Crystal structure of a putative transcriptional regulator SCO0520 from Streptomyces coelicolor A3(2) reveals an unusual dimer among TetR family proteins

Journal of Structural and Functional Genomics

Volumn 12, Issue 3, 2011, Pages 149-157

  Filippova, Ekaterina V ^a,c,d   Chruszcz, Maksymilian ^a,d   Cymborowski, Marcin ^a,d   Gu, Jun ^b,d   Savchenko, Alexei ^b,d   Edwards, Aled ^b,d   Minor, Wladek ^a,d  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c NORTHWESTERN UNIVERSITY   (United States)

^d Midwest Center for Structural Genomics   (United States)

Author keywords

Helix turn helix DNA binding motif; Structural genomics; TetR transcriptional regulator; X ray crystal structure

Indexed keywords

BACTERIAL PROTEIN; DIMER; PROTEIN SCO0520; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA BINDING; DNA CONFORMATION; DNA STRUCTURE; GENE FUNCTION; LIGAND BINDING; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; SCO0520 GENE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STREPTOMYCES COELICOLOR; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; DNA-BINDING PROTEINS; HELIX-TURN-HELIX MOTIFS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; STREPTOMYCES COELICOLOR; TRANSCRIPTION FACTORS;

STREPTOMYCES COELICOLOR;

EID: 80054873723     PISSN: 1345711X     EISSN: 15700267     Source Type: Journal    
DOI: 10.1007/s10969-011-9112-4     Document Type: Article

References (56)

1. SD Bentley KF Chater AM Cerdeno-Tarraga GL Challis NR Thomson KD James DE Harris MA Quail H Kieser D Harper A Bateman S Brown G Chandra CW Chen M Collins A Cronin A Fraser A Goble J Hidalgo T Hornsby S Howarth CH Huang T Kieser L Larke L Murphy K Oliver S O'Neil E Rabbinowitsch MA Rajandream K Rutherford S Rutter K Seeger D Saunders S Sharp R Squares S Squares K Taylor T Warren A Wietzorrek J Woodward BG Barrell J Parkhill DA Hopwood 2002 Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2) Nature 417 141 147 12000953 10.1038/417141a
2. KF Chater 1993 Genetics of differentiation in Streptomyces Annu Rev Microbiol 47 685 713 7504906 10.1146/annurev.mi.47.100193.003345 1:CAS:528:DyaK3sXms1emsb0%3D
3. M Redenbach HM Kieser D Denapaite A Eichner J Cullum H Kinashi DA Hopwood 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 8843436 10.1046/j.1365-2958.1996.6191336.x 1:CAS:528:DyaK28Xks1Gjtbc%3D
4. JL Ramos M Martinez-Bueno AJ Molina-Henares W Teran K Watanabe X Zhang MT Gallegos R Brennan R Tobes 2005 The TetR family of transcriptional repressors Microbiol Mol Biol Rev 69 326 356 15944459 10.1128/MMBR.69.2.326-356.2005 1:CAS:528:DC%2BD2MXmtFartro%3D
5. P Orth F Cordes D Schnappinger W Hillen W Saenger W Hinrichs 1998 Conformational changes of the Tet repressor induced by tetracycline trapping J Mol Biol 279 439 447 9642048 10.1006/jmbi.1998.1775 1:CAS:528:DyaK1cXjvFKjsLg%3D
6. P Orth D Schnappinger W Hillen W Saenger W Hinrichs 2000 Structural basis of gene regulation by the tetracycline inducible Tet repressor-operator system Nat Struct Biol 7 215 219 10700280 10.1038/73324 1:CAS:528:DC%2BD3cXhvFShtLw%3D
7. + reveals mechanism of antibiotic resistance J Mol Biol 247 260 280 7707374 10.1006/jmbi.1994.0138 1:CAS:528:DyaK2MXkvV2rsr4%3D
8. W Hinrichs C Kisker M Duvel A Muller K Tovar W Hillen W Saenger 1994 Structure of the Tet repressor-tetracycline complex and regulation of antibiotic resistance Science 264 418 420 8153629 10.1126/science.8153629 1:CAS:528:DyaK2cXkslyis78%3D
9. MA Schumacher MC Miller S Grkovic MH Brown RA Skurray RG Brennan 2001 Structural mechanisms of QacR induction and multidrug recognition Science 294 2158 2163 11739955 10.1126/science.1066020 1:CAS:528:DC%2BD3MXptVOmsbw%3D
10. MA Schumacher MC Miller S Grkovic MH Brown RA Skurray RG Brennan 2002 Structural basis for cooperative DNA binding by two dimers of the multidrug-binding protein QacR EMBO J 21 1210 1218 11867549 10.1093/emboj/21.5. 1210 1:CAS:528:DC%2BD38XitFylt7g%3D
11. MA Schumacher MC Miller RG Brennan 2004 Structural mechanism of the simultaneous binding of two drugs to a multidrug-binding protein EMBO J 23 2923 2930 15257299 10.1038/sj.emboj.7600288 1:CAS:528:DC%2BD2cXmt1Wqurc%3D
12. DS Murray MA Schumacher RG Brennan 2004 Crystal structures of QacR-diamidine complexes reveal additional multidrug-binding modes and a novel mechanism of drug charge neutralization J Biol Chem 279 14365 14371 14726520 10.1074/jbc.M313870200 1:CAS:528:DC%2BD2cXis1elu70%3D
13. R Natsume Y Ohnishi T Senda S Horinouchi 2004 Crystal structure of a gamma-butyrolactone autoregulator receptor protein in Streptomyces coelicolor A3(2) J Mol Biol 336 409 419 14757054 10.1016/j.jmb.2003.12.040 1:CAS:528:DC%2BD2cXntVKrsg%3D%3D
14. LG Dover PE Corsino IR Daniels SL Cocklin V Tatituri GS Besra K Futterer 2004 Crystal structure of the TetR/CamR family repressor Mycobacterium tuberculosis EthR implicated in ethionamide resistance J Mol Biol 340 1095 1105 15236969 10.1016/j.jmb.2004.06.003 1:CAS:528:DC%2BD2cXlsVejsrk%3D
15. F Frenois J Engohang-Ndong C Locht AR Baulard V Villeret 2004 Structure of EthR in a ligand bound conformation reveals therapeutic perspectives against tuberculosis Mol Cell 16 301 307 15494316 10.1016/j.molcel.2004.09.020 1:CAS:528:DC%2BD2cXhtVWit7rO
16. N Willand B Dirie X Carette P Bifani A Singhal M Desroses F Leroux E Willery V Mathys R Deprez-Poulain G Delcroix F Frenois M Aumercier C Locht V Villeret B Deprez AR Baulard 2009 Synthetic EthR inhibitors boost antituberculous activity of ethionamide Nat Med 15 537 544 19412174 10.1038/nm.1950 1:CAS:528:DC%2BD1MXltlSrsLk%3D
17. SS Rajan X Yang L Shuvalova F Collart WF Anderson 2006 Crystal structure of Yfir, an unusual TetR/CamR-type putative transcriptional regulator from Bacillus subtilis Proteins 65 255 257 16862575 10.1002/prot.21073 1:CAS:528:DC%2BD28Xpt1ClsrY%3D
18. M Li R Gu CC Su MD Routh KC Harris ES Jewell G McDermott EW Yu 2007 Crystal structure of the transcriptional regulator AcrR from Escherichia coli J Mol Biol 374 591 603 17950313 10.1016/j.jmb.2007.09.064 1:CAS:528: DC%2BD2sXht1Kjs73F
19. AR Willems K Tahlan T Taguchi K Zhang ZZ Lee K Ichinose MS Junop JR Nodwell 2008 Crystal structures of the Streptomyces coelicolor TetR-like protein ActR alone and in complex with actinorhodin or the actinorhodin biosynthetic precursor (S)-DNPA J Mol Biol 376 1377 1387 18207163 10.1016/j.jmb.2007.12.061 1:CAS:528:DC%2BD1cXitVejurk%3D
20. KD Koclega M Chruszcz MD Zimmerman M Cymborowski E Evdokimova W Minor 2007 Crystal structure of a transcriptional regulator TM1030 from Thermotoga maritima solved by an unusual MAD experiment J Struct Biol 159 424 432 17588774 10.1016/j.jsb.2007.04.012 1:CAS:528:DC%2BD2sXhtVWht7%2FE
21. L Premkumar CL Rife SS Krishna D McMullan MD Miller P Abdubek E Ambing T Astakhova HL Axelrod JM Canaves D Carlton HJ Chiu T Clayton M DiDonato L Duan MA Elsliger J Feuerhelm R Floyd SK Grzechnik J Hale E Hampton GW Han J Haugen L Jaroszewski KK Jin HE Klock MW Knuth E Koesema JS Kovarik A Kreusch I Levin TM McPhillips AT Morse E Nigoghossian L Okach S Oommachen J Paulsen K Quijano R Reyes F Rezezadeh D Rodionov R Schwarzenbacher G Spraggon H van den Bedem A White G Wolf Q Xu KO Hodgson J Wooley AM Deacon A Godzik SA Lesley IA Wilson 2007 Crystal structure of TM1030 from Thermotoga maritima at 2.3 A resolution reveals molecular details of its transcription repressor function Proteins 68 418 424 17444523 10.1002/prot.21436 1:CAS:528:DC%2BD2sXmt1Oku7Y%3D
22. U Okada K Kondo T Hayashi N Watanabe M Yao T Tamura I Tanaka 2008 Structural and functional analysis of the TetR-family transcriptional regulator SCO0332 from Streptomyces coelicolor Acta Crystallogr D 64 198 205 18219120 10.1107/S0907444907059835
23. RG Zhang T Skarina JE Katz S Beasley A Khachatryan S Vyas CH Arrowsmith S Clarke A Edwards A Joachimiak A Savchenko 2001 Structure of Thermotoga maritima stationary phase survival protein SurE: a novel acid phosphatase Structure 9 1095 1106 11709173 10.1016/S0969-2126(01)00675-X 1:CAS:528:DC%2BD3MXosFOisL0%3D
24. G Rosenbaum R Alkire G Evans FJ Rotella K Lazarski R Zhang SL Ginell N Duke I Naday J Lazarz MJ Molitsky L Keefe J Gonczy L Rock R Sanishvili MA Walsh E Westbrook A Joachimiak 2006 The Structural Biology Center 19ID undulator beamline: facility specifications and protein crystallographic results J Synchrotron Radiat 13 30 45 16371706 10.1107/S0909049505036721 1:CAS:528:DC%2BD2MXhtlCiur%2FE
25. Z Otwinowski W Minor 1997 Processing of X-ray diffraction data collected in oscillation mode Macromol Crystallogr A 276 307 326 10.1016/S0076-6879(97) 76066-X 1:CAS:528:DyaK2sXivFehsbw%3D
26. W Minor M Cymborowski Z Otwinowski M Chruszcz 2006 HKL-3000: the integration of data reduction and structure solution-from diffraction images to an initial model in minutes Acta Crystallogr D 62 859 866 16855301 10.1107/S0907444906019949
27. GM Sheldrick 2008 A short history of SHELX Acta Crystallogr A 64 112 122 18156677 10.1107/S0108767307043930
28. Otwinowski Z (1991) Proceedings of the CCP4 study weekend, isomorphous replacement and anomalous scattering. Wolf W, Evans PR, Leslie AGW (eds). Daresbury Laboratory, Warrington, pp 80-86
29. KD Cowtan P Main 1993 Improvement of macromolecular electron-density maps by the simultaneous application of real and reciprocal space constraints Acta Crystallogr A 49 148 157 10.1107/S0108767392008262 1:STN:280: DC%2BD2czpsVOluw%3D%3D
30. KD Cowtan KYJ Zhang 1999 Density modification for macromolecular phase improvement Progr Biophys Mol Biol 72 245 270 10.1016/S0079-6107(99)00008-5 1:STN:280:DC%2BD3c%2FkvVKksw%3D%3D
31. CCP4 1994 The CCP4 suite: programs for protein crystallography Acta Crystallogr D 50 760 763 10.1107/S0907444994003112
32. TC Terwilliger J Berendzen 1999 Automated MAD and MIR structure solution Acta Crystallogr D 55 849 861 10089316 10.1107/S0907444999000839 1:STN:280:DyaK1M7ptV2ktg%3D%3D
33. TC Terwilliger 2002 Automated structure solution, density modification and model building Acta Crystallogr D 58 1937 1940 12393925 10.1107/ S0907444902016438
34. A Perrakis R Morris VS Lamzin 1999 Automated protein model building combined with iterative structure refinement Nat Struct Biol 6 458 463 10331874 10.1038/8263 1:CAS:528:DyaK1MXjtlajurs%3D
35. TA Jones JY Zou SW Cowan M Kjeldgaard 1991 Improved methods for building protein models in electron-density maps and the location of errors in these models Acta Crystallogr A 47 110 119 2025413 10.1107/S0108767390010224
36. P Emsley K Cowtan 2004 Coot: model-building tools for molecular graphics Acta Crystallogr D 60 2126 2132 15572765 10.1107/S0907444904019158
37. GN Murshudov AA Vagin EJ Dodson 1997 Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr D 53 240 255 15299926 10.1107/S0907444996012255 1:STN:280:DC%2BD2czpsFegsw%3D%3D
38. AA Vaguine J Richelle SJ Wodak 1999 SFCHECK: a unified set of procedures for evaluating the quality of macromolecular structure-factor data and their agreement with the atomic model Acta Crystallogr D 55 191 205 10089410 10.1107/S0907444998006684 1:STN:280:DyaK1M7ptVyntw%3D%3D
39. RA Laskowski MW Macarthur DS Moss JM Thornton 1993 Procheck-a program to check the stereochemical quality of protein structures J Appl Crystallogr 26 283 291 10.1107/S0021889892009944 1:CAS:528:DyaK3sXit12lurY%3D
40. H Yang V Guranovic S Dutta HM Berman JD Westbrook 2004 Automated and accurate deposition of structures solved by X-ray diffraction to the Protein Data Bank Acta Crystallogr D 60 1833 1839 15388930 10.1107/S0907444904019419
41. SC Lovell IW Davis WB Arendall PI de Bakker JM Word MG Prisant JS Richardson DC Richardson 2003 Structure validation by Calpha geometry: phi, psi and Cbeta deviation Proteins 50 437 450 12557186 10.1002/prot.10286 1:CAS:528:DC%2BD3sXpvVKlsA%3D%3D
42. HM Berman J Westbrook Z Feng G Gilliland TN Bhat H Weissig IN Shindyalov PE Bourne 2000 The protein data bank Nucleic Acids Res 28 235 242 10592235 10.1093/nar/28.1.235 1:CAS:528:DC%2BD3cXhvVKjt7w%3D
43. Delano WL (2002) The Pymol molecular graphics system. DeLano Scientific, San Carlos, CA
44. L Potterton S McNicholas E Krissinel J Gruber K Cowtan P Emsley GN Murshudov S Cohen A Perrakis M Noble 2004 Developments in the CCP4 molecular-graphics project Acta Crystallogr D 60 2288 2294 15572783 10.1107/S0907444904023716
45. SF Altschul W Gish W Miller EW Meyers DJ Lipman 1990 Basic local alignment search tool J Mol Biol 215 403 410 2231712 1:CAS:528: DyaK3MXitVGmsA%3D%3D
46. JD Thompson DG Higgins TJ Gibson 1994 ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res 22 4673 4680 7984417 10.1093/nar/22.22.4673 1:CAS:528:DyaK2MXitlSgu74%3D
47. P Gouet X Robert E Courcelle 2003 ESPript/ENDscript: Extracting and 23 rendering sequence and 3D information from atomic structures of proteins Nucleic Acids Res 31 3320 3323 12824317 10.1093/nar/gkg556 1:CAS:528: DC%2BD3sXltVWjtLw%3D
48. Holm L, Sander C. (1995) 3-D lookup: fast protein structure database searches at 90% reliability. In: Proceedings of 3rd international conference on intelligent systems for molecular biology (ISMB'95), pp179-187
49. JF Gibrat T Madej SH Bryant 1996 Surprising similarities in structure comparison Curr Opin Struct Biol 6 377 385 8804824 10.1016/S0959-440X(96)80058-3 1:CAS:528:DyaK28XjvFSgsLg%3D
50. T Madej JF Gibrat SH Bryant 1995 Threading a database of protein cores Proteins 23 356 3690 8710828 10.1002/prot.340230309 1:CAS:528:DyaK2MXpslOqu7g%3D
51. RA Laskowski JD Watson JM Thornton 2005 ProFunc: a server for predicting protein function from 3D structure Nucleic Acids Res 33 89 93 10.1093/nar/gki414
52. S Wang O Kirillova M Chruszcz D Gront MD Zimmerman MT Cymborowski IA Shumilin T Skarina E Gorodichtchenskaia A Savchenko AM Edwards W Minor 2009 The crystal structure of the AF2331 protein from Archaeoglobus fulgidus DSM 4304 forms an unusual interdigitated dimer with a new type of alpha + beta fold Protein Sci 18 2410 2419 19768810 10.1002/pro.251 1:CAS:528:DC%2BD1MXhtlequ7zN
53. H Ponstingl K Henrick JM Thornton 2000 Discriminating between homodimeric and monomeric proteins in the crystalline state Proteins 41 47 57 10944393 10.1002/1097-0134(20001001)41:1<47::AID-PROT80>3.0.CO;2-8 1:STN:280:DC%2BD3cvosVWnsQ%3D%3D
54. H Ponstingl T Kabir JM Thornton 2003 Automatic inference of protein quaternary structure from crystals J Appl Crystal 36 1116 1122 10.1107/S0021889803012421 1:CAS:528:DC%2BD3sXntV2msbc%3D
55. Z Yu SE Reichheld A Savchenko J Parkinson AR Davidson 2010 A comprehensive analysis of structural and sequence conservation in the TetR family transcriptional regulators J Mol Biol 400 847 864 20595046 10.1016/j.jmb.2010.05.062 1:CAS:528:DC%2BC3cXos1yrs7o%3D
56. H Jornvall B Persson M Krook S Atrian R Gonzalez-Duarte J Jeffery D Ghosh 1995 Short-chain dehydrogenases/reductases (SDR) Biochemistry 34 6003 6013 7742302 10.1021/bi00018a001 1:STN:280:DyaK2M3mtVOqtQ%3D%3D