Structural and biochemical evidence for a boat-like transition state in β-mannosidases

Nature Chemical Biology

Volumn 4, Issue 5, 2008, Pages 306-312

  Tailford, Louise E ^a   Offen, Wendy A ^b   Smith, Nicola L ^a   Dumon, Claire ^a   Morland, Carl ^a   Gratien, Julie ^c   Heck, Marie Pierre ^c   Stick, Robert V ^d   Blériot, Yves ^e   Vasella, Andrea ^f   Gilbert, Harry J ^a   Davies, Gideon J ^b  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

^c DIF   (France)

^d UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^e SORBONNE UNIVERSITÉ   (France)

^f ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BETA MANNOSIDASE; ENZYME INHIBITOR; IMIDAZOLE DERIVATIVE; POLYCYCLIC AROMATIC HYDROCARBON DERIVATIVE;

ARTICLE; BACTEROIDES THETAIOTAOMICRON; CORRELATION ANALYSIS; CRYSTAL STRUCTURE; ENERGY; ENZYME CONFORMATION; ENZYME INHIBITION; ENZYME STRUCTURE; HYDROLYSIS; MOLECULAR MIMICRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING;

BACTEROIDES THETAIOTAOMICRON; HARNESS;

EID: 42249089356     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.81     Document Type: Article

References (46)

1. Davies, G.J., Ducros, V.M.-A., Varrot, A. & Zechel, D.L. Mapping the conformational itinerary of β-glycosidases by X-ray crystallography. Biochem. Soc. Trans. 31, 523-527 (2003).
2. Davies, G., Sinnott, M.L. & Withers, S.G. in Comprehensive Biological Catalysis Vol. 1 (ed. Sinnott, M.L.) 119-209 (Academic Press, London, 1997).
3. Vasella, A., Davies, G. & Böhm, M. Glycosidase mechanisms. Curr. Opin. Chem. Biol. 6, 619-629 (2002).
4. Crich, D. & Li, L.F. 4,6-O-benzylidene-directed beta- mannopyranosylation and alphaglucopyranosylation: the 2-deoxy-2-fluoro and 3-deoxy-3-fluoro series of donors and the importance of the O2-C2-C3-O3 interaction. J. Org. Chem. 72, 1681-1690 (2007).
5. Crich, D. & Chandrasekera, N.S. Mechanism of 4,6-0-benzylidene- directed betamannosylation as determined by alpha-deuterium kinetic isotope effects. Angew. Chem. Int. Ed. 43, 5386-5389 (2004).
6. Granovsky, M. et al. Suppression of tumor growth and metastasis in Mgat5-deficient mice. Nat. Med. 6, 306-312 (2000).
7. Li, B. et al. Inhibition of Golgi mannosidase II with mannostatin A analogues: synthesis, biological evaluation, and structure-activity relationship studies. ChemBioChem 5, 1220-1227 (2004).
8. Shah, N., Kuntz, D.A. & Rose, D.R. Comparison of kifunensine and 1-deoxymannojirimycin binding to class I and II alpha-mannosidases demonstrates different saccharide distortions in inverting and retaining catalytic mechanisms. Biochemistry 42, 13812-13816 (2003).
9. Wen, X., Yuan, Y., Kuntz, D.A., Rose, D.R. & Pinto, B.M. A combined STD-NMR/molecular modeling protocol for predicting the binding modes of the glycosidase inhibitors kifunensine and salacinol to Golgi alpha-mannosidase II. Biochemistry 44, 6729-6737 (2005).
10. 2,5 conformation for the transition-state. Angew. Chem. Int. Ed. 41, 2824-2827 (2002).
11. Stoddart, J.F. Stereochemistry of Carbohydrates (Wiley Interscience, Toronto, 1971).
12. Walaszek, Z., Horton, D. & Ekiel, I. Conformational studies on aldonolactones by NMR spectroscopy. Conformations of D-glucono-1,5-lactone and D-manno-1,5-lactone in solution. Carbohydr. Res. 106, 193-201 (1982).
13. Heck, M.P. et al. Cyclic amidine sugars as transition-state analogue inhibitors of glycosidases: potent competitive inhibitors of mannosidases. J. Am. Chem. Soc. 126, 1971-1979 (2004).
14. Numao, S., Kuntz, D.A., Withers, S.G. & Rose, D.R. Insights into the mechanism of Drosophila melanogaster Golgi alpha-mannosidase II through the structural analysis of covalent reaction intermediates. J. Biol. Chem. 278, 48074-48083 (2003).
15. Tailford, L.E. et al. Mannose foraging by Bacteroides thetaiotaomicron: structure and specificity of the b-mannosidase, Man2a. J. Biol. Chem. 282, 11291-11299 (2007).
16. Best, W.M. et al. The synthesis of a carbohydrate-like dihydrooxazine and tetrahydrooxazine as putative inhibitors of glycoside hydrolases: a direct synthesis of isofagomine. Can. J. Chem. 80, 857-865 (2002).
17. Macdonald, J.M. & Stick, R.V. The synthesis of a D-glucose-like piperidin-2-one: isofagomine lactam. Aust. J. Chem. 57, 449-453 (2004).
18. 2,5 boat. Tetrahedr. Lett. 47, 8887-8891 (2006).
19. Goddard-Borger, E.D. & Stick, R.V. An expeditious synthesis of isofagomine. Aust. J. Chem. 60, 211-213 (2007).
20. Meloncelli, P.J. & Stick, R.V. Improvements to the synthesis of isofagomine, noeuromycin, azafagomine, and isofagomine lactam, and a synthesis of azanoeuromycin and 'guanidine' isofagomine. Aust. J. Chem. 59, 827-833 (2006).
21. Terinek, M. & Vasella, A. Synthesis of C(2)-substituted manno-configured tetrahydroimidazopyridines and their evaluation as inhibitors of snail beta-mannosidase. Helv. Chim. Acta 86, 3482-3509 (2003).
22. Bohm, M., Lorthiois, E., Meyyappan, M. & Vasella, A. Isoquinuclidine mimics of beta-D-glucopyranosides: differences and similarities in the mechanism of action of some beta-D-glucosidases and a beta-D-mannosidase. Helv. Chim. Acta 86, 3818-3835 (2003).
23. Legler, G. & Julich, E. Synthesis of 5-amino-5-deoxy-D-mannopyranose and 1,5-di-deoxy-1,5-imino-D-mannitol, and inhibition of alpha-D-mannosidases and beta-D-mannosidases. Carbohydr. Res. 128, 61-72 (1984).
24. Gloster, T.M. et al. Glycosidase inhibition: an assessment of the binding of eighteen putative transition-state mimics. J. Am. Chem. Soc. 129, 2345-2354 (2007).
25. Gloster, T.M. et al. Structural, kinetic and thermodynamic analysis of glucoimidazole-derived glycosidase inhibitors. Biochemistry 45, 11879-11884 (2006).
26. Wicki, J., Williams, S.J. & Withers, S.G. Transition-state mimicry by glycosidase inhibitors: a critical kinetic analysis. J. Am. Chem. Soc. 129, 4530-4531 (2007).
27. Zechel, D.L. et al. Iminosugar glycosidase inhibitors: structural and thermodynamic dissection of the binding of isofagomine and 1-deoxynojirimycin to two β-glucosidases. J. Am. Chem. Soc. 125, 14313-14323 (2003).
28. Zechel, D.L. et al. Mechanism, mutagenesis, and chemical rescue of beta-mannosidase from Cellulomonas fimi. Biochemistry 42, 7195-7204 (2003).
29. Capon, B. Mechanism in carbohydrate chemistry. Chem. Rev. 69, 407-498 (1969).
30. Vincent, F. et al. Common inhibition of both b-glucosidase and b-mannosidase by isofagomine lactam reflects different conformational itineraries for pyranoside hydrolysis. ChemBioChem 5, 1596-1599 (2004).
31. Money, V.A. et al. Substrate distortion by a lichenase highlights the different conformational itineraries harnessed by related glycoside hydrolases. Angew. Chem. Int. Ed. 45, 5136-5140 (2006).
32. Bartlett, P.A. & Marlowe, C.K. Phosphonamidates as transition-state analog inhibitors of thermolysin. Biochemistry 22, 4618-4624 (1983).
33. Whitworth, G.E. et al. Analysis of PUGNAc and NAG-thiazoline as transition state analogues for human O-GlcNAcase: structural and mechanistic insights into inhibitor selectivity and transition state poise. J. Am. Chem. Soc. 129, 635-644 (2007).
34. Berland, C.R., Sigurskjold, B.W., Stoffer, B., Frandsen, T.P. & Svensson, B. Thermodynamics of inhibitor binding to mutant forms of glucoamylase from Aspergillus niger determined by isothermal titration calorimetry. Biochemistry 34, 10153-10161 (1995).
35. Withers, S.G., Namchuk, M. & Mosi, R. in Iminosugars As Glycosidase Inhibitors. Nojirimycin and Beyond (ed. Stütz, A.E.) 188-206 (Wiley-VCH, Weinheim, Germany, 1999).
36. Mosi, R. et al. Reassessment of acarbose as a transition state analogue inhibitor of cyclodextrin glycosyltransferase. Biochemistry 37, 17192-17198 (1998).
37. Mader, M.M. & Bartlett, P.A. Binding energy and catalysis: the implications for transition state analogs and catalytic antibodies. Chem. Rev. 97, 1281-1301 (1997).
38. Liu, H.Z., Liang, X.F., Søhoel, H., Bülow, A. & Bols, M. Noeuromycin, a glycosyl cation mimic that strongly inhibits glycosidases. J. Am. Chem. Soc. 123, 5116-5117 (2001).
39. Tong, M.K., Papandreou, G. & Ganem, B. Potent, broad-spectrum inhibition of glycosidases by an amidine derivative of D-glucose. J. Am. Chem. Soc. 112, 6137-6139 (1990).
40. Papandreou, G., Tong, M.K. & Ganem, B. Amidine, amidrazone, and amidoxime derivatives of monosaccharide aldonolactams: synthesis and evaluation as glycosidase inhibitors. J. Am. Chem. Soc. 115, 11682-11690 (1993).
41. Hoos, R. et al. D-Gluconhydroximo-1,5-lactam and related N-arylcarbamates - theoretical calculations, structure, synthesis, and inhibitory effect on beta-glucosidases. Helv. Chim. Acta 76, 2666-2686 (1993).
42. Snider, M.J. & Wolfenden, R. Site-bound water and the shortcomings of a less than perfect transition state analogue. Biochemistry 40, 11364-11371 (2001).
43. Murshudov, G.N., Vagin, A.A. & Dodson, E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997).
44. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).
45. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
46. Esnouf, R.M. An extensively modified version of MolScript that includes greatly enhanced coloring capabilities. J. Mol. Graph. Model. 15, 132-134 (1997).