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

Volumn 43, Issue 10, 2004, Pages 2926-2934

  Roux, Céline ^a   Lee, Ji Hyun ^b   Jeffery, Constance J ^b   Salmon, Laurent ^a  

^a UNIVERSITÉ PARIS SUD   (France)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYST ACTIVITY; ENZYME INHIBITION; ISOMERIZATION; MICROORGANISMS; PROTEINS;

THREAPEUTICS;

BIOCHEMISTRY;

5 PHOSPHOARABINOATE; 5 PHOSPHOARABINOHYDROXAMIC ACID; ENZYME INHIBITOR; GLUCOSE 6 PHOSPHATE ISOMERASE; HYDROXAMIC ACID DERIVATIVE; ISOMERASE; KETOSE; MANNOSE PHOSPHATE ISOMERASE; MANNOSE PHOSPHATE ISOMERASE INHIBITOR; METAL DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM; CATALYSIS; COMPETITIVE INHIBITION; CRYSTALLOGRAPHY; DRUG DESIGN; DRUG TARGETING; ENZYME INHIBITION; ISOMERIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PSEUDOMONAS AERUGINOSA; REACTION ANALYSIS; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; SPECIES DIFFERENCE; STRUCTURE ACTIVITY RELATION; YEAST;

BACTERIAL PROTEINS; BINDING, COMPETITIVE; CATALYSIS; COENZYMES; ENZYME INHIBITORS; FRUCTOSEPHOSPHATES; GLUCOSE-6-PHOSPHATE ISOMERASE; HYDROXAMIC ACIDS; ISOMERISM; KINETICS; MANNOSE-6-PHOSPHATE ISOMERASE; MANNOSEPHOSPHATES; METALS; MODELS, CHEMICAL; PSEUDOMONAS AERUGINOSA; SACCHAROMYCES CEREVISIAE PROTEINS; SUGAR PHOSPHATES;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; PAA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; SACCHAROMYCES CEREVISIAE;

EID: 1542327648     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi035688h     Document Type: Article

References (53)

1. Slein, B. W. (1950) Phosphomannose isomerase, J. Biol. Chem. 186, 753-761.
2. 13C EXSY NMR, Mol. Cell. Biochem. 115, 137-142.
3. Rose, I. A., O'Connell, E. L., and Schray, K. J. (1973) Mannose 6-phosphate: anomeric form used by phosphomannose isomerase and its 1-epimerization by phosphoglucose isomerase, J. Biol. Chem. 248, 2232-2234.
4. Schray, K. J., Waud, J. M., and Ehrhardt Howell, E. (1978) Phosphomannose isomerase: isomefization of the predicted β-D-fructose 6-phosphate, Arch. Biochem. Biophys. 189, 106-108.
5. Payton, M. A., Rheinnecker, M., Klig, L. S., DeTiani, M., and Bowden, E. (1991) A novel Saccharomyces cerevisiae secretory mutant possesses a thermolabile phosphomannose isomerase, J. Bacteriol. 173, 2006-2010.
6. Smith, D. J., Proudfoot, A. E. I., De Tiani, M., Wells, T. N. C., and Payton, M. A. (1995) Cloning and heterologous expression of the Candida albicans gene PM1 1 encoding phosphomannose isomerase, Yeast 11, 301-310.
7. Patterson, J. H., Waller, R. F., Jeevarajah, D., Billman-Jacobe, H., and McConville, M. J. (2003) Mannose metabolism is required for mycobacterial growth, Biochem. J. 372, 77-86.
8. Garami, A., and Ilg, T. (2001) The role of the phosphomannose isomerase in Leishmania mexicana glycoconjugate synthesis and virulence, J. Biol. Chem. 276, 6566-6575.
9. Shinabarger, D., Berry, A., May, T. B., Rothmel, R., Fialho, A., and Chakrabarty, A. M. (1991) Purification and characterization of phosphomannose isomerase-guanosine diphospho-D-mannose pyrophosphorylase, J. Biol. Chem. 266, 2080-2088.
10. Panneerselvam, K., Etchison, J. R., and Freeze, H. H. (1997) Human fibroplasts prefers mannose over glucose as a source of mannose for N-glycosylation, J. Biol. Chem. 272, 23123-23129.
11. De Koning, T. J., Dorland, L., Van Diggelen, O. P., Boonman, A. M. C., De Jong, G. J., Van Noort, W. L., De Schryver, J., Duran, M., Van den Berg, I. E. T., Gerwig, G. J., Berger, R., and Poll-The, B. T. (1998) A novel disorder of N-glycosylation due to phosphomannose isomerase deficiency, Biochem. Biophys. Res. Commun. 245, 38-42.
12. Jaeken, J., Matthijs, G., Saudubray, J. M., Dionisi-Vici, C., Bertini, E., De Lonlay, P., Henri, H., Carchon, H., Schollen, E., and Van Schaftingen, E. (1998) Phosphomannose isomerase deficiency: a carbohydrate-deficient glycoprotein syndrome with hepatic-intestinal presentation, Am. J. Hum. Genet. 62, 1535-1539.
13. Hendriksz, C. J., McClean, P., Henderson, M. J., Keir, D. G., Worthington, V. C., Imtiaz, F., Schollen, E., Matthijs, G., and Winchester, B. G. (2001) Successful treatment of carbohydrate deficient glycoprotein syndrome type Ib with oral mannose, Arch. Dis. Child. 85, 339-340.
14. Proudfoot, A. E. I., Turcatti, G., Wells, T. N. C., Payton, M. A., and Smith, D. J. (1994) Purification, cDNA cloning and heterologous expression of human phosphomannose isomerase, Eur. J. Biochem. 219, 415-423.
15. Proudfoot, A. E. I., and Payton, M. A. (1994) Purification and characterization of fungal and mammalian phosphomannose isomerases, J. Protein Chem. 13, 619-627.
16. Wells, T. N. C., and Payton, M. A. (1994) Inhibition of phosphomannose isomerase by mercury ions, Biochemistry 33, 7641-7646.
17. Jensen, S. O., and Reeves, P. R. (1998) Domain organisation in phosphomannose isomerase (types I and II), Biochim. Biophys. Acta 1382, 5-7.
18. Wills, E. A., Roberts, I. S., Del Poeta, M., Rivera, J., Casadevall, A., Cox, G. M., and Perfect, J. R. (2001) Identification and characterization of the Cryptococcus neoformans phosphomannose isomerase-encoding gene, MAN1, and its impact on pathogenicity, Mol. Microbiol. 40, 610-620.
19. Gracy, R. W., and Noltman, E. A. (1968) Studies on phosphomannose isomerase I. Isolation, homogeneity measurements, and determination of some physical properties, J. Biol. Chem. 243, 3161-3168.
20. Gracy, R. W., and Noltman, E. A. (1968) Studies on phosphomannose isomerase II. Characterization as a zinc metalloenzyme, J. Biol. Chem. 243, 4109-4116.
21. Cleasby, A., Wonacott, A., Skarzynski, T., Hubbard, R. E., Davies, G. J., Proudfoot, A. E. I., Bernard, A. R., Payton, M. A., and Wells, T. N. C. (1996) The X-ray crystal structure of phosphomannose isomerase from Candida albicans at 1.7 Å resolution, Nat. Struct. Biol. 3, 470-479.
22. Papoutsopoulou, S. V., and Kyriakidis, D. A. (1997) Phosphomannose isomerase of Xanthomonas campestris: a zinc activated enzyme, Mol. Cell. Biochem. 177, 183-191.
23. Ideguchi, T., Hu, C., Kim, B. H., Nishise, H., Yamashita, J., and Kakuno, T. (1993) An open reading frame in the Rhodospirillum rubrum plasmid, pKY1, similar to algA, encoding the bifunctionnal enzyme phosphomannose isomerase-guanosine, diphospho-D-mannose pyrophosphorylase (PMI-GMP), Biochim. Biophys. Acta 1172, 329-331.
24. Griffin, A. M., Poelwijk, E. S., Morris, V. J., and Gasson, M. J. (1997) Cloning of the aceF gene encoding the phosphomannose isomerase and GDP-mannose pyrophosphorylase activities involved in acetan biosynthesis in Acetobacter xylinum, FEMS Microbiol. Lett. 154, 389-396.
25. Jiang, X. M., Neal, B., Santiago, F., Lee, S. J., Romana, L. K., and Reeves, P. R. (1991) Structure and sequence of the rfb (O antigen) gene cluster of Salmonella serovar typhimurium (strain LT2), Mol. Microbiol. 5, 695-713.
26. Collins, L. V., and Hackett, J. (1991) Sequence of the phosphomannose isomerase-encoding gene of Salmonella typhimurium, Gene 103, 135-136.
27. Wu, B., Zhang, Y., Zheng, R., Guo, C., and Wang, P. G. (2002) Bifunctional phosphomannose isomerase/GDP-D-mannose pyrophosphorylase is the point of control for GDP-D-mannose biosynthesis in Helicobacter pylori, FEBS Lett. 519, 87-92.
28. Schmidt, M., Arnold, W., Niemann, A., Kleickmann, A., and Puhler, A. (1992) The Rhizobium meliloti pmi gene encodes a new type of phosphomannose isomerase, Gene 122, 35-43.
29. Chirgwin, J. M., and Noltmann, E. A. (1975) The enediolate analogue 5-phosphoarabinonate as a mechanistic probe for phosphoglucose isomerase, J. Biol. Chem. 250, 7272-7276.
30. Hardré, R., Bonnette, C., Salmon, L., and Gaudemer, A. (1998) Synthesis and evaluation of a new inhibitor of phosphoglucose isomerase: the enediolate analogue 5-phospho-D-arabinohydroxamate, Bioorg. Med. Chem. Lett. 8, 3435-3438.
31. Salmon, L., Prost, E., Merienne, C., Hardré, R., and Morgant, G. (2001) A convenient synthesis of aldonhydroxamic acids in water and crystal structure of L-erythronhydroxamic acid, Carbohydr. Res. 335, 195-204.
32. Sá-Correia, I., Darzins, A., Wang, S.-K., Berry, A., and Chakrabarty, A. M. (1987) Alginate biosynthetic enzymes in mucoid and nonmucoid Pseudomonas aeruginosa: Overproduction of phosphomannose isomerase, phosphomannosemutase, and GDP-mannose pyrophosphorylase by overexpression of the phosphomannose isomerase (pmi) gene, J. Bacteriol. 169, 3224-3231.
33. Van Schaftingen, E., and Jaeken, J. (1995) Phosphomannomutase deficiency is a cause of carbohydrate-deficient glycoprotein syndrome type I, FEBS Lett. 377, 318-320.
34. Noltmann, E. A. (1966) Phosphoglucose isomerase: rabbit muscle (crystalline), Methods Enzymol. 9, 557-565.
35. Hardré, R., and Salmon, L. (1999) Competitive inhibitors of yeast phosphoglucose isomerase: synthesis and evaluation of new types of phosphorylated sugars from the synthon D-arabinonolactone-5-phosphate, Carbohydr. Res. 318, 110-115.
36. Percheron, F. (1962) Dosage colorimétrique du fructose et des fructofuranosides, C. R. Hebd. Séances Acad. Sci. 255, 2521-2522.
37. Zender, R., and Falbriard, A. (1966) Analyse colorimétrique des céto-hexoses et de l'inuline par la réaction à l'acide thiobarbiturique. Conditions de la réaction, Clin. Chim. Acta 13, 246-250.
38. Malaisse-Lagae, F., Liemans, V., Yaylali, B., Sener, A., and Malaisse, W. J. (1989) Phosphoglucoisomerase-catalysed interconversion of hexose phosphates; comparison with phosphomannoisomerase, Biochim. Biophys. Acta 998, 118-125.
39. Coulin, F., Magnenat, E., Proudfoot, A. E. I., Payton, M. A., Scully, P., and Wells, T. N. C. (1993) Identification of Cys-150 in the active site of phosphomannose isomerase from Candida albicans, Biochemistry 32, 14139-14144.
40. Wells, T. N. C., Scully, P., and Magnenat, E. (1994) Arginine 304 is an active site residue in phosphomannose isomerase from Candida albicans, Biochemistry 33, 5772-5782.
41. Rose, I. A., and O'Connell, E. L. (1960) Stereospecificity of the sugar-phosphate isomerase reactions; a uniformity, Biochim. Biophys. Acta 42, 159-160.
42. Lee, B. T., and Norman, K. M. (1984) Phosphomannose isomerase and phosphogludose isomerase in seeds of Cassia colutoides and some other legumes that synthesize galactomannan, Phytochemistry 23, 983-987.
43. Jaeken, J., Pirard, M., Adamowicz, M., Pronicka, E., and Van Schaftingen, E. (1996) Inhibition of phosphomannose isomerase by fructose 1-phosphate: an explanation for defective N-glycosylation in hereditary fructose intolerance, Pediatr. Res. 40, 764-766.
44. Hardré, R., Salmon, L., and Opperdoes, F. R. (2000) Competitive inhibition of Trypanosoma brucei phosphoglucose isomerase by D-arabinose-5-phosphate derivatives, J. Enzyme Inhib. 15, 509-115.
45. Collins, K. D. (1974) An activated intermediate analogue. The use of phosphoglycolohydroxamate as a stable analogue of a transiently occurring dihydroxyacetone phosphate-derived enolate in enzymatic catalysis, J. Biol. Chem. 249, 136-142.
46. Allen, K. N., Lavie, A., Petsko, G. A., and Ringe, D. (1995) 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 34, 3742-3749.
47. Bartlett, P. A., and Marlowe, C. K. (1983) Phosphoramidates as transition state analogue inhibitors of thermolysin, Biochemistry 22, 4618-4624.
48. Hall, D. R., Leonard, G. A., Reed, C. D., Watt, C. I., Berry, A., and Hunter, W. N. (1999) The crystal structure of Escherichia coli class II fructose-1,6-bisphosphate aldolase in complex with phosphoglycolohydroxamate reveals details of mechanism and specificity, J. Mol. Biol. 287, 383-394.
49. Garmer, D. R., Gresh, N., and Roques, B.-P. (1998) Modeling of inhibitor-metalloenzyme interactions and selectivity using molecular mechanics grounded in quantum chemistry, Proteins 31, 42-60.
50. Muri, E. M. F., Nieto, M. J., Sindelar, R. D., and Williamson, J. S. (2002) Hydroxamic acids as pharmaceutical agents, Curr. Med. Chem. 9, 1631-1653.
51. Gracy, R. W., and Noltman, E. A. (1968) 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. 243, 5410-5419.
52. Seeholzer, S. H. (1993) Phosphoglucose isomerase: A ketol isomerase with aldol C2-epimerase activity, Proc. Natl. Acad. Sci. U.S.A. 90, 1237-1241.
53. El Yazal, J., and Pang, Y.-P. (2000) Proton dissociation energies of zinc-coordinated hydroxamic acids and their relative affinities for zinc: insight into design of inhibitors of zinc-containing proteinases, J. Phys. Chem. B 104, 6499-6504.