Geometric Attributes of Retaining Glycosyltransferase Enzymes Favor an Orthogonal Mechanism

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Schuman, Brock ^a   Evans, Stephen V ^a   Fyles, Thomas M ^a  

^a UNIVERSITY OF VICTORIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOSYLTRANSFERASE; NUCLEOPHILE;

ARTICLE; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME KINETICS; ENZYME MECHANISM; ENZYME STABILITY; ENZYME SUBSTRATE; MASS SPECTROMETRY; NUCLEAR MAGNETIC RESONANCE; STEREOCHEMISTRY; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

CATALYTIC DOMAIN; GLYCOSYLTRANSFERASES; MODELS, MOLECULAR; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84881007618     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071077     Document Type: Article

References (66)

1. Pastores GM, Elstein D, Hrebicek M, Zimran A, (2007) Effect of miglustat on bone disease in adults with type 1 Gaucher disease: a pooled analysis of three multinational, open-label studies. Clin Ther 29: 1645-1654.
2. Yoshida A, Kobayashi K, Manya H, Taniguchi K, Kano H, et al. (2001) Muscular dystrophy and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1. Dev Cell 1: 717-724.
3. Wennekes T, van den Berg RJ, Donker W, van der Marel GA, Strijland A, et al. (2007) Development of adamantan-1-yl-methoxy-functionalized 1-deoxynojirimycin derivatives as selective inhibitors of glucosylceramide metabolism in man. J Org Chem 72: 1088-1097.
4. Ma B, Simala-Grant JL, Taylor DE, (2006) Fucosylation in prokaryotes and eukaryotes. Glycobiology 16: 158R-184R.
5. Umesiri FE, Sanki AK, Boucau J, Ronning DR, Sucheck SJ, (2010) Recent advances toward the inhibition of mAG and LAM synthesis in Mycobacterium tuberculosis. Med Res Rev 30: 290-326.
6. Mas E, Pasqualini E, Caillol N, El Battari A, Crotte C, et al. (1998) Fucosyltransferase activities in human pancreatic tissue: comparative study between cancer tissues and established tumoral cell lines. Glycobiology 8: 605-613.
7. Mulichak AM, Losey HC, Walsh CT, Garavito RM, (2001) Structure of the UDP-Glucosyltransferase GtfB that modifies the heptapeptide aglycone in the biosynthesis of vancomycin group antibiotics. Structure 9: 547-557.
8. Raetz CRH, Whitfield C, (2002) Lipopolysaccharide endotoxins. Annual Review of Biochemistry 71: 635-700.
9. Harrington PR, Lindesmith L, Yount B, Moe CL, Baric RS, (2002) Binding of Norwalk virus-like particles to ABH histo-blood group antigens is blocked by antisera from infected human volunteers or experimentally vaccinated mice. J Virol 76: 12335-12343.
10. Wong SM, St Michael F, Cox A, Ram S, Akerley BJ, (2011) ArcA-Regulated Glycosyltransferase Lic2B Promotes Complement Evasion and Pathogenesis of Nontypeable Haemophilus influenzae. Infect Immun 79: 1971-1983.
11. Freiberger F, Claus H, Günzel A, Oltmann-Norden I, Vionnet J, et al. (2007) Biochemical characterization of a Neisseria meningitidis polysialyltransferase reveals novel functional motifs in bacterial sialyltransferases. Molecular Microbiology 65: 1258-1275.
12. Byrne GW, Stalboerger PG, Du Z, Davis TR, McGregor CG, (2011) Identification of new carbohydrate and membrane protein antigens in cardiac xenotransplantation. Transplantation 91: 287-292.
13. Weil R, 3rd, Nozawa M, Chernack W, McIntosh R, Reemtsma K (1973) Effect of Concanavalin A on rat heart allografts. Surg Forum 24: 194-196.
14. Hakomori S, (1996) Tumor malignancy defined by aberrant glycosylation and sphingo(glyco)lipid metabolism. Cancer Res 56: 5309-5318.
15. Gschaidmeier H, Seidel A, Burchell B, Bock KW, (1995) Formation of mono- and diglucuronides and other glycosides of benzo(a)pyrene-3,6-quinol by V79 cell-expressed human phenol UDP-glucuronosyltransferases of the UGT1 gene complex. Biochem Pharmacol 49: 1601-1606.
16. Yamamoto H, Kaneko Y, Rebbaa A, Bremer EG, Moskal JR, (1997) alpha 2,6-sialyltransferase gene transfection into a human glioma cell line (U373 MG) results in decreased invasivity. Journal of Neurochemistry 68: 2566-2576.
17. Werther JL, Rivera-MacMurray S, Bruckner H, Tatematsu M, Itzkowitz SH, (1994) Mucin-associated sialosyl-Tn antigen expression in gastric cancer correlates with an adverse outcome. Br J Cancer 69: 613-616.
18. Ravindranath MH, Tsuchida T, Morton DL, Irie RF, (1991) Ganglioside Gm3-Gd3 Ratio as an Index for the Management of Melanoma. Cancer 67: 3029-3035.
19. Mathieu S, Gerolami R, Luis J, Carmona S, Kol O, et al. (2007) Introducing alpha(1,2)-linked fucose into hepatocarcinoma cells inhibits vasculogenesis and tumor growth. International Journal of Cancer 121: 1680-1689.
20. Marionneau S, Le Moullac-Vaidye B, Le Pendu J, (2002) Expression of histo-blood group A antigen increases resistance to apoptosis and facilitates escape from immune control of rat colon carcinoma cells. Glycobiology 12: 851-856.
21. Itzkowitz SH, Dahiya R, Byrd JC, Kim YS, (1990) Blood group antigen synthesis and degradation in normal and cancerous colonic tissues. Gastroenterology 99: 431-442.
22. Buzzi S, Buzzi L, (1974) Cancer immunity after treatment of Ehrlich tumor with diphtheria toxin. Cancer Res 34: 3481-3486.
23. Kapitonov D, Yu RK, (1999) Conserved domains of glycosyltransferases. Glycobiology 9: 961-978.
24. Chelsky D, Parsons SM, (1975) Stereochemical course of the adenosine triphosphate phosphoribosyltransferase reaction in histidine biosynthesis. J Biol Chem 250: 5669-5673.
25. Soya N, Fang Y, Palcic MM, Klassen J, (2011) Trapping and characterization of covalent intermediates of mutant retaining glycosyltransferases. Glycobiology 21: 547-552.
26. Lairson LL, Chiu CPC, Ly HD, He SM, Wakarchuk WW, et al. (2004) Intermediate trapping on a mutant retaining alpha-galactosyltransferase identifies an unexpected aspartate residue. Journal of Biological Chemistry 279: 28339-28344.
27. Martinez-Fleites C, Proctor M, Roberts S, Bolam DN, Gilbert HJ, et al. (2006) Insights into the synthesis of lipopolysaccharide and antibiotics through the structures of two retaining glycosyltransferases from family GT4. Chemistry & Biology 13: 1143-1152.
28. Gibson RP, Turkenburg JP, Charnock SJ, Lloyd R, Davies GJ, (2002) Insights into trehalose synthesis provided by the structure of the retaining glucosyltransferase OtsA. Chem Biol 9: 1337-1346.
29. Pedersen LC, Dong J, Taniguchi F, Kitagawa H, Krahn JM, et al. (2003) Crystal structure of an alpha 1,4-N-acetylhexosaminyltransferase (EXTL2), a member of the exostosin gene family involved in heparan sulfate biosynthesis. Journal of Biological Chemistry 278: 14420-14428.
30. Lobsanov YD, Romero PA, Sleno B, Yu BM, Yip P, et al. (2004) Structure of Kre2p/Mnt1p- A yeast alpha 1,2-mannosyltransferase involved in mannoprotein biosynthesis. Journal of Biological Chemistry 279: 17921-17931.
31. Sommer N, Depping R, Piotrowski M, Ruger W, (2004) Bacteriophage T4 alpha-glucosyltransferase: a novel interaction with gp45 and aspects of the catalytic mechanism. Biochemical and Biophysical Research Communications 323: 809-815.
32. Reinert DJ, Jank T, Aktories K, Schulz GE, (2005) Structural basis for the function of Clostridium difficile toxin B. Journal of Molecular Biology. 351: 973-981.
33. Flint J, Taylor E, Yang M, Bolam DN, Tailford LE, et al. (2005) Structural dissection and high-throughput screening of mannosylglycerate synthase. Nat Struct Mol Biol 12: 608-614.
34. Nagano N, Noguchi T, Akiyama Y, (2007) Systematic comparison of catalytic mechanisms of hydrolysis and transfer reactions classified in the EzCatDB database. Proteins: Structure, Function, and Bioinformatics 66: 147-159.
35. Sinnott ML, Jencks WP, (1980) Solvolysis of D-Glucopyranosyl Derivatives in Mixtures of Ethanol and 2,2,2-Trifluoroethanol. Journal of the American Chemical Society 102: 2026-2032.
36. Lee SS, Hong SY, Errey JC, Izumi A, Davies GJ, et al. (2011) Mechanistic evidence for a front-side, S(N)i-type reaction in a retaining glycosyltransferase. Nat Chem Biol 7: 631-638.
37. Chan J, Tang A, Bennet AJ, (2011) A Stepwise Solvent-Promoted SNi Reaction of α-d-Glucopyranosyl Fluoride: Mechanistic Implications for Retaining Glycosyltransferases. Journal of the American Chemical Society 134: 1212-1220.
38. Gomez H, Polyak I, Thiel W, Lluch JM, Masgrau L, (2012) Retaining Glycosyltransferase Mechanism Studied by QM/MM Methods: Lipopolysaccharyl-alpha-1,4-galactosyltransferase C Transfers alpha-Galactose via an Oxocarbenium Ion-like Transition State. Journal of the American Chemical Society 134: 4743-4752.
39. Lairson LL, Henrissat B, Davies GJ, Withers SG, (2008) Glycosyltransferases: Structures, functions, and mechanisms. Annual Review of Biochemistry 77: 521-555.
40. Katritzky AR, Brycki BE, (1990) The mechanisms of nucleophilic substitution in aliphatic compounds. Chemical Society Reviews 19: 83-105.
41. Bourne Y, Henrissat B, (2001) Glycoside hydrolases and glycosyltransferases: families and functional modules. Curr Opin Struct Biol 11: 593-600.
42. Coutinho PM, Deleury E, Davies GJ, Henrissat B, (2003) An evolving hierarchical family classification for glycosyltransferases. J Mol Biol 328: 307-317.
43. Tumbale P, Brew K, (2009) Characterization of a metal-independent CAZy family 6 glycosyltransferase from Bacteroides ovatus. J Biol Chem 284: 25126-25134.
44. Schuman B, Fisher SZ, Kovalevsky A, Borisova SN, Palcic MM, et al. (2011) Preliminary joint neutron time-of-flight and X-ray crystallographic study of human ABO(H) blood group A glycosyltransferase. Acta Crystallographica Section F 67: 258-262.
45. Evans SV (1993) SETOR: hardware-lighted three-dimensional solid model representations of macromolecules. J Mol Graph 11: 134-138, 127-138.
46. Alfaro JA, Zheng RB, Persson M, Letts JA, Polakowski R, et al. (2008) ABO(H) blood group A and B glycosyltransferases recognize substrate via specific conformational changes. J Biol Chem 283: 10097-10108.
47. Ramakrishnan B, Boeggeman E, Qasba PK, (2004) Effect of the Met344His mutation on the conformational dynamics of bovine beta-1,4-galactosyltransferase: crystal structure of the Met344His mutant in complex with chitobiose. Biochemistry 43: 12513-12522.
48. Persson K, Ly HD, Dieckelmann M, Wakarchuk WW, Withers SG, et al. (2001) Crystal structure of the retaining galactosyltransferase LgtC from Neisseria meningitidis in complex with donor and acceptor sugar analogs. Nat Struct Biol 8: 166-175.
49. Kakuda S, Shiba T, Ishiguro M, Tagawa H, Oka S, et al. (2004) Structural basis for acceptor substrate recognition of a human glucuronyltransferase, GlcAT-P, an enzyme critical in the biosynthesis of the carbohydrate epitope HNK-1. J Biol Chem 279: 22693-22703.
50. Pedersen LC, Darden TA, Negishi M, (2002) Crystal structure of beta 1,3-glucuronyltransferase I in complex with active donor substrate UDP-GlcUA. J Biol Chem 277: 21869-21873.
51. Schuman B, Persson M, Landry RC, Polakowski R, Weadge JT, et al. (2010) Cysteine-to-serine mutants dramatically reorder the active site of human ABO(H) blood group B glycosyltransferase without affecting activity: structural insights into cooperative substrate binding. J Mol Biol 402: 399-411.
52. Felder CE, Prilusky J, Silman I, Sussman JL, (2007) A server and database for dipole moments of proteins. Nucleic Acids Research 35: W512-W521.
53. Grote RF, Hynes JT, (1980) The stable states picture of chemical reactions. II. Rate constants for condensed and gas phase reaction models. The Journal of Chemical Physics 73: 2715-2732.
54. Gertner BJ, Wilson KR, Zichi DA, Lee S, Hynes JT, (1988) Non-equilibrium solvation in SN1 and SN2 reactions in polar solvents. Faraday Discussions of the Chemical Society 85: 297-308.
55. Kim HJ, Hynes JT, (1990) Role of solvent electronic polarization in electron-transfer processes. The Journal of Physical Chemistry 94: 2736-2740.
56. Adlercreutz D, Yoshimura Y, Mannerstedt K, Wakarchuk WW, Bennett EP, et al. (2012) Thiogalactopyranosides are Resistant to Hydrolysis by α-Galactosidases. ChemBioChem 13: 1673-1679.
57. Schramm VL, Shi W, (2001) Atomic motion in enzymatic reaction coordinates. Current Opinion in Structural Biology 11: 657-665.
58. Errey JC, Lee SS, Gibson RP, Martinez Fleites C, Barry CS, et al. (2010) Mechanistic insight into enzymatic glycosyl transfer with retention of configuration through analysis of glycomimetic inhibitors. Angew Chem Int Ed Engl 49: 1234-1237.
59. André I, Tvaroska I, Carver JP, (2003) On the reaction pathways and determination of transition-state structures for retaining [alpha]-galactosyltransferases. Carbohydrate Research 338: 865-877.
60. Sindhuwinata N, Munoz E, Munoz FJ, Palcic MM, Peters H, et al. (2010) Binding of an acceptor substrate analog enhances the enzymatic activity of human blood group B galactosyltransferase. Glycobiology 20: 718-723.
61. Cheng J, Huang S, Yu H, Li Y, Lau K, et al. (2010) Trans-sialidase activity of Photobacterium damsela alpha2,6-sialyltransferase and its application in the synthesis of sialosides. Glycobiology 20: 260-268.
62. Vetting MW, Frantom PA, Blanchard JS, (2008) Structural and enzymatic analysis of MshA from Corynebacterium glutamicum: substrate-assisted catalysis. J Biol Chem 283: 15834-15844.
63. Howard S, He S, Withers SG, (1998) Identification of the active site nucleophile in jack bean alpha-mannosidase using 5-fluoro-beta-L-gulosyl fluoride. J Biol Chem 273: 2067-2072.
64. Numao S, Kuntz DA, Withers SG, Rose DR, (2003) Insights into the mechanism of Drosophila melanogaster Golgi alpha-mannosidase II through the structural analysis of covalent reaction intermediates. Journal of Biological Chemistry 278: 48074-48083.
65. Di Marco VB, Bombi GG, (2006) Electrospray mass spectrometry (ESI-MS) in the study of metal-ligand solution equilibria. Mass Spectrom Rev 25: 347-379.
66. Guthrie RD, Jencks WP, (1989) IUPAC recommendations for the representation of reaction mechanisms. Accounts of Chemical Research 22: 343-349.