The crystal structure of the global anaerobic transcriptional regulator FNR explains its extremely fine-tuned monomer-dimer equilibrium

Science Advances

Volumn 1, Issue 11, 2015, Pages

  Volbeda, Anne ^a   Darnault, Claudine ^a   Renoux, Oriane ^a   Nicolet, Yvain ^a   Fontecilla Camps, Juan C ^a  

^a UNIV GRENOBLE ALPES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BINS; DIMERS; DNA;

AEROBIC RESPIRATION; CARBOXYL-TERMINAL; DIMER INTERFACE; DNA BINDING DOMAIN; FACULTATIVE ANAEROBES; MONOMER-DIMER EQUILIBRIUM; NITRATE REDUCTION; TRANSCRIPTIONAL REGULATOR;

CRYSTAL STRUCTURE;

EID: 84959530266     PISSN: None     EISSN: 23752548     Source Type: Journal    
DOI: 10.1126/sciadv.1501086     Document Type: Article

References (33)

1. P. J. Kiley, H. Beinert, Oxygen sensing by the global regulator, FNR: The role of the ironsulfur cluster. FEMS Microbiol. Rev. 22, 341-352 (1998).
2. H. Körner, H. J. Sofia, W. G. Zumft, Phylogeny of the bacterial superfamily of Crp-Fnr transcription regulators: Exploiting the metabolic spectrum by controlling alternative gene programs. FEMS Microbiol. Rev. 27, 559-592 (2003).
3. B. A. Lazazzera, H. Beinert, N. Khoroshilova, M. C. Kennedy, P. J. Kiley, DNA binding and dimerization of the Fe-S-containing FNR protein from Escherichia coli are regulated by oxygen. J. Biol. Chem. 271, 2762-2768 (1996).
4. N. Khoroshilova, H. Beinert, P. J. Kiley, Association of a polynuclear iron-sulfur center with a mutant FNR protein enhances DNA binding. Proc. Natl. Acad. Sci. U.S.A. 92, 2499-2503 (1995).
5. J. Green, B. Bennett, P. Jordan, E. T. Ralph, A. J. Thomson, J. R. Guest, Reconstitution of the [4Fe-4S- cluster in FNR and demonstration of the aerobic-anaerobic transcription switch in vitro. Biochem. J. 316, 887-892 (1996).
6. J. C. Crack, J. Green, M. R. Cheesman, N. E. Le Brun, A. J. Thomson, Superoxide-mediated amplification of the oxygen-induced switch from [4Fe-4S- to [2Fe-2S- clusters in the transcriptional regulator FNR. Proc. Natl. Acad. Sci. U.S.A. 104, 2092-2097 (2007).
7. C. Scott, J. Green, Miscoordination of the iron-sulfur clusters of the anaerobic transcription factor, FNR, allows simple repression but not activation. J. Biol. Chem. 277, 1749-1754 (2002).
8. V. R. Sutton, A. Stubna, T. Patschkowski, E. Münck, H. Beinert, P. J. Kiley, Superoxide destroys the [2Fe-2S-2+ cluster of FNR from Escherichia coli. Biochemistry 43, 791-798 (2004).
9. B. A. Lazazzera, D. M. Bates, P. J. Kiley, The activity of the Escherichia coli transcription factor FNR is regulated by a change in oligomeric state. Genes Dev. 7, 1993-2005 (1993).
10. J. Green, M. D. Rolfe, L. J. Smith, Transcriptional regulation of bacterial virulence gene expression by molecular oxygen and nitric oxide. Virulence 5, 794-809 (2014).
11. J. C. Crack, J. Green, A. J. Thomson, N. E. Le Brun, Iron-sulfur clusters as biological sensors: The chemistry of reactions with molecular oxygen and nitric oxide. Acc. Chem. Res. 47, 3196-3205 (2014).
12. D. B. McKay, T. A. Steitz, Structure of catabolite gene activator protein at 2.9 Å resolution suggests binding to left-handed B-DNA. Nature 290, 744-749 (1981).
13. A. N. Septer, J. L. Bose, A. K. Dunn, E. V. Stabb, FNR-mediated regulation of bioluminescence and anaerobic respiration in the light-organ symbiont Vibrio fischeri. FEMS Microbiol. Lett. 306, 72-81 (2010).
14. M. Bonnet, M. Kurz, S. Mesa, C. Briand, H. Hennecke, M. G. Grütter, The structure of Bradyrhizobium japonicum transcription factor FixK2 unveils sites of DNA binding and oxidation. J. Biol. Chem. 288, 14238-14246 (2013).
15. L. J. Moore, P. J. Kiley, Characterization of the dimerization domain in the FNR transcription factor. J. Biol. Chem. 276, 45744-45750 (2001).
16. L. J. Moore, E. L. Mettert, P. J. Kiley, Regulation of FNR dimerization by subunit charge repulsion. J. Biol. Chem. 281, 33268-33275 (2006).
17. A. J. Jervis, J. C. Crack, G. White, P. J. Artymiuk, M. R. Cheesman, A. J. Thomson, N. E. Le Brun, J. Green, The O2 sensitivity of the transcription factor FNR is controlled by Ser24 modulating the kinetics of [4Fe-4S- to [2Fe-2S- conversion. Proc. Natl. Acad. Sci. U.S.A. 106, 4659-4664 (2009).
18. D. M. Bates, B. A. Lazazzera, P. J. Kiley, Characterization of FNR mutant proteins indicates two distinct mechanisms for altering oxygen regulation of the Escherichia coli transcription factor FNR. J. Bacteriol. 177, 3972-3978 (1995).
19. C. V. Popescu, D. M. Bates, H. Beinert, E. Münck, P. J. Kiley, Mössbauer spectroscopy as a tool for the study of activation/inactivation of the transcription regulator FNR in whole cells of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 95, 13431-13435 (1998).
20. D. M. Bates, C. V. Popescu, N. Khoroshilova, K. Vogt, H. Beinert, E. Münck, P. J. Kiley, Substitution of leucine 28 with histidine in the Escherichia coli transcription factor FNR results in increased stability of the [4Fe-4S-2+ cluster to oxygen. J. Biol. Chem. 275, 6234-6240 (2000).
21. Y. Nicolet, R. Rohac, L. Martin, J. C. Fontecilla-Camps, X-ray snapshots of possible intermediates in the time course of synthesis and degradation of protein-bound Fe4S4 clusters. Proc. Natl. Acad. Sci. U.S.A. 110, 7188-7192 (2013).
22. X. Li, L. He, K. H. Che, S. F. Funderburk, L. Pan, N. Pan, M. Zhang, Z. Yue, Y. Zhao, Imperfect interface of Beclin1 coiled-coil domain regulates homodimer and heterodimer formation with Atg14L and UVRAG. Nat. Commun. 3, 662 (2012).
23. N. Khoroshilova, C. Popescu, E. Münck, H. Beinert, P. J. Kiley, Iron-sulfur cluster disassembly in the FNR protein of Escherichia coli by O2: [4Fe-4S- to [2Fe-2S- conversion with loss of biological activity. Proc. Natl. Acad. Sci. U.S.A. 94, 6087-6092 (1997).
24. Y. Nicolet, L. Zeppieri, P. Amara, J. C. Fontecilla-Camps, Crystal structure of tryptophan lyase (NosL): Evidence for radical formation at the amino group of tryptophan. Angew. Chem. Int. Ed. Engl. 53, 11840-11844 (2014).
25. J. I. Elliott, J. M. Brewer, The inactivation of yeast enolase by 2,3-butanedione. Arch. Biochem. Biophys. 190, 351-357 (1978).
26. G. Evans, R. F. Pettifer, CHOOCH: A program for deriving anomalous-scattering factors from X-ray fluorescence spectra. J. Appl. Crystallogr. 34, 82-86 (2001).
27. W. Kabsch, XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
28. P. R. Evans, G. N. Murshudov, How good are my data and what is the resolution? Acta Crystallogr. D Biol. Crystallogr. 69, 1204-1214 (2013).
29. M. D. Winn, C. C. Ballard, K. D. Cowtan, E. J. Dodson, P. Emsley, P. R. Evans, R. M. Keegan, E. B. Krissinel, A. G. W. Leslie, A. McCoy, S. J. McNicholas, G. N. Murshudov, N. S. Pannu, E. A. Potterton, H. R. Powell, R. J. Read, A. Vagin, K. S. Wilson, Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242 (2011).
30. A. J. McCoy, R. W. Grosse-Kunstleve, P. D. Adams, M. D. Winn, L. C. Storoni, R. J. Read, Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
31. G. N.Murshudov, P. Skubák, A. A. Lebedev,N. S. Pannu, R. A. Steiner, R. A. Nicholls, M. D. Winn, F. Long, A. A. Vagin, REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367 (2011).
32. P. Emsley, B. Lohkamp, W. G. Scott, K. Cowtan, Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
33. P. D. Adams, P. V. Afonine, G. Bunkóczi, V. B. Chen, I. W. Davis, N. Echols, J. J. Headd, L.-W. Hung, G. J. Kapral, R. W. Grosse-Kunstleve, A. J. McCoy, N. W. Moriarty, R. Oeffner, R. J. Read, D. C. Richardson, J. S. Richardson, T. C. Terwilliger, P. H. Zwart, PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).