Differentiated, promoter-specific response of [4Fe-4S] NsrR DNA binding to reaction with nitric oxide

Journal of Biological Chemistry

Volumn 291, Issue 16, 2016, Pages 8663-8672

  Crack, Jason C ^a   Svistunenko, Dimitri A ^a   Munnoch, John ^b   Thomson, Andrew J ^a   Hutchings, Matthew I ^b   Le Brun, Nick E ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b UNIVERSITY OF ESSEX   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; DNA; GENE EXPRESSION; GENES; IRON COMPOUNDS; MOLECULES; NITRIC OXIDE;

GENE PROMOTER; HIGH AFFINITY; IRON-SULFUR CLUSTERS; KINETIC STUDY; NITROSYLATION REACTIONS; SPECTROSCOPIC EVIDENCE; STREPTOMYCES COELICOLOR; STRESS RESPONSE;

BINS;

DOUBLE STRANDED DNA; MEMBRANE PROTEIN; NITRIC OXIDE; PROTEIN NSRR; UNCLASSIFIED DRUG; BACTERIAL DNA; BACTERIAL PROTEIN; IRON SULFUR PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; GEL MOBILITY SHIFT ASSAY; GENE; GENE CLUSTER; GENE EXPRESSION REGULATION; HMPA1 GENE; HMPA2 GENE; LIPOPHILICITY; NITROSYLATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; STOICHIOMETRY; STREPTOMYCES COELICOLOR; TRANSCRIPTION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

BACTERIAL PROTEINS; DNA, BACTERIAL; IRON-SULFUR PROTEINS; NITRIC OXIDE; PROMOTER REGIONS, GENETIC; STREPTOMYCES COELICOLOR; TRANSCRIPTION FACTORS;

EID: 84965043986     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.693192     Document Type: Article

References (40)

1. Seth, D., Hausladen, A., Wang, Y. J., and Stamler, J. S. (2012) Endogenous protein S-nitrosylation in E. coli: regulation by Oxy R. Science 336, 470-473
2. Weiss, B. (2006) Evidence for mutagenesis by nitric oxide during nitrate metabolism in Escherichia coli. J. Bacteriol. 188, 829-833
3. Broillet, M. C. (1999) S-Nitrosylation of proteins. Cell Mol. Life Sci. 55, 1036-1042
4. Kwon, Y. M., and Weiss, B. (2009) Production of 3-nitrosoindole derivatives by Escherichia coli during anaerobic growth. J. Bacteriol. 191, 5369-5376
5. Crack, J.C., Green, J., and Thomson., A. J., and LeBrun, N. E.(2012) Iron-sulfur cluster sensor-regulators. Curr. Opin. Chem. Biol. 16, 35-44
6. Drapier, J. C. (1997) Interplay between NO and [Fe-S] clusters: relevance to biological systems. Methods 11, 319-329
7. Szabó, C., Ischiropoulos, H., and Radi, R. (2007) Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat. Rev. Drug Discov. 6, 662-680
8. Bruckdorfer, R. (2005) The basics about nitric oxide. Mol. Aspects Med. 26, 3-31
9. Crack, J.C., Green, J., and Thomson., A. J., and LeBrun, N. E.(2014) Iron-sulfur clusters as biological sensors: the chemistry of reactions with molecular oxygen and nitric oxide. Acc. Chem. Res. 47, 3196-3205
10. Spiro, S. (2007) Regulators of bacterial responses to nitric oxide. FEMS Microbiol. Rev. 31, 193-211
11. 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
12. Vine, C. E., and Cole, J. A. (2011) Unresolved sources, sinks, and pathways for the recovery of enteric bacteria from nitrosative stress. FEMS Microbiol. Lett. 325, 99-107
13. Kers, J. A., and Wach., M. J., Krasnoff, S. B., Widom, J., Cameron, K. D., Bukhalid, R. A., Gibson, D. M., Crane, B. R., and Loria, R. (2004) Nitration of a peptide phytotoxin by bacterial nitric oxide synthase. Nature 429, 79-82
14. Partridge, J. D., and Bodenmiller., D. M., Humphrys, M. S., and Spiro, S. (2009) NsrR targets in the Escherichia coli genome: new insights into DNA sequence requirements for binding and a role for NsrR in the regulation of motility. Mol. Microbiol. 73, 680-694
15. Kommineni, S., Lama, A., Popescu, B., and Nakano, M. M. (2012) Global transcriptional control by NsrR in Bacillus subtilis. J. Bacteriol. 194, 1679-1688
16. Heurlier, K., and Thomson., M. J., Aziz, N., and Moir, J. W. (2008) The nitric oxide (NO)-sensing repressor NsrR of Neisseria meningitidis has a compact regulon of genes involved in NO synthesis and detoxification. J. Bacteriol. 190, 2488-2495
17. Stevanin, T. M., and Read., R. C., and Poole, R. K. (2007) The hmp gene encoding the NO-inducible flavohaemoglobin in Escherichia coli confers a protective advantage in resisting killing within macrophages, but not in vitro: links with swarming motility. Gene 398, 62-68
18. Schwartz, C. J., and Giel., J. L., Patschkowski, T., Luther, C., Ruzicka, F. J., Beinert, H., and Kiley, P. J. (2001) IscR, an Fe-S cluster-containing transcription factor, represses expression of Escherichia coli genes encoding Fe-S cluster assembly proteins. Proc. Natl. Acad. Sci. U.S.A. 98, 14895-14900
19. Rajagopalan, S., and Teter., S. J., Zwart, P. H., Brennan, R. G., Phillips, K. J., and Kiley, P. J. (2013) Studies of IscR reveal a unique mechanism for metal-dependent regulation of DNA binding specificity. Nat. Struct. Mol. Biol. 20, 740-747
20. 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
21. Isabella, V. M., and Lapek., J. D., Jr., 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
22. Yukl, E. T., and 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
23. Tucker, N. P., and 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
24. Crack, J. C., Munnoch, J., Dodd, E. L., Knowles, F., Al Bassam, M. M., Kamali, S., Holland, A. A., Cramer, S. P., Hamilton, C. J., Johnson, M. K., Thomson, A. J., Hutchings, M. I., and Le Brun, N. E. (2015) NsrR from Streptomyces coelicolor is a nitric oxide-sensing [4Fe-4S] cluster protein with a specialized regulatory function. J. Biol. Chem. 290, 12689-12704
25. Crack, J. C., Green, J., Thomson, A. J., and Le Brun, N. E. (2014) Techniques for the production, isolation, and analysis of iron-sulfur proteins. Methods Mol. Biol. 1122, 33-48
26. Smith, P. K., and Krohn., R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, N. M., Olson, B. J., and Klenk, D. C. (1985) Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85
27. Cruz-Ramos, H., Crack, J., Wu, G., Hughes, M. N., Scott, C., Thomson, A. J., Green, J., and Poole, R. K. (2002) NO sensing by FNR: regulation of the Escherichia coli NO-detoxifying flavohaemoglobin, Hmp. EMBO J. 21, 3235-3244
28. Kibbe, W. A. (2007) OligoCalc: an online oligonucleotide properties calculator. Nucleic Acids Res. 35, W43-46
29. 2-reactivity of [4Fe-4S] fumarate and nitrate reduction (FNR) regulator. Biochem. J. 463, 83-92
30. Svistunenko, D. A. (2005) Reaction of haem containing proteins and enzymes with hydroperoxides: the radical view. Biochim. Biophys. Acta 1707, 127-155
31. Svistunenko, D. A., Davies, N., Brealey, D., Singer, M., and Cooper, C. E. (2006) Mitochondrial dysfunction in patients with severe sepsis: an EPR interrogation of individual respiratory chain components. Biochim. Biophys. Acta 1757, 262-272
32. Crack, J. C., and Smith., L. J., Stapleton, M. R., Peck, J., Watmough, N. J., Buttner, M. J., Buxton, R. S., Green, J., Oganesyan, V. S., Thomson, A. J., and Le Brun, N. E. (2011) Mechanistic insight into the nitrosylation of the [4Fe-4S] cluster of WhiB-like proteins. J. Am. Chem. Soc. 133, 1112-1121
33. 4 cluster nitrosylation is conserved among NO-responsive regulators. J. Biol. Chem. 288, 11492-11502
34. Kuzmic, P. (1996) Program DYNAFIT for the analysis of enzyme kinetic data: application to HIV proteinase. Anal. Biochem. 237, 260-273
35. 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 S-nitrosothiols with Fe(II). Inorg. Chim. Acta 318, 1-7
36. Vanin, A. F., and Kiladze., S. V., and Kubrina, L. N. (1977) Factors influencing formation of dinitrosyl complexes of non-heme iron in the organs of animals in vivo. Biofizika 22, 850-855
37. Tsai, M. L., and Tsou., C. C., and Liaw, W. F. (2015) Dinitrosyl iron complexes (DNICs): from biomimetic synthesis and spectroscopic characterization toward unveiling the biological and catalytic roles of DNICs. Acc. Chem. Res. 48, 1184-1193
38. Tinberg, C. E., and Tonzetich., Z. J., Wang, H., Do, L.H., Yoda, Y., Cramer, S. P., and Lippard, S.J. (2010) Characterization ofiron dinitrosyl species formed in the reaction of nitric oxide with a biological Rieske center. J. Am. Chem. Soc. 132, 18168-18176
39. Tonzetich, Z.J., Wang, H., Mitra, D., Tinberg, C. E., Do, L.H., Jenney, F. E., Jr., Adams, M. W., Cramer, S. P., and Lippard, S. J. (2010) Identification of protein-bound dinitrosyl iron complexes bynuclear resonance vibrational spectroscopy. J. Am. Chem. Soc. 132, 6914-6916
40. Lewandowska, H., Kalinowska, M., Brzóska, K., Wójciuk, K., Wójciuk, G., and Kruszewski, M. (2011) Nitrosyl iron complexes: synthesis, structure and biology. Dalton Trans 40, 8273-8289