Large improvement in the thermal stability of a tetrameric malate dehydrogenase by single point mutations at the dimer-dimer interface

Journal of Molecular Biology

Volumn 341, Issue 5, 2004, Pages 1215-1226

  Bjørk, Alexandra ^a   Dalhus, Bjørn ^a   Mantzilas, Dimitrios ^a   Sirevg, Reidun ^a   Eijsink, Vincent G H ^b  

^a UNIVERSITY OF OSLO   (Norway)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

crystal structures; electrostatic subunit interactions; site directed mutagenesis; tetrameric malate dehydrogenase; thermal stability

Indexed keywords

DIMER; GLUTAMIC ACID; GLYCINE; LYSINE; MALATE DEHYDROGENASE; OLIGOMER;

ARTICLE; CATALYSIS; CHLOROFLEXUS AURANTIACUS; CRYSTAL STRUCTURE; ELECTRICITY; LOW TEMPERATURE; MUTATION; NONHUMAN; PH; PHOTOTROPHIC BACTERIUM; PRIORITY JOURNAL; THERMOSTABILITY;

BACTERIA (MICROORGANISMS); CHLOROFLEXUS AURANTIACUS; PHOTOBACTERIA;

EID: 4143143467     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.06.079     Document Type: Article

References (66)

1. C. Vieille, and G.J. Zeikus Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability Microbiol. Mol. Biol. Rev. 65 2001 1 43
2. V. Villeret, B. Clantin, C. Tricot, C. Legrain, M. Roovers, and V. Stalon The crystal structure of Pyrococcus furiosus ornithine carbamoyltransferase reveals a key role for oligomerization in enzyme stability at extremely high temperatures Proc. Natl Acad. Sci. USA 95 1998 2801 2866
3. H. Walden, G.S. Bell, R.J. Russell, B. Siebers, R. Hensel, and G.L. Taylor Tiny TIM: a small, tetrameric, hyperthermostable triosephosphate isomerase J. Mol. Biol. 306 2001 745 757
4. N. Maeda, T. Kanai, H. Atomi, and T. Imanaka The unique pentagonal structure of an archaeal Rubisco is essential for its high thermostability J. Biol. Chem. 277 2002 31656 31662
5. C.A. Kelly, M. Nishiyama, Y. Ohnishi, T. Beppu, and J.J. Birktoft Determinants of protein thermostability observed in the 1.9- crystal structure of malate dehydrogenase from the thermophilic bacterium Thermus flavus Biochemistry 32 1993 3913 3922
6. K.S.P. Yip, T.J. Stillman, K.L. Britton, P.J. Artymiuk, P.J. Baker, and S.E. Sedelnikova The structure of Pyrococcus furiosus glutamate dehydrogenase reveals a key role for ion-pair networks in maintaining enzyme stability at extreme temperatures Structure 3 1995 1147 1158
7. R.J. Russell, J.M. Ferguson, D.W. Hough, M.J. Danson, and G.L. Taylor The crystal structure of citrate synthase from the hyperthermophilic archaeon Pyrococcus furiosus at 1.9 resolution Biochemistry 36 1997 9983 9994
8. C.F. Aguilar, I. Sanderson, M. Moracci, M. Ciaramella, R. Nucci, M. Rossi, and L.H. Pearl Crystal structure of the beta-glycosidase from the hyperthermophilic archeon Sulfolobus solfataricus: resilience as a key factor in thermostability J. Mol. Biol. 271 1997 789 802
9. C. Vetriani, D.L. Maeder, N. Tolliday, K.S. Yip, T.J. Stillman, and K.L. Britton Protein thermostability above 100 degreesC: a key role for ionic interactions Proc. Natl Acad. Sci. USA 95 1998 12300 12305
10. E. Nordberg Karlsson, S.J. Crennell, C. Higgins, S. Nawaz, L. Yeoh, D.W. Hough, and M.J. Danson Citrate synthase from Thermus aquaticus: a thermostable bacterial enzyme with a five-membered inter-subunit ionic network Extremophiles 7 2003 9 16
11. M.F. Perutz, and H. Raidt Stereochemical basis of heat stability in bacterial ferredoxins and in haemoglobin A2 Nature 255 1975 256 259
12. A.H. Elcock The stability of salt bridges at high temperatures: implications for hyperthermophilic proteins J. Mol. Biol. 284 1998 489 502
13. L. Xiao, and B. Honig Electrostatic contributions to the stability of hyperthermophilic proteins J. Mol. Biol. 289 1999 1435 1444
14. A. Szilagyi, and P. Zavodszky Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey Struct. Fold. Des. 8 2000 493 504
15. A. Karshikoff, and R. Ladenstein Ion pairs and the thermotolerance of proteins from hyperthermophiles: a "traffic rule" for hot roads Trends Biochem. Sci. 26 2001 550 556
16. R. Thoma, M. Hennig, R. Sterner, and K. Kirschner Structure and function of mutationally generated monomers of dimeric phosphoribosylanthranilate isomerase from Thermotoga maritima Struct. Fold. Des. 8 2000 265 276
17. M.A. Arnott, R.A. Michael, C.R. Thompson, D.W. Hough, and M.J. Danson Thermostability and thermoactivity of citrate synthases from the thermophilic and hyperthermophilic archaea, Thermoplasma acidophilum and Pyrococcus furiosus J. Mol. Biol. 304 2000 657 668
18. B. Clantin, C. Tricot, T. Lonhienne, V. Stalon, and V. Villeret Probing the role of oligomerization in the high thermal stability of Pyrococcus furiosus ornithine carbamoyltransferase by site-specific mutants Eur. J. Biochem. 268 2001 3937 3942
19. B. Cobucci-Ponzano, M. Moracci, B. Di Lauro, M. Ciaramella, R. D'Avino, and M. Rossi Ionic network at the C-terminus of the beta-glycosidase from the hyperthermophilic archaeon Sulfolobus solfataricus: functional role in the quaternary structure thermal stabilization Proteins: Struct. Funct. Genet. 48 2002 98 106
20. A. Bjørk, D. Mantzilas, R. Sirevg, and V.G.H. Eijsink Electrostatic interactions across the dimer-dimer interface contribute to the pH-dependent stability of a tetrameric malate dehydrogenase FEBS Letters 553 2003 423 426
21. J.C. Williams, J.P. Zeelen, G. Neubauer, G. Vriend, J. Backmann, and P.A. Michels Structural and mutagenesis studies of leishmania triosephosphate isomerase: a point mutation can convert a mesophilic enzyme into a superstable enzyme without losing catalytic power Protein Eng. 12 1999 243 250
22. J.H. Lebbink, S. Knapp, J. van der Oost, D. Rice, R. Ladenstein, and W.M. de Vos Engineering activity and stability of Thermotoga maritima glutamate dehydrogenase. II: construction of a 16-residue ion-pair network at the subunit interface J. Mol. Biol. 289 1999 357 369
23. O. Bogin, I. Levin, Y. Hacham, S. Tel-Or, M. Peretz, F. Frolow, and Y. Burstein 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
24. L.P. Gerk, O. Leven, and B. Muller-Hill Strengthening the dimerisation interface of Lac repressor increases its thermostability by 40 deg. C J. Mol. Biol. 299 2000 805 812
25. R.T. Sauer, K. Hehir, R.S. Stearman, M.A. Weiss, A. Jeitler-Nilsson, E.G. Suchanek, and C.O. Pabo An engineered intersubunit disulfide enhances the stability and DNA binding of the N-terminal domain of lambda repressor Biochemistry 25 1986 5992 5998
26. M. Shirakawa, H. Matsuo, and Y. Kyogoku Intersubunit disulfide-bonded lambda-Cro protein Protein Eng. 4 1991 545 552
27. R.S. Gokhale, S. Agarwalla, V.S. Francis, D.V. Santi, and P. Balaram Thermal stabilization of thymidylate synthase by engineering two disulfide bridges across the dimer interface J. Mol. Biol. 235 1994 89 94
28. T. Kabashima, Y. Li, N. Kanada, K. Ito, and T. Yoshimoto Enhancement of the thermal stability of pyroglutamyl peptidase I by introduction of an intersubunit disulfide bond Biochim. Biophys. Acta 1547 2001 214 220
29. A. Bjørk, B. Dalhus, D. Mantzilas, V.G.H. Eijsink, and R. Sirevg Stabilization of a tetrameric malate dehydrogenase by introduction of a disulfide bridge at the dimmer-dimer interface J. Mol. Biol. 334 2003 811 821
30. B. Dalhus, M. Saarinen, U.H. Sauer, P. Eklund, K. Johansson, and A. Karlsson Structural basis for thermophilic protein stability: structures of thermophilic and mesophilic malate dehydrogenases J. Mol. Biol. 318 2002 707 721
31. J.J. Birktoft, R.A. Bradshaw, and L.J. Banaszak Structure of porcine heart cytoplasmic malate dehydrogenase: combining X-ray diffraction and chemical sequence data in structural studies Biochemistry 26 1987 2722 2734
32. M.D. Hall, D.G. Levitt, and L.J. Banaszak Crystal structure of Escherichia coli malate dehydrogenase. A complex of the apoenzyme and citrate at 1.87 resolution J. Mol. Biol. 226 1992 867 882
33. W.B. Gleason, Z. Fu, J. Birktoft, and L. Banaszak Refined crystal structure of mitochondrial malate dehydrogenase from porcine heart and the consensus structure for dicarboxylic acid oxidoreductases Biochemistry 33 1994 2078 2088
34. G. Vriend WHAT IF: a molecular modeling and drug design program J. Mol. Graph. 8 1990 52 56
35. A. Martin, I. Kather, and F.X. Schmid Origins of the high stability of an in vitro-selected cold-shock protein J. Mol. Biol. 318 2002 1341 1349
36. B. Van den Burg, G. Vriend, O.R. Veltman, G. Venema, and V.G.H. Eijsink Engineering an enzyme to resist boiling Proc. Natl Acad. Sci. USA 95 1998 2056 2060
37. J. Hasegawa, H. Shimahara, M. Mizutani, S. Uchiyama, H. Arai, and M. Ishii Stabilization of Pseudomonas aeruginosa cytochrome c(551) by systematic amino acid substitutions based on the structure of thermophilic Hydrogenobacter thermophilus cytochrome c(552) J. Biol. Chem. 274 1999 37533 37537
38. D. Perl, U. Mueller, U. Heinemann, and F.X. Schmid Two exposed amino acid residues confer thermostability on a cold shock protein Nature Struct. Biol. 7 2000 380 383
39. M. Sandgren, P.J. Gualfetti, A. Shaw, L.S. Gross, M. Saldajeno, and A.G. Day Comparison of family 12 glycoside hydrolases and recruited substitutions important for thermal stability Protein Sci. 12 2003 848 860
40. A. Irimia, F.M. Vellieux, D. Madern, G. Zaccai, A. Karshikoff, and G. Tibbelin The 2.9 resolution crystal structure of malate dehydrogenase from Archaeoglobus fulgidus: mechanisms of oligomerisation and thermal stabilisation J. Mol. Biol. 335 2004 343 356
41. A.S. Langelandsvik, I.H. Steen, N.K. Birkeland, and T. Lien Properties and primary structure of a thermostable L-malate dehydrogenase from Archaeoglobus fulgidus Arch. Microbiol. 168 1997 59 67
42. R. Jaenicke, and G. Böhm The stability of proteins in extreme environments Curr. Opin. Struct. Biol. 8 1998 738 748
43. G. Hernandez, F.E. Jenney Jr, M.W. Adams, and D.M. LeMaster Millisecond time scale conformational flexibility in a hyperthermophile protein at ambient temperature Proc. Natl Acad. Sci. USA 97 2000 3166 3170
44. R. Jaenicke Do ultrastable proteins from hyperthermophiles have high or low conformational rigidity? Proc. Natl Acad. Sci. USA 97 2000 2962 2964
45. A. Svingor, J. Kardos, I. Hajdu, A. Nemeth, and P. Zavodszky A better enzyme to cope with cold. Comparative flexibility studies on psychrotrophic, mesophilic, and thermophilic IPMDHs J. Biol. Chem. 276 2001 28121 28125
46. S. D'Amico, J.C. Marx, C. Gerday, and G. Feller Activity-stability relationships in extremophilic enzymes J. Biol. Chem. 278 2003 7891 7896
47. L. Giver, A. Gershenson, P.O. Freskgard, and F.H. Arnold Directed evolution of a thermostable esterase Proc. Natl Acad. Sci. USA 95 1998 12809 12813
48. H. Zhao, and F.H. Arnold Directed evolution converts subtilisin E into a functional equivalent of thermitase Protein Eng. 12 1999 47 53
49. M. Lehmann, D. Kostrewa, M. Wyss, R. Brugger, A. D'Arcy, L. Pasamontes, and A.P. van Loon From DNA sequence to improved functionality: using protein sequence comparisons to rapidly design a thermostable consensus phytase Protein Eng. 13 2000 49 57
50. P.L. Wintrode, and F.H. Arnold Temperature adaptation of enzymes: lessons from laboratory evolution Advan. Protein Chem. 55 2000 161 225
51. K. Miyazaki, P.L. Wintrode, R.A. Grayling, D.N. Rubingh, and F.H. Arnold Directed evolution study of temperature adaptation in a psychrophilic enzyme J. Mol. Biol. 297 2000 1015 1026
52. H. Flores, and A.D. Ellington Increasing the thermal stability of an oligomeric protein, beta-glucuronidase J. Mol. Biol. 315 2002 325 337
53. J.H. Lebbink, R.I. Eggen, A.C. Geerling, V. Consalvi, R. Chiaraluce, R. Scandurra, and W.M. de Vos Exchange of domains of glutamate dehydrogenase from the hyperthermophilic archaeon Pyrococcus furiosus and the mesophilic bacterium Clostridium difficile: effects on catalysis, thermoactivity and stability Protein Eng. 8 1995 1287 1294
54. T.M. Thomas, and R.K. Scopes The effects of temperature on the kinetics and stability of mesophilic and thermophilic 3-phosphoglycerate kinases Biochem. J. 330 1998 1087 1095
55. R.M. Daniel, and M.J. Danson Assaying activity and assessing thermostability of hyperthermophilic enzymes Methods Enzymol. 334 2001 283 293
56. R.M. Daniel, M.J. Danson, and R. Eisenthal The temperature optima of enzymes: a new perspective on an old phenomenon Trends Biochem. Sci. 26 2001 223 225
57. B. Synstad, O. Emmerhoff, and R. Sirevg Malate dehydrogenase from the green gliding bacterium Chloroflexus aurantiacus is phylogenetically related to lactic dehydrogenases Arch. Microbiol. 165 1996 346 353
58. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
59. A.K. Rolstad, E. Howland, and R. Sirevg Malate dehydrogenase from the thermophilic green bacterium Chloroflexus aurantiacus: purification, molecular weight, amino acid composition, and partial amino acid sequence J. Bacteriol. 170 1988 2947 2953
60. C.N. Pace Measuring and increasing protein stability Trends Biotechnol. 8 1990 93 98
61. Otwinoski, Z. & Minor, W. (1997). Processing of X-ray data collected in oscillation mode. In Methods in Enzymology, Macromolecular Crystallography, Part A (Carter, C. W. J. & Sweet, R. M., eds.), vol. 276, pp. 307-326, Academic Press, New York.
62. A.T. Brünger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, and R.W. Grosse-Kunstleve Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallog. sect. D Biol. Crystallog. 54 1998 905 921
63. T.A. Jones, J.Y. Zou, S.W. Cowan, and M. Kjeldgaard 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
64. R.M. Esnouf Further additions to MolScript version 1.4, including reading and contouring of electron-density maps Acta Crystallog. sect. D Biol Crystallog. 55 1999 938 940
65. E.A. Meritt Raster3D: photorealistic molecular graphics Methods Enzymol. 277 1997 505 524
66. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Thornton PROCHECK: a program to check the stereochemistry quality of protein structures J. Appl. Crystallog. 26 1993 283 291