Biosynthesis and Reactivity of Cysteine Persulfides in Signaling

Journal of the American Chemical Society

Volumn 138, Issue 1, 2016, Pages 289-299

  Yadav, Pramod K ^a   Martinov, Michael ^b   Vitvitsky, Victor ^a   Seravalli, Javier ^c   Wedmann, Rudolf ^d   Filipovic, Milos R ^d   Banerjee, Ruma ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b CENTER FOR THEORETICAL PROBLEMS OF PHYSICOCHEMICAL PHARMACOLOGY   (Russian Federation)

^c UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^d UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CYSTINES; ENZYMES; PHYSIOLOGY; POLYSULFIDES; SULFUR COMPOUNDS;

DECOMPOSITION PRODUCTS; DETAILED KINETICS; INTRINSIC REACTIVITY; PHYSIOLOGICAL EFFECTS; POST-TRANSLATIONAL MODIFICATIONS; PRIMARY PRODUCTS; REACTIVE CYSTEINE; SUBSTRATE CONCENTRATIONS;

AMINO ACIDS;

CYSTATHIONINE BETA SYNTHASE; CYSTATHIONINE GAMMA LYASE; CYSTEINE DERIVATIVE; CYSTEINE PERSULFIDE DERIVATIVE; CYSTINE; ENZYME; GAMMA CYSTATHIONINE GAMMA LYASE; HOMOCYSTEINE; HOMOCYSTINE; SULFIDE; SULFURTRANSFERASE; THIOL; UNCLASSIFIED DRUG; CYSTEINE; CYSTEINE PERSULFIDE; DISULFIDE;

ARTICLE; BIOSYNTHESIS; DECOMPOSITION; IN VITRO STUDY; KINETICS; SYNTHESIS; ANALOGS AND DERIVATIVES; CELL CULTURE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; SIGNAL TRANSDUCTION;

CELLS, CULTURED; CHROMATOGRAPHY, LIQUID; CYSTEINE; DISULFIDES; KINETICS; MASS SPECTROMETRY; SIGNAL TRANSDUCTION;

EID: 84954448866     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/jacs.5b10494     Document Type: Article

References (62)

1. Lavu, M.; Bhushan, S.; Lefer, D. J. Clin. Sci. 2011, 120, 219 10.1042/CS20100462
2. Abe, K.; Kimura, H. J. Neurosci. 1996, 16, 1066
3. Kimura, Y.; Goto, Y.; Kimura, H. Antioxid. Redox Signaling 2010, 12, 1 10.1089/ars.2008.2282
4. Kimura, Y.; Kimura, H. FASEB J. 2004, 18, 1165 10.1096/fj.04-1815fje
5. Zanardo, R. C.; Brancaleone, V.; Distrutti, E.; Fiorucci, S.; Cirino, G.; Wallace, J. L. FASEB J. 2006, 20, 2118 10.1096/fj.06-6270fje
6. Li, L.; Bhatia, M.; Zhu, Y. Z.; Zhu, Y. C.; Ramnath, R. D.; Wang, Z. J.; Anuar, F. B.; Whiteman, M.; Salto-Tellez, M.; Moore, P. K. FASEB J. 2005, 19, 1196
7. Mustafa, A. K.; Gadalla, M. M.; Sen, N.; Kim, S.; Mu, W.; Gazi, S. K.; Barrow, R. K.; Yang, G.; Wang, R.; Snyder, S. H. Sci. Signaling 2009, 2, ra72 10.1126/scisignal.2000464
8. Cuevasanta, E.; Lange, M.; Bonanata, J.; Coitino, E. L.; Ferrer-Sueta, G.; Filipovic, M. R.; Alvarez, B. J. Biol. Chem. 2015, 290, 26866 10.1074/jbc.M115.672816
9. Carballal, S.; Trujillo, M.; Cuevasanta, E.; Bartesaghi, S.; Moller, M. N.; Folkes, L. K.; Garcia-Bereguiain, M. A.; Gutierrez-Merino, C.; Wardman, P.; Denicola, A.; Radi, R.; Alvarez, B. Free Radical Biol. Med. 2011, 50, 196 10.1016/j.freeradbiomed.2010.10.705
10. Mishanina, T. V.; Libiad, M.; Banerjee, R. Nat. Chem. Biol. 2015, 11, 457 10.1038/nchembio.1834
11. Kabil, O.; Banerjee, R. J. Biol. Chem. 2010, 285, 21903 10.1074/jbc.R110.128363
12. Kabil, O.; Banerjee, R. Antioxid. Redox Signaling 2014, 20, 770 10.1089/ars.2013.5339
13. Kabil, O.; Motl, N.; Banerjee, R. Biochim. Biophys. Acta, Proteins Proteomics 2014, 1844, 1355 10.1016/j.bbapap.2014.01.002
14. Kimura, Y.; Mikami, Y.; Osumi, K.; Tsugane, M.; Oka, J.; Kimura, H. FASEB J. 2013, 27, 2451 10.1096/fj.12-226415
15. Ida, T.; Sawa, T.; Ihara, H.; Tsuchiya, Y.; Watanabe, Y.; Kumagai, Y.; Suematsu, M.; Motohashi, H.; Fujii, S.; Matsunaga, T.; Yamamoto, M.; Ono, K.; Devarie-Baez, N. O.; Xian, M.; Fukuto, J. M.; Akaike, T. Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 7606 10.1073/pnas.1321232111
16. Vitvitsky, V.; Yadav, P. K.; Kurthen, A.; Banerjee, R. J. Biol. Chem. 2015, 290, 8310 10.1074/jbc.M115.639831
17. Kimura, Y.; Toyofuku, Y.; Koike, S.; Shibuya, N.; Nagahara, N.; Lefer, D.; Ogasawara, Y.; Kimura, H. Sci. Rep. 2015, 5, 14774 10.1038/srep14774
18. Greiner, R.; Palinkas, Z.; Basell, K.; Becher, D.; Antelmann, H.; Nagy, P.; Dick, T. P. Antioxid. Redox Signaling 2013, 19, 1749 10.1089/ars.2012.5041
19. Toohey, J. I. Biochem. J. 1989, 264, 625 10.1042/bj2640625
20. Libiad, M.; Yadav, P. K.; Vitvitsky, V.; Martinov, M.; Banerjee, R. J. Biol. Chem. 2014, 289, 30901 10.1074/jbc.M114.602664
21. Yadav, P. K.; Yamada, K.; Chiku, T.; Koutmos, M.; Banerjee, R. J. Biol. Chem. 2013, 288, 20002 10.1074/jbc.M113.466177
22. Mueller, E. G. Nat. Chem. Biol. 2006, 2, 185 10.1038/nchembio779
23. Cavallini, D.; Mondovi, B.; De Marco, C.; Sciosciasantoro, A. Arch. Biochem. Biophys. 1962, 96, 456 10.1016/0003-9861(62)90436-8
24. Chiku, T.; Padovani, D.; Zhu, W.; Singh, S.; Vitvitsky, V.; Banerjee, R. J. Biol. Chem. 2009, 284, 11601 10.1074/jbc.M808026200
25. Roman-Morales, E.; Pietri, R.; Ramos-Santana, B.; Vinogradov, S. N.; Lewis-Ballester, A.; Lopez-Garriga, J. Biochem. Biophys. Res. Commun. 2010, 400, 489 10.1016/j.bbrc.2010.08.068
26. Kabil, O.; Vitvitsky, V.; Xie, P.; Banerjee, R. Antioxid. Redox Signaling 2011, 15, 363 10.1089/ars.2010.3781
27. Pan, J.; Carroll, K. S. ACS Chem. Biol. 2013, 8, 1110 10.1021/cb4001052
28. Singh, S.; Padovani, D.; Leslie, R. A.; Chiku, T.; Banerjee, R. J. Biol. Chem. 2009, 284, 22457 10.1074/jbc.M109.010868
29. Singh, S.; Banerjee, R. Biochim. Biophys. Acta, Proteins Proteomics 2011, 1814, 1518 10.1016/j.bbapap.2011.02.004
30. Hildebrandt, T. M.; Grieshaber, M. K. FEBS J. 2008, 275, 3352 10.1111/j.1742-4658.2008.06482.x
31. Stipanuk, M. H.; Beck, P. W. Biochem. J. 1982, 206, 267 10.1042/bj2060267
32. Chen, X.; Jhee, K. H.; Kruger, W. D. J. Biol. Chem. 2004, 279, 52082 10.1074/jbc.C400481200
33. Vitvitsky, V.; Dayal, S.; Stabler, S.; Zhou, Y.; Wang, H.; Lentz, S. R.; Banerjee, R. Am. J. Physiol.: Regul., Integr. Comp. Physiol. 2004, 287, R39 10.1152/ajpregu.00036.2004
34. Zhu, W.; Lin, A.; Banerjee, R. Biochemistry 2008, 47, 6226 10.1021/bi800351a
35. Taoka, S.; Ohja, S.; Shan, X.; Kruger, W. D.; Banerjee, R. J. Biol. Chem. 1998, 273, 25179 10.1074/jbc.273.39.25179
36. Wood, J. L. Methods Enzymol. 1987, 143, 25 10.1016/0076-6879(87)43009-7
37. Zhang, D.; Macinkovic, I.; Devarie-Baez, N. O.; Pan, J.; Park, C. M.; Carroll, K. S.; Filipovic, M. R.; Xian, M. Angew. Chem., Int. Ed. 2014, 53, 575 10.1002/anie.201305876
38. Park, C. M.; Macinkovic, I.; Filipovic, M. R.; Xian, M. Methods Enzymol. 2015, 555, 39 10.1016/bs.mie.2014.11.033
39. Artaud, I.; Galardon, E. ChemBioChem 2014, 15, 2361 10.1002/cbic.201402312
40. Hansen, R. E.; Roth, D.; Winther, J. R. Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 422 10.1073/pnas.0812149106
41. Chen, W.; Liu, C.; Peng, B.; Zhao, Y.; Pacheco, A.; Xian, M. Chem. Sci. 2013, 4, 2892 10.1039/c3sc50754h
42. Bittles, A. H.; Carson, N. A. J. Med. Genet 1974, 11, 121 10.1136/jmg.11.2.121
43. Prudova, A.; Bauman, Z.; Braun, A.; Vitvitsky, V.; Lu, S. C.; Banerjee, R. Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 6489 10.1073/pnas.0509531103
44. Vitvitsky, V.; Witcher, M.; Banerjee, R.; Thoene, J. Mol. Genet. Metab. 2010, 99, 384 10.1016/j.ymgme.2009.12.010
45. Town, M.; Jean, G.; Cherqui, S.; Attard, M.; Forestier, L.; Whitmore, S. A.; Callen, D. F.; Gribouval, O.; Broyer, M.; Bates, G. P.; van't Hoff, W.; Antignac, C. Nat. Genet. 1998, 18, 319 10.1038/ng0498-319
46. Kimura, H. Antioxid. Redox Signaling 2015, 22, 347 10.1089/ars.2014.6082
47. Yamanishi, T.; Tuboi, S. J. Biochem 1981, 89, 1913
48. Jones, D. P.; Go, Y. M.; Anderson, C. L.; Ziegler, T. R.; Kinkade, J. M., Jr.; Kirlin, W. G. FASEB J. 2004, 18, 1246 10.1096/fj.03-0971fje
49. Bannai, S. J. Biol. Chem. 1986, 261, 2256
50. Pader, I.; Sengupta, R.; Cebula, M.; Xu, J.; Lundberg, J. O.; Holmgren, A.; Johansson, K.; Arner, E. S. Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 6964 10.1073/pnas.1317320111
51. Prudova, A.; Martinov, M. V.; Vitvitsky, V.; Ataullakhanov, F.; Banerjee, R. Biochim. Biophys. Acta, Mol. Basis Dis. 2005, 1741, 331 10.1016/j.bbadis.2005.04.008
52. Vitvitsky, V.; Kabil, O.; Banerjee, R. Antioxid. Redox Signaling 2012, 17, 22 10.1089/ars.2011.4310
53. Vitvitsky, V.; Martinov, M.; Ataullakhanov, F.; Miller, R. A.; Banerjee, R. Mech. Ageing Dev. 2013, 134, 321 10.1016/j.mad.2013.05.004
54. Mudd, S. H.; Finkelstein, J. D.; Irreverre, F.; Laster, L. Science 1964, 143, 1443 10.1126/science.143.3613.1443
55. Refsum, H.; Ueland, P. M.; Nygard, O.; Vollset, S. E. Annu. Rev. Med. 1998, 49, 31 10.1146/annurev.med.49.1.31
56. Fu, M.; Zhang, W.; Wu, L.; Yang, G.; Li, H.; Wang, R. Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 2943 10.1073/pnas.1115634109
57. Thomas, K.; Wong, K.; Withington, J.; Bultitude, M.; Doherty, A. Nat. Rev. Urol. 2014, 11, 270 10.1038/nrurol.2014.51
58. Portillo-Ledesma, S.; Sardi, F.; Manta, B.; Tourn, M. V.; Clippe, A.; Knoops, B.; Alvarez, B.; Coitino, E. L.; Ferrer-Sueta, G. Biochemistry 2014, 53, 6113 10.1021/bi500389m
59. Bailey, T. S.; Zakharov, L. N.; Pluth, M. D. J. Am. Chem. Soc. 2014, 136, 10573 10.1021/ja505371z
60. Weerapana, E.; Wang, C.; Simon, G. M.; Richter, F.; Khare, S.; Dillon, M. B.; Bachovchin, D. A.; Mowen, K.; Baker, D.; Cravatt, B. F. Nature 2010, 468, 790 10.1038/nature09472
61. Roman, H. B.; Hirschberger, L. L.; Krijt, J.; Valli, A.; Kozich, V.; Stipanuk, M. H. Antioxid. Redox Signaling 2013, 19, 1321 10.1089/ars.2012.5010
62. Finkelstein, J. D.; Martin, J. J. J. Biol. Chem. 1986, 261, 1582