The hyperthermophile protein Sso10a is a dimer of winged helix DNA-binding domains linked by an antiparallel coiled coil rod

Journal of Molecular Biology

Volumn 341, Issue 1, 2004, Pages 73-91

  Chen, Liqing ^a,b   Chen, Li Rong ^b,c   Zhou, Xiaoyin E ^a,b   Wang, Yujun ^a,b   Kahsai, Mebrahtu A ^a   Clark, Andrew T ^a   Edmondson, Stephen P ^a   Liu, Zhi Jie ^b,c   Rose, John P ^b,c   Wang, Bi Cheng ^b,c   Meehan, Edward J ^a,b   Shriver, John W ^a  

^a UNIVERSITY OF ALABAMA IN HUNTSVILLE   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c University of Georgia ^*  (United States)

Author keywords

antiparallel coiled coil; chromium X ray source; DSC, differential scanning calorimetry; hyperthermophile; SAS, single wavelength anomalous scattering; sulfur SAS phasing; winged helix turn helix

Indexed keywords

ALANINE; AMINO ACID; ASPARTIC ACID; CHROMIUM; DNA BINDING PROTEIN; PROTEIN SSO10A; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CHROMATIN STRUCTURE; CRYSTAL STRUCTURE; DIFFERENTIAL SCANNING CALORIMETRY; DNA HELIX; GENE SEQUENCE; ION PAIR CHROMATOGRAPHY; PRIORITY JOURNAL; PROTEIN ANALYSIS; SULFOLOBUS SOLFATARICUS; THERMOSTABILITY; TRANSCRIPTION REGULATION; ULTRACENTRIFUGATION; X RAY;

ARCHAEA; CRENARCHAEOTA; EURYARCHAEOTA; SULFOLOBUS; SULFOLOBUS SOLFATARICUS;

EID: 4143109111     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.05.044     Document Type: Article

References (111)

1. Choli T., Henning P., Wittmann-Liebold B., Reinhardt R. Isolation, characterization, and microsequence analysis of a small basic methylated DNA-binding protein from the Archaebacterium, Sulfolobus solfataricus. Biochim. Biophys. Acta. 950:1988;193-203
2. pp. 185-218 Dijk J., Reinhardt R. The structure of DNA-binding proteins from eu- and archaebacteria. Gualerzi C., Pon C. Bacterial Chromatin. 1986;Springer, Berlin
3. Lurz R., Grote M., Dijk J., Reinhardt R., Dobrinski B. Electron microscopic study of DNA complexes with proteins from the archaebacterium Sulfolobus acidocaldarius. EMBO J. 5:1986;3715-3721
4. White M.F., Bell S.D. Holding it together: chromatin in the Archaea. Trends Genet. 18:2002;621-626
5. Wardleworth B.N., Russell R.J., Bell S.D., Taylor G.L., White M.F. Structure of Alba: an archaeal chromatin protein modulated by acetylation. EMBO J. 21:2002;4654-4662
6. Edmondson S.P., Shriver J.W. DNA binding proteins Sac7d and Sso7d from Sulfolobus. Methods Enzymol. 334:2001;129-145
7. Bell S.D., Botting C.H., Wardleworth B.N., Jackson S.P., White M.F. The interaction of Alba, a conserved archaeal chromatin protein, with Sir2 and its regulation by acetylation. Science. 296:2002;148-151
8. Edmondson S.P., Kahsai M., Gupta R., Shriver J.W. Characterization of Sac10a, a conserved Archaeal DNA binding protein from Sulfolobus acidocaldarius. J. Bacteriol. 2004;. In the press
9. She Q., Singh R.K., Confalonieri F., Zivanovic Y., Allard G., Awayez M.J., et al. The complete genome of the crenarchaeon Sulfolobus solfataricus P2. Proc. Natl Acad. Sci. USA. 98:2001;7835-7840
10. Teale M.J., Kahsai M., Singh S.K., Edmondson S.P., Gupta R., Shriver J.W., Meehan E. Cloning, expression, crystallization and preliminary X-ray analysis of the DNA-binding protein Sso10a from Sulfolobus solfataricus. Acta Crystallog. sect. D. 59:2003;1320-1322
11. Lupas A. Prediction and analysis of coiled-coil structures. Methods Enzymol. 266:1996;513-525
12. Adams M.W., Dailey H.A., DeLucas L.J., Luo M., Prestegard J.H., Rose J.P., Wang B.C. The Southeast Collaboratory for Structural Genomics: a high-throughput gene to structure factory. Acc. Chem. Res. 36:2003;191-198
13. Yang C., Pflugrath J.W., Courville D.A., Stence C.N., Ferrara J.D. Away from the edge: SAD phasing from the sulfur anomalous signal measured in-house with chromium radiation. Acta Crystallog. sect. D. 59:2003;1943-1957
14. +-regulated photoprotein obelin at 1.7 Å resolution determined directly from its sulfur substructure. Protein Sci. 9:2000;2085-2093
15. Rose J.P., Wu C.K., Liu Z.J., Newton M.G., Wang B.C. Using single wavelength anomalous scattering data for in-house protein structure determination. The Rigaku J. 18:2001;4-12
16. Brennan R.G. The winged-helix DNA-binding motif: another helix-turn-helix takeoff. Cell. 74:1993;773-776
17. Gajiwala K.S., Burley S.K. Winged helix proteins. Curr. Opin. Struct. Biol. 10:2000;110-116
18. Wintjens R., Rooman M. Structural classification of HTH DNA-binding domains and protein-DNA interaction modes. J. Mol. Biol. 262:1996;294-313
19. Greenfield N.J., Hitchcock-DeGregori S.E. Conformational intermediates in the folding of a coiled-coil model peptide of the N-terminus of tropomyosin and alpha alpha-tropomyosin. Protein Sci. 2:1993;1263-1273
20. Crick F.H.C. The packing of alpha-helices: simple coiled coils. Acta Crystallog. 6:1953;689-697
21. Barlow D.J., Thornton J.M. Ion-pairs in proteins. J. Mol. Biol. 168:1983;867-885
22. Schultz S.C., Shields G.C., Steitz T.A. Crystal structure of a CAP-DNA complex: the DNA is bent by 90 degrees. Science. 253:1991;1001-1007
23. Lai E., Clark K.L., Burley S.K., Darnell J.E. Jr. Hepatocyte nuclear factor 3/fork head or "winged helix" proteins: a family of transcription factors of diverse biologic function. Proc. Natl Acad. Sci. USA. 90:1993;10421-10423
24. Aravind L., Koonin E.V. DNA-binding proteins and evolution of transcription regulation in the archaea. Nucl. Acids. Res. 27:1999;4658-4670
25. Meinhart A., Blobel J., Cramer P. An extended winged helix domain in general transcription factor E/IIE alpha. J. Biol. Chem. 278:2003;48267-48274
26. Shin J.H., Grabowski B., Kasiviswanathan R., Bell S.D., Kelman Z. Regulation of minichromosome maintenance helicase activity by Cdc6. J. Biol. Chem. 278:2003;38059-38067
27. Alekshun M.N., Levy S.B., Mealy T.R., Seaton B.A., Head J.F. The crystal structure of MarR, a regulator of multiple antibiotic resistance, at 2.3 Å resolution. Nature Struct. Biol. 8:2001;710-714
28. Cook W.J., Kar S.R., Taylor K.B., Hall L.M. Crystal structure of the cyanobacterial metallothionein repressor SmtB: a model for metalloregulatory proteins. J. Mol. Biol. 275:1998;337-346
29. Pohl E., Holmes R.K., Hol W.G. Motion of the DNA-binding domain with respect to the core of the diphtheria toxin repressor (DtxR) revealed in the crystal structures of apo- and holo-DtxR. J. Biol. Chem. 273:1998;22420-22427
30. Bussiere D.E., Bastia D., White S.W. Crystal structure of the replication terminator protein from B. subtilis at 2.6 Å Cell. 80:1995;651-660
31. Zheng N., Fraenkel E., Pabo C.O., Pavletich N.P. Structural basis of DNA recognition by the heterodimeric cell cycle transcription factor E2F-DP. Genes Dev. 13:1999;666-674
32. Passner J.M., Steitz T.A. The structure of a CAP-DNA complex having two cAMP molecules bound to each monomer. Proc. Natl Acad. Sci. USA. 94:1997;2843-2847
33. Lupas A. Coiled coils: new structures and new functions. Trends Biochem. Sci. 21:1996;375-382
34. Oakley M.G., Hollenbeck J.J. The design of antiparallel coiled coils. Curr. Opin. Struct. Biol. 11:2001;450-457
35. Godsey M.H., Zheleznova Heldwein E.E., Brennan R.G. Structural biology of bacterial multidrug resistance gene regulators. J. Biol. Chem. 277:2002;40169-40172
36. Changela A., Chen K., Xue Y., Holschen J., Outten C.E., O'Halloran T.V., Mondragon A. Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR. Science. 301:2003;1383-1387
37. Pellegrini L., Tan S., Richmond T.J. Structure of serum response factor core bound to DNA. Nature. 376:1995;490-498
38. Hall D.R., Gourley D.G., Leonard G.A., Duke E.M., Anderson L.A., Boxer D.H., Hunter W.N. The high-resolution crystal structure of the molybdate-dependent transcriptional regulator (ModE) from Escherichia coli: a novel combination of domain folds. EMBO J. 18:1999;1435-1446
39. Brown N.L., Stoyanov J.V., Kidd S.P., Hobman J.L. The MerR family of transcriptional regulators. FEMS Microbiol. Rev. 27:2003;145-163
40. Yang W., Steitz T.A. Crystal structure of the site-specific recombinase gamma delta resolvase complexed with a 34 bp cleavage site. Cell. 82:1995;193-207
41. Finnin M.S., Cicero M.P., Davies C., Porter S.J., White S.W., Kreuzer K.N. The activation domain of the MotA transcription factor from bacteriophage T4. EMBO J. 16:1997;1992-2003
42. Weaver L.H., Kwon K., Beckett D., Matthews B.W. Corepressor-induced organization and assembly of the biotin repressor: a model for allosteric activation of a transcriptional regulator. Proc. Natl Acad. Sci. USA. 98:2001;6045-6050
43. Heldwein E.E., Brennan R.G. Crystal structure of the transcription activator BmrR bound to DNA and a drug. Nature. 409:2001;378-382
44. Burkhard P., Stetefeld J., Strelkov S.V. Coiled coils: a highly versatile protein folding motif. Trends Cell Biol. 11:2001;82-88
45. Brown J.H., Kim K.H., Jun G., Greenfield N.J., Dominguez R., Volkmann N., et al. Deciphering the design of the tropomyosin molecule. Proc. Natl Acad. Sci. USA. 98:2001;8496-8501
46. O'Shea E.K., Klemm J.D., Kim P.S., Alber T. X-ray structure of the GCN4 leucine zipper, a two-stranded, parallel coiled coil. Science. 254:1991;539-544
47. Bouchard C., Staller P., Eilers M. Control of cell proliferation by Myc. Trends Cell Biol. 8:1998;202-206
48. Walshaw J., Woolfson D.N. Socket: a program for identifying and analysing coiled-coil motifs within protein structures. J. Mol. Biol. 307:2001;1427-1450
49. Monera O.D., Kay C.M., Hodges R.S. Electrostatic interactions control the parallel and antiparallel orientation of alpha-helical chains in two-stranded alpha-helical coiled-coils. Biochemistry. 33:1994;3862-3871
50. Monera O.D., Zhou N.E., Kay C.M., Hodges R.S. Comparison of antiparallel and parallel two-stranded alpha-helical coiled-coils. Design, synthesis, and characterization. J. Biol. Chem. 268:1993;19218-19227
51. Phelan P., Gorfe A.A., Jelesarov I., Marti D.N., Warwicker J., Bosshard H.R. Salt bridges destabilize a leucine zipper designed for maximized ion pairing between helices. Biochemistry. 41:2002;2998-3008
52. Burkhard P., Ivaninskii S., Lustig A. Improving coiled-coil stability by optimizing ionic interactions. J. Mol. Biol. 318:2002;901-910
53. Spek E.J., Bui A.H., Lu M., Kallenbach N.R. Surface salt bridges stabilize the GCN4 leucine zipper. Protein Sci. 7:1998;2431-2437
54. Lopez-Lacomba J.L., Guzman M., Cortijo M., Mateo P.L., Aguirre R., Harvey S.C., Cheung H.C. Differential scanning calorimetric study of the thermal unfolding of myosin rod, light meromyosin, and subfragment 2. Biopolymers. 28:1989;2143-2159
55. Bertazzon A., Tsong T.Y. Study of effects of pH on the stability of domains in myosin rod by high-resolution differential scanning calorimetry. Biochemistry. 29:1990;6453-6459
56. O'Brien R., Sturtevant J.M., Wrabl J., Holtzer M.E., Holtzer A. A scanning calorimetric study of unfolding equilibria in homodimeric chicken gizzard tropomyosins. Biophys. J. 70:1996;2403-2407
57. Singh A., Hitchcock-DeGregori S.E. Local destabilization of the tropomyosin coiled coil gives the molecular flexibility required for actin binding. Biochemistry. 42:2003;14114-14121
58. Moll J.R., Ruvinov S.B., Pastan I., Vinson C. Designed heterodimerizing leucine zippers with a ranger of pIs and stabilities up to 10(-15) M. Protein Sci. 10:2001;649-655
59. Zhu H., Celinski S.A., Scholtz J.M., Hu J.C. The contribution of buried polar groups to the conformational stability of the GCN4 coiled coil. J. Mol. Biol. 300:2000;1377-1387
60. Peters J., Baumeister W., Lupas A. Hyperthermostable surface layer protein tetrabrachion from the archaebacterium Staphylothermus marinus: evidence for the presence of a right-handed coiled coil derived from the primary structure. J. Mol. Biol. 257:1996;1031-1341
61. Wagschal K., Tripet B., Lavigne P., Mant C., Hodges R.S. The role of position a in determining the stability and oligomerization state of alpha-helical coiled coils: 20 amino acid stability coefficients in the hydrophobic core of proteins. Protein Sci. 8:1999;2312-2329
62. Tripet B., Wagschal K., Lavigne P., Mant C.T., Hodges R.S. Effects of side-chain characteristics on stability and oligomerization state of a de novo-designed model coiled-coil: 20 amino acid substitutions in position "d" J. Mol. Biol. 300:2000;377-402
63. Lavigne P., Crump M.P., Gagne S.M., Hodges R.S., Kay C.M., Sykes B.D. Insights into the mechanism of heterodimerization from the 1H-NMR solution structure of the c-Myc-Max heterodimeric leucine zipper. J. Mol. Biol. 281:1998;165-181
64. Lumb K.J., Kim P.S. Measurement of interhelical electrostatic interactions in the GCN4 leucine zipper. Science. 268:1995;436-439
65. Lupas A., Van Dyke M., Stock J. Predicting coiled coils from protein sequences. Science. 252:1991;1162-1164
66. Woolfson D.N., Alber T. Predicting oligomerization states of coiled coils. Protein Sci. 4:1995;1596-1607
67. McClain D.L., Gurnon D.G., Oakley M.G. Importance of potential interhelical salt-bridges involving interior residues for coiled-coil stability and quaternary structure. J. Mol. Biol. 324:2002;257-270
68. Lavigne P., Kondejewski L.H., Houston M.E. Jr, Sonnichsen F.D., Lix B., Skyes B.D., et al. Preferential heterodimeric parallel coiled-coil formation by synthetic Max and c-Myc leucine zippers: a description of putative electrostatic interactions responsible for the specificity of heterodimerization. J. Mol. Biol. 254:1995;505-520
69. Spassov V., Karshikoff A.D., Ladenstein R. The optimization of protein-solvent interactions: thermostability and the role of hydrophobic and electrostatic interactions. Protein Sci. 4:1995;1516-1527
70. Jaenicke R. Glyceraldehyde-3-phosphate dehydrogenase from Thermotoga maritima: strategies of protein stabilization. FEMS Microbiol. Rev. 18:1996;215-224
71. Rice D.W., Yip K.S., Stillman T.J., Britton K.L., Fuentes A., Connerton I., et al. Insights into the molecular basis of thermal stability from the structure determination of Pyrococcus furiosus glutamate dehydrogenase. FEMS Microbiol. Rev. 18:1996;105-117
72. Yip K.S., Britton K.L., Stillman T.J., Lebbink J., de Vos W.M., Robb F.T., et al. Insights into the molecular basis of thermal stability from the analysis of ion-pair networks in the glutamate dehydrogenase family. Eur. J. Biochem. 255:1998;336-346
73. Haney P.J., Badger J.H., Buldak G.L., Reich C.I., Woese C.R., Olsen G.J. Thermal adaptation analyzed by comparison of protein sequences from mesophilic and extremely thermophilic Methanococcus species. Proc. Natl Acad. Sci. USA. 96:1999;3578-3583
74. Kumar S., Nussinov R. Salt bridge stability in monomeric proteins. J. Mol. Biol. 293:1999;1241-1255
75. Szilagyi A., Zavodszky P. Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey. Struct. Fold. Des. 8:2000;493-504
76. Bogin O., Levin I., Hacham Y., Tel-Or S., Peretz M., Frolow F., Burstein Y. Structural basis for the enhanced thermal stability of alcohol dehydrogenase mutants from the mesophilic bacterium Clostridium beijerinckii: contribution of salt bridging. Protein Sci. 11:2002;2561-2574
77. Karshikoff A., Ladenstein R. Ion pairs and the thermotolerance of proteins from hyperthermophiles: a "traffic rule" for hot roads. Trends Biochem. Sci. 26:2001;550-556
78. Chakravarty S., Varadarajan R. Elucidation of factors responsible for enhanced thermal stability of proteins: a structural genomics based study. Biochemistry. 41:2002;8152-8161
79. Alsop E., Silver M., Livesay D.R. Optimized electrostatic surfaces parallel increased thermostability: a structural bioinformatic analysis. Protein Eng. 16:2003;871-874
80. Chen Y.W., Bycroft M., Wong K.B. Crystal structure of ribosomal protein L30e from the extreme thermophile Thermococcus celer: thermal stability and RNA binding. Biochemistry. 42:2003;2857-2865
81. La D., Silver M., Edgar R.C., Livesay D.R. Using motif-based methods in multiple genome analyses: a case study comparing orthologous mesophilic and thermophilic proteins. Biochemistry. 42:2003;8988-8998
82. Hendsch Z.S., Tidor B. Do salt bridges stabilize proteins? A continuum electrostatic analysis. Protein Sci. 3:1994;211-226
83. Wimley W.C., Gawrisch K., Creamer T.P., White S.H. Direct measurement of salt-bridge solvation energies using a peptide model system: implications for protein stability. Proc. Natl Acad. Sci. USA. 93:1996;2985-2990
84. Horovitz A., Serrano L., Avron B., Bycroft M., Fersht A.R. Strength and co-operativity of contributions of surface salt bridges to protein stability. J. Mol. Biol. 216:1990;1031-1044
85. Waldburger C.D., Schildbach J.F., Sauer R.T. Are buried salt bridges important for protein stability and conformational specificity? Nature Struct. Biol. 2:1995;122-128
86. Yu Y., Monera O.D., Hodges R.S., Privalov P.L. Ion pairs significantly stabilize coiled-coils in the absence of electrolyte. J. Mol. Biol. 255:1996;367-372
87. Vetriani C., Maeder D.L., Tolliday N., Yip K.S., Stillman T.J., Britton K.L., et al. Protein thermostability above 100 °C: a key role for ionic interactions. Proc. Natl Acad. Sci. USA. 95:1998;12300-12305
88. Xiao L., Honig B. Electrostatic contributions to the stability of hyperthermophilic proteins. J. Mol. Biol. 289:1999;1435-1444
89. Frankenberg N., Welker C., Jaenicke R. Does the elimination of ion pairs affect the thermal stability of cold shock protein from the hyperthermophilic bacterium Thermotoga maritima? FEBS Letters. 454:1999;299-302
90. Strop P., Mayo S.L. Contribution of surface salt bridges to protein stability. Biochemistry. 39:2000;1251-1255
91. Perl D., Schmid F.X. Electrostatic stabilization of a thermophilic cold shock protein. J. Mol. Biol. 313:2001;343-357
92. Delbruck H., Mueller U., Perl D., Schmid F.X., Heinemann U. Crystal structures of mutant forms of the Bacillus caldolyticus cold shock protein differing in thermal stability. J. Mol. Biol. 313:2001;359-369
93. Lassila K.S., Datta D., Mayo S.L. Evaluation of the energetic contribution of an ionic network to beta-sheet stability. Protein Sci. 11:2002;688-690
94. Luisi D.L., Snow C.D., Lin J.J., Hendsch Z.S., Tidor B., Raleigh D.P. Surface salt bridges, double-mutant cycles, and protein stability: an experimental and computational analysis of the interaction of the Asp 23 side chain with the N-terminus of the N-terminal domain of the ribosomal protein l9. Biochemistry. 42:2003;7050-7060
95. Makhatadze G.I., Loladze V.V., Ermolenko D.N., Chen X., Thomas S.T. Contribution of surface salt bridges to protein stability: guidelines for protein engineering. J. Mol. Biol. 327:2003;1135-1148
96. Marti D.N., Bosshard H.R. Electrostatic interactions in leucine zippers: thermodynamic analysis of the contributions of Glu and His residues and the effect of mutating salt bridges. J. Mol. Biol. 330:2003;621-637
97. Godsey M.H., Baranova N.N., Neyfakh A.A., Brennan R.G. Crystal structure of MtaN, a global multidrug transporter gene activator. J. Biol. Chem. 276:2001;47178-47184
98. Gill S., von Hippel P. Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182:1989;319-326
99. Sreerama N., Woody R.W. Estimation of protein secondary structure from CD spectra: comparison of CONTIN, SELCON and CDSSTR methods with an expanded reference set. Anal. Biochem. 282:2000;252-260
100. Shriver J., Peters W., Szary N., Clark A., Edmondson S. Calorimetry of hyperthermophile proteins. Methods Enzymol. 334:2001;389-422
101. Rosgen J., Hallerbach B., Hinz H.J. The Janus nature of proteins: systems at the verge of the microscopic and macroscopic world. Biophys. Chem. 74:1998;153-161
102. Terwilliger T.C., Berendzen J. Automated MAD and MIR structure solution. Acta Crystallog. sect. D. 55:1999;849-861
103. Wang B.C. Resolution of phase ambiguity in macromolecular crystallography. Methods Enzymol. 115:1985;90-112
104. Lamzin V.S., Perrakis A. Current state of automated crystallographic data analysis. Nature Struct. Biol. 7:2000;978-981
105. Schneider T.R., Sheldrick G.M. Substructure solution with SHELXD. Acta Crystallog. sect. D. 58:2002;1772-1779
106. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D. 54:1998;905-921
107. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119
108. Holm L., Sander C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233:1993;123-138
109. Holm L., Sander C. Dictionary of recurrent domains in protein structures. Proteins: Struct. Funct. Genet. 33:1998;88-96
110. Kraulis P.J. Molscript - a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950
111. Ramakrishnan V., Finch J.T., Graziano V., Lee P.L., Sweet R.M. Crystal structure of globular domain of histone H5 and its implications for nucleosome binding. Nature. 362:1993;219-223