Studies of IscR reveal a unique mechanism for metal-dependent regulation of DNA binding specificity

Nature Structural and Molecular Biology

Volumn 20, Issue 6, 2013, Pages 740-747

  Rajagopalan, Senapathy ^a   Teter, Sarah J ^b   Zwart, Petrus H ^c   Brennan, Richard G ^d   Phillips, Kevin J ^a,e   Kiley, Patricia J ^b  

^a HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e University of Houston   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA BASE; IRON SULFUR PROTEIN; PROTEIN VARIANT;

ANISOTROPY; ARTICLE; BINDING AFFINITY; BINDING SITE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DNA BINDING; GENE TARGETING; HYDROGEN BOND; MUTAGENESIS; OPERON; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA INTERACTION; X RAY CRYSTALLOGRAPHY;

CRYSTALLOGRAPHY, X-RAY; DNA, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; METALS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; SUBSTRATE SPECIFICITY; TRANSCRIPTION FACTORS;

ESCHERICHIA COLI;

EID: 84878896186     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2568     Document Type: Article

References (42)

1. Johnson, D.C., Dean, D.R., Smith, A.D. & Johnson, M.K. Structure, function, and formation of biological iron-sulfur clusters. Annu. Rev. Biochem. 74, 247-281 (2005). (Pubitemid 40995508)
2. Fleischhacker, A.S. & Kiley, P.J. Iron-containing transcription factors and their roles as sensors. Curr. Opin. Chem. Biol. 15, 335-341 (2011).
3. Crack, J.C., Green, J., Thomson, A.J. & Le Brun, N.E. Iron-sulfur cluster sensor-regulators. Curr. Opin. Chem. Biol. 16, 35-44 (2012).
4. Guerra, A.J. & Giedroc, D.P. Metal site occupancy and allosteric switching in bacterial metal sensor proteins. Arch. Biochem. Biophys. 519, 210-222 (2012).
5. Fleischhacker, A.S. et al. Characterization of the [2Fe-2S] cluster of Escherichia coli transcription factor IscR. Biochemistry 51, 4453-4462 (2012).
6. Nesbit, A.D., Giel, J.L., Rose, J.C. & Kiley, P.J. Sequence-specific binding to a subset of IscR-regulated promoters does not require IscR Fe-S cluster ligation. J. Mol. Biol. 387, 28-41 (2009).
7. Yeo, W.S., Lee, J.H., Lee, K.C. & Roe, J.H. IscR acts as an activator in response to oxidative stress for the suf operon encoding Fe-S assembly proteins. Mol. Microbiol. 61, 206-218 (2006).
8. Giel, J.L. et al. Regulation of iron-sulphur cluster homeostasis through transcriptional control of the Isc pathway by [2Fe-2S]-IscR in Escherichia coli. Mol. Microbiol. 87, 478-492 (2013).
9. Rodionov, D.A., Gelfand, M.S., Todd, J.D., Curson, A.R. & Johnston, A.W. Computational reconstruction of iron-and manganese-responsive transcriptional networks in ?-proteobacteria. PLoS Comput. Biol. 2, e163 (2006).
10. Shepard, W. et al. Insights into the Rrf2 repressor family-the structure of CymR, the global cysteine regulator of Bacillus subtilis. FEBS J. 278, 2689-2701 (2011).
11. Schwartz, C.J. et al. IscR, an Fe-S cluster-containing transcription factor, represses expression of Escherichia coli genes encoding Fe-S cluster assembly proteins. Proc. Natl. Acad. Sci. USA 98, 14895-14900 (2001). (Pubitemid 34013941)
12. Giel, J.L., Rodionov, D., Liu, M., Blattner, F.R. & Kiley, P.J. IscR-dependent gene expression links iron-sulphur cluster assembly to the control of O2-regulated genes in Escherichia coli. Mol. Microbiol. 60, 1058-1075 (2006).
13. Lazazzera, B.A., Beinert, H., Khoroshilova, N., Kennedy, M.C. & Kiley, P.J. 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). (Pubitemid 26047894)
14. Hidalgo, E. & Demple, B. An iron-sulfur center essential for transcriptional activation by the redox-sensing SoxR protein. EMBO J. 13, 138-146 (1994).
15. Gaudu, P. & Weiss, B. SoxR, a [2Fe-2S] transcription factor, is active only in its oxidized form. Proc. Natl. Acad. Sci. USA 93, 10094-10098 (1996). (Pubitemid 26314580)
16. Ebright, R.H. et al. Role of glutamic acid-181 in DNA-sequence recognition by the catabolite gene activator protein (CAP) of Escherichia coli: altered DNA-sequence-recognition properties of [Val181]CAP and [Leu181]CAP. Proc. Natl. Acad. Sci. USA 84, 6083-6087 (1987).
17. Komori, H. et al. Crystal structure of a prokaryotic replication initiator protein bound to DNA at 2.6-Å resolution. EMBO J. 18, 4597-4607 (1999). (Pubitemid 29415515)
18. MacPherson, S., Larochelle, M. & Turcotte, B. A fungal family of transcriptional regulators: the zinc cluster proteins. Microbiol. Mol. Biol. Rev. 70, 583-604 (2006). (Pubitemid 44484686)
19. Reeves, R. & Nissen, M.S. The AT-DNA-binding domain of mammalian high mobility group I chromosomal proteins. A novel peptide motif for recognizing DNA structure. J. Biol. Chem. 265, 8573-8582 (1990).
20. Rohs, R. et al. Origins of specificity in protein-DNA recognition. Annu. Rev. Biochem. 79, 233-269 (2010).
21. Rohs, R. et al. The role of DNA shape in protein-DNA recognition. Nature 461, 1248-1253 (2009).
22. Haran, T.E. & Mohanty, U. The unique structure of A-tracts and intrinsic DNA bending. Q. Rev. Biophys. 42, 41-81 (2009).
23. Coulocheri, S.A., Pigis, D.G., Papavassiliou, K.A. & Papavassiliou, A.G. Hydrogen bonds in protein-DNA complexes: where geometry meets plasticity. Biochimie 89, 1291-1303 (2007). (Pubitemid 47562627)
24. Ding, H., Hidalgo, E. & Demple, B. The redox state of the [2Fe-2S] clusters in SoxR protein regulates its activity as a transcription factor. J. Biol. Chem. 271, 33173-33175 (1996). (Pubitemid 27010121)
25. Watanabe, S., Kita, A., Kobayashi, K. & Miki, K. Crystal structure of the [2Fe-2S] oxidative-stress sensor SoxR bound to DNA. Proc. Natl. Acad. Sci. USA 105, 4121-4126 (2008). (Pubitemid 351754345)
26. Imlay, J.A. Iron-sulphur clusters and the problem with oxygen. Mol. Microbiol. 59, 1073-1082 (2006).
27. Nesbit, A.D., Fleischhacker, A.S., Teter, S.J. & Kiley, P.J. ArcA and AppY antagonize IscR repression of hydrogenase 1 expression under anaerobic conditions, revealing a novel mode of O2 regulation of gene expression in Escherichia coli. J. Bacteriol. 194, 6892-6899 (2012).
28. Shin, J.-H. et al. Graded expression of zinc-responsive genes through two regulatory zinc-binding sites in Zur. Proc. Natl. Acad. Sci. USA 108, 5045-5050 (2011).
29. Ohmura, T., Ueda, T., Hashimoto, Y. & Imoto, T. Tolerance of point substitution of methionine for isoleucine in hen egg white lysozyme. Protein Eng. 14, 421-425 (2001). (Pubitemid 32762379)
30. Leahy, D.J., Erickson, H.P., Aukhil, I., Joshi, P. & Hendrickson, W.A. Crystallization of a fragment of human fibronectin: introduction of methionine by site-directed mutagenesis to allow phasing via selenomethionine. Proteins 19, 48-54 (1994). (Pubitemid 24151483)
31. Battye, T.G., Kontogiannis, L., Johnson, O., Powell, H.R. & Leslie, A.G. iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D Biol. Crystallogr. 67, 271-281 (2011).
32. Collaborative Computational Project, Number
33. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).
34. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997). (Pubitemid 27085611)
35. Terwilliger, T.C. & Berendzen, J. Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr. 55, 849-861 (1999). (Pubitemid 29194533)
36. Adams, P.D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
37. Terwilliger, T.C. Maximum-likelihood density modification. Acta Crystallogr. D Biol. Crystallogr. 56, 965-972 (2000). (Pubitemid 30622779)
38. Emsley, P., Lohkamp, B., Scott, W.G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
39. McCoy, A.J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007). (Pubitemid 47080256)
40. Painter, J. & Merritt, E.A. Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr. D Biol. Crystallogr. 62, 439-450 (2006).
41. McNicholas, S., Potterton, E., Wilson, K.S. & Noble, M.E. Presenting your structures: the CCP4mg molecular-graphics software. Acta Crystallogr. D Biol. Crystallogr. 67, 386-394 (2011).
42. Fischer, D.S. & Price, D.C. A simple serum iron method using the new sensitive chromogen tripyridyl-s-triazine. Clin. Chem. 10, 21-31 (1964).