Crystal structure of recombinant human triosephosphate isomerase at 2.8 A resolution. Triosephosphate isomerase-related human genetic disorders and comparison with the trypanosomal enzyme
Mande, S. C.; Mainfroid, V.; Kalk, K. H.et al.
1994 • In Protein Science: A Publication of the Protein Society, 3 (5), p. 810-21
[en] The crystal structure of recombinant human triosephosphate isomerase (hTIM) has been determined complexed with the transition-state analogue 2-phosphoglycolate at a resolution of 2.8 A. After refinement, the R-factor is 16.7% with good geometry. The asymmetric unit contains 1 complete dimer of 53,000 Da, with only 1 of the subunits binding the inhibitor. The so-called flexible loop, comprising residues 168-174, is in its "closed" conformation in the subunit that binds the inhibitor, and in the "open" conformation in the other subunit. The tips of the loop in these 2 conformations differ up to 7 A in position. The RMS difference between hTIM and the enzyme of Trypanosoma brucei, the causative agent of sleeping sickness, is 1.12 A for 487 C alpha positions with 53% sequence identity. Significant sequence differences between the human and parasite enzymes occur at about 13 A from the phosphate binding site. The chicken and human enzymes have an RMS difference of 0.69 A for 484 equivalent residues and about 90% sequence identity. Complementary mutations ensure a great similarity in the packing of side chains in the core of the beta-barrels of these 2 enzymes. Three point mutations in hTIM have been correlated with severe genetic disorders ranging from hemolytic disorder to neuromuscular impairment. Knowledge of the structure of the human enzyme provides insight into the probable effect of 2 of these mutations, Glu 104 to Asp and Phe 240 to Ile, on the enzyme. The third mutation reported to be responsible for a genetic disorder, Gly 122 to Arg, is however difficult to explain. This residue is far away from both catalytic centers in the dimer, as well as from the dimer interface, and seems unlikely to affect stability or activity. Inspection of the 3-dimensional structure of trypanosomal triosephosphate isomerase, which has a methionine at position 122, only increased the mystery of the effects of the Gly to Arg mutation in the human enzyme.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Mande, S. C.
Mainfroid, V.
Kalk, K. H.
Goraj, K.
Martial, Joseph ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Biologie et génétique moléculaire
Hol, W. G.
Language :
English
Title :
Crystal structure of recombinant human triosephosphate isomerase at 2.8 A resolution. Triosephosphate isomerase-related human genetic disorders and comparison with the trypanosomal enzyme
Publication date :
1994
Journal title :
Protein Science: A Publication of the Protein Society
ISSN :
0961-8368
eISSN :
1469-896X
Publisher :
Cold Spring Harbor Laboratory Press, Woodbury, United States - New York
Alber T, Banner DW, Bloomer AC, Petsko GA, Phillips DC, Rivers PS, Wilson IA (1981) On the three‐dimensional structure and catalytic mechanism of triosephosphate isomerase. Philos Trans R Soc (Lond) B 293:159-171.
Alber T, Kawasaki G. (1982) Nucleotide sequence of the triosephosphate isomerase gene of Saccharomyces cerevisiae. J Mol Appl Genet 1:419-434.
Banner DW, Bloomer AC, Petsko GA, Phillips DC, Pogson CI, Wilson IA, Corran PH, Furth AJ, Milman JD, Offord RE, Priddle JD, Waley SG (1975) Structure of chicken muscle triosephosphate isomerase determined crystallographically at 2.5 A resolution using amino acid sequence data. Nature 255:609-614.
Bash PA, Field MJ, Davenport RC, Petsko GA, Ringe D, Karplus M. (1991) Computer simulation and analysis of the reaction pathway of triosephosphate isomerase. Biochemistry 30:5826-5832.
Blacklow SC, Liu KD, Knowles JR (1991) Stepwise improvements in catalytic effectiveness: Independence and interdependence in combinations of point mutations of a sluggish triosephosphate isomerase. Biochemistry 30:8470-8476.
Bradford MM (1976) A rapid and sensitive method for the quantitation of protein‐dye binding. Anal Biochem 72:248-254.
Brándén CI (1991) The most frequently occurring folding motif in proteins The TIM barrel. Current Opinion in Structural Biology 1:978-983.
Brünger AT X‐PLOR user manual, New Haven, Connecticut, Yale University Press; 1990.
Chang ML, Artymiuk PJ, Wu X, Hollàn S, Lammi A, Maquat LE (1993) Human triosephosphate isomerase deficiency resulting from mutation of Phe 240. Am J Hum Genet 52:1260-1269.
Cheng J, Mielnicke LM, Pruitt SC, Maquat LE (1990) Nucleotide sequence of murine triosephosphate isomerase cDNA. Nucleic Acids Res 18:4261.
Corran PH, Waley SG (1975) The amino acid sequence of the rabbit muscle triosephosphate isomerase. Biochem J 145:335-344.
Crowther RA (1972) The fast rotation function. The molecular replacement method , Rossmann MG,. Int Sci Rev Ser 13., New York, Gordon & Breach; 173-178.
Crowther RA, Blow DM (1967) A method of positioning a known molecule in an unknown crystal structure. Acta Crystallographica 23:544-548.
Daar IO, Artymiuk PJ, Phillips DC, Maquat LE (1986) Human triosephosphate isomerase deficiency: A single amino acid substitution results in a thermolabile enzyme. Proc Natl Acad Sci USA 83:7903-7907.
Davenport RC, Bash PA, Seaton BA, Karplus M, Petsko GA, Ringe D. (1991) Structure of the triosephosphate isomerase‐phosphoglycolohydroxamat complex: An analogue of the intermediate on the reaction pathway. Biochemistry 30:5821-5826.
De Moerlooze L, Struman L, Renard A, Martial JA (1992) Stabilization of T7‐promoter‐based pARHS expression vectors using the par B locus. Gene 119:91-93.
Devereux J, Haeberli P, Smithies O. (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387-395.
Eber SW, Pekrun A, Bardosi A, Gahr M, Krietsch WKG, Kruger J, Matthei R, Schroter W. (1991) Triosephosphate isomerase deficiency: Haemolytic anaemia, myopathy with altered mitochondria and mental retardation due to a new variant with accelerated enzyme catabolism and diminished specific activity. Eur J Pediatr 150:761-766.
Eikmanns BJ (1992) Identification, sequence analysis and expression of a Corynebacterium glutamicum gene cluster encoding the three glycolytic enzymes, glyceraldehyde‐3‐phosphate dehydrogenase, 3‐phosphoglycerate kinase and triosephosphate isomerase. J Bacteriol 174:6076-6086.
Farber GK (1993) An α/β‐barrel full of evolutionary trouble. Curr Opin Struct Biol 3:409-412.
Fothergill‐Gilmore L, Michels P. (1993) Evolution of glycolysis. Progress in Biophysics and Molecular Biology 59:105-235.
Friedman KD, Rosen NL, Newrnan PJ, Montgomery RR (1990) Screening of γgt 11 libraries. PCR protocols: A guide to methods and applications , San Diego, Academic Press; 253-258.
Goraj K, Renard A, Martial JA (1990) Synthesis, purification and initial structural characterization of octarellin, a de novo polypeptide modelled on the α/β barrel proteins. Protein Eng 3:259-266.
Herzberg O, Moult J. (1991) Analysis of the steric strain in the polypeptide backbone of protein molecules. Proteins Struct Funct Genet 11:223-229.
Hol WGJ, van Duijnen PT, Berendsen HJC (1978) The α‐helix dipole and the properties of proteins. Nature 273:443-446.
Jones TA, Zou JY, Cowan SW (1991) Improved methods for building models in electron density maps and location of errors in these models. Acta Crystallographica Section A Foundations of Crystallography 47:110-119.
Kabsch W. (1988) Evaluation of single‐crystal diffraction data from a positionsensitive detector. Journal of Applied Crystallography 21:916-924.
Knowles JR (1991) Enzyme catalysis: Not different, just better. Nature 350:121-124.
Knowles JR, Albery WJ (1977) Perfection in enzyme catalysis: The energetics of triosephosphate isomerase. Acc Chem Res 10:105-111.
Kolb E, Harris JI, Bridgen J. (1974) Triosephosphate isomerase from the coelcanth. Biochem J 137:185-197.
Komives EA, Chang LC, Lolis E, Tilton RF, Petsko GA, Knowles JR (1991) Electrophilic catalysis in triosephosphate isomerase. The role of histidine95. Biochemistry 30:3011-3019.
Kraulis PJ (1991) MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 24:946-950.
Lesk AM, Brαndén CI, Chothia C. (1989) Structural principles of α/β proteins: The packing of the interior of the sheet. Proteins Struct Funct Genet 5:139-148.
Lolis E, Alber T, Davenport RC, Rose D, Hartman FC, Petsko GA (1990) Structure of yeast triosephosphate isomerase at 1.9 Å resolution. Biochemistry 29:6609-6618.
Lolis E, Petsko GA (1990) Crystallographic analysis of the complex between triosephosphate isomerase and 2‐phosphoglycolate at 2.5 A resolution: Implications for catalysis. Biochemistry 29:6619-6625.
Lu HS, Yuan PM, Gracy RW (1984) Primary structure of human triosephosphate isomerase. J Biol Chem 259:11958-11968.
Mainfroid V, Goraj K, Rentier‐Delrue F, Houbrechts A, Loiseau A, Gohimont AC, Noble MEM, Borchert TV, Wierenga RK, Martial JA (1993) Replacing the (βα)‐unit 8 of E. coli TIM with its chicken homologue leads to a stable and active hybrid enzyme. Protein Eng 6:393-900.
Mande SC, Suguna K. (1989) Fast algorithm for macromolecular packing calculation. Journal of Applied Crystallography 22:627-629.
Maquat LE, Chilcote R, Ryan PM (1985) Human triosephosphate isomerase cDNA and protein structure: Studies of triosephosphate isomerase deficiency in man. J Biol Chem 260:3748-3753.
Marchionni M, Gilbert W. (1986) The triosephosphate isomerase gene from maize: Introns antedate the plant animal divergence. Cell 46:133-141.
Matthews BW (1968) Solvent content of protein crystals. J Mol Biol 33:491-497.
Matthews BW (1993) Structural and genetic analysis of protein stability. Annu Rev Biochem 62:139-160.
McKnight GL, O'Hara PJ, Parker ML (1986) Nucleotide sequence of the triosephosphate isomerase gene from Aspergillus nidulans: Implications for a difference loss of introns. Cell 46:143-147.
Messerschmidt A, Pflugrath J. (1987) Crystal orientation and X‐ray pattern prediction routines for area detector diffractometer systems in macromolecular crystallography. J Appl Crystallogr 20:436-439.
et O, Opperdoes FR (1984) Simultaneous purification of hexokinase, class‐I fructose‐bisphosphate aldolase, triosephosphate isomerase and phosphoglycerate kinase from Trypanosoma brucei. Eur J Biochem 144:475-483.
Noble MEM, Wierenga RK, Lambeir AM, Opperdoes FR, Thunnissen AM, Kalk KH, Groendijk H, Hol WGJ (1991) The adaptability of the active site of trypanosomal triosephosphate isomerase as observed in the crystal structures of three different complexes. Proteins Struct Funct Genet 10:50-69.
Noble MEM, Zeelen JP, Wierenga RK (1993) Structures of the “open” and “closed” states of trypanosomal triosephosphate isomerase, as observed in a new crystal form: Implications for the reaction mechanism. Proteins Struct Funct Genet 16:311-326.
Noble MEM, Zeelen JP, Wierenga RK, Mainfroid V, Goraj K, Gohimont AC, Martial JA (1993) Structure of triosephosphate isomerase from Escherichia coli determined at 2.6 Å resolution. Acta Crystallographica Section D Biological Crystallography 49:403-417.
Okada N, Koizumi N, Tanaka T, Ohkubo H, Nakanishi S, Yamada Y. (1989) Isolation, sequence and bacterial expression of a cDNA for (s)‐tetrahydroberberine oxidase from cultured berberine‐producing Coptis japonica cells. Proc Natl Acad Sci USA 86:534-538.
Old SE, Mohrenweiser HW (1988) Nucleotide sequence of the triosephosphate isomerase gene from Macaca mulatta. Nucleic Acids Res 16:9055.
Perry BA, Mohrenweiser HW (1992) Human triosephosphate isomerase: Substitution of Arg for Gly at position 122 in a thermolabile electromorph variant, TPI‐Manchester. Hum Genet 88:634-638.
Pichersky E, Gottlieb LD, Hess JF (1984) Nucleotide sequence of the triosephosphate isomerase gene of Escherichia coli. Mol Gen Genet 195:314-320.
Ramachandran GN, Sasisekharan V. (1968) Conformation of polypeptides and proteins. Adv Protein Chem 23:283-438.
Read RJ (1986) Improved Fourier coefficients for maps using phases from partial structures with errors. Acta Crystallographica Section A Foundations of Crystallography 42:140-149.
Rentier‐Delrue F, Mande SC, Moyens S, Mainfroid V, Goraj K, Lion M, Hol WGJ, Martial JA (1993) Cloning and overexpression of the triosephosphate isomerase genes from psychrophilic and thermophilic bacteria. Journal of Molecular Biology 229:85-93.
Richardson JS, Richardson DC (1988) Amino acid preferences for specific locations at the ends of α‐helices. Science 240:1648-1652.
Russell PR (1985) Transcription of the triosephosphate isomerase gene of Schizosaccharomyces pombe initiates from a start point different from that in Saccharomyces cerevisiae. Gene 40:125-130.
Shaw‐Lee RL, Lissemore JL, Sullivan DT (1991) Structure and expression of the triosephosphate isomerase gene of Drosophila melanogaster. MGG Molecular & General Genetics 230:225-229.
Straus D, Gilbert W. (1985) Chicken triosephosphate isomerase complements an Escherichia coli deficiency. Proc Natl Acad Sci USA 82:2014-2018.
Studier FW, Moffatt BA (1986) Use of bacteriophage T7 RNA polymerase to direct selective high‐level expression of cloned genes. J Mol Biol 189:113-130.
Swinkels BW, Gibson WC, Osinga KA, Kramer R, Veeneman GH, van Boom JH, Borst P. (1986) Characterization of the gene for microbody (glycosomal) triosephosphate isomerase of Trypanosoma brucei. EMBO J 5:1291-1298.
Tittiger C, Whyard S, Walker VK (1993) A novel intron site in the triosephosphate isomerase gene from the mosquito Culex tarsalis. Nature 361:470-472.
Urfer R, Kirschner K. (1992) The importance of surface loops for stabilizing an eightfold βα protein. Protein Sci 1:31-45.
Verlinde, Noble MEM, Kalk KH, Groendijk H, Wierenga RK, Hol WGJ (1991) Anion binding at the active site of trypanosomal triosephosphate isomerase. Monohydrogen phosphate does not mimic sulphate. Eur J Biochem 198:53-57.
Verlinde CLMJ, Rudenko G, Hol WGJ (1992) In search of new lead compounds for trypanosomiasis drug design: A protein structure‐based linkedfragment approach. J Comput Aided Mol Design 6:131-147.
Verlinde CLMJ, Witmans CJ, Pijning T, Kalk K, Hol WGJ, Callens M, Opperdoes FR (1992) Structure of the complex between trypanosomal triosephosphate isomerase and N‐hydroxy‐4‐phosphono‐butanamide: Binding at the active site despite an “open” flexible loop conformation. Protein Sci 1:1578-1584.
Eleventh program report, tropical disease research, Geneva, World Health Organization; 1992.
Wierenga RK, Noble MEM, Davenport RC (1992) Comparison of the refined crystal structures of liganded and unliganded chicken, yeast and trypanosomal triosephosphate isomerase. J Mol Biol 224:1115-1126.
Wierenga RK, Noble MEM, Postma JPM, Groendijk H, Kalk KH, Hol WGJ, Opperdoes FR (1991) The crystal structure of the “open” and the “closed” conformation of the flexible loop of trypanosomal triosephosphate isomerase. Proteins Struct Funct Genet 10:33-49.
Wierenga RK, Noble MEM, Vriend G, Nauche S, Hol WGJ (1991) Refined 1.83 Å structure of trypanosomal triosephosphate isomerase crystallized in the presence of 2.4 M‐ammonium sulphate. A comparison with the structure of the trypanosomal triosephosphate isomerase‐glycerol‐3‐phosphate complex. J Mol Biol 220:995-1015.
Wolfenden R. (1969) Transition state analogues for enzyme catalysis. Nature 233:704-705.