NsrR from streptomyces coelicolor is a nitric oxide-sensing [4Fe-4S] cluster protein with a specialized regulatory function

Journal of Biological Chemistry

Volumn 290, Issue 20, 2015, Pages 12689-12704

  Crack, Jason C ^a   Munnoch, John ^a   Dodd, Erin L ^a   Knowles, Felicity ^a   Al Bassam, Mahmoud M ^a   Kamali, Saeed ^b   Holland, Ashley A ^c   Cramer, Stephen P ^b   Hamilton, Chris J ^a   Johnson, Michael K ^c   Thomson, Andrew J ^a   Hutchings, Matthew I ^a   Le Brun, Nick E ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BACTERIA; DETOXIFICATION; MASS SPECTROMETRY; NITRIC OXIDE; PROTEINS;

FLAVOHEMOGLOBINS; GLOBAL REGULATORS; INVERTED REPEAT; LOW MOLECULAR WEIGHT; NATIVE MASS SPECTROMETRIES; REGULATORY FUNCTIONS; RESONANCE RAMAN SPECTROSCOPY; STREPTOMYCES COELICOLOR;

TRANSCRIPTION;

IRON SULFUR PROTEIN; NITRIC OXIDE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NSRR; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; DNA BINDING PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL GENE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA SEQUENCE; HMPA1 GENE; HMPA2 GENE; IN VIVO STUDY; INVERTED REPEAT; NONHUMAN; NSRR GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN FUNCTION; REGULATORY MECHANISM; STREPTOMYCES COELICOLOR; GENETICS; METABOLISM; PHYSIOLOGY; REGULON;

STREPTOMYCES COELICOLOR;

BACTERIAL PROTEINS; DNA-BINDING PROTEINS; IRON-SULFUR PROTEINS; NITRIC OXIDE; PROMOTER REGIONS, GENETIC; REGULON; STREPTOMYCES COELICOLOR;

EID: 84929340857     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.643072     Document Type: Article

References (62)

1. Hess, D. T., and Stamler, J. S. (2012) Regulation by S-nitrosylation of protein post-translational modification. J. Biol. Chem. 287, 4411-4418
2. Seth, D., Hausladen, A., Wang, Y. J., and Stamler, J. S. (2012) Endogenous protein S-nitrosylation in E. coli: regulation by OxyR. Science 336, 470-473
3. Kwon, Y. M., and Weiss, B. (2009) Production of 3-nitrosoindole derivatives by Escherichia coli during anaerobic growth. J. Bacteriol. 191, 5369-5376
4. Weiss, B. (2006) Evidence for mutagenesis by nitric oxide during nitrate metabolism in Escherichia coli. J. Bacteriol. 188, 829-833
5. Crack, J. C., Green, J., Thomson, A. J., and Le Brun, N. E. (2012) Iron-sulfur cluster sensor-regulators. Curr. Opin. Chem. Biol. 16, 35-44
6. Bruckdorfer, R. (2005) The basics about nitric oxide. Mol. Aspects Med. 26, 3-31
7. 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
8. Sudhamsu, J., and Crane, B. R. (2009) Bacterial nitric oxide synthases: what are they good for? Trends Microbiol. 17, 212-218
9. Demple, B. (2002) Signal transduction by nitric oxide in cellular stress responses. Mol. Cell Biochem. 234, 11-18
10. Crack, J. C., Stapleton, M. R., Green, J., Thomson, A. J., and Le Brun, N. E. (2013) Mechanism of [4Fe-4S](Cys)4 cluster nitrosylation is conserved among NO-responsive regulators. J. Biol. Chem. 288, 11492-11502
11. Hutchings, M. I., Crack, J. C., Shearer, N., Thompson, B. J., Thomson, A. J., and Spiro, S. (2002) Transcription factor FnrP from Paracoccus denitrificans contains an iron-sulfur cluster and is activated by anoxia: identification of essential cysteine residues. J. Bacteriol. 184, 503-508
12. 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
13. Partridge, J. D., 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
14. Stevanin, T. M., 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
15. 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
16. Rajagopalan, S., 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
17. 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
18. Isabella, V. M., 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
19. 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
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. 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
22. Kieser, T., Bibb, M. J., Buttner, M. J., Chater, K. F., and Hopwood, D. A. (2000) Practical Streptomyces Genetics, p. 412, John Innes Foundation, Norwich
23. Gregory, M. A., Till, R., and Smith, M. C. (2003) Integration site for Streptomyces phage phiBT1 and development of site-specific integrating vectors. J. Bacteriol. 185, 5320-5323
24. Kibbe, W. A. (2007) OligoCalc: an online oligonucleotide properties calculator. Nucleic Acids Res. 35, W43-W46
25. Al-Bassam, M. M., Bibb, M. J., Bush, M. J., Chandra, G., and Buttner, M. J. (2014) Response regulator heterodimer formation controls a key stage in Streptomyces development. PLoS Genet. 10, e1004554
26. Fernández-Martinez, L. T., Del Sol, R., Evans, M. C., Fielding, S., Herron, P. R., Chandra, G., and Dyson, P. J. (2011) A transposon insertion singlegene knockout library and new ordered cosmid library for the model organism Streptomyces coelicolor A3(2). Antonie Van Leeuwenhoek 99, 515-522
27. Redenbach, M., Kieser, H. M., Denapaite, D., Eichner, A., Cullum, J., Kinashi, H., and Hopwood, D. A. (1996) A set of ordered cosmids and a detailed genetic and physical map for the 8 Mb Streptomyces coelicolor A3(2) chromosome. Mol. Microbiol. 21, 77-96
28. 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
29. Smith, P. K., 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
30. Crack, J. C., Gaskell, A. A., Green, J., Cheesman, M. R., Le Brun, N. E., and Thomson, A. J. (2008) Influence of the environment on the [4Fe-4S]2+ to [2Fe-2S]2+ cluster switch in the transcriptional regulator FNR. J. Am. Chem. Soc. 130, 1749-1758
31. Crack, J. C., den Hengst, C. D., Jakimowicz, P., Subramanian, S., Johnson, M. K., Buttner, M. J., Thomson, A. J., and Le Brun, N. E. (2009) Characterization of [4Fe-4S]-containing and cluster-free forms of Streptomyces WhiD. Biochemistry 48, 12252-12264
32. Stewart, M. J., Jothivasan, V. K., Rowan, A. S., Wagg, J., and Hamilton, C. J. (2008) Mycothiol disulfide reductase: solid phase synthesis and evaluation of alternative substrate analogues. Org. Biomol. Chem. 6, 385-390
33. Riddles, P. W., Blakeley, R. L., and Zerner, B. (1983) Reassessment of Ellman's reagent. Methods Enzymol. 91, 49-60
34. Lagarec, K., and Rancourt, D. C. (1998) Recoil: Mössbauer spectral analysis software for Windows, version 1.0, University of Ottawa, Canada
35. 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
36. Stephens, P. J., Thomson, A. J., Dunn, J. B., Keiderling, T. A., Rawlings, J., Rao, K. K., and Hall, D. O. (1978) Circular dichroism and magnetic circular dichroism of iron-sulfur proteins. Biochemistry 17, 4770-4778
37. Beinert, H., Holm, R. H., and Münck, E. (1997) Iron-sulfur clusters: Nature's modular, multipurpose structures. Science 277, 653-659
38. Dickson, D. P. E., Johnson, C. E., Thompson, C. L., Cammack, R., Evans, M. C. W., Hall, D. O., Rao, K. K., and Weser, U. (1974) Mössbauer effect studies on the four iron centres of two iron-sulphur proteins. J. Phys. Colloques 10.1051/jphyscol:1974659
39. Cicchillo, R. M., Lee, K. H., Baleanu-Gogonea, C., Nesbitt, N. M., Krebs, C., and Booker, S. J. (2004) Escherichia coli lipoyl synthase binds two distinct [4Fe-4S] clusters per polypeptide. Biochemistry 43, 11770-11781
40. Hernández, H. L., Pierrel, F., Elleingand, E., García-Serres, R., Huynh, B. H., Johnson, M. K., Fontecave, M., and Atta, M. (2007) MiaB, a bifunctional radical-S-adenosylmethionine enzyme involved in the thiolation and methylation of tRNA, contains two essential [4Fe-4S] clusters. Biochemistry 46, 5140-5147
41. Fleischhacker, A. S., Stubna, A., Hsueh, K. L., Guo, Y., Teter, S. J., Rose, J. C., Brunold, T. C., Markley, J. L., Münck, E., and Kiley, P. J. (2012) Characterization of the [2Fe-2S] cluster of Escherichia coli transcription factor IscR. Biochemistry 51, 4453-4462
42. Czernuszewicz, R. S., Macor, K. A., Johnson, M. K., Gewirth, A., and Spiro, T. G. (1987) Vibrational-mode structure and symmetry in proteins and analogs containing Fe4S4 clusters: resonance Raman evidence for different degrees of distortion in HiPIP and Ferredoxin. J. Am. Chem. Soc. 109, 7178-7187
43. Conover, R. C., Kowal, A. T., Fu, W. G., Park, J. B., Aono, S., Adams, M. W., and Johnson, M. K. (1990) Spectroscopic characterization of the novel iron-sulfur cluster in Pyrococcus furiosus ferredoxin. J. Biol. Chem. 265, 8533-8541
44. Brereton, P. S., Duderstadt, R. E., Staples, C. R., Johnson, M. K., and Ad-ams, M. W. (1999) Effect of serinate ligation at each of the iron sites of the [Fe4S4] cluster of Pyrococcus furiosus ferredoxin on the redox, spectroscopic, and biological properties. Biochemistry 38, 10594-10605
45. Zhang, B., Crack, J. C., Subramanian, S., Green, J., Thomson, A. J., Le Brun, N. E., and Johnson, M. K. (2012) Reversible cycling between cysteine persulfide-ligated [2Fe-2S] and cysteine-ligated [4Fe-4S] clusters in the FNR regulatory protein. Proc. Natl. Acad. Sci. U.S.A. 109, 15734-15739
46. Nakano, M. M., Geng, H., Nakano, S., and Kobayashi, K. (2006) The nitric oxide-responsive regulator NsrR controls ResDE-dependent gene expression. J. Bacteriol. 188, 5878-5887
47. Jothivasan, V. K., and Hamilton, C. J. (2008) Mycothiol: synthesis, biosynthesis and biological functions of the major low molecular weight thiol in actinomycetes. Nat. Prod. Rep. 25, 1091-1117
48. Newton, G. L., Bewley, C. A., Dwyer, T. J., Horn, R., Aharonowitz, Y., Cohen, G., Davies, J., Faulkner, D. J., and Fahey, R. C. (1995) The structure of U17 isolated from Streptomyces clavuligerus and its properties as an antioxidant thiol. Eur. J. Biochem. 230, 821-825
49. Newton, G. L., Fahey, R. C., Cohen, G., and Aharonowitz, Y. (1993) Low molecular weight thiols in streptomycetes and their potential role as antioxidants. J. Bacteriol. 175, 2734-2742
50. Crack, J. C., 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
51. Calzolai, L., Gorst, C. M., Zhao, Z. H., Teng, Q., Adams, M. W., and La Mar, G. N. (1995) 1H NMR investigation of the electronic and molecular structure of the four-iron cluster ferredoxin from the hyperthermophile Pyrococcus furiosus: identification of Asp14 as a cluster ligand in each of the four redox states. Biochemistry 34, 11373-11384
52. George, S. J., Armstrong, F. A., Hatchikian, E. C., and Thomson, A. J. (1989) Electrochemical and spectroscopic characterization of the conversion of the 7Fe into the 8Fe form of ferredoxin III from Desulfovibrio africanus: Identification of a [4Fe-4S] cluster with one non-cysteine ligand. Biochem. J. 264, 275-284
53. Gruner, I., Frädrich, C., Böttger, L. H., Trautwein, A. X., Jahn, D., and Härtig, E. (2011) Aspartate 141 is the fourth ligand of the oxygen-sensing [4Fe-4S]2+ cluster of Bacillus subtilis transcriptional regulator Fnr. J. Biol. Chem. 286, 2017-2021
54. Schwartz, C. J., 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
55. Karlinsey, J. E., Bang, I. S., Becker, L. A., Frawley, E. R., Porwollik, S., Robbins, H. F., Thomas, V. C., Urbano, R., McClelland, M., and Fang, F. C. (2012) The NsrR regulon in nitrosative stress resistance of Salmonella enterica serovar Typhimurium. Mol. Microbiol. 85, 1179-1193
56. Branchu, P., Matrat, S., Vareille, M., Garrivier, A., Durand, A., Crépin, S., Harel, J., Jubelin, G., and Gobert, A. P. (2014) NsrR, GadE, and GadX interplay in repressing expression of the Escherichia coli O157:H7 LEE pathogenicity island in response to nitric oxide. PLoS Pathog. 10, e1003874
57. Heurlier, K., 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
58. Moir, J. W. (2011) A snapshot of a pathogenic bacterium mid-evolution: Neisseria meningitidis is becoming a nitric oxide-tolerant aerobe. Biochem. Soc. Trans. 39, 1890-1894
59. Kers, J. A., 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
60. Gust, B., Challis, G. L., Fowler, K., Kieser, T., and Chater, K. F. (2003) PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc. Natl. Acad. Sci. U.S.A. 100, 1541-1546
61. Bentley, S. D., Chater, K. F., Cerdeño-Tárraga, A. M., Challis, G. L., Thomson, N. R., James, K. D., Harris, D. E., Quail, M. A., Kieser, H., Harper, D., Bateman, A., Brown, S., Chandra, G., Chen, C. W., Collins, M., Cronin, A., Fraser, A., Goble, A., Hidalgo, J., Hornsby, T., Howarth, S., Huang, C. H., Kieser, T., Larke, L., Murphy, L., Oliver, K., O'Neil, S., Rabbinowitsch, E., Rajandream, M. A., Rutherford, K., Rutter, S., Seeger, K., Saunders, D., Sharp, S., Squares, R., Squares, S., Taylor, K., Warren, T., Wietzorrek, A., Woodward, J., Barrell, B. G., Parkhill, J., and Hopwood, D. A. (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417, 141-147
62. Cervantes, S., Bunnik, E. M., Saraf, A., Conner, C. M., Escalante, A., Sardiu, M. E., Ponts, N., Prudhomme, J., Florens, L., and Le Roch, K. G. (2014) The multifunctional autophagy pathway in the human malaria parasite, Plasmodium falciparum. Autophagy 10, 80-92