The crystal structure of triosephosphate isomerase (TIM) from Thermotoga maritima: a comparative thermostability structural analysis of ten different TIM structures
Maes, Dominique; Zeelen, Johan P.; Thanki, Narmadaet al.
[en] The molecular mechanisms that evolution has been employing to adapt to environmental temperatures are poorly understood. To gain some further insight into this subject we solved the crystal structure of triosephosphate isomerase (TIM) from the hyperthermophilic bacterium Thermotoga maritima (TmTIM). The enzyme is a tetramer, assembled as a dimer of dimers, suggesting that the tetrameric wild-type phosphoglycerate kinase PGK-TIM fusion protein consists of a core of two TIM dimers covalently linked to 4 PGK units. The crystal structure of TmTIM represents the most thermostable TIM presently known in its 3D-structure. It adds to a series of nine known TIM structures from a wide variety of organisms, spanning the range from psychrophiles to hyperthermophiles. Several properties believed to be involved in the adaptation to different temperatures were calculated and compared for all ten structures. No sequence preferences, correlated with thermal stability, were apparent from the amino acid composition or from the analysis of the loops and secondary structure elements of the ten TIMs. A common feature for both psychrophilic and T. maritima TIM is the large number of salt bridges compared with the number found in mesophilic TIMs. In the two thermophilic TIMs, the highest amount of accessible hydrophobic surface is buried during the folding and assembly process.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Maes, Dominique; Vrije Universiteit Brussel > Vlaams Interuniversitair Instituut voor Biotechnologie
Zeelen, Johan P.; European Molecular Biology Laboratory
Thanki, Narmada; European Molecular Biology Laboratory
Beaucamp, Nicola; Universität Regensburg > Institut für Biophysik und physikalische Biochemie
Alvarez, Marco
Thi, Minh Hoa Dao; Vrije Universiteit Brussel > Vlaams Interuniversitair Instituut voor Biotechnologie
Backmann, Jan; Vrije Universiteit Brussel > Vlaams Interuniversitair Instituut voor Biotechnologie
Martial, Joseph ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Biologie et génétique moléculaire
Wyns, Lode; Vrije Universiteit Brussel > Vlaams Interuniversitair Instituut voor Biotechnologie
Jaenicke, Rainer; Universität Regensburg > Institut für Biophysik und physikalische Biochemie
Wierenga, Rik K.; European Molecular Biology Laboratory
Language :
English
Title :
The crystal structure of triosephosphate isomerase (TIM) from Thermotoga maritima: a comparative thermostability structural analysis of ten different TIM structures
Publication date :
1999
Journal title :
Proteins
ISSN :
0887-3585
eISSN :
1097-0134
Publisher :
Wiley Liss, Inc., New York, United States - New York
Jaenicke R, Böhm G. The stability of proteins in extreme environments. Curr Opin Struct Biol 1998;8:738-748.
Russell RJM, Gerike U, Danson MJ, Hough DW, Taylor GL. Structural adaptations of the cold-active citrate synthase from an Antarctic bacterium. Structure 1998;6:351-361.
Alvarez M, Zeelen JP, Mainfroid V, et al. Triose-phophate isomerase (TIM) of the psychrophilic bacterium Vibrio marinus. J Biol Chem 1998;273:2199-2206.
Aghajari N, Feller G, Gerday C, Haser R. Structure of the psychrophilic Alteromonas haloplanctisα-amylase give insight into cold adaptation at a molecular level. Structure 1998;6:1503-1516.
Querol E, Perez-Pons JA, Mozo-Villarias A. Analysis of protein conformational characteristics related to thermostability. Protein Eng. 1996;9:265-271.
Jaenicke R, Schurig H, Beaucamp N, Ostendorp R. Structure and stability of hyperstable proteins:glycolytic enzymes from hyperthermophilic bacterium Thermotoga maritima. Adv Protein Chem 1996;48:181-269.
Voght G, Argos P. Protein thermal stability: hydrogen bonds or internal packing. Folding Design 1997;2:S40-S46.
Knowles JR. To build an enzyme. Philos Trans R Soc Lond B Biol Sci 1991;B332:115-121.
Noble MEM, Zeelen JP, Wierenga RK. Structure of the open and closed state of trypanosomal triosephosphate isomerase, as observed in a new crystal form: implications for the reaction mechanism. Proteins 1993;16:311-326.
Joseph D, Petsko GA, Karplus M. Anatomy of a conformational change: Hinged "lid" motion of the triose phosphate isomerase loop. Science 1990;249:1425-1428.
Schliebs W, Thanki, N, Eritja R, Wierenga R. Active site properties of monomeric triosephosphate isomerase (monoTIM) as deduced from mutational and structural studies. Protein Sci 1996;5:229-239.
Banner DW, Bloomer AC, Petsko GA, et al. Structure of chicken muscle triose phosphate isomerase determined crystallographically at 2.5 Å resolution. Nature 1975;255:609-614.
Wierenga RK, Noble MEM, Davenport RC. Comparison of the refined crystal structures of liganded and the unliganded chicken, yeast and trypanosomal triosephosphate isomerase. J Mol Biol 1992;224:1115-1126.
Lolis E, Alber T, Davenport RC, Rose D, Hartman FC, Petsko GA. Structure of yeast triosephosphate isomerase at 1.9 Å resolution. Biochemistry 1990;29:6609-6618.
Wierenga RK, Noble MEM, Vriend G, Nauche S, Hol WGJ. Refined 1.83Å structure of trypanosomal triosephosphate isomerase crystallized in the presence of 2.4M-ammonium sulphate. J Mol Biol 1991;220:995-1015.
Noble MEM, Zeelen JP, Wierenga RK. Structure of triosephosphate isomerase from Escherichia coli determined at 2.6Å resolution. Acta Crystallogr 1993;D49:403-417.
Mande SC, Mainfroid V, Kalk KH, Goraj K, Martial JA, Hol WGJ. Crystal structure of recombinant human triosphosphate isomerase at 2.8 Å resolution. Triosephosphate isomerase-related human genetic disorders and comparison with the trypanosomal enzyme. Protein Sci 1994;3:810-821.
Velanker SS, Ray SS, Gokhale RS, Hemalatha Balaram SS, Murthy MRN. Triosephosphate isomerase from Plasmodium falciparum: the crystal structure provides insights into antimalarial drug design. Structure 1997;5:751-761.
Williams JC, Zeelen JP, Neubauer G, Vriend G, Backmann J, Michels PA, Lambeir AM, Wierenga RK. Structural and mutational studies of leishmania triosephosphate isomerase: a point mutation can convert a mesophilic enzyme into a superstable enzyme without losing catalytic power. Prot Eng 1999;12:243.
Maldonado E, Soriano-Garcia M, Moreno A, et al. Differences in the intersubunit contacts in triosephosphate isomerase from two closely related pathogenic trypanosomes. J Mol Biol 1998;283:193-203.
Delboni LF, Mande SC, Rentier-Delrue F, et al. Crystal structure of recombinant triosephosphate isomerase from Bacillus stearothermophilus. An analysis of potential thermostability factors in six isomerases with known three-dimensional structures points to the importance of hydrophobic interactions. Protein Sci 1995;4: 2594-2604.
Schurig H, Beaucamp N, Ostendorp R, Jaenicke R, Adler E, Knowles JR. PGK and TIM from the hyperthermophilic bacterium Thermotoga maritima form a covalent bifunctional enzyme complex. EMBO J 1995;14:442-452.
Beaucamp N, Hofmann A, Kellerer B, Jaenicke R. Dissection of the gene of the bifunctional PGK-TIM fusion protein from the hyperthermophilic bacterium Thermotoga maritima: design and characterization of the separate triosephosphate isomerase Protein Sci 1997;6:2159-2165.
Yphantis DA. Equilibrium ultracentrifugation of dilute solutions. Biochemistry 1994;3:297-317.
Otwinowski Z. DENZO. An oscillation data processing program for macromolecular crystallography. New Haven: Yale University Press; 1993.
Collaborative Computational Project Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr D 1994;D50: 760-763.
Navazza J. AMoRe: an automated package for molecular replacement. Acta Crystallogr 1994;A50:157-163.
Jones TA, Zou JY, Cowan SW, Kjelgaard M. Improved methods for building protein models in electron density amps and the location of errors in these models. Acta Crystallogr 1991;A47:110-119.
Brünger AT. X-PLOR. Version 3.1. A system for X-ray crystallography and NMR. New Haven: Yale University Press; 1992.
Brünger AT, Adams PD, Clore MG, et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D 1998;D54:905-921.
Laskowski RA, MacArthur MW, Moss DS, Thornton JM. PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 1993;26:283-291.
Vriend G. WHAT IF: a molecular modeling and drug design program. J Mol Graph 1990;8:52-56.
Devereux J, Haeberli P, Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 1984;12:387-395.
Kabsch W, Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 1983;22:2577-2637.
Richardson JS, Richardson DC. Amino acid preferences for specific locations at the ends of a helices. Science 1988;240:1648-1652.
Connolly ML. Computation of molecular volume. J Am Chem Soc 1985;107:1118-1124.
Hubbard SJ, Thornton JM. NACCESS [computer program]. Department of Biochemistry and Molecular Biology, University College, London; 1993.
McDonald I, Thornton J. Satisfying hydrogen bonding potential in proteins. J Mol Biol 1994;238:777-793.
Barlow DJ, Thornton MJ. Ion-pairs in proteins. J Mol Biol 1983;168:867-885.
Edsall JT. The size, shape and hydration of protein molecules. In: The proteins. Chemistry, biological activity and methods. New York: Neurath & Bailey;1953. p 636.
Durchschlag H, Jaenicke R. Partial specific volume changes of proteins: densimetric studies. Biochem Biophys Res Commun 1982;108:1074-1079.
Kohlhoff M, Dahm A, Hensel R. Tetrameric triosephosphate isomerase from hyperthermophilic Archaea. FEBS Lett 1996;383: 245-250.
Bell GS, Russell RJM, Kohlhoff M, et al. Preliminary crystallographic studies of triosephosphate isomerase (TIM) from the hyperthermophilic Archaeon Pyrococcus woesei. Acta Crystallogr 1998;D54:1419-1421.
Das G, Hickey DR, McLendon D, McLendon G, Sherman F. Dramatic thermostabilisation of yeast iso-1-cytochrome c by an asparagine => isoleucine replacement at position 57. Proc Nat. Acad Sci USA 1989;86:496-499.
Van den Burg B, Vriend G, Veltman OR, Venema G, Eijsink VGH. Engineering an enzyme to resist boiling. Biochemistry 1998;95: 2056-2060.
Usher KC, de la Cruz AFA, Dahlquist FW, Swanson RV, Simon MI, Remington SJ. Crystal structures of CheY from Thermotoga maritima do not support conventional explanations for the structural basis of enhanced thermostability. Protein Sci 1998;7:403-412.
Böhm G, Jaenicke R. Relevance of sequence statistics for the properties of extremophilic proteins. Int J Pept Protein Res 1994;43:97-106.
Matthews BW, Nicholson H, Becktel WJ. Enhanced thermostability from site-directed mutations that decrease the entropy of unfolding. Proc Natl Acad Sci USA 1987;84:6663-6667.
Russell RJM, Taylor GL. Engineering thermostability: lessons from thermophilic proteins. Curr Opin Biotech 1995;9:370-374.
Petukhov L, Kil Y, Kuramitsu S, Lanzov V. Insights into thermal resistance of proteins from intrinsic stability of their α-helices. Proteins 1997;29:309-320.
Facchiano AM, Colonna G, Ragone R. Helix stabilizing factors and stabilization of thermophilic proteins: an X-ray based study. Protein Eng 1998;11:753-760.
Nicholson H, Becktel W, Matthews BW. Enhanced protein thermostability from designed mutations that interact with α-helix dipoles. Nature 1988;336:651-656.
Serrano L, Fersht AR. Capping and α-helix stability. Nature 1989;342:296-299.
Lee B, Vasmatzis G. Stabilization of protein structures. Curr Opin Struct Biol 1997;8:423-428.
Dill KA. Dominant forces in protein folding. Biochemistry 1990;29: 7133-7155.
Eisenberg D, McLachlan AD. Solvation energy in protein folding and binding. Nature 1986;319:199-203.
Xie D, Freire E. Molecular basis of cooperativity in protein folding. Thermodynamic and structural conditions for the stabilization of compact denatured states. Proteins 1994;19:291-301.
Dahiyat BI, Mayo SL. Protein design automation. Protein Sci 1996;5:895-903.
Backmann J, Schäfer G, Wyns L, Bönisch H. Thermodynamics and kinetics of unfolding of the trimeric adenylate kinase from the archeon Sulfolobus acidocaldarius. J Mol Biol 1998;284:817-833.
Tanner JT, Hecht RM, Krause KL. Determinants of enzyme thermostability observed in the molecular structure of Thermus aquatus D-glyceraldehyde-3-phosphate dehydrogenase at 2.5Å resolution. Biochemistry 1996;35:2597-2609.
Perutz MF, Raidt H. Stereochemical basis of heat stability in bacterial ferredoxins and in haemoglobin A2. Nature 1975;255: 256-259.
Goldman A. How to make my blood boil. Structure 1995;3:1277-1279.
Yip KSP, Stillman TJ, Britton KL, et al. The structure of Pyrococcus furiosus glutamate dehydrogenase reveals a key role for ion-pair networks in maintaining enzyme stability at extreme temperatures. Structure 1995;3:1147-1158.
Vetriani C, Maeder DL, Tolliday N, et al. Protein thermostability above 100°C: a key role for ionic interactions. Proc Natl Acad Sci USA 1998;95:12300-12305.
Nakashima H, Nishikwa K, Ooi T. The folding type of a protein is relevant to the amino acid composition. J Biochem 1986;99:153-162.