Protein conformational changes of the oxidative stress sensor, SoxR, upon redox changes of the [2Fe-2S] cluster probed with ultraviolet resonance raman spectroscopy

Biochemistry

Volumn 50, Issue 44, 2011, Pages 9468-9474

  Kobayashi, Kazuo ^a   Mizuno, Misao ^a   Fujikawa, Mayu ^a   Mizutani, Yasuhisa ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL SENSOR; CONFORMATIONAL CHANGE; DNA-BINDING DOMAIN; ONE-ELECTRON OXIDATION; SOXRS REGULON; STRUCTURAL CHANGE; ULTRAVIOLET RESONANCE RAMAN; ULTRAVIOLET RESONANCE RAMAN SPECTROSCOPY;

DNA; ESCHERICHIA COLI; OLIGONUCLEOTIDES; RAMAN SPECTROSCOPY; RESONANCE; SPECTROSCOPIC ANALYSIS; TRANSCRIPTION FACTORS;

SENSORS;

OLIGONUCLEOTIDE; TRANSCRIPTION FACTOR SOX; TRANSCRIPTION FACTOR SOXR; TRYPTOPHAN; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; CONFORMATIONAL TRANSITION; DNA BINDING MOTIF; ENVIRONMENTAL CHANGE; HYDROPHILICITY; HYDROPHOBICITY; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CONFORMATION; RAMAN SPECTROMETRY;

BACTERIAL PROTEINS; DNA, BACTERIAL; ESCHERICHIA COLI PROTEINS; IRON-SULFUR PROTEINS; MUTAGENESIS, SITE-DIRECTED; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEIN CONFORMATION; SPECTROPHOTOMETRY, ULTRAVIOLET; SPECTRUM ANALYSIS, RAMAN; TRANSCRIPTION FACTORS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 80155186777     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201526y     Document Type: Article

References (58)

1. Rodgers, K. R. (1999) Heme-based sensors in biological systems Curr. Opin. Chem. Biol. 3, 158-167 (Pubitemid 29145782)
2. Gilles-Gonzalez, M.-A. and Gonzalez, G. (2005) Heme-based sensors: defining characteristics, recent developments, and regulatory hypotheses J. Inorg. Biochem. 99, 1-22 (Pubitemid 39642968)
3. OHalloran, T. V. (1993) Transition metals in control of gene expression Science 261, 715-725
4. Brown, N. L., Stoyanov, J. V., Kidd, S. P., and Hobman, J. L. (2003) The MerR family of transcriptional regulators FEBS Microbiol. Rev. 27, 145-163 (Pubitemid 36694653)
5. OHalloran, T. V., Frantz, B., Shin, M. K., Ralston, D. M., and Wright, J. G. (1989) The MerR heavy-metal receptor mediates positive activation in a topological novel transcription complex Cell 56, 119-129
6. Outten, C. E., Outten, F. W., and OHalloran, T. V. (1999) DNA distortion mechanism for transcriptional activation by ZntR, a Zn(II)-responsive MerR homologue in Escherichia coli J. Biol. Chem. 274, 37517-37524 (Pubitemid 30026804)
7. Changela, A., Chen, K., Xue, Y., Holschen, J., Outten, C. E., OHalloran, T. V., and Mondragón, A. (2003) Molecular Basis of Metal-Ion Selectivity and Zeptomolar Sensitivity by CueR Science 301, 1383-1387 (Pubitemid 37075815)
8. Frantz, B. and OHalloran, T. V. (1990) DNA distortion accompanies transcriptional activation by the metal-responsive gene-regulatory protein MerR Biochemistry 29, 4747-4751 (Pubitemid 20183735)
9. Checa, S. K., Espariz, M., Audero, M. E., Botta, P. E., Spinelli, S. V., and Soncini, F. C. (2007) Bacterial sensing of and resistance to gold salts Mol. Microbiol. 63, 1307-1318
10. Lee, S. W., Glickmann, E., and Cooksey, D. A. (2001) Chromosomal Locus for Cadmium Resistance in Pseudomonas putida Consisting of a Cadmium-Transporting ATPase and a MerR Family Response Regulator Appl. Environ. Microbiol. 67, 1437-1444 (Pubitemid 33644906)
11. Borremans, B., Hobman, J. L., Provoost, A., Brown, N. L., and van Der Lelie, D. J. (2001) Cloning and Functional Analysis of the pbr Lead Resistance Determinant of Ralstonia metallidurans CH34 J. Bacteriol. 183, 5651-5658 (Pubitemid 32898612)
12. Hidalgo, E. and Demple, B. (1994) An iron-sulfur center essential for transcriptional activation by the redox-sensing SoxR protein EMBO J. 13, 138-146
13. Wu, J., Dunham, W. R., and Weiss, B. (1995) Overproduction and physical characterization of SoxR, a [2Fe-2S] protein that governs an oxidative response regulon in Escherichia coli J. Biol. Chem. 270, 10323-10327
14. Ahmed, M., Borsch, C. M., Taylor, S. S., Vazquez-Laslop, N., and Neyfakh, A. A. (1994) A Protein That Activates Expression of a Multidrug Efflux Transporter Substrates J. Biol. Chem. 269, 28506-28513 (Pubitemid 24354599)
15. Heldwein, E. E. and Brennan, R. G. (2001) Crystal structure of the transcription activator BmrR bound to DNA and a drug Nature 409, 378-382 (Pubitemid 32151247)
16. Kahmann, J. D., Sass, H.-J., Allan, M. G., Haruo, S., Thompson, C. J., and Grzesiek, S. (2003) Structural basis for antibiotic recognition by the TipA class of multidrug-resistance transcriptional regulators EMBO J. 22, 1824-1834 (Pubitemid 36460139)
17. Newberry, K. J. and Brennan, R. G. (2004) The Structural Mechanism for Transcription Activation by MerR Family Member Multidrug Transporter Activation, N Terminus J. Biol. Chem. 279, 20356-20362 (Pubitemid 38623481)
18. Newberry, K. J., Huffman, J. L., Miller, M. C., Vazquez-Laslop, N., Neyfakh, A. A., and Brennan, R. G. (2008) Structures of BmrR-Drug Complexes Reveal a Rigid Multidrug Binding Pocket and Transcription Activation through Tyrosine Expulsion J. Biol. Chem. 283, 26795-26804
19. Baranova, N. N., Danchin, A., and Neyfakh, A. A. (1999) Mta, a global MerR-type regulator of the Bacillus subtilis multidrug-efflux transporters Mol. Microbiol. 31, 1549-1559 (Pubitemid 29110110)
20. Ansari, A. Z., Bradner, J. E., and OHalloran, T. V. (1995) DNA-bend modulation in a repressor-to-activator switching mechanism Nature 374, 371-375
21. Hidalgo, E. and Demple, B. (1997) Spacing of promoter elements regulates the basal expression of the soxS gene and converts SoxR from a transcriptional activator into a repressor EMBO, J. 16, 1056-1065 (Pubitemid 27113184)
22. Gaudu, P. and Weiss, B. (1996) SoxR, a [2Fe-2S] transcription factor, is active only in its oxidized form Proc. Natl. Acad. Sci. U. S. A. 93, 10094-10098 (Pubitemid 26314580)
23. Hidalgo, E., Ding, H., and Demple, B. (1997) Redox Signal Transduction: Mutations Shifting [2Fe-2S] Centers of the SoxR Sensor-Regulator to the Oxidized Form Cell 88, 121-129 (Pubitemid 27180336)
24. Ding, H., Hidalgo, E., and Demple, B. (1996) The Redox State of the [2Fe-2S] Clusters in SoxR Protein Regulates its Activity as a Transcription Factor J. Biol. Chem. 271, 33173-33175 (Pubitemid 27010121)
25. Hidalgo, E., Ding, H., and Demple, B. (1997) Redox signal transduction via iron-sulfur clusters in the SoxR transcription activator Trends Biochem. Sci. 22, 207-210 (Pubitemid 27246636)
26. Watanabe, S., Kita, A., Kobayashi, K., and Miki, K. (2008) Crystal structure of the [2Fe-2S] oxidative-stress sensor SoxR bound to DNA Proc. Natl. Acad. Sci. U. S. A. 105, 4121-4126 (Pubitemid 351754345)
27. Harada, I. and Takeuchi, H. (1986) Raman and ultraviolet resonance Raman spectra of proteins and related compounds in Spectroscopy and Biological Systems (Clark, R. J. H. and Hester, R. E., Eds.) pp 113-175, John Wiley, New York.
28. El-Mashtoly, S. F., Takahashi, H., Shimizu, T., and Kitagawa, T. (2007) Ultraviolet Resonance Raman Evidence for Utilization of the Heme 6-Propionate Hydrogen-Bond Network in Signal Transmission from Heme to Protein in Ec DOS Protein J. Am. Chem. Soc. 129, 3556-3563 (Pubitemid 46502717)
29. Sato, A., Gao, Y., Kitagawa, T., and Mizutani, Y. (2007) Primary protein response after ligand photodissociation in carbonmonoxy myoglobin Proc. Natl. Acad. Sci. U. S. A. 104, 9627-9632 (Pubitemid 47175317)
30. Mizuno, M., Shibata, M., Yamada, J., Kandori, H., and Mizutani, Y. (2009) Picosecond Time-Resolved Ultraviolet Resonance Raman Spectroscopy of Bacteriorhodopsin: Primary Protein Response to Photoisomerization of Retinal J. Phys. Chem. B 113, 12121-12128
31. Watanabe, S., Kita, A., Kobayashi, K., Takahashi, Y., and Miki, K. (2006) Crystallization and preliminary X-ray crystallographic studies of the oxidative-stress sensor SoxR and its complex with DNA Acta Crystallogr., Sect. F: Struct. Biol. Cryst. Commun. 62, 1275-1277 (Pubitemid 44915684)
32. Schlamadinger, D. E., Gable, J. E., and Kim, J. E. (2009) Hydrogen Bonding and Solvent Polarity Markers in the UV Resonance Spectrum of Tryptophan: Application to membrane Proteins J. Phys. Chem. B 113, 14769-14778
33. Hashimoto, S., Obata, K., Takeuchi, H., Needleman, R., and Lanyi, J. K. (1997) Ultrviolet Resonance Raman Spectra of Trp-182 and Trp-189 in Bacteriorhodopsin: Novel Information on the Structure of Trp-182 and Its Steric Interaction with Retinal Biochemistry 36, 11583-11590 (Pubitemid 27424083)
34. Takeuchi, H. (2003) Raman structural markers of tryptophan and histidine side chains in proteins Biopolymers 72, 305-317 (Pubitemid 37087283)
35. -1 in the Raman spectra of tryptophan and related compounds Spectrochim. Acta, Part A 42, 307-312
36. Miura, T., Takeuchi, H., and Harada, I. (1989) Tryptophan Raman Bands Sensitive to Hydrogen Bonding and Side-Chain Conformation J. Raman Spectrosc. 20, 667-671
37. Miura, T., Takeuchi, H., and Harada, I. (1988) Characterization of Individual Tryptophan Side Chains in Proteins Using Raman Spectroscopy and Hydrogen-Deuterium Exchange Kinetics Biochemistry 27, 88-94
38. 2,1 Dihedral Angle-W3 Band Frequency Relationship to a Full Rotation: Correlations and Caveats Biochemistry 48, 2777-2787
39. Haruta, N. and Kitagawa, T. (2001) Protein Conformation Change of Myogobin upon Ligand Binding Probed by Ultraviolet Resonance Raman Spectroscopy Biochemistry 41, 6595-6604
40. Fodor, S. P., Rava, R. P., Hays, T. R., and Spiro, T. G. (1985) Ultraviolet Resonance Raman Spectroscopy of DNA with 200-266-nm Laser Excitation J. Am. Chem. Soc. 107, 1520-1529
41. Perno, J. P., Grygon, C. A., and Spiro, T. G. (1989) Ultraviolet Raman Excitation Profiles for the Nucleic Acid Duplexes Poly(rA)-Poly(rU) and Poly(dG-dC) J. Phys. Chem. 93, 5672-5678
42. 3 Tract: Evidence for a Premelting Transition and Three-Centered H-Bonds Biochemistry 41, 69-77 (Pubitemid 34049382)
43. Chen, J., Bender, S. L., Keough, J. M., and Barry, B. A. (2009) Tryptophan as a Probe of Photosystem I Electron Transfer Reactions: A UV Resonance Raman Study J. Phys. Chem. B 113, 11367-11370
44. Matsuno, M. and Takeuchi, H. (1998) Effect of Hydrogen Bonding and Hydrophobic Interactions on the Ultraviolet Resonance Raman intensities of Indole Ring Vibrations Bull. Chem. Soc. Jpn. 71, 851-857 (Pubitemid 128499846)
45. Fujisawa, T., Terajima, M., and Kimura, Y. (2006) Excitation wavelength dependence of the Raman-Stokes shift of N, N -dimethyl- p -nitroaniline J. Chem. Phys. 124, 184503-184509
46. Schoute, L. C. T., Helburn, R., and Kelley, A. M. (2007) Solvent Effects on the Resonance Raman and Hyperpolarizability of N, N -dimethyl- p -nitroaniline J. Phys. Chem. A 111, 1251-1258 (Pubitemid 46384219)
47. Xue, Y., Davis, A. V., Balakrishnan, G., Stasser, J. P., Staehlin, B. M., Focia, P., Spiro, T. G., Penner-Hahn, J. E., and OHalloran, T. V. (2008) Cu(I) recognition via cation-π and methionine interactions in CusF Nat. Chem. Biol. 4, 107-109
48. Wen, Z. Q. and Thomas, G. J., Jr. (2000) Ultraviolet-Resonance Raman Spectroscopy of Filamentous Virus Pf3: interactions of Trp 38 Specific to the Assembled Virion Subunit Biochemistry 39, 146-152 (Pubitemid 30033329)
49. Okada, A., Miua, T., and Takeuchi, H. (2001) Protonation of Histidine-Tryptophan Interaction in the Activation of the M2 Ion Channel from Influenza A Virus Biochemistry 40, 6053-6060 (Pubitemid 32466308)
50. Kumaraswami, M., Newberry, K. J., and Brennan, R. G. (2010) Conformational Plasticity of the Coiled-Coil Domain of BmrR is Required for bmr Operator Binding: The Structure of Unliganded BmrR J. Mol. Biol. 398, 264-275
51. 19F-NMR Reveals Metal and Operator-induced Allostery in MerR J. Mol. Biol. 371, 79-92 (Pubitemid 47030451)
52. Rodgers, K. R., Su, C., Subramaniam, S., and Spiro, T. G. (1992) Hemoglobin R→T Structural Dynamics from Simultaneous Monitoring of Tyrosine and Tryptophan Time-Resolved UV Resonance Raman Signals J. Am. Chem. Soc. 114, 3697-3709
53. -1 region J. Raman Spectrosc. 20, 233-237
54. Gorodetsky, A. A., Dietrich, L. E. P., Lee, P. E., Demple, B., Newman, D. K., and Barton, J. K. (2008) DNA binding shifts the redox potential of transcription factor SoxR Proc. Natl. Acad. Sci. U. S. A. 105, 3684-3689 (Pubitemid 351723458)
55. Morales, R., Charon, M. H., Hudry-Clergeon, G., Petillot, Y., Norager, S., Medina, M., and Frey, M. (1999) Refined X-ray structures of the oxidized, at 1.3 Å, and reduced, at 1.17 Å, [2Fe-2S] ferredoxin from the cynobacteroum Anabaena PCC7119 show redox-linked conformational change Biochemistry 38, 15764-15773 (Pubitemid 129520469)
56. Sevrikoukova, I. F. (2005) Redox-dependent structural reorganization in putidaredoxin, a vertebrate-type [2Fe-2S] ferredoxin from Pseudomonas putida J. Mol. Biol. 347, 607-621
57. Noodleman, L., Peng, C. Y., Case, D. A., and Mouesca, J.-M. (1995) Orbital interactions, electron delocalization and spin coupling in iron-sulfur clusters Coord. Chem. Rev. 144, 199-244 (Pubitemid 126000788)
58. Newberry, K. J., Huffman, J. L., Miller, M. C., Vazquez-Laslop, N., Neyfakh, A. A., and Brennan, R. G. (2008) Structures of BmrR-Drug Complexes Reveal a Rigid Multidrug Binding Pocket and Transcription Activation through Tyrosine Expulsion J. Biol. Chem. 283, 26795-26804