bacterial-type SECIS elements and co-expression with the selA, selB and selC genes. J. Mol. Biol. 292, 1003-1016 (1999).
49. J. Xu, S. E. Eriksson, M. Cebula, T. Sandalova, E. Hedström, I. Pader, Q. Cheng, C. R. Myers, W. E. Antholine, P. Nagy, U. Hellman, G. Selivanova, Y. Lindqvist, E. S. J. Arnér, The conserved Trp114 residue of thioredoxin reductase 1 has a redox sensor-like function triggering oligomerization and crosslinking upon oxidative stress related to cell death. Cell Death Dis. 6, e1616 (2015).
50. Q. Cheng, S. Stone-Elander, E. S. J. Arnér, Tagging recombinant proteins with a Sel-tag for purification, labeling with electrophilic compounds or radiolabeling with 11C. Nat. Protoc. 1, 604-613 (2006).
51. O. Rengby, L. Johansson, L. A. Carlson, E. Serini, A. Vlamis-Gardikas, P. Kårsnäs, E. S. J. Arnér, Assessment of production conditions for efficient use of Escherichia coli in high-yield heterologous recombinant selenoprotein synthesis. Appl. Environ. Microbiol. 70, 5159-5167 (2004).
52. J. E. Tropea, S. Cherry, D. S. Waugh, Expression and purification of soluble His6-tagged TEV protease. Methods Mol. Biol. 498, 297-307 (2009).
53. B. McDonagh, Diagonal electrophoresis for detection of protein disulphide bridges. Methods Mol. Biol. 519, 305-310 (2009).
54. C. B. Brachmann, A. Davies, G. J. Cost, E. Caputo, J. Li, P. Hieter, J. D. Boeke, Designer deletion strains derived from Saccharomyces cerevisiae S288C: A useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14, 115-132 (1998).
55. V. Vichai, K. Kirtikara, Sulforhodamine B colorimetric assay for cytotoxicity screening. Nat. Protoc. 1, 1112-1116 (2006).
56. A. Shevchenko, M. Wilm, O. Vorm, M. Mann, Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858 (1996).
57. J. Havliš, H. Thomas, M. Šebela, A. Shevchenko, Fast-response proteomics by accelerated in-gel digestion of proteins. Anal. Chem. 75, 1300-1306 (2003).
58. J. C. Garber, R. W. Barbee, J. T. Bielitzki, L. A. Clayton, J. C. Donovan, D. F. Kohn, N. S. Lipman, P. Locke, J. Melcher, F. W. Quimby, P. V. Turner, G. A. Wood, H. Wurbel, Guide for the Care and Use of Laboratory Animals (The National Academies Press, Washington DC, ed. 8, 2011).
59. E. A. Winzeler, D. D. Shoemaker, A. Astromoff, H. Liang, K. Anderson, B. Andre, R. Bangham, R. Benito, J. D. Boeke, H. Bussey, A. M. Chu, C. Connelly, K. Davis, F. Dietrich, S. W. Dow, M. El Bakkoury, F. Foury, S. H. Friend, E. Gentalen, G. Giaever, J. H. Hegemann, T. Jones, M. Laub, H. Liao, N. Liebundguth, D. J. Lockhart, A. Lucau-Danila, M. Lussier, N. M'Rabet, P. Menard, M. Mittmann, C. Pai, C. Rebischung, J. L. Revuelta, L. Riles, C. J. Roberts, P. Ross-MacDonald, B. Scherens, M. Snyder, S. Sookhai-Mahadeo, R. K. Storms, S. Véronneau, M. Voet, G. Volckaert, T. R. Ward, R. Wysocki, G. S. Yen, K. Yu, K. Zimmermann, P. Philippsen, M. Johnston, R. W. Davis, Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285, 901-906 (1999).