1hox Citations

Crystal structure of rabbit phosphoglucose isomerase complexed with its substrate D-fructose 6-phosphate.

Biochemistry 40 7799-805 (2001)
Cited: 45 times
EuropePMC logo PMID: 11425306

Abstract

Phosphoglucose isomerase (PGI, EC 5.3.1.9) catalyzes the interconversion of D-glucose 6-phosphate (G6P) and D-fructose 6-phosphate (F6P) and plays important roles in glycolysis and gluconeogenesis. Biochemical characterization of the enzyme has led to a proposed multistep catalytic mechanism. First, the enzyme catalyzes ring opening to yield the open chain form of the substrate. Then isomerization proceeds via proton transfer between C2 and C1 of a cis-enediol(ate) intermediate to yield the open chain form of the product. Catalysis proceeds in both the G6P to F6P and F6P to G6P directions, so both G6P and F6P are substrates. X-ray crystal structure analysis of rabbit and bacterial PGI has previously identified the location of the enzyme active site, and a recent crystal structure of rabbit PGI identified Glu357 as a candidate functional group for transferring the proton. However, it was not clear which active site amino acid residues catalyze the ring opening step. In this paper, we report the X-ray crystal structure of rabbit PGI complexed with the cyclic form of its substrate, D-fructose 6-phosphate, at 2.1 A resolution. The location of the substrate relative to the side chains of His388 suggest that His388 promotes ring opening by protonating the ring oxygen. Glu216 helps to position His388, and a water molecule that is held in position by Lys518 and Thr214 accepts a proton from the hydroxyl group at C2. Comparison to a structure of rabbit PGI with 5PAA bound indicates that ring opening is followed by loss of the protonated water molecule and conformational changes in the substrate and the protein so that a helix containing amino acids 513-520 moves in toward the substrate to form additional hydrogen bonds with the substrate.

Articles - 1hox mentioned but not cited (4)

  1. Structural studies of phosphoglucose isomerase from Mycobacterium tuberculosis H37Rv. Anand K, Mathur D, Anant A, Garg LC. Acta Crystallogr Sect F Struct Biol Cryst Commun 66 490-497 (2010)
  2. Bdellovibrio bacteriovorus phosphoglucose isomerase structures reveal novel rigidity in the active site of a selected subset of enzymes upon substrate binding. Meek RW, Cadby IT, Lovering AL. Open Biol 11 210098 (2021)
  3. Size of the protein-protein energy funnel in crowded environment. Jenkins NW, Kundrotas PJ, Vakser IA. Front Mol Biosci 9 1031225 (2022)
  4. Structural analysis of arabinose-5-phosphate isomerase from Bacteroides fragilis and functional implications. Chiu HJ, Grant JC, Farr CL, Jaroszewski L, Knuth MW, Miller MD, Elsliger MA, Deacon AM, Godzik A, Lesley SA, Wilson IA. Acta Crystallogr D Biol Crystallogr 70 2640-2651 (2014)


Reviews citing this publication (2)

Articles citing this publication (39)

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  2. From DNA to fitness differences: sequences and structures of adaptive variants of Colias phosphoglucose isomerase (PGI). Wheat CW, Watt WB, Pollock DD, Schulte PM. Mol Biol Evol 23 499-512 (2006)
  3. Distinct metal dependence for catalytic and structural functions in the L-arabinose isomerases from the mesophilic Bacillus halodurans and the thermophilic Geobacillus stearothermophilus. Lee DW, Choe EA, Kim SB, Eom SH, Hong YH, Lee SJ, Lee HS, Lee DY, Pyun YR. Arch Biochem Biophys 434 333-343 (2005)
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  5. The crystal structure of mouse phosphoglucose isomerase at 1.6A resolution and its complex with glucose 6-phosphate reveals the catalytic mechanism of sugar ring opening. Solomons JT, Zimmerly EM, Burns S, Krishnamurthy N, Swan MK, Krings S, Muirhead H, Chirgwin J, Davies C. J Mol Biol 342 847-860 (2004)
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  8. The first crystal structure of the novel class of fructose-1,6-bisphosphatase present in thermophilic archaea. Nishimasu H, Fushinobu S, Shoun H, Wakagi T. Structure 12 949-959 (2004)
  9. Binding of 5-phospho-D-arabinonohydroxamate and 5-phospho-D-arabinonate inhibitors to zinc phosphomannose isomerase from Candida albicans studied by polarizable molecular mechanics and quantum mechanics. Roux C, Gresh N, Perera LE, Piquemal JP, Salmon L. J Comput Chem 28 938-957 (2007)
  10. Crystal structure of phosphoglucose isomerase from pig muscle and its complex with 5-phosphoarabinonate. Davies C, Muirhead H. Proteins 49 577-579 (2002)
  11. The crystal structure of glucose-6-phosphate isomerase from Leishmania mexicana reveals novel active site features. Cordeiro AT, Michels PA, Delboni LF, Thiemann OH. Eur J Biochem 271 2765-2772 (2004)
  12. Cupin-type phosphoglucose isomerases (Cupin-PGIs) constitute a novel metal-dependent PGI family representing a convergent line of PGI evolution. Hansen T, Schlichting B, Felgendreher M, Schönheit P. J Bacteriol 187 1621-1631 (2005)
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  14. Characterization of the cupin-type phosphoglucose isomerase from the hyperthermophilic archaeon Thermococcus litoralis. Jeong JJ, Fushinobu S, Ito S, Jeon BS, Shoun H, Wakagi T. FEBS Lett 535 200-204 (2003)
  15. A novel phosphoglucose isomerase (PGI)/phosphomannose isomerase from the crenarchaeon Pyrobaculum aerophilum is a member of the PGI superfamily: structural evidence at 1.16-A resolution. Swan MK, Hansen T, Schönheit P, Davies C. J Biol Chem 279 39838-39845 (2004)
  16. Species specificity of the cytokine function of phosphoglucose isomerase. Amraei M, Nabi IR. FEBS Lett 525 151-155 (2002)
  17. The structures of inhibitor complexes of Pyrococcus furiosus phosphoglucose isomerase provide insights into substrate binding and catalysis. Berrisford JM, Akerboom J, Brouns S, Sedelnikova SE, Turnbull AP, van der Oost J, Salmon L, Hardré R, Murray IA, Blackburn GM, Rice DW, Baker PJ. J Mol Biol 343 649-657 (2004)
  18. Probing the active site of the sugar isomerase domain from E. coli arabinose-5-phosphate isomerase via X-ray crystallography. Gourlay LJ, Sommaruga S, Nardini M, Sperandeo P, Dehò G, Polissi A, Bolognesi M. Protein Sci 19 2430-2439 (2010)
  19. Crystal structures of mouse autocrine motility factor in complex with carbohydrate phosphate inhibitors provide insight into structure-activity relationship of the inhibitors. Tanaka N, Haga A, Naba N, Shiraiwa K, Kusakabe Y, Hashimoto K, Funasaka T, Nagase H, Raz A, Nakamura KT. J Mol Biol 356 312-324 (2006)
  20. Evidence supporting a cis-enediol-based mechanism for Pyrococcus furiosus phosphoglucose isomerase. Berrisford JM, Hounslow AM, Akerboom J, Hagen WR, Brouns SJ, van der Oost J, Murray IA, Michael Blackburn G, Waltho JP, Rice DW, Baker PJ. J Mol Biol 358 1353-1366 (2006)
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  23. The crystal structure of rabbit phosphoglucose isomerase complexed with D-sorbitol-6-phosphate, an analog of the open chain form of D-glucose-6-phosphate. Lee JH, Jeffery CJ. Protein Sci 14 727-734 (2005)
  24. The reaction mechanism of type I phosphomannose isomerases: new information from inhibition and polarizable molecular mechanics studies. Roux C, Bhatt F, Foret J, de Courcy B, Gresh N, Piquemal JP, Jeffery CJ, Salmon L. Proteins 79 203-220 (2011)
  25. Structural analogues of reactive intermediates as inhibitors of glucosamine-6-phosphate synthase and phosphoglucose isomerase. Milewski S, Janiak A, Wojciechowski M. Arch Biochem Biophys 450 39-49 (2006)
  26. Crystal structure of Bacillus subtilis YckF: structural and functional evolution. Sanishvili R, Wu R, Kim DE, Watson JD, Collart F, Joachimiak A. J Struct Biol 148 98-109 (2004)
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  28. Crystal structure of phosphoglucose isomerase from Trypanosoma brucei complexed with glucose-6-phosphate at 1.6 A resolution. Arsenieva D, Appavu BL, Mazock GH, Jeffery CJ. Proteins 74 72-80 (2009)
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  31. Phosphoglucose Isomerase Is Important for Aspergillus fumigatus Cell Wall Biogenesis. Zhou Y, Yan K, Qin Q, Raimi OG, Du C, Wang B, Ahamefule CS, Kowalski B, Jin C, van Aalten DMF, Fang W. mBio 13 e0142622 (2022)
  32. Cloning, biochemical characterisation, tissue localisation and possible post-translational regulatory mechanism of the cytosolic phosphoglucose isomerase from developing sunflower seeds. Troncoso-Ponce MA, Rivoal J, Cejudo FJ, Dorion S, Garcés R, Martínez-Force E. Planta 232 845-859 (2010)
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  37. Cytosolic phosphoglucose isomerase is essential for microsporogenesis and embryogenesis in Arabidopsis. Liu HC, Chen HC, Huang TH, Lue WL, Chen J, Suen DF. Plant Physiol 191 177-198 (2023)
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  39. Metabolic Profiling of Sugars and Organic Acids, and Expression Analyses of Metabolism-Associated Genes in Two Yellow-Peel Pitaya Species. Xie F, Chen C, Chen J, Yuan Y, Hua Q, Zhang Z, Zhao J, Hu G, Chen J, Qin Y. Plants (Basel) 11 694 (2022)