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High resolution crystal structures of T4 phage beta-glucosyltransferase: induced fit and effect of substrate and metal binding.

Moréra S, Larivière L, Kurzeck J, Aschke-Sonnenborn U, Freemont PS, Janin J, Rüger W
J Mol Biol 311 569-77 (2001)
Related entries: 1jej, 1jg7, 1jiu, 1jiv, 1jix

Cited: 43 times
EuropePMC logo PMID: 11493010

Abstract

beta-Glucosyltransferase (BGT) is a DNA-modifying enzyme encoded by bacteriophage T4 that transfers glucose from uridine diphosphoglucose to 5-hydroxymethyl cytosine bases of phage T4 DNA. We report six X-ray structures of the substrate-free and the UDP-bound enzyme. Four also contain metal ions which activate the enzyme, including Mg(2+) in forms 1 and 2 and Mn(2+) or Ca(2+). The substrate-free BGT structure differs by a domain movement from one previously determined in another space group. Further domain movements are seen in the complex with UDP and the four UDP-metal complexes. Mg(2+), Mn(2+) and Ca(2+) bind near the beta-phosphate of the nucleotide, but they occupy slightly different positions and have different ligands depending on the metal and the crystal form. Whilst the metal site observed in these complexes with the product UDP is not compatible with a role in activating glucose transfer, it approximates the position of the positive charge in the oxocarbonium ion thought to form on the glucose moiety of the substrate during catalysis.

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Reviews citing this publication (8)

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  6. The crystal structure of human UDP-glucuronosyltransferase 2B7 C-terminal end is the first mammalian UGT target to be revealed: the significance for human UGTs from both the 1A and 2B families. Radominska-Pandya A, Bratton SM, Redinbo MR, Miley MJ. Drug Metab Rev 42 133-144 (2010)
  7. Monotopic Membrane Proteins Join the Fold. Allen KN, Entova S, Ray LC, Imperiali B. Trends Biochem Sci 44 7-20 (2019)
  8. Glycogen synthase: towards a minimum catalytic unit? Cid E, Geremia RA, Guinovart JJ, Ferrer JC. FEBS Lett 528 5-11 (2002)

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  7. Mutations in POGLUT1, encoding protein O-glucosyltransferase 1, cause autosomal-dominant Dowling-Degos disease. Basmanav FB, Oprisoreanu AM, Pasternack SM, Thiele H, Fritz G, Wenzel J, Größer L, Wehner M, Wolf S, Fagerberg C, Bygum A, Altmüller J, Rütten A, Parmentier L, El Shabrawi-Caelen L, Hafner C, Nürnberg P, Kruse R, Schoch S, Hanneken S, Betz RC. Am J Hum Genet 94 135-143 (2014)
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  9. Structure of the Escherichia coli heptosyltransferase WaaC: binary complexes with ADP and ADP-2-deoxy-2-fluoro heptose. Grizot S, Salem M, Vongsouthi V, Durand L, Moreau F, Dohi H, Vincent S, Escaich S, Ducruix A. J Mol Biol 363 383-394 (2006)
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  12. The highly conserved domain of unknown function 1792 has a distinct glycosyltransferase fold. Zhang H, Zhu F, Yang T, Ding L, Zhou M, Li J, Haslam SM, Dell A, Erlandsen H, Wu H. Nat Commun 5 4339 (2014)
  13. Crystal structures of the T4 phage beta-glucosyltransferase and the D100A mutant in complex with UDP-glucose: glucose binding and identification of the catalytic base for a direct displacement mechanism. Larivière L, Gueguen-Chaignon V, Moréra S. J Mol Biol 330 1077-1086 (2003)
  14. Biochemical characterization of recombinant β-glucosyltransferase and analysis of global 5-hydroxymethylcytosine in unique genomes. Terragni J, Bitinaite J, Zheng Y, Pradhan S. Biochemistry 51 1009-1019 (2012)
  15. Substrate-induced conformational changes in the essential peripheral membrane-associated mannosyltransferase PimA from mycobacteria: implications for catalysis. Guerin ME, Schaeffer F, Chaffotte A, Gest P, Giganti D, Korduláková J, van der Woerd M, Jackson M, Alzari PM. J Biol Chem 284 21613-21625 (2009)
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  17. Biochemical Characterization of a Recombinant UDP-glucosyltransferase from Rice and Enzymatic Production of Deoxynivalenol-3-O-β-D-glucoside. Michlmayr H, Malachová A, Varga E, Kleinová J, Lemmens M, Newmister S, Rayment I, Berthiller F, Adam G. Toxins (Basel) 7 2685-2700 (2015)
  18. Structure and mechanism of GumK, a membrane-associated glucuronosyltransferase. Barreras M, Salinas SR, Abdian PL, Kampel MA, Ielpi L. J Biol Chem 283 25027-25035 (2008)
  19. Modulation of amylose content by structure-based modification of OsGBSS1 activity in rice (Oryza sativa L.). Liu D, Wang W, Cai X. Plant Biotechnol J 12 1297-1307 (2014)
  20. The role of tryptophan 314 in the conformational changes of beta1,4-galactosyltransferase-I. Ramasamy V, Ramakrishnan B, Boeggeman E, Qasba PK. J Mol Biol 331 1065-1076 (2003)
  21. A base-flipping mechanism for the T4 phage beta-glucosyltransferase and identification of a transition-state analog. Larivière L, Moréra S. J Mol Biol 324 483-490 (2002)
  22. Thermodynamics of binding of divalent magnesium and manganese to uridine phosphates: implications for diabetes-related hypomagnesaemia and carbohydrate biocatalysis. Zea CJ, Camci-Unal G, Pohl NL. Chem Cent J 2 15 (2008)
  23. Inhibition of fucosyltransferase VII by gallic acid and its derivatives. Niu X, Fan X, Sun J, Ting P, Narula S, Lundell D. Arch Biochem Biophys 425 51-57 (2004)
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  26. Structural characterization of O- and C-glycosylating variants of the landomycin glycosyltransferase LanGT2. Tam HK, Härle J, Gerhardt S, Rohr J, Wang G, Thorson JS, Bigot A, Lutterbeck M, Seiche W, Breit B, Bechthold A, Einsle O. Angew Chem Int Ed Engl 54 2811-2815 (2015)
  27. Fluorescent analogs of UDP-glucose and their use in characterizing substrate binding by toxin A from Clostridium difficile. Bhattacharyya S, Kerzmann A, Feig AL. Eur J Biochem 269 3425-3432 (2002)
  28. Structural and functional analysis of validoxylamine A 7'-phosphate synthase ValL involved in validamycin A biosynthesis. Zheng L, Zhou X, Zhang H, Ji X, Li L, Huang L, Bai L, Zhang H. PLoS One 7 e32033 (2012)
  29. 3PFDB--a database of best representative PSSM profiles (BRPs) of protein families generated using a novel data mining approach. Shameer K, Nagarajan P, Gaurav K, Sowdhamini R. BioData Min 2 8 (2009)
  30. Two Novel Fungal Phenolic UDP Glycosyltransferases from Absidia coerulea and Rhizopus japonicus. Xie K, Dou X, Chen R, Chen D, Fang C, Xiao Z, Dai J. Appl Environ Microbiol 83 e03103-16 (2017)
  31. Unusual sugar nucleotide recognition elements of mesophilic vs. thermophilic glycogen synthases. Zea CJ, Pohl NL. Biopolymers 79 106-113 (2005)
  32. Facile enzymatic synthesis of base J-containing oligodeoxyribonucleotides and an analysis of the impact of base J on DNA replication in cells. Ji D, Wang Y. PLoS One 9 e103335 (2014)


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