Mechanistic studies on formation of the dinitrosyl iron complex of the [2Fe-2S] cluster of SoxR protein

Journal of Biochemistry

Volumn 156, Issue 3, 2014, Pages 163-172

  Fujikawa, Mayu ^a   Kobayashi, Kazuo ^a   Kozawa, Takahiro ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Dinitrosyl iron complex; Iron sulfur cluster; Nitric oxide; Pulse radiolysis; Transcription factor

Indexed keywords

DINITROSYL IRON COMPLEX; FERREDOXIN; IRON COMPLEX; IRON SULFUR PROTEIN; NITRIC OXIDE; SODIUM NITRITE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOXR; UNCLASSIFIED DRUG; 3-(2-HYDROXY-1-METHYL-2-NITROSOHYDRAZINO)-N-METHYL-1-PROPANAMINE; BACTERIAL PROTEIN; HYDRAZINE DERIVATIVE; IRON; NITRIC OXIDE DONOR; NITROGEN OXIDE; PROTEIN BINDING; SOXR PROTEIN, BACTERIA; SULFUR; VEGETABLE PROTEIN;

ARTICLE; CHEMICAL REACTION; CLUSTER ANALYSIS; COMPARATIVE STUDY; NITROSYLATION; NONHUMAN; PULSE RADIOLYSIS; RADIATION ABSORPTION; REACTION ANALYSIS; SPINACH; ULTRAVIOLET RADIATION; CHEMICAL MODEL; CHEMISTRY; DRUG EFFECTS; ELECTRON SPIN RESONANCE; KINETICS; METABOLISM; OXIDATION REDUCTION REACTION; RADIATION RESPONSE; SPECTROPHOTOMETRY;

BACTERIAL PROTEINS; ELECTRON SPIN RESONANCE SPECTROSCOPY; FERREDOXINS; HYDRAZINES; IRON; IRON-SULFUR PROTEINS; KINETICS; MODELS, CHEMICAL; NITRIC OXIDE; NITRIC OXIDE DONORS; NITROGEN OXIDES; OXIDATION-REDUCTION; PLANT PROTEINS; PROTEIN BINDING; SODIUM NITRITE; SPECTROPHOTOMETRY; SPINACIA OLERACEA; SULFUR; TRANSCRIPTION FACTORS;

EID: 84906079585     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvu029     Document Type: Article

References (74)

1. Ignarro, L.J., Buga, G.M., Wood, K.S., Byrns, R.E., and Chaudhuri, G. (1987) Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl Acad. Sci. USA 84, 9265-9269
2. Rapoport, R.M., Draznin, M.B., and Murad, F. (1983) Endothelium-dependent relaxation in rat aorta may be mediated through cyclic GMP-dependent protein phosphorylation. Nature 306, 174-176
3. Furchgott, R.F. and Vanhoutte, P.M. (1989) Endothelium-derived relaxing and contracting factors. FASEB J. 3, 2007-2018
4. Prast, H. and Philippu, A. (2001) Nitric oxide as modulator of neuronal function. Prog. Neurobiol. 64, 51-68
5. Bogdan, C. (2001) Nitric oxide and the immune response. Nat. Immunol. 2, 907-916
6. MacMicking, J., Xie, Q.W., and Nathan, C. (1997) Nitric oxide and macrofage function. Annu. Rev. Immunol. 15, 323-350
7. Broillet, M.C. (1999) S-Nitrosylation of proteins. Cell. Mol. Life Sci. 55, 1036-1042
8. Kwon, Y.M. and Weiss, B. (2009) Production of 3-nitrosoindole derivatives by Escherichia coli during anaerobic growth. J. Bactriol. 191, 5369-5376
9. Weiss, B. (2006) Evidence for mutagenesis by nitric oxide during nitrate metabolism in Escherichia coli. J. Bacteriol. 188, 829-833
10. Nathan, C. (2003) Specificity of a third kind: reactive oxygen and nitrogen intermediates in cell sign. J. Clin. Invest. 111, 769-778
11. Richardson, A.R., Payne, E.C., Younger, N., Karlinsey, J.E., Thomas, V.C., Becker, L.A., Navarre, W.W., Castor, M.E., Libby, S.J., and Fang, F.C. (2011) Multiple targets of nitric oxide in the tricarboxylic acid cycle of Salmonella enterica serovar typhimurium. Cell Host Microbe 10, 33-43
12. Spiro, S. (2007) Regulators of bacterial responses to nitric oxide. FEMS Mirobiol. Rev. 31, 193-211
13. Autréaux, B.D., Tucker, N.P., Dixon, R., and Spiro, S. (2005) A non-haem iron centre in the transcription factor NorR senses nitric oxide. Nature 437, 769-772
14. Bodenmiller, D.M. and Spiro, S. (2006) The yjeB (nsrR) gene of Escherichia coli encodes a nitric oxide-sensitive transcriptional regulator. J. Bateriol. 188, 874-881
15. Corker, H. and Poole, R.K. (2003) Nitric oxide formation by Escherichia coli: dependence on nitrite reductase, the NO-sensing regulator FNR, and flavohemoglobin Hmp. J. Biol. Chem. 278, 31584-31592
16. Gardner, A.M., Gessner, C.R., and Gardner, P.R. (2003) Regulation of the nitric oxide reduction operon (norRVW) in Escherichia coli. J. Biol. Chem. 278, 10081-10086
17. Nakano, M.M., Geng, H., Nakano, S., and Kobayashi, K. (2006) The nitric oxide-responsive regulator NsrR controls ResDE-dependent gene expression. J. Bactriol. 188, 5878-5887
18. Mukhopadhyay, P., Zheng, M., Bedzyk, L.A., LaRossa, R.A., and Storz, G. (2004) Prominent roles of the NorR and Fur regulators in the Escherichia coli transcriptional response to reactive nitrogen species. Proc. Natl Acad. Sci. USA 101, 745-750
19. Tucker, N.P., Hicks, M.P., Clarke, T.A., Crack, J.C., Chandra, G., LeBrun, N.E., Dixon, R., and Hutchings, M.J. (2008) The transcriptional repressor protein NsrR senses nitric oxide directly via a [2Fe-2S] cluster. PLoS ONE 3, e3623
20. Yukl, E.T., Elbaz, M.A., Nakano, M.M., and Moënne- Loccoz, P. (2008) Transcription factor, NsrR from Bacillus subtilis senses nitric oxide with a 4Fe-4S cluster. Biochemistry 47, 13084-13092
21. Nunoshiba, T., deRojas-Walker, T., Wishnok, J.S., and Tannenbaum, S.R. (1993) Activation by nitric oxide of an oxidative-stress response that defends Escherichia coli against activated macrophages. Proc. Natl Acad. Sci. USA 90, 9993-9997
22. Cruz-Ramos, H., Crack, J., Wu, G., Hughes, M.H., Scott, C., Thomson, A.J., Green, J., and Poole, R.K. (2002) NO sensing by FNR: regulation of the Escherichia coli NO-detoxifying flavohemoglobin, Hmp. EMBO J. 21, 3235-3244
23. Castro, L., Rodriguez, M., and Radi, R. (1994) Aconitase is readily inactivated by peroxynitrite, but not by its precursor, nitric oxide. J. Biol. Chem. 269, 29409-29415
24. Drapier, J.C., Hirling, H., Wietzerbin, J., Kaldz, P., and Kühn, L.C. (1993) Biosynthesis of nitric oxide activates iron regulatory factor in macrophages. EMBO J. 12, 3643-3649
25. Sellers, V.M., Johnson, M.K., and Dailey, H.A. (1996) Function of the [2Fe-2S] Cluster in mammalian ferrochelatase: a possible role as a nitric oxide sensor. Biochemistry 35, 2669-2704
26. Sun, F., Ji, Q., Jones, M.B., Deng, X., Ling, H., Frank, B., Telser, J., Peterson, S.N., Bae, T., and He, C. (2012) J. Am. Chem. Soc. 134, 305-314
27. Butler, A.R. and Megson, I.L. (2002) Non-heme iron nitrosyls in biology. Chem. Rev. 102, 1155-1166
28. Lewandowska, H., Kalinowska, M., Brzòska, K., Wòjciuk, K., Wòjciuk, G., and Kruszewski, M. (2011) Nitrosyl iron complexes-synthesis, structure and biology. Dalton Trans. 40, 8273-8289
29. Vanin, A.F. (2009) Dinitrosyl iron complexes with thiolate ligands: physico-chemistry, biochemistry and physiology. Nitric Oxide 21, 1-13
30. Costanzo, S., Menage, S., Purrello, R., Bonomo, R.P., and Fontecave, M. (2001) Re-examination of the formation of dinitrosyl-iron complexes during reaction of Snitrothiols with Fe(II). Inorg. Chim. Acta 318, 1-7
31. Pieper, G.M., Halligan, N.L., Hilton, G., Konorev, E.A., Felix, C.C., Rosa, A.M., Adams, M.B., and Griffith, O.W. (2003) Non-heme iron protein: a potential target of nitric oxide in acute cardiac allograft rejection. Proc. Natl Acad. Sci. USA 100, 3125-3130
32. Kenedy, M.C., Antholine, W.E., and Beinert, H. (1997) An EPR investigation of the products of the reaction of cytosolic and mitochondrial aconitases with nitric oxide. J. Biol. Chem. 272, 20340-20347
33. Ding, H. and Demple, B. (2000) Direct nitric oxide signal transduction via nitrosylation of iron-sulfur centers in the SoxR transcription activation. Proc. Natl Acad. Sci. USA 97, 5146-5150
34. Tonzetich, Z.J., Wang, H., Mitra, D., Tinberg, C.E., Do, L.H., Jenney, F.E. Jr, Adams, M.W.W., Cramer, S.P., and Lippard, S.J. (2010) Identification of protein-bound dinitrosyl iron complexes by nuclear resonance vibrational spectroscopy. J. Am. Chem. Soc. 132, 6914-6916
35. Tinberg, C.E., Tonzetich, Z.J., Wang, H., Do, L.H., Yoda, Y., Cramer, S.P., and Lippard, S.J. (2010) Characterization of iron dinitrosyl species formed in the reaction of nitric oxide with a biological riske center. J. Am. Chem. Soc. 132, 18168-18176
36. Harrop, T.C., Tonzetich, Z.J., Reisner, E., and Lippard, S.J. (2008) Reactions of synthetic [2Fe-2S] and [4Fe-4S] clusters with nitric oxide and nitrosothiols. J. Am. Chem. Soc. 130, 15602-15610
37. Tennyson, A.G., Dhar, S., and Lippard, S.J. (2008) Synthesis and characterization of {Ni(NO)}10 and {Co(NO)2}10 complexes supported by thiolate ligands. J. Am. Chem. Soc. 130, 15087-15098
38. Brown, N.L., Stoyanov, J.M., Kidd, S.P., and Hobman, J.L. (2003) The MerR family of transcriptional regulators. FEMS Microbiol. Rev. 27, 145-163
39. Kobayashi, K., Fujikawa, M., and Kozawa, T. (2014) Oxidative stress sensing by the iron-sulfur cluster in the transcription factor. J. Inorg. Biochem. 133, 87-91
40. Watanabe, S., Kita, A., Kobayashi, K., and Miki, K. (2008) Crystal structure of the [2Fe-2S] oxidative stress SoxR bound to DNA. Proc. Natl Acad. Sci. USA 105, 4121-4126
41. Hidalgo, E. and Demple, B. (1994) An iron-sulfur center essential for transcriptional activation by the redoxsensing SoxR protein. EMBO J. 13, 138-146
42. Hidalgo, E., Ding, H., and Demple, B. (1997) Redox signal transduction: mutations shifting [2Fe-2S] centers of the SoxR sensor-regulator to the oxidized form. Cell 88, 121-129
43. Blanchard, J.L., Wholey, W.Y., Conlon, E.M., and Pomposiello, P.J. (2007) Rapid changes in gene expression dynamics in response to superoxide reveal soxRSdependent and independent transcriptional networks. PLoS ONE 2, e1186
44. Fujikawa, M., Kobayashi, K., and Kozawa, T. (2012) Direct oxidation of the [2Fe-2S] cluster in SoxR protein by superoxide. J. Biol. Chem. 287, 35702-35708
45. Nunoshiba, T., deRojas-Walker, T., Wishnok, J.S., and Tannenbaum, S.R. (1995) Roles of nitric oxide in inducible resistance of Escherichia coli to activated murine macrophages. Infect. Immun. 63, 794-798
46. Demple, B. (2002) Signal transduction by nitric oxide in cellular stress responses. Mol. Cell. Biochem. 234/235, 11-18
47. Lo, F.-C., Chen, C.-L., Lee, C.-M., Tsai, M.-C., Lu, T.-T., Liaw, W.-F., and Yu, S.S.-F. (2008) A study of NO trafficking from dinitrosyl-iron complexes to the recombinant E. coli transcriptional factor Sox R. J. Biol. Inorg. Chem. 13, 961-972
48. Lo, F.-C., Lee, J.-F., Liaw, W.-F., Hsu, I.-J., Tsai, Y.-F., Chan, S.C., and Yu, S.S.-F. (2012) The metal core structures in the recombinant Escherichia coli transcription factor Sox R. Chem. Eur. J. 18, 2565-2577
49. Grätzel, M., Henglein, H., Lilie, J., and Beck, G. (1969) Pulsradiolytische untersuchung einiger elementarprozesse der oxydation und reduktion des nitritions. Ber. Busenges. Phys. Chem. 73, 646-653
50. Kobayashi, K., Miki, M., and Tagawa, S. (1995) Pulseradiolysis study of the reaction of nitric oxide with superoxide. J. Chem. Soc. Dalton Tran. 17, 2885-2889
51. Fujii, S., Kobayashi, K., Tagawa, S., and Yoshimura, T. (2000) Reaction of nitric oxide with the iron(III) complex of N-(dithio-carboxy)sarcosine: a new type of reductive nitrosylation involving iron(IV) as an intermediate. J. Chem. Soc. Dalton Trans. 19, 3310-3315
52. Filipovic, M.R., Miljkovic, J.L., Nauser, T., Royzen, M., Klos, K., Shubina, T., Koppenol, W.H., Lippard, S.J., and Ivanović- Burmazović. (2012) Chemical characterization of the smallest S-nitrosothiol, HSNO; cellular cross-talk of H2S and S-nitrosothiols. J. Am. Chem. Soc. 134, 12016-12027
53. Tonzetich, Z.J., McQuade, L.E., and Lippard, S.J. (2010) Detecting and understanding the roles of nitric oxide in biology. Inorg. Chem. 49, 6338-6348
54. Crack, J.C., Smith, L.J., Stapleton, M.R., Peck, J., Watmough, J., Buttner, M.J., Buxton, R.S., Green, J., Oganesyan, V.S., Thomson, A.J., and LeBrun, N.E.L. (2010) Mechanistic insight into the nitrosylation of the [4Fe-4S] cluster of WhiB-like proteins. J. Am. Chem. Soc. 133, 1112-1121
55. Crack, J.C., Stapleton, M.R., Green, J., Thomson, A.J., and LeBrun, N.E. (2013) Mechansm of [4Fe-4S](Cys)4 cluster nitration is conserved among NO-responsive regulators. J. Biol. Chem. 288, 11492-11502
56. Hiwatashi, A., Ichikawa, Y., Maruya, N., Yamano, T., and Aki, K. (1976) Properties of crystalline reduced nicotinamide adenine dinucleotide phosphate-adrenodoxin reductase from bovine adrenocortical mitochondria. I. Physicochemical properties of holo- and apo-NADPHadrenodoxin reductase and interaction between nonheme iron proteins and the reductase. Biochemistry 15, 3082-3090
57. Nakamura, M., Saeki, K., and Takahashi, Y. (1999) Hyperproduction of recombinant ferredoxins in Escherichia coli by coexpression of the ORF1-ORF2- iscS-iscU-iscA-hscB-hscA-fdx-ORF3 gene cluster. J. Biochem. 126, 10-18
58. Watanabe, S., Kita, A., Kobayashi, K., Takahashi, Y., and Miki, K. (2006) Crystallization and preliminary Xray crystallographic studies of the oxidative stress sensor SoxR and its complex with DNA. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 62, 1275-1277
59. Wu, J., Dunham, W.R., and Weiss, B. (1995) Overproduction and physical characterization of Sox R, a [2Fe-2S] protein that governs an oxidative response regulon in Escherichia coli. J. Biol. Chem. 270, 10323-10327
60. Hase, T., Wada, K., and Matsubara, H. (1997) Horsetail (Equisetum arvense) ferredoxins I and II: amino acid sequences and gene duplication. J. Biochem. 82, 267-276
61. Kobayashi, K., Tsubaki, M., and Tagawa, S. (1998) Distinct roles of two heme centers for transmembrane electron transfer in cytochrome b561 from bovine adrenal chromaffin vesicles as revealed by pulse radiolysis. J. Biol. Chem. 273, 16038-16042
62. Gordon, S. and Hart, E.J. (1964) Spectrophotometric detection of hydrated electrons in Co60 g-ray irradiated solutions. J. Am. Chem. Soc. 86, 5343-5344
63. Sörbo, B. (1957) A colorimetric method for the determination of thiosulfate. Biochim. Biophys. Acta 23, 412-416
64. Petering, D., Fee, J.A., and Palmer, G. (1971) The oxygen sensitivity of spinach ferredoxin and other ironsulfur proteins: the formation of protein-bound sulfurzero. J. Biol. Chem. 246, 643-653
65. Stone, J.R. and Marletta, M.A. (1996) Spectral and ligand-binding properties of an unusual hemoprotein, the ferric form of soluble guanylate cyclase. Biochemistry 35, 1093-1099
66. Kharitonov, V.G., Sharma, V.S., Magde, D., and Koesling, D. (1999) Kinetics and equilibria of soluble guanylate cyclase ligation by CO: effect of YC-1. Biochemistry 38, 10699-10706
67. Dietrich, L.E., Price-Whelan, A., Petersen, A., Whiteley, M., and Newman, D.K. (2006) The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol. Microbiol. 61, 1308-1321
68. Rypniewski, W.R., Breiter, D.R., Benning, M.M., Wesenber, G., Oh, B.H., Markley, J.L., Rayment, I., and Holden, H.M. (1991) Crystallization and structure determination of 2.5-Åresolution of the oxidized ironsulfur [2Fe-2S] ferredoxin isolated from Anabaena 7120. Refined crystal structure of spinach ferredoxin reductase at 1.7 A ̊resolution: oxidized. Biochemistry 30, 4126-4131
69. Müller, A., Müller, J.J., Muller, Y.A., Uhlmann, H., Bernhardt, R., and Heinemann, U. (1998) New aspects of electron transfer revealed by the crystal structure of a truncated bovine adrenodoxin Adx(4-108). Structure 6, 269-280
70. Ding, H. and Demple, B. (1997) In vivo kinetics of a redox-regulated transcriptional switch. Proc. Natl Acad. Sci. USA 94, 8445-8449
71. Kobayashi, K. and Tagawa, S. (1999) Isolation of reductase for SoxR that governs an oxidative response regulon from Escherichia coli. FEBS Lett. 45, 227-230
72. Koo, M.S., Lee, J.H., Rah, S.Y., Yeo, W.S., Lee, J.W., Lee, K.L., Koh, Y.S., Kang, S.O., and Roe, J.H. (2003) A reducing system of the superoxide sensor SoxR in Escherichia coli. EMBO J. 22, 2614-2622
73. Rogers, P.A. and Ding, H. (2001) L-Cysteine-mediated destabilization of dinitrosyl iron complexes in proteins. J. Biol. Chem. 277, 30980-30986
74. Yang, W., Rogers, P.A., and Ding, H. (2002) Repair of nitric oxide-modified ferredoxin [2Fe-2S] cluster by cysteine desulfurase (IscS). J. Biol. Chem. 277, 12868-12873