Spectroscopic analysis of protein Fe-NO complexes

Biochemical Society Transactions

Volumn 39, Issue 5, 2011, Pages 1293-1298

  Bellota Antón, César ^a   Munnoch, John ^a   Robb, Kirsty ^a   Adamczyk, Katrin ^a   Candelaresi, Marco ^a   Parker, Anthony W ^b   Dixon, Ray ^c   Hutchings, Matthew I ^d   Hunt, Neil T ^a   Tucker, Nicholas P ^a  

^a UNIVERSITY OF STRATHCLYDE   (United Kingdom)

^b Science and Technology Facilities Council   (United Kingdom)

^c JOHN INNES CENTRE   (United Kingdom)

^d UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

Cytochrome c; Electron paramagnetic resonance (EPR); Myoglobin; NorR; NsrR; Ultrafast two dimensional IR spectroscopy

Indexed keywords

BACTERIAL PROTEIN; CYTOCHROME C; IRON COMPLEX; MYOGLOBIN; NITRIC OXIDE; NORR PROTEIN; NSRR PROTEIN; UNCLASSIFIED DRUG;

ELECTRON SPIN RESONANCE; IN VITRO STUDY; IN VIVO STUDY; NITROSYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; RAMAN SPECTROMETRY; REVIEW; SPECTROSCOPY; ULTRAVIOLET SPECTROSCOPY;

ANIMALS; BACTERIAL PROTEINS; CYTOCHROMES C; HEME; IRON; MYOGLOBIN; NITRIC OXIDE; SPECTRUM ANALYSIS; TRANS-ACTIVATORS;

BACTERIA (MICROORGANISMS); EUKARYOTA;

EID: 80053379761     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0391293     Document Type: Review

References (56)

1. Alderton, W.K., Cooper, C.E. and Knowles, R.G. (2001) Nitric oxide synthases: structure, function and inhibition. Biochem. J. 357, 593-615 (Pubitemid 32735142)
2. Hill, B.G., Dranka, B.P., Bailey, S.M., Lancaster, J.R. and Darley-Usmar, V.M. (2010) What part of NO don't you understand? Some answers to the cardinal questions in nitric oxide biology. J. Biol. Chem. 285, 19699-19704
3. Kass, D.A., Takimoto, E., Nagayama, T. and Champion, H.C. (2007) Phosphodiesterase regulation of nitric oxide signaling. Cardiovasc. Res. 75, 303-314 (Pubitemid 46961917)
4. Jones-Carson, J., Laughlin, J., Hamad, M.A., Stewart, A.L., Voskuil, M.I. and Vázquez-Torres, A. (2008) Inactivation of [Fe-S] metalloproteins mediates nitric oxide-dependent killing of Burkholderia mallei. PLoS ONE 3, e1976
5. Brunori, M. (2001) Nitric oxide, cytochrome c oxidase and myoglobin. Trends Biochem. Sci. 26, 21-23
6. Mills, P.C., Rowley, G., Spiro, S., Hinton, J.C.D. and Richardson, D.J. (2008) A combination of cytochrome c nitrite reductase (NrfA) and flavorubredoxin (NorV) protects Salmonella enterica serovar Typhimurium against killing by NO in anoxic environments. Microbiology 154, 1218-1228 (Pubitemid 351736278)
7. Rodionov, D.A., Dubchak, I.L., Arkin, A.P., Alm, E.J. and Gelfand, M.S. (2005) Dissimilatory metabolism of nitrogen oxides in bacteria: comparative reconstruction of transcriptional networks. PLoS Comput. Biol. 1, e55
8. Fang, F.C. (2004) Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat. Rev. Microbiol. 2, 820-832
9. Hutchings, M.I., Mandhana, N. and Spiro, S. (2002) The NorR protein of Escherichia coli activates expression of the flavorubredoxin gene norV in response to reactive nitrogen species. J. Bacteriol. 184, 4640-4643 (Pubitemid 34832595)
10. Bodenmiller, D.M. and Spiro, S. (2006) The yjeB (nsrR) gene of Escherichia coli encodes a nitric oxide-sensitive transcriptional regulator. J. Bacteriol. 188, 874-881 (Pubitemid 43146402)
11. Tucker, N.P., D'Autréaux, B., Studholme, D.J., Spiro, S. and Dixon, R. (2004) DNA binding activity of the Escherichia coli nitric oxide sensor NorR suggests a conserved target sequence in diverse proteobacteria. J. Bacteriol. 186, 6656-6660 (Pubitemid 39258150)
12. Tucker, N.P., Le Brun, N.E., Dixon, R. and Hutchings, M.I. (2010) There's NO stopping NsrR, a global regulator of the bacterial NO stress response. Trends Microbiol. 18, 149-156
13. D'Autréaux, B., 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 (Pubitemid 41486549)
14. Tucker, N.P., Hicks, M.G., Clarke, T.A., Crack, J.C., Chandra, G., Le Brun, N.E., Dixon, R. and Hutchings, M.I. (2008) The transcriptional repressor protein NsrR senses nitric oxide directly via a [2Fe-2S] cluster. PLoS ONE 3, e3623
15. 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
16. Isabella, V.M., Lapek, Jr, J.D., Kennedy, E.M. and Clark, V.L. (2009) Functional analysis of NsrR, a nitric oxide-sensing Rrf2 repressor in Neisseria gonorrhoeae. Mol. Microbiol. 71, 227-239
17. Giardina, G., Rinaldo, S., Johnson, K.A., Di Matteo, A., Brunori, M. and Cutruzzolà, F. (2008) NO sensing in Pseudomonas aeruginosa: structure of the transcriptional regulator DNR. J. Mol. Biol. 378, 1002-1015
18. Erbil, W.K., Price, M.S., Wemmer, D.E. and Marletta, M.A. (2009) A structural basis for H-NOX signaling in Shewanella oneidensis by trapping a histidine kinase inhibitory conformation. Proc. Natl. Acad. Sci. U.S.A. 106, 19753-19760
19. Wang, Y., Dufour, Y.S., Carlson, H.K., Donohue, T.J., Marletta, M.A. and Ruby, E.G. (2010) H-NOX-mediated nitric oxide sensing modulates symbiotic colonization by Vibrio fischeri. Proc. Natl. Acad. Sci. U.S.A. 107, 8375-8380
20. Spiro, S. (2008) Metalloregulatory proteins and nitric oxide signalling in bacteria. Biochem. Soc. Trans. 36, 1160-1164
21. Fleischhacker, A.S. and Kiley, P.J. (2011) Iron-containing transcription factors and their roles as sensors. Curr. Opin. Chem. Biol. 15, 335-341
22. Stern, K.G. (1937) Spectroscopy of catalase. J. Gen. Physiol. 20, 631-648
23. Hogg, N. (2010) Detection of nitric oxide by electron paramagnetic resonance spectroscopy. Free Radical Biol. Med. 49, 122-129
24. Stone, J.R., Sands, R.H., Dunham, W.R. and Marletta, M.A. (1995) Electron paramagnetic resonance spectral evidence for the formation of a pentacoordinate nitrosyl-heme complex on soluble guanylate cyclase. Biochem. Biophys. Res. Commun. 207, 572-577
25. Ding, H. and Demple, B. (2000) Direct nitric oxide signal transduction via nitrosylation of iron-sulfur centers in the SoxR transcription activator. Proc. Natl. Acad. Sci. U.S.A. 97, 5146-5150 (Pubitemid 30313686)
26. Hunt, N.T. (2009) 2D-IR spectroscopy: ultrafast insights into biomolecule structure and function. Chem. Soc. Rev. 38, 1837-1848
27. Thomas, M.R., Brown, D., Franzen, S. and Boxer, S.G. (2001) FTIR and resonance Raman studies of nitric oxide binding to H93G cavity mutants of myoglobin. Biochemistry 40, 15047-15056 (Pubitemid 33136128)
28. Nienhaus, K., Palladino, P. and Nienhaus, G.U. (2008) Structural dynamics of myoglobin: FTIR-TDS study of NO migration and binding. Biochemistry 47, 935-948 (Pubitemid 351147799)
29. Kruglik, S.G., Yoo, B., Franzen, S., Vos, M.H., Martin, J. and Negrerie, M. (2010) Picosecond primary structural transition of the heme is retarded after nitric oxide binding to heme proteins. Proc. Natl. Acad. Sci. U.S.A. 107, 13678-13683
30. Benabbas, A., Ye, X., Kubo, M., Zhang, Z., Maes, E.M., Montfort, W.R. and Champion, P.M. (2010) Ultrafast dynamics of diatomic ligand binding to nitrophorin 4. J. Am. Chem. Soc. 132, 2811-2820
31. Kubo, M., Gruia, F., Benabbas, A., Barabanschikov, A., Montfort, W.R., Maes, E.M. and Champion, P.M. (2008) Low-frequency mode activity of heme: femtosecond coherence spectroscopy of iron porphine halides and nitrophorin. J. Am. Chem. Soc. 130, 9800-9811
32. Ye, X., Ionascu, D., Gruia, F., Yu, A., Benabbas, A. and Champion, P.M. (2007) Temperature-dependent heme kinetics with nonexponential binding and barrier relaxation in the absence of protein conformational substates. Proc. Natl. Acad. Sci. U.S.A. 104, 14682-14687 (Pubitemid 350003203)
33. Ye, X., Yu, A. and Champion, P.M. (2006) Dynamics of nitric oxide rebinding and escape in horseradish peroxidase. J. Am. Chem. Soc. 128, 1444-1445 (Pubitemid 43214845)
34. Coyle, C.M., Vogel, K.M., Rush, T.S., Kozlowski, P.M., Williams, R., Spiro, T.G., Dou, Y., Ikeda-Saito, M., Olson, J.S. and Zgierski, M.Z. (2003) FeNO structure in distal pocket mutants of myoglobin based on resonance Raman spectroscopy. Biochemistry 42, 4896-4903 (Pubitemid 36532041)
35. Pullan, S.T., Gidley, M.D., Jones, R.A., Barrett, J., Stevanin, T.M., Read, R.C., Green, J. and Poole, R.K. (2007) Nitric oxide in chemostat-cultured Escherichia coli is sensed by Fnr and other global regulators: unaltered methionine biosynthesis indicates lack of S nitrosation. J. Bacteriol. 189, 1845-1855 (Pubitemid 46446147)
36. D'Autréaux, B., Tucker, N., Spiro, S. and Dixon, R. (2008) Characterization of the nitric oxide-reactive transcriptional activator NorR. Methods Enzymol. 437, 235-251
37. 2+ oxidase with metal coordination sites for small molecules and substrate. J. Biol. Chem. 264, 21677-21681
38. Han, A.Y., Lee, A.Q. and Abu-Omar, M.M. (2006) EPR and UV-vis studies of the nitric oxide adducts of bacterial phenylalanine hydroxylase: effects of cofactor and substrate on the iron environment. Inorg. Chem. 45, 4277-4283
39. Tucker, N.P., D'Autréaux, B., Yousafzai, F.K., Fairhurst, S.A., Spiro, S. and Dixon, R. (2008) Analysis of the nitric oxide-sensing non-heme iron center in the NorR regulatory protein. J. Biol. Chem. 283, 908-918
40. Klink, A., Elsner, B., Strube, K. and Cramm, R. (2007) Characterization of the signaling domain of the NO-responsive regulator NorR from Ralstonia eutropha H16 by site-directed mutagenesis. J. Bacteriol. 189, 2743-2749 (Pubitemid 46556056)
41. 54- interaction surface in the enhancer binding protein NorR. Mol. Microbiol. 77, 1278-1288
42. Bush, M., Ghosh, T., Tucker, N., Zhang, X. and Dixon, R. (2011) Transcriptional regulation by the dedicated nitric oxide sensor, NorR: a route towards NO detoxification. Biochem. Soc. Trans. 39, 289-293
43. Rogers, P.A. and Ding, H. (2001) L-Cysteine-mediated destabilization of dinitrosyl iron complexes in proteins. J. Biol. Chem. 276, 30980-30986
44. Kommineni, S., Yukl, E., Hayashi, T., Delepine, J., Geng, H., Moënne-Loccoz, P. and Nakano, M.M. (2010) Nitric oxide-sensitive and -insensitive interaction of Bacillus subtilis NsrR with a ResDE-controlled promoter. Mol. Microbiol. 78, 1280-1293
45. Hamm, P., Lim, M. and Hochstrasser, R.M. (1998) Structure of the amide I band of peptides measured by femtosecond nonlinear-infrared spectroscopy. J. Phys. Chem. B 102, 6123-6138 (Pubitemid 128581186)
46. Khalil, M., Demirdöven, N. and Tokmakoff, A. (2003) Coherent 2D IR spectroscopy: molecular structure and dynamics in solution. J. Phys. Chem. A 107, 5258
47. Ganim, Z., Chung, H.S., Smith, A.W., DeFlores, L.P., Jones, K.C. and Tokmakoff, A. (2008) Amide I two-dimensional infrared spectroscopy of proteins. Acc. Chem. Res. 41, 432
48. Ganim, Z. and Tokmakoff, A. (2006) Spectral signatures of heterogeneous protein ensembles revealed by MD simulations of 2D-IR spectra. Biophys. J. 91, 2636-2646 (Pubitemid 44511717)
49. Chung, H., Ganim, Z. and Jones, K. (2007) Transient 2D IR spectroscopy of ubiquitin unfolding dynamics. Proc. Natl. Acad. Sci. U.S.A. 104, 14237
50. Hamm, P., Lim, M. and DeGrado, W. (1999) The two-dimensional IR nonlinear spectroscopy of a cyclic penta-peptide in relation to its three-dimensional structure. Proc. Natl. Acad. Sci. U.S.A. 96, 2036
51. Ishikawa, H., Kwak, K., Chung, J.K., Kim, S. and Fayer, M.D. (2008) Direct observation of fast protein conformational switching. Proc. Natl. Acad. Sci. U.S.A. 105, 8619-8624 (Pubitemid 351987729)
52. Shim, S., Strasfeld, D. and Ling, Y. (2007) Automated 2D IR spectroscopy using a mid-IR pulse shaper and application of this technology to the human islet amyloid polypeptide. Proc. Natl. Acad. Sci. U.S.A. 104, 14197
53. Hunt, N.T., Greetham, G.M., Towrie, M., Parker, A.W. and Tucker, N.P. (2011) Relationship between protein structural fluctuations and rebinding dynamics in ferric haem nitrosyls. Biochem. J. 433, 459-468
54. Tucker, N.P., Ghosh, T., Bush, M., Zhang, X. and Dixon, R. (2010) Essential roles of three enhancer sites in σ54-dependent transcription by the nitric oxide sensing regulatory protein NorR. Nucleic Acids Res. 38, 1182-1194
55. Szundi, I., Rose, M.J., Sen, I., Eroy-Reveles, A.A., Mascharak, P.K. and Einarsdóttir, O. (2006) A new approach for studying fast biological reactions involving nitric oxide: generation of NO using photolabile ruthenium and manganese NO donors. Photochem. Photobiol. 82, 1377-1384 (Pubitemid 44710773)
56. 13C labeling of a membrane protein for solid-state NMR investigations. J. Biomol. NMR 14, 71-74