High-resolution X-ray structure of the DMA-binding protein HU from the hyper-thermophilic Thermotoga maritima and the determinants of its thermostability

Extremophiles

Volumn 7, Issue 2, 2003, Pages 111-122

  Christodoulou, Evangelos ^a   Rypniewski, Wojciech R ^b   Vorgias, Constantinos E ^a  

^a UNIVERSITY OF ATHENS   (Greece)

^b DESY   (Germany)

Author keywords

Hyper thermostable histone like protein HU; Mutants; Thermotoga maritima; X ray structure

Indexed keywords

BACILLUS SUBTILIS; GEOBACILLUS STEAROTHERMOPHILUS; THERMOTOGA MARITIMA;

BACTERIAL DNA; BACTERIAL PROTEIN; DNA BINDING PROTEIN; HISTONE LIKE PROTEIN HU, BACTERIA; HISTONE-LIKE PROTEIN HU, BACTERIA; PROTEIN SUBUNIT; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BACILLUS SUBTILIS; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; DIMERIZATION; DRUG STABILITY; ELECTRICITY; GENETICS; GEOBACILLUS STEAROTHERMOPHILUS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; TEMPERATURE; THERMOTOGA MARITIMA; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BACILLUS STEAROTHERMOPHILUS; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BASE SEQUENCE; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; DNA, BACTERIAL; DNA-BINDING PROTEINS; DRUG STABILITY; ELECTROSTATICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN SUBUNITS; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TEMPERATURE; THERMOTOGA MARITIMA;

EID: 0041821240     PISSN: 14310651     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00792-002-0302-7     Document Type: Article

References (76)

1. Akasako A, Haruki M, Oobatake M, Kanaya S (1995) High resistance of Escherichia coli ribonuclease HI variant with quintuple thermostabilizing mutations to thermal denaturation, acid denaturation, and proteolytic degradation. Biochemistry 34:8115-8122
2. Boelens R, Vis H, Vorgias CE, Wilson KS, Kaptein R (1996) Structure and dynamics of the DNA binding protein HU from Bacillus stearothermophilus by NMR spectroscopy. Biopolymers 40:553-559
3. Bogin O, Peretz M, Hacham Y, Korkhin Y, Frolow F, Kalb (Gilboa) AJ, Burstein Y (1998) Enhanced thermal stability of Clostridium beijerinckii alcohol dehydrogenase after strategic substitution of amino acid residues with prolines from the homologous thermophilic Thermoanaerobacter brockii alcohol dehydrogenase. Protein Sci 7:1156-1163
4. Broyles SS, Pettijohn DE (1986) Interaction of the Escherichia coli HU protein with DNA. Evidence for formation of nucleosome-like structures with altered DNA helical pitch. J Mol Biol 187:47-60
5. Brünger AT (1992) Free R value: a novel statistical quantity for assessing the accurancy of crystal structures. Nature 355:472-475
6. Burley SK, Petsko GA (1985) Aromatic-aromatic interaction: a mechanism of protein structure stabilization. Science 229:23-28
7. Cambilliau C, Claverie JM (2000) Structural and genomic correlates of hyperthermostability. J Biol Chem 275:32383-32386
8. Castaing BC, Zelwer C, Laval J, Boiteux S (1995) HU protein of Escherichia coli binds specifically to DNA that contains single-strand breaks or gaps. J Biol Chem 270:10291-10296
9. Christodoulou E, Vorgias CE (1998) Cloning, overproduction, purification and crystallization of the DNA binding protein HU from the hyperthermophilic eubacterium Thermotoga maritima. Acta Crystallogr D Biol Crystallogr 54:1043-1045
10. Christodoulou E, Vorgias CE (2002) The thermostability of DNA-binding protein HU from mesophilic, thermophilic, and extreme thermophilic bacteria. Extremophiles 6:21-31
11. Claret L, Rouviere-Yaniv J (1996) Regulation of HUα and HUβ by CRP and FIS in Escherichia coli. J Mol Biol 263:126-139
12. Collaborative Computational Project Number 4 (1994) The CCP4 suite: Programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50:760-763
13. Craigie R, Arndt-Jovin, DJ, Mizuuchi D (1985) A defined system for the DNA strand-transfer reaction at the initiation of bacteriophage Mu transposition: protein and DNA substrate requirements. Proc Natl Acad Sci USA 82:7570-7574
14. Drlica K, Rouviére-Yaniv J (1987) Histonelike proteins of bacteria. Microbiol Rev 51:301-319
15. Eijsink VG, Dijkstra BW, Vriend G, van der Zee J, Veltman OR, van der Vinne B, van den Burg B, Kempe S, Venema G (1992) The effect of cavity-filling mutations on the thermostability of Bacillus stearothermophilus neutral protease. Protein Eng 5:421-426
16. Elcock AH (1998) The stability of salt bridges at high temperatures: implications for hyperthermophilic proteins. J Mol Biol 284:489-502
17. Esser D, Rudolph R, Jaeicke R, Böhm G (1999) The HU protein from Thermotoga maritima: recombinant expression, purification and physicochemical characterization of an extremely hyperthermophilic DNA-binding protein. J Mol Biol 291:1135-1146
18. Flashner Y, Gralla JD (1988) DNA dynamic flexibility and protein recognition: differential stimulation by bacterial histone-like protein HU. Cell 54:713-721
19. French S, Wilson KS (1978) On treatment of negative intensity observations. Acta Crystallogr A 34:517-525
20. Grove A, Lynette L (2001) High-affinity DNA binding of HU protein from the hyperthermophile Thermotoga maritima. J Mol Biol 311:491-502
21. Haney PJ, Badger JH, Buldak GL, Reich CI, Woese CR, Olsen GJ (1999) Thermal adaptation analyzed by comparison of protein sequences from mesophilic and extremely thermophilic Methanococcus species. Proc Natl Acad Sci USA 96:3578-3583
22. Hensel R, Jakob I (1994) Stability of glycer-aldehyde-3-phosphate dehydrogenase from hyperthermophilic archaea at high temperature. Syst Appl Microbiol 16:742-745
23. Jaenicke R, Böhm G (1998) The stablility of proteins in extreme environments. Curr Opin Struct Biol 8:738-748
24. Jones TA, Zou JY, Kjeldgaard M (1991) Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 47:110-119
25. Karshikoff A, Ladenstein R (1998) Proteins from thermophilic and mesophilic organisms essentially do not differ in packing. Protein Eng 11:867-872
26. Karshikoff A, Ladenstein R (2001) Ion pairs and the thermotolerance of proteins from hyperthermophiles: a "traffic rule" for hot roads. Trends Biochem Sci 26:550-556
27. Kawamura S, Kakuta Y, Tanaka I, Hikichi K, Kuhara S, Yamasaki N, Kimura M (1996) Glycine-15 in the bend between two a-helices can explain the thermostability of DNA binding protein HU from Bacillus stearothermophilus. Biochemistry 35:1195-1200
28. Kawamura S, Abe Y, Ueda T, Masumoto K, Imoto T, Yamasaki N, Kimura M (1998) Investigation of the Structural Basis for Thermostability of DNA-binding Protein HU from Bacillus stearothermophilus. J Biol Chem 273:19982-19987
29. Kawashima T, Amano N, Koike H, Makino S, Higuchi S, Kawashima-Ohya Y, Watanabe K, Yamazaki M, Kanehori K, Kawamoto T, Nunoshiba T, Yamamoto Y, Aramaki H, Makino K, Suzuki M (2000) Archaeal adaptation to higher temperatures revealed by genomic sequence of Thermoplasma volcanium. Proc Natl Acad Sci USA 97:14257-14262
30. Kimura S, Nakamura H, Hashimoto T, Oobatake M, Kanaya S (1992) Stabilization of escherichia coli ribonuclease hi by strategic replacement of amino acid residues with those from the thermophilic counterpart. J Biol Chem 267:21535-21542
31. Kraulis PJ (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 24:946-960
32. Kumar S, Tsai CJ, Nussinov R (2000) Factors enhancing protein thermostability. Protein Eng 13:179-191
33. Ladenstein R, Antranikian G (1998) Proteins from hyperthermophiles: stability and enzymatic catalysis close to the boiling point of water. Adv Biochem Eng Biotechnol 61:37-85
34. Lamzin VS, Wilson KS (1993) Automated refinement of protein models. Acta Crystallogr D Biol Crystallogr 49:129-147
35. Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26:283-291
36. Lehmann M, Wyss M (2001) Engineering proteins for thermostability: the use of sequence alignments versus rational design and directed evolution. Curr Opin Biotech 12:371-375
37. Mensa-Wilmot K, Carroll K, McMacken R (1989) Transcriptional activation of bacteriophage lambda DNA replication in vitro: regulatory role of histone-like protein HU of Escherichia coli. EMBO J 8:2393-2402
38. Murshudov GN, Vagin AA, Lebedev A, Wilson KS, Dodson EJ (1999) Efficient anisotropic refinement of macromolecular structures using FFT. Acta Crystallogr D Biol Crystallogr 55:(1):247-255
39. Navaza J (1994) AMoRe: an automated package for molecular replacement. Acta Crystallogr A 50:157-163
40. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Academic Press, London
41. Padas PM, Wilson KS, Vorgias CE (1992) The DNA-binding protein HU from mesophilic and thermophilic bacilli: gene cloning, overproduction and purification. Gene 117:39-44
42. Perrin S, Gilliland G (1990) Site-specific mutagenesis using asymmetric polymerase chain reaction and a single mutant primer. Nucleic Acids Res 18:7433-7438
43. Pettijohn DE (1988) Histone-like proteins and bacterial chromosome structure. J Biol Chem 263:12793-12796
44. Querol E, Perez-Pons JA, Mozo-Villarias A (1996) Analysis of protein conformational characteristics related to thermostability. Protein Eng 9:265-271
45. Ramachandran GN, Sasisekharan V (1968) Conformation of polypeptides and proteins. Adv Protein Chem 23:283-437
46. Rice PA, Yang SW, Mizuuchi K, Nash H (1996) Crystal structure of an IHF-DNA complex: a protein-induced DNA U-turn. Cell 87:1295-1306
47. Rouviére-Yaniv J, Gros F (1975) Characterization of a novel, low-molecular-weight DNA-binding protein from Escherichia coli. Proc Natl Acad Sci USA 72:3428-3432
48. Rouvière-Yaniv J, Yaniv M, Germond J (1979) E. coli DNA binding protein HU forms nucleosomelike structures with double-stranded DNA. Cell 17:265-274
49. Russell RJ, Taylor GL (1995) Engineering thermostability: lessons from thermophilic proteins. Curr Opin Biotech 6:370-374
50. Russell RJ, Ferguson JM, Hough DW, Danson MJ, Taylor GL (1997) The crystal structure of citrate synthase from the hyperthermophilic archaeon Pyrococcus furiosus at 1.9 Å resolution. Biochemistry 36:9983-9994
51. Salminen T, Teplyakov A, Kankare J, Cooperman BS, Lahti R, Goldman A (1996) An unusual route to thermostability disclosed by the comparison of Thermus thermophilus and Escherichia coli inorganic pyrophosphatases. Protein Sci 5:1014-1025
52. Sandberg WS, Terwilliger TC (1989) Influence of interior packing and hydrophobicity on the stability of a protein. Science 245:54-57
53. Serrano L, Day AG, Fersht AR (1993) Step-wise mutation of barnase to binase. A procedure for engineering increased stability of proteins and an experimental analysis of the evolution of protein stability. J Mol Biol 233:305-312
54. Shih P, Kirsch JF (1995) Design and structural analysis of an engineered thermostable chicken lysozyme. Protein Sci 4:1063-2072
55. Spector S, Wang A, Carp SA, Robblee J, Hendsch ZS, Fairman R, Tidor B, Raleigh DP (2000) Rational modification of protein stability by the mutation of charged surface residues. Biochemistry 39:872-879
56. Sriprapundh D, Vieille C, Zeikus JG (2000) Molecular determinants of xylose isomerase thermal stability and activity: analysis of thermozymes by site-directed mutagenesis. Protein Eng 13:259-265
57. Steen IH, Madern D, Karlstrom M, Lien T, Ladenstein R, Birkeland NK (2001) Comparison of isocitrate dehydrogenase from three hyperthermophiles reveals differences in thermostability, cofactor specificity, oligomeric state, and phylogenetic affiliation. J Biol Chem 276:43924-43931
58. Sterner R, Liebl W (2001) Thermophilic adaptation of proteins. Crit Rev Biochem Mol Biol 36:39-106
59. Szilagyi A, Zavodszky P (2000) Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey. Struct Fold Des 8:493-504
60. Tanaka I, Appelt K, Dijk J, White SW, Wilson KS (1984) 3-Å resolution structure of a protein with histone-like properties in prokaryotes. Nature 310:376-381
61. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal_X windows interface flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876-4882
62. Van den Burg B, Vriend G, Veltman OR, Venema G, Eijsink VG (1998) Engineering an enzyme to resist boiling. Proc Natl Acad Sci USA 95:2056-2060
63. Van Silfhout RG, Hermes C (1995) X-ray instrumentation for a focused wiggler beamline at the EMBL Outstation Hamburg. Rev Sci Instrum 66:1818-1820
64. Vis H, Mariani M, Vorgias CE, Wilson KS, Kaptein R, Boelens R (1995) Solution structure of the HU Protein from Bacillus stearothermophilus. J Mol Biol 254:692-703
65. Vogt G, Argos P (1997) Protein thermal stability: hydrogen bonds or internal packing? Fold Des 2:40-46
66. Vogt G, Woell S, Argos P (1997) Protein thermal stability, hydrogen bonds, and ion pairs. J Mol Biol 269:631-643
67. Watanabe K, Hata Y, Kizaki H, Katsube Y, Suzuki Y (1997) The refined crystal structure of Bacillus cereus oligo-1,6-glucosidase at 2.0 A resolution: structural characterization of proline-substitution sites for protein thermostabilization. J Mol Biol 269:142-153
68. White SW, Appelt K, Wilson KS, Tanaka I (1989) A protein structural motif that bends DNA. Proteins 5:281-288
69. White SW, Wilson KS, Appelt K, Tanaka I (1999) The high-resolution structure of DNA-binding protein HU from Bacillus stearothermophilus. Acta Crystallogr D Biol Crystallogr 55:801-809
70. Wilson KS, Vorgias CE, Tanaka I, White SW, Kimura M (1990) The thermostability of DNA-binding protein HU from Bacilli. Protein Eng 4:11-22
71. Wintrode PL, Arnold FH (2001) Temperature adaptation of enzymes: lessons from laboratory evolution. Adv Protein Chem 55:161-225
72. Wojtuszewski K, Hawkins ME, Cole JL, Mukerji I (2001) HU binding to DNA: evidence for multiple complex formation and DNA bending. Biochemistry 27:2588-2598
73. Wright HT (1991) Nonenzymatic deamidation of asparaginyl and glutaminyl residues in proteins. Crit Rev Biochem Mol Biol 26:4632-4636
74. Xiao L, Honig B (1999) Electrostatic contributions to the stability of hyperthermophilic proteins. J Mol Biol 289:1435-1444
75. Yip KS, Stillman TJ, Britton KL., Artymiuk PJ, Baker PJ, Sedelnikova SE, Engel PC, Pasquo A, Chiaraluce R, Consalvi V (1995) The structure of Pyrococcus furiosus glutamate dehydrogenase reveals a key role for ion-pair networks in maintaining enzyme stability at extreme temperatures. Structure 3:1147-1158
76. Zuber H (1988) Temperature adaptation of lactate dehydrogenase. Structural, functional and genetic aspects. Biophys Chem 29:171-179