Structure and mechanism of human UDP-xylose synthase: Evidence for a promoting role of sugar ring distortion in a three-step catalytic conversion of UDP-glucuronic acid

Journal of Biological Chemistry

Volumn 287, Issue 37, 2012, Pages 31349-31358

  Eixelsberger, Thomas ^a   Sykora, Sabine ^a   Egger, Sigrid ^a,b,c   Brunsteiner, Michael ^a,d   Kavanagh, Kathryn L ^b   Oppermann, Udo ^b   Brecker, Lothar ^e   Nidetzky, Bernd ^a,c,d  

^a GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c AUSTRIAN CENTRE OF INDUSTRIAL BIOTECHNOLOGY   (Austria)

^d RESEARCH CENTER PHARMACEUTICAL ENGINEERING GMBH   (Austria)

^e UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

AXIAL POSITIONS; CARBOXYLATE GROUPS; CATALYTIC CONVERSION; CATALYTIC SITES; CELL SIGNALING; CHAIR CONFORMATIONS; ENOLATES; ENZYMATIC REACTION; EXTRACELLULAR MATRICES; GLYCOSAMINOGLYCANS; KETO GROUPS; MOLECULAR DYNAMICS SIMULATIONS; PROMOTING ROLE; PROTEIN CORE; PROTEOGLYCANS; PROTON DONORS; PROTONATED; REACTIVE SUBSTRATES; SIDE-CHAINS; STRONG INTERFERENCE; SUGAR RING DISTORTION; SYNTHASES; UDP-GLUCURONIC ACID;

BIOSYNTHESIS; CARBOXYLATION; CATALYSIS; GLUCOSE; MOLECULAR DYNAMICS; OLEFINS; PROTONATION;

REACTION INTERMEDIATES;

ARGININE; EPIMERASE; GLUTAMIC ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE; OXIDOREDUCTASE; SUGAR; TYROSINE; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE; URIDINE DIPHOSPHATE 4 KETO DEXTRO GLUCURONIC ACID; URIDINE DIPHOSPHATE 4 KETO PENTOSE; URIDINE DIPHOSPHATE GLUCURONIC ACID; URIDINE DIPHOSPHATE XYLOSE; URIDINE DIPHOSPHATE XYLOSE SYNTHASE;

ARTICLE; CARBOHYDRATE ANALYSIS; CARBOHYDRATE METABOLISM; CATALYSIS; CHEMICAL MODIFICATION; CHEMICAL REACTION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DECARBOXYLATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME BINDING; ENZYME MECHANISM; ENZYME STRUCTURE; HUMAN; HYDROGENATION; MOLECULAR DYNAMICS; OXIDATION; PHYLOGENY; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTON TRANSPORT; SEQUENCE ALIGNMENT; STRUCTURE ANALYSIS;

CARBOXY-LYASES; CATALYSIS; CRYSTALLOGRAPHY, X-RAY; HUMANS; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP; URIDINE DIPHOSPHATE GLUCURONIC ACID;

MAMMALIA;

EID: 84866118842     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.386706     Document Type: Article

References (49)

1. Theocharis, A. D., Skandalis, S. S., Tzanakakis, G. N., and Karamanos, N. K. (2010) Proteoglycans in health and disease. Novel roles for proteoglycans in malignancy and their pharmacological targeting. FEBS J. 277, 3904-3923
2. Bernfield, M., Götte, M., Park, P. W., Reizes, O., Fitzgerald, M. L., Lincecum, J., and Zako, M. (1999) Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68, 729-777
3. Bishop, J. R., Schuksz, M., and Esko, J. D. (2007) Heparan sulfate proteoglycans fine-tune mammalian physiology. Nature 446, 1030-1037
4. Iozzo, R. V. (1998) Matrix proteoglycans. From molecular design to cellular function. Annu. Rev. Biochem. 67, 609-652
5. Lander, A. D., and Selleck, S. B. (2000) The elusive functions of proteoglycans. In vivo veritas. J. Cell Biol. 148, 227-232
6. Schaefer, L., and Schaefer, R. M. (2010) Proteoglycans. From structural compounds to signaling molecules. Cell Tissue Res. 339, 237-246
7. Prydz, K., and Dalen, K. T. (2000) Synthesis and sorting of proteoglycans. Commentary. J. Cell Sci. 113, 193-205
8. Kearns, A. E., Vertel, B. M., and Schwartz, N. B. (1993) Topography of glycosylation and UDP-xylose production. J. Biol. Chem. 268, 11097-11104
9. Moriarity, J. L., Hurt, K. J., Resnick, A. C., Storm, P. B., Laroy, W., Schnaar, R. L., and Snyder, S. H. (2002) UDP-glucuronate decarboxylase, a key enzyme in proteoglycan synthesis. Cloning, characterization, and localization. J. Biol. Chem. 277, 16968-16975
10. Eames, B. F., Singer, A., Smith, G. A., Wood, Z. A., Yan, Y. L., He, X., Polizzi, S. J., Catchen, J. M., Rodriguez-Mari, A., Linbo, T., Raible, D. W., and Postlethwait, J. H. (2010) UDP xylose synthase 1 is required for morphogenesis and histogenesis of the craniofacial skeleton. Dev. Biol. 341, 400-415
11. Bar-Peled, M., and O'Neill, M. A. (2011) Plant nucleotide sugar formation, interconversion, and salvage by sugar recycling. Annu. Rev. Plant Biol. 62, 127-155
12. Bar-Peled, M., Griffith, C. L., and Doering, T. L. (2001) Functional cloning and characterization of a UDP-glucuronic acid decarboxylase. The pathogenic fungus Cryptococcus neoformans elucidates UDP-xylose synthesis. Proc. Natl. Acad. Sci. U.S.A. 98, 12003-12008
13. Coyne, M. J., Fletcher, C. M., Reinap, B., and Comstock, L. E. (2011) UDP-glucuronic acid decarboxylases of Bacteroides fragilis and their prevalence in bacteria. J. Bacteriol. 193, 5252-5259
14. Gu, X., Lee, S. G., and Bar-Peled, M. (2011) Biosynthesis of UDP-xylose and UDP-arabinose in Sinorhizobium meliloti 1021. First characterization of a bacterial UDP-xylose synthase, and UDP-xylose 4-epimerase. Microbiology 157, 260-269
15. Rosenberger, A. F., Hangelmann, L., Hofinger, A., and Wilson, I. B. (2012) UDP-xylose and UDP-galactose synthesis in Trichomonas vaginalis. Mol. Biochem. Parasitol. 181, 53-56
16. Schutzbach, J. S., and Feingold, D. S. (1970) Biosynthesis of uridine diphosphate D-xylose IV. Mechanism of action of uridine diphosphoglucuronate carboxylyase. J. Biol. Chem. 245, 2476-2482
17. Gu, X., Glushka, J., Yin, Y., Xu, Y., Denny, T., Smith, J., Jiang, Y., and Bar-Peled, M. (2010) Identification of a bifunctional UDP-4-keto-pentose/ UDP-xylose synthase in the plant pathogenic bacterium Ralstonia solanacearum strain GMI1000, a distinct member of the 4,6-dehydratase and decarboxylase family. J. Biol. Chem. 285, 9030-9040
18. He, X. M., and Liu, H. W. (2002) Formation of unusual sugars. Mechanistic studies and biosynthetic applications. Annu. Rev. Biochem. 71, 701-754
19. Tanner, M. E. (2008) Transient oxidation as a mechanistic strategy in enzymatic catalysis. Curr. Opin. Chem. Biol. 12, 532-538
20. Kavanagh, K. L., Jörnvall, H., Persson, B., and Oppermann, U. (2008) The SDR superfamily. Functional and structural diversity within a family of metabolic and regulatory enzymes. Cell Mol. Life Sci. 65, 3895-3906
21. Frey, P. A. (1996) The Leloir pathway. A mechanistic imperative for three enzymes to change the stereochemical configuration of a single carbon in galactose. FASEB J. 10, 461-470
22. Thibodeaux, C. J., Melançon, C. E., and Liu, H. W. (2007) Unusual sugar biosynthesis and natural product glycodiversification. Nature 446, 1008-1016
23. Collaborative Computational Project (1994) The CCP4 Suite. Programs for protein crystallography. Acta Crystallogr. Sect. D Biol. Crystallogr. 50, 760-763
24. Sheldrick, G. M., and Schneider, T. R. (1997) SHELXL. High-resolution refinement. Methods Enzymol. 277, 319-343
25. Emsley, P., and Cowtan, K. (2004) COOT. Model-building tools for molecular graphics. Acta Crystallogr. Sect. D Biol. Crystallogr. 60, 2126-2132
26. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. Sect. D Biol. Crystallogr. 53, 240-255
27. Hess, B., Kutzner, C., van der Spoel, D., and Lindahl, E. (2008) GROMACS 4. Algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 4, 435-447
28. Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., and Simmerling, C. (2006) Comparison of multiple amber force fields and development of improved protein backbone parameters. Proteins 65, 712-725
29. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926
30. Wang, J., Wolf, R. M., Caldwell, J. W., Kollman, P. A., and Case, D. A. (2004) Development and testing of a general amber force field. J. Comput. Chem. 25, 1157-1174
31. Wang, J., Wang, W., Kollman, P. A., and Case, D. A. (2006) Automatic atom-type and bond-type perception in molecular mechanical calculations. J. Mol. Graph. Model. 25, 247-260
32. Mobley, D. L., Chodera, J. D., and Dill, K. A. (2006) On the use of orientational restraints and symmetry corrections in alchemical free energy calculations. J. Chem. Phys. 125, 084902
33. a predictions. J. Chem. Theory Comput. 7, 525-537
34. Hoover, W. G. (1985) Canonical dynamics. Equilibrium phase-space distributions. Phys. Rev. A 31, 1695-1697
35. Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., and Pedersen, L. G. (1995) A smooth particle mesh Ewald potential. J. Chem. Phys. 103, 8577-8592
36. Berendsen, H. J. C., Postma, J. P. M., Van Gunsteren, W. F., DiNola, A., and Haak, J. R. (1984) Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684
37. Hess, B., Bekker, H., Berendsen, H. J., and Fraaije, J. G. (1997) LINCS. A linear constraint solver for molecular simulations. J. Comput. Chem. 18, 1463-1472
38. 2O. J. Inorg. Biochem. 98, 161-166
39. Krissinel, E., and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797
40. Filling, C., Berndt, K. D., Benach, J., Knapp, S., Prozorovski, T., Nordling, E., Ladenstein, R., Jörnvall, H., and Oppermann, U. (2002) Critical residues for structure and catalysis in short-chain dehydrogenases/reductases. J. Biol. Chem. 277, 25677-25684
41. Gatzeva-Topalova, P. Z., May, A. P., and Sousa, M. C. (2004) Crystal structure of Escherichia coli ArnA (PmrI) decarboxylase domain.Akey enzyme for lipid a modification with 4-amino-4-deoxy-L-arabinose and polymyxin resistance. Biochemistry 43, 13370-13379
42. Gatzeva-Topalova, P. Z., May, A. P., and Sousa, M. C. (2005) Structure and mechanism of ArnA. Conformational change implies ordered dehydrogenase mechanism in key enzyme for polymyxin resistance. Structure 13, 929-942
43. Williams, G. J., Breazeale, S. D., Raetz, C. R., and Naismith, J. H. (2005) Structure and function of both domains of ArnA, a dual function decarboxylase and a formyltransferase, involved in 4-amino-4-deoxy-L-arabinose biosynthesis. J. Biol. Chem. 280, 23000-23008
44. Mikhailov, D., Mayo, K. H., Vlahov, I. R., Toida, T., Pervin, A., and Linhardt, R. J. (1996) NMR solution conformation of heparin-derived tetrasaccharide. Biochem. J. 318, 93-102
45. O skew-boat conformation in L-iduronic acid. Angew. Chem. Int. Ed. 50, 11637-11639
46. Pan, Y., Kee, C. W., Jiang, Z., Ma, T., Zhao, Y., Yang, Y., Xue, H., and Tan, C. H. (2011) Expanding the utility of bronsted base catalysis. Biomimetic enantioselective decarboxylative reactions. Chem. Eur. J. 17, 8363-8370
47. Broach, B., Gu, X., and Bar-Peled, M. (2012) Biosynthesis of UDP-glucuronic acid and UDP-galacturonic acid in Bacillus cereus subsp. cytotoxis NVH 391-98. FEBS J. 279, 100-112
48. Choi, S. H., Ruszczycky, M. W., Zhang, H., and Liu, H. W. (2011) A fluoro analogue of UDP-α-D-glucuronic acid is an inhibitor of UDP-α-D-apiose/UDP-α-D-xylose synthase. Chem. Commun. 47, 10130-10132
49. Gebb, C., Baron, D., and Grisebach, H. (1975) Spectroscopic evidence for formation of a 4-keto intermediate in UDP-apiose UDP-xylose synthase reaction. Eur. J. Biochem. 54, 493-498