The reaction mechanism of type I phosphomannose isomerases: New information from inhibition and polarizable molecular mechanics studies

Proteins: Structure, Function and Bioinformatics

Volumn 79, Issue 1, 2011, Pages 203-220

  Roux, Céline ^a   Bhatt, Forum ^b   Foret, Johanna ^a   De Courcy, Benoit ^c,d   Gresh, Nohad ^d   Piquemal, Jean Philip ^c   Jeffery, Constance J ^b   Salmon, Laurent ^a  

^a UNIVERSITÉ PARIS SUD   (France)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c LABORATOIRE DE CHIMIE THÉORIQUE   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Aldose ketose isomerase; Competitive inhibitor; Computational studies; Hydroxamic acid; Metalloenzyme

Indexed keywords

MANNOSE 6 PHOSPHATE; MANNOSE PHOSPHATE ISOMERASE; MANNOSE PHOSPHATE ISOMERASE 1; UNCLASSIFIED DRUG;

AB INITIO CALCULATION; ARTICLE; CANDIDA ALBICANS; CATALYSIS; CONTROLLED STUDY; ENERGY; ENZYME INHIBITION; ENZYME MECHANISM; ESCHERICHIA COLI; ISOMERIZATION; MOLECULAR MECHANICS; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTON TRANSPORT;

AMINO ACID SEQUENCE; BINDING, COMPETITIVE; CANDIDA ALBICANS; CATALYTIC DOMAIN; ESCHERICHIA COLI; FRUCTOSEPHOSPHATES; HUMANS; HYDRAZINES; HYDROXAMIC ACIDS; KINETICS; MANNOSE-6-PHOSPHATE ISOMERASE; MANNOSEPHOSPHATES; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; SUGAR PHOSPHATES;

CANDIDA ALBICANS; ESCHERICHIA COLI; PSEUDOMONAS AERUGINOSA;

EID: 78649761495     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22873     Document Type: Article

References (83)

1. Jensen SO, Reeves PR. Domain organisation in phosphomannose isomerase (types I and II). Biochem Biophys Acta 1998; 1382: 5-7.
2. Malaisse-Lagae F, Liemans V, Yaylali B, Sener A, Malaisse WJ. Phosphoglucoisomerase-catalysed interconversion of hexose phosphates; comparison with phosphomannoisomerase. Biochim Biophys Acta 1989; 998: 118-125.
3. Rose IA, O'Connell EL, Schray KJ. Mannose 6-phosphate: anomeric form used by phosphomannose isomerase and its 1-epimerization by phosphoglucose isomerase. J Biol Chem 1973; 248: 2232-2234.
4. Proudfoot AEI, Turcatti G, Wells TNC, Payton MA, Smith DJ. Purification, cDNA cloning and heterologous expression of human phosphomannose isomerase. Eur J Biochem 1994; 219: 415-423.
5. Swan MK, Hansen T, Schönheit P, Davies C. A novel phosphoglucose/phosphomannose isomerase from Pyrobaculum aerophilum is a member of the PGI superfamily: structural evidence at 1.16 Å resolution. J Biol Chem 2004; 279: 39838-39845.
6. Swan MK, Hansen T, Schönheit P, Davies C. Structural basis for phosphomannose isomerase activity in phosphoglucose isomerase from Pyrobaculum aerophilum: a subtle difference between distantly related enzymes. Biochemistry 2004; 43: 14088-14095.
7. Gracy RW, Noltmann EA. Studies on phosphomannose isomerase I. Isolation, homogeneity measurements, and determination of some physical properties. J Biol Chem 1968; 243: 3161-3168.
8. Proudfoot AEI, Payton MA, Wells TNC. Purification and characterization of fungal and mammalian phosphomannose isomerases. J Protein Chem 1994; 13: 619-627.
9. Wells TNC, Payton MA, Proudfoot AEI. Phosphomannose isomerase from Saccharomyces cerevisiae contains two inhibitory metal ion binding site. Biochemistry 1993; 32: 1294-1301.
10. Pitkänen J, Törmä A, Alff S, Huopaniemi SPM, Renkonen R. Excess mannose limits the growth of phosphomannose isomerase PMI40 deletion strain of Saccharomyces cerevisiae. J Biol Chem 2004; 279: 55737-55743.
11. Coulin F, Magnenat E, Proudfoot AEI, Payton MA, Scully P, Wells TNC. Identification of Cys-150 in the active site of phosphomannose isomerase from Candida albicans. Biochemistry 1993; 32: 14139-14144.
12. Cleasby A, Wonacott A, Skarzynski T, Hubbard RE, Davies GJ, Proudfoot AEI, Bernard AR, Payton MA, Wells TNC. The X-ray crystal structure of phosphomannose isomerase from Candida albicans at 1.7 Å resolution. Nat Struct Biol 1996; 3: 470-479.
13. Wells TNC, Scully P, Magnenat E. Arginine 304 is an active site residue in phosphomannose isomerase from Candida albicans. Biochemistry 1994; 33: 5777-5782.
14. Smith JJ, Thomson AJ, Proudfoot AEI, Wells TNC. Identification of an Fe(III)-dihydroxyphenylalanine site in recombinant phosphomannose isomerase from Candida albicans. Eur J Biochem 1997; 244: 325-333.
15. Miles JS, Guest JR. Nucleotide sequence and transcriptional start point of the phosphomannose isomerase gene (manA) of Escherichia coli. Gene 1991; 32: 41-48.
16. Sagurthi SR, Gowda G, Savithri HS, Murthy MRN. Structures of mannose-6-phosphate isomerase from Salmonella typhimurium bound to metal atoms and substrate: implications for catalytic mechanism. Acta Crystallogr Sect D 2009; 65: 724-732.
17. Wu B, Zhang Y, Zheng R, Guo C, Wang PG. Bifunctional phosphomannose isomerase/GDP-D-mannose pyrophosphorylase is the point of control for GDP-D-mannose biosynthesis in Helicobacter pylori. FEBS Lett 2002; 519: 87-92.
18. Patterson JH, Waller RF, Jeevarajah D, Billman-Jacobe H, McConville MJ. Mannose metabolism is required for mycobacterial growth. Biochem J 2003; 372: 77-86.
19. Shinabarger D, Berry A, May TB, Rothmel R, Fialho A, Chakrabarty AM. Purification and characterization of phosphomannose isomerase-guanosine diphospho-D-mannose pyrophosphorylase. J Biol Chem 1991; 266: 2080-2088.
20. Garami A, Ilg T. The role of the phosphomannose isomerase in Leishmania mexicana glycoconjugate synthesis and virulence. J Biol Chem 2001; 276: 6566-6575.
21. Payton MA, Rheinnecker M, Klig LS, DeTiani M, Bowden E. A novel Saccharomyces cerevisiae secretory mutant possesses a thermolabile phosphomannose isomerase. J Bacteriol 1991; 173: 2006-2010.
22. Smith DJ, Proudfoot AEI, De Tiani M, Wells TNC, Payton MA. Cloning and heterologous expression of the Candida albicans gene PMI 1 encoding phosphomannose isomerase. Yeast 1995; 11: 301-310.
23. Wills EA, Roberts IS, Del Poeta M, Rivera J, Casadevall A, Cox GM, Perfect J. Identification and characterization of the Cryptococcus neoformans phosphomannose isomerase-encoding gene, MAN1, and its impact on pathogenicity. Mol Microbiol 2001; 40: 610-620.
24. Smith DJ, Payton MA. Hyphal tip extension in Aspergillus nidulans requires the manA gene, which encodes phosphomannose isomerase. Mol Cell Biol 1994; 14: 6030-6038.
25. Foret J, de Courcy B, Gresh N, Piquemal J, Salmon L. Synthesis and evaluation of non-hydrolyzable D-mannose 6-phosphate surrogates reveal 6-deoxy-6-dicarboxymethyl-D-mannose as a new strong inhibitor of phosphomannose isomerases. Bioorg Med Chem 2009; 17: 7100-7107.
26. Xiao J, Guo Z, Guo Y, Chu F, Sun P. Computational study of human phosphomannose isomerase: insights from homology modeling and molecular dynamics simulation of enzyme bound substrate. J Mol Graph Model 2006; 25: 289-295.
27. Whitlow M, Howard AJ, Finzel BC, Poulos TL, Winborne E, Gilliland GL. A metal-mediated hydride shift mechanism for xylose isomerase based on the 1.6 Å Streptomyces rubiginosus with xylitol and D-xylose. Proteins 1991; 9: 153-173.
28. Allen KN, Lavie A, Farber GK, Glasfeld A, Petsko GA, Ringe D. Isotopic exchange plus substrate and inhibition kinetics of D-xylose isomerase do not support a proton-transfer mechanism. Biochemistry 1994; 33: 1481-1487.
29. Allen KN, Lavie A, Glasfeld A, Tanada TN, Gerrity DP, Carlson SC, Farber GK, Petsko GA, Ringe D. Role of the divalent metal ion in sugar binding, ring opening, and isomerization by D-xylose isomerase: replacement of a catalytic metal by an amino acid. Biochemistry 1994; 33: 1488-1494.
30. Allen KN, Lavie A, Petsko GA, Ringe D. Design, synthesis and characterization of a potent xylose isomerase inhibitor, D-threonohydroxamic acid, and high-resolution X-ray crystallographic structure of the enzyme-inhibitor complex. Biochemistry 1995; 34: 3742-3749.
31. Fenn TD, Ringe D, Petsko GA. Xylose isomerase in substrate and inhibitor michaelis states: atomic resolution studies of a metal-mediated hydride shift. Biochemistry 2004; 43: 6464-6474.
32. Korndörfer IP, Fessner WD, Matthews BW. The structure of rhamnose isomerase from Escherichia coli and its relation with xylose isomerase illustrates a change between inter and intra-subunit complementation during evolution. J Mol Biol 2000; 300: 917-933.
33. Davenport RC, Bash PA, Seaton BA, Karplus M, Petsko GA, Ringe D. Structure of the triosephosphate isomerase-phosphoglycolohydroxamate complex: an analogue of the intermediate on the reaction pathway. Biochemistry 1991; 30: 5821-5826.
34. Rose I, O'Connell E. Intramolecular hydrogen transfer in the phosphoglucose isomerase. J Biol Chem 1961; 236: 3086-3092.
35. Topper YJ. On the mechanism of action of phosphoglucose isomerase and phosphomannose isomerase. J Biol Chem 1957; 225: 419-425.
36. Gracy RW, Noltmann EA. Studies on phosphomannose isomerase. III. A mechanism for catalysis and for the role of zinc in the enzymatic and the nonenzymatic isomerization. J Biol Chem 1968; 243: 5410-5419.
37. Gracy R, Noltmann E. Studies on phosphomannose isomerase. II. Characterization as a zinc metalloenzyme. J Biol Chem 1968; 243: 4109-4116.
38. Noltmann EA. Aldose-ketose isomerases. In: Boyer PD, editor. The enzymes, Vol. 3. New York: Academic Press; 1972. pp 271-354.
39. Bentley R. Configurational and conformational aspects of carbohydrate biochemistry. Annu Rev Biochem 1972; 41: 953-996.
40. Berrisford JM, Hounslow AM, Akerboom J, Hagen WR, Brouns SJJ, van der Oost J, Murray IA, Blackburn GM, Waltho JP, Rice DW, Baker PJ. Evidence supporting a cis-enediol-based mechanism for Pyrococcus furiosus phosphoglucose isomerase. J Mol Biol 2006; 358: 1353-1366.
41. Kim Y, Lezondra L, Joachimiak A. Crystal structure analysis of the mannose-6-phosphate isomerase from Bacillus subtilis, DOI: 10.2210/pdb1qwr/pdb 2004.
42. Patskovsky Y, Ramagopal U, Toro R, Sauder JM, Iizuka M, Dickey M, Maletic M, Wasserman SR, Koss J, Burley SK, Almo SC. Crystal structure of mannose-6-phosphate isomerase from Helicobacter pylori, DOI: 10.2210/pdb2qh5/pdb 2007.
43. Cuff ME, Skarina T, Edwards A, Savchenko A, Joachimiak A. The structure of a putative mannosephosphate isomerase from Archaeoglobus fulgidus, DOI: 10.2210/pdb1zx5/pdb 2005.
44. Roux C, Gresh N, Perera LE, Piquemal J, Salmon L. 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. J Comput Chem 2007; 28: 938-957.
45. Roux C, Lee JH, Jeffery CJ, Salmon L. Inhibition of type I and type II phosphomannose isomerases by the reaction intermediate analogue 5-phospho-D-arabinonohydroxamic acid supports a catalytic role for the metal cofactor. Biochemistry 2004; 43: 2926-2934.
46. Gresh N, Cisneros GA, Darden TA, Piquemal J. Anisotropic, polarizable molecular mechanics studies of inter- and intramolecular interactions and ligand-macromolecule complexes. A bottom-up strategy. J Chem Theory Comput 2007; 3: 1960-1986.
47. Gresh N, Roques B. Thermolysin-inhibitor binding: effect of the His231 Ala mutation on the relative affinities of thiolate versus phosphoramidate inhibitors-a model theoretical investigation incorporating a continuum reaction field hydration model. Biopolymers 1997; 41: 145-164.
48. Garmer DR, Gresh N, Roques B. Modeling of inhibitor-metalloenzyme interactions and selectivity using molecular mechanics grounded in quantum chemistry. Proteins 1998; 31: 42-60.
49. Antony J, Gresh N, Olsen L, Hemmingsen L, Schofield C, Bauer R. Binding of D- and L-captopril inhibitors to metallo-beta-lactamase studied by polarizable molecular mechanics and quantum mechanics. J Comput Chem 2002; 23: 1281-1296.
50. Antony J, Piquemal J, Gresh N. Complexes of thiomandelate and captopril mercaptocarboxylate inhibitors to metallo-lactamase by polarizable molecular mechanics. Validation on model binding sites by quantum chemistry. J Comput Chem 2005; 26: 1131-1147.
51. Gresh N, Shi GB. Conformation-dependent intermolecular interaction energies of the triphosphate anion with divalent metal cations. Application to the ATP-binding site of a binuclear bacterial enzyme. A parallel quantum chemical and polarizable molecular mechanics investigation. J Comput Chem 2004; 25: 160-168.
52. 2+ with guanine, adenine, and the guanine-cytosine and adenine-thymine base pairs. Structures and energies characterized by polarizable molecular mechanics and ab initio calculations. J Phys Chem B 1999; 103: 11415-11427.
53. Gresh N, Derreumaux P. Generating conformations for two zinc-binding sites of HIV-1 nucleocapsid protein from random conformations by a hierarchical procedure and polarizable force field. J Phys Chem B 2003; 107: 4862-4870.
54. Gresh N, Sponer JE, Spacková N, Leszczynski J, Sponer J. Theoretical study of binding of hydrated Zn(II) and Mg(II) cations to 5'-guanosine monophosphate. Toward polarizable molecular mechanics for DNA and RNA. J Phys Chem B 2003; 107: 8669-8681.
55. Gresh N, Piquemal J, Krauss M. Representation of Zn(II) complexes in polarizable molecular mechanics. Further refinements of the electrostatic and short-range contributions. Comparisons with parallel ab initio computations. J Comput Chem 2005; 26: 1113-1130.
56. de Courcy B, Pedersen LG, Parisel O, Gresh N, Silvi B, Pilmé J, Piquemal J. Understanding selectivity of hard and soft metal cations within biological systems using the subvalence concept. 1. Application to blood coagulation: direct cation-protein electronic effects versus indirect interactions through water networks. J Chem Theory Comput 2010; 6: 1048-1063.
57. de Courcy B, Piquemal J, Garbay C, Gresh N. Polarizable water molecules in ligand-macromolecule recognition. Impact on the relative affinities of competing pyrrolopyrimidine inhibitors for FAK kinase. J Am Chem Soc 2010; 132: 3312-3320.
58. Hardré R, Salmon L. Competitive inhibitors of yeast phosphoglucose isomerase: synthesis and evaluation of new types of phosphorylated sugars from the synthon D-arabinonolactone-5-phosphate. Carbohydr Res 1999; 318: 110-115.
59. Chirgwin JM, Noltmann EA. The enediolate analogue 5-phosphoarabinonate as a mechanistic probe for phosphoglucose isomerase. J Biol Chem 1975; 250: 7272-7276.
60. Hardré R, Bonnette C, Salmon L, Gaudemer A. Synthesis and evaluation of a new inhibitor of phosphoglucose isomerase: the enediolate analogue 5-phospho-D-arabinohydroxamate. Bioorg Med Chem Lett 1998; 8: 3435-3438.
61. Salmon L, Prost E, Merienne C, Hardré R, Morgant G. A convenient synthesis of aldonohydroxamic acids in water and crystal structure of L-erythronohydroxamic acid. Carbohydr Res 2001; 335: 195-204.
62. Van Schaftingen E, Jaeken J. Phosphomannomutase deficiency is a cause of carbohydrate-deficient glycoprotein syndrome type I. FEBS Lett 1995; 377: 318-320.
63. Noltmann EA. Phosphoglucose isomerase: rabbit muscle (crystalline). Methods Enzymol 1966; 9: 557-565.
64. Piquemal J, Gresh N, Giessner-Prettre C. Improved formulas for the calculation of the electrostatic contribution to the intermolecular interaction energy from multipolar expansion of the electronic distribution. J Phys Chem A 2003; 107: 10353-10359.
65. Piquemal J, Chelli R, Procacci P, Gresh N. Key role of the polarization anisotropy of water in modeling classical polarizable force fields. J Phys Chem A 2007; 111: 8170-8176.
66. Piquemal J, Chevreau H, Gresh N. Toward a separate reproduction of the contributions to the Hartree-Fock and DFT intermolecular interaction energies by polarizable molecular mechanics with the SIBFA potential. J Chem Theory Comput 2007; 3: 824-837.
67. Claverie P, Daudey JP, Langlet J, Pullman B, Piazzola D, Huron MJ. Studies of solvent effects. 1. Discrete, continuum, and discrete-continuum models and their comparison for some simple cases: ammonium(1+) ion, methanol, and substituted ammonium(1+) ion. J Phys Chem 1978; 82: 405-418.
68. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994; 22: 4673-4680.
69. Combet C, Blanchet C, Geourjon C, Deléage G. NPS@: network protein sequence analysis. Trends Biochem Sci 2000; 25: 147-150.
70. Gouet P, Robert X, Courcelle E. ESPript/ENDscript: extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic Acids Res 2003; 31: 3320-3323.
71. Accelrys. DS visualizer. San Diego, USA: Accelrys Software Inc.; 2005.
72. Persistence of Vision Raytracer. Persistence of Vision Raytracer, Version 3.62. Williamstown, Victoria, Australia: Persistence of Vision Pty Ltd.; 2004.
73. GIMP. GNU image manipulation program, Version 2.6. The GIMP Team; Boston, MA, 2001.
74. Jenkins LMM, Hara T, Durell SR, Hayashi R, Inman JK, Piquemal J, Gresh N, Appella E. Specificity of acyl transfer from 2-mercaptobenzamide thioesters to the HIV-1 nucleocapsid protein. J Am Chem Soc 2007; 129: 11067-11078.
75. Cantor SM, Peniston QP. The reduction of aldoses at the dropping mercury cathode: estimation of the aldehydo structure in aqueous solutions. J Am Chem Soc 1940; 62: 2113-2121.
76. Lee JH, Chang KZ, Patel V, Jeffery CJ. Crystal structure of rabbit phosphoglucose isomerase complexed with its substrate D-fructose 6-phosphate. Biochemistry 2001; 40: 7799-7805.
77. Solomons JTG, Zimmerly EM, Burns S, Krishnamurthy N, Swan MK, Krings S, Muirhead H, Chirgwin J, Davies C. The crystal structure of mouse phosphoglucose isomerase at 1.6 Å resolution and its complex with glucose 6-phosphate reveals the catalytic mechanism of sugar ring opening. J Mol Biol 2004; 342: 847-860.
78. Lee JH, Jeffery CJ. 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. Protein Sci 2005; 14: 727-734.
79. Roos AK, Burgos E, Ericsson DJ, Salmon L, Mowbray SL. Competitive inhibitors of Mycobacterium tuberculosis ribose-5-phosphate isomerase B reveal new information about the reaction mechanism. J Biol Chem 2005; 280: 6416-6422.
80. Maple J, Dinur U, Hagler AT. Derivation of force field for molecular mechanics and dynamics from ab initio energy surfaces. Proc Natl Acad Sci USA 1988; 85: 5350-5354.
81. a values. Proteins 2005; 61: 704-721.
82. a values for protein-ligand complexes. Proteins 2008; 73: 765-783.
83. Advanced Chemistry Development Labs. ACD/Chemsketch, Version 12.01. Toronto, Canada: Advanced Chemistry Development Labs, Inc.; 2009.