Structural analysis of Golgi α-mannosidase II inhibitors identified from a focused glycosidase inhibitor screen

Biochemistry

Volumn 47, Issue 38, 2008, Pages 10058-10068

  Kuntz, Douglas A ^a   Tarling, Chris A ^c   Withers, Stephen G ^c   Rose, David R ^a,b  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENIC COMPOUNDS; BINDING SITES; CHLORINE COMPOUNDS; COMPLEXATION; ENZYME ACTIVITY; FOOD ADDITIVES; HYDROGEN; HYDROGEN BONDS; KETONES; NITROGEN; NONMETALS; SUBSTRATES; SUGARS; ZINC;

ACID-BASE; ACTIVE SITES; CANCER.; COVALENT REACTION; GLYCOSIDASE; GLYCOSIDE HYDROLASE; HIGH RESOLUTIONS; HIGH THROUGHPUT SCREENINGS; IN-SILICO; INHIBITORY ACTIVITIES; MANNOSIDASE; N-GLYCOSYLATION; NITROGEN ATOMS; PATHOLOGICAL CONDITIONS; POSITIVELY CHARGED; STRUCTURAL DATA; TRANSITION STATES; X-RAY CRYSTALLOGRAPHIC ANALYSIS;

STRUCTURAL ANALYSIS;

ALPHA MANNOSIDASE; BETA GLUCOSIDASE; GLUCOHYDROXYIMINOLACTAM; GLUCOIMIDAZOLE; GLYCOSIDASE INHIBITOR; HYDROXYL GROUP; MANNOIMIDAZOLE; MANNOSE; MANNOSIDASE INHIBITOR; N OCTYL 6 EPIVALIENAMINE; NITROGEN; UNCLASSIFIED DRUG; ZINC;

ACID BASE BALANCE; ARTICLE; CATALYST; CONFORMATIONAL TRANSITION; DRUG DESIGN; DRUG IDENTIFICATION; DRUG PROTEIN BINDING; DRUG SCREENING; DRUG STRUCTURE; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME SUBSTRATE; GOLGI COMPLEX; HYDROGEN BOND; KINETICS; MOLECULAR MIMICRY; PRIORITY JOURNAL; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

ANIMALS; CELLS, CULTURED; CRYSTALLOGRAPHY, X-RAY; DROSOPHILA MELANOGASTER; DRUG EVALUATION, PRECLINICAL; ENZYME INHIBITORS; GLYCOSIDE HYDROLASES; GOLGI APPARATUS; MANNOSIDASES; PROTEIN STRUCTURE, SECONDARY; PROTEINS;

EID: 52249111139     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi8010785     Document Type: Article

References (54)

1. Henrissat, B. (1991) A classification of glycosyl hydrolases based on amino-acid sequence similarities. Biochem. J. 280, 309-316.
2. Broquist, H. P. (1985) The indolizidine alkaloids, slaframine and swainsonine: Contaminants in animal forages. Annu. Rev. Nutr. 5, 391-409.
3. Tulsiani, D. R., Broquist, H. P., James, L. F., and Touster, O. (1988) Production of hybrid glycoproteins and accumulation of oligosaccharides in the brain of sheep and pigs administered swainsonine or locoweed. Arch. Biochem. Biophys. 264, 607-617.
4. Bernacki, R. J., Niedbala, M. J., and Korytnyk, W. (1985) Glycosidases in cancer and invasion. Cancer Metastasis Rev. 4, 81-101.
5. Dennis, J. W., Granovsky, M., and Warren, C. E. (1999) Glycoprotein glycosylation and cancer progression. Biochim. Biophys. Acta 1473, 21-34.
6. Dube, D. H., and Bertozzi, C. R. (2005) Glycans in cancer and inflammation. Potential for therapeutics and diagnostics. Nat. Rev. Drug Discovery 4, 477-488.
7. Hakomori, S. (2002) Glycosylation defining cancer malignancy: new wine in an old bottle. Proc. Nat. Acad. Sci. U.S.A. 99, 10231-10233.
8. Goss, P. E., Reid, C. L., Bailey, D., and Dennis, J. W. (1997) Phase IB clinical trial of the oligosaccharide processing inhibitor swainsonine in patients with advanced malignancies. Clin. Cancer Res. 3, 1077-1086.
9. Kumar, N. S., Kuntz, D. A., Wen, X., Pinto, B. M., and Rose, D. R. (2008) Binding of sulfonium-ion analogues of di-epi-swainsonine and 8-epi-lentiginosine to Drosophila Golgi α-mannosidase II: The role of water in inhibitor binding. Proteins. 71, 1484-1496.
10. Zhong, W., Kuntz, D. A., Ember, B., Singh, H., Moremen, K. W., Rose, D. R., and Boons, G.-J. (2008) Probing the substrate specificity of Golgi α-mannosidase II using synthetic oligosaccharides and a catalytic nucleophile mutant. J. Am. Chem. Soc. 130, 8975-8983.
11. Jones, G., Willett, P., Glen, R. C., Leach, A. R., and Taylor, R. (1997) Development and validation of a genetic algorithm for flexible docking. J. Mol. Biol. 267, 727-748.
12. Englebienne, P., Fiaux, H., Kuntz, D. A., Corbeil, C. R., Gerber-Lemaire, S., Rose, D. R., and Moitessier, N. (2007) Evaluation of docking programs for predicting binding of Golgi α-mannosidase II inhibitors: a comparison with crystallography. Proteins 69, 160-176.
13. Caines, M. E., Hancock, S. M., Tarling, C. A., Wrodnigg, T. M., Stick, R. V., Stütz, A. E., Vasella, A., Withers, S. G., and Strynadka, N. C. (2007) The structural basis of glycosidase inhibition by five-membered iminocyclitols: the clan a glycoside hydrolase endoglycoceramidase as a model system. Angew. Chem., Int. Ed. 46, 4474-4476.
14. van den Elsen, J. M., Kuntz, D. A., and Rose, D. R. (2001) Structure of Golgi α-mannosidase II: a target for inhibition of growth and metastasis of cancer cells. EMBO J. 20, 3008-3017.
15. Zechel, D. L. (2001) Phd thesis, University of British Columbia.
16. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326.
17. Collaborative Computational Project, Number 4. (1994). The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D50, 760-763.
18. Brunger, A. T., Adams, P. D., Clore, G. M., Delano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D54, 905-921.
19. Lamzin, V. S., Perrakis, A., and Wilson, K. S. (2001) The ARP/WARP suite for automated construction and refinement of protein models, in Int. Tables for Crystallography. Vol. F: Crystallography of biological macromolecules (Rossmann, M. G., and Arnold, E., Eds.) pp 720-722, Kluwer Academic Publishers, Dordrecht, The Netherlands.
20. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D60, 2126-2132.
21. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D53, 240-255.
22. Sheldrick, G. M., and Schneider, T. R. (1997) SHELX: high resolution refinement. Methods Enzymol. 277, 319-343.
23. Krissinel, E., and Henrick, K. (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D60, 2256-2268.
24. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, G., Weissig, H., Shindyalov, I. N., and Bourne, P. E. (2000) The Protein Data Bank. Nucleic Acids Res. 28, 235-242.
25. Shah, N., Kuntz, D. A., and Rose, D. R. (2003) Comparative structural analysis of the binding of the inhibitor kifunensine to Class I and Class II α-mannosidases. Biochemistry 42, 13812-13816.
26. Vasella, A., Davies, G. J., and Bohm, M. (2002) Glycosidase mechanisms. Curr. Opin. Chem. Biol. 5, 619-629.
27. Money, V. A., Smith, N. L., Scaffidi, A., Stick, R. V., Gilbert, H. J., and Davies, G. J. (2006) Substrate distortion by a lichenase highlights the different conformational itineraries harnessed by related glycoside hydrolases. Angew. Chem., Int. Ed. 45, 5136-5140.
28. Dorfmueller, H. C., Borodkin, V. S., Schimpl, M., Shepherd, S. M., Shpiro, N. A., and van Aalten, D. M. (2006) GlcNAcstatin: a picomolar, selective O-GlcNAcase inhibitor that modulates intracellular O-glcNAcylation levels. J. Am. Chem. Soc. 128, 16484-16485.
29. Granier, T., Panday, N., and Vasella, A. (1997) Structure-activity relations for imidazo-pyridine-type inhibitors of β-D- glucosidases. Helv. Chim. Acta 80, 979-987.
30. Panday, N., Canac, Y., and Vasella, A. (2000) Very strong inhibition of β-glucosidases by C(2)-substituted tetrahydroimidazopyridines. Helv. Chim. Acta 83, 58-79.
31. Numao, S., Kuntz, D. A., Withers, S. G., and Rose, D. R. (2003) Insights into the mechanism of Drosophila melanogaster Golgi α-mannosidase through the structural analysis of covalent reaction intermediates. J. Biol. Chem. 278, 48074-48083.
32. Tailford, L. E., Offen, W. A., Smith, N. L., Dumon, C., Morland, C., Gratien, J., Heck, M.-P., Stick, R. V., Blériot, Y., Vasella, A., Gilbert, H. J., and Davies, G. J. (2008) Structural and biochemical evidence for a boat-like transition state in β-mannosidases. Nat. Chem. Biol. 5, 306-312.
33. Liu, H., Liangm, X., Søhoel, H., Bülow, A., and Bols, M. (2001) Noeuromycin, a glycosyl cation mimic that strongly inhibitis glycosidases. J. Am. Chem. Soc. 123, 5116-5117.
34. Jespersen, T. M., Dong, W., Sierks, M. R., Skrydstrup, T., Lundt, I., and Bols, M. (1994) Isofagomine, a potent, new glycosidase inhibitor. Angew. Chem., Int. Ed. Engl. 33, 1778-1779.
35. Fuhrmann, U., Bause, E., Legler, G., and Ploegh, H. (1984) ) Novel mannosidase inhibitor blocking conversion of high mannose to complex oligosaccharides. Nature 307, 755-758.
36. Kuntz, D. A., Liu, H., Bols, M., and Rose, D. R. (2006) The role of the active site Zn in the catalytic mechanism of the GH38 Golgi α-mannosidase II: implications from noeuromycin inhibition. Biocatal. Biotransform. 24, 55-61.
37. Gloster, T. M., Roberts, S., Perugino, G., Rossi, M., Moracci, M., Panday, N., Terinek, M., Vasella, A., and Davies, G. J. (2006) Structural, kinetic and thermodynamic analysis of glucoimidazole-derived glycosidase inhibitors. Biochemistry 45, 11879-11884.
38. Ogawa, S., Ashiura, M., Uchida, C., Watanabe, S., Yamazaki, C., Yamagishi, K., and Inokuchi, J. (1996) Synthesis of potent β-D- glucocerebrosidase inhibitors: N-alkyl-β-valienamines. Bioorg. Med. Chem. Lett. 6, 929-932.
39. Lin, H., Sugimoto, Y., Ohsaki, Y., Ninomiya, H., Oka, A., Taniguchi, M., Ida, H., Eto, Y., Ogawa, S., Matsuzaki, Y., Sawa, M., Inoue, T., Higaki, K., Nanba, E., Ohno, K., and Suzuki, Y. (2004) N-octyl-β-valienamine up-regulates activity of F213I mutant β-glucosidase in cultured cells: a potential chemical chaperone therapy for Gaucher disease. Biochim. Biophys. Acta 1689, 219-228.
40. Lei, K., Ninomiya, H., Suzuki, M., Inoue, T., Sawa, M., Iida, M., Ida, H., Eto, Y., Ogawa, S., Ohno, K., and Suzuki, Y. (2007) Enzyme enhancement activity of N-octyl-β-valienamine on β-glucosidase mutants associated with Gaucher disease. Biochim. Biophys. Acta 1772, 587-596.
41. Li, C., Begum, A., Numao, S., Park, K. H., Withers, S. G., and Brayer, G. D. (2005) Acarbose rearrangement mechanism implied by the kinetic and structural analysis of human pancreatic alpha-amylase in complex with analogues and their elongated counterparts. Biochemistry 44, 3347-3357.
42. Scaffidi, A., Stubbs, K. A., Dennis, R. J., Taylor, E. J., Davies, G. J., Vocadlo, D. J., and Stick, R. V. (2007) A 1-acetamido derivative of 6-epi-valienamine: an inhibitor of a diverse group of β-N- acetylglucosaminidases. Org. Biomol. Chem. 5, 3013-3019.
43. Hoos, R., Naughton, A. B., Thiel, W., Vasella, A., Weber, W., Rupitz, K., and Withers, S. G. (1993) D-Gluconhydroximino-1,5-lactam and related N-arylcarbamates. Theoretical calculations, structure, synthesis, and inhibitory effect on β-glucosidases. Helv. Chim. Acta 76, 2666-2686.
44. Gloster, T. M., Meloncelli, P., Stick, R. V., Zechel, D., Vasella, A., and Davies, G. J. (2007) Glycosidase inhibition: an assessment of the binding of 18 putative transition-state mimics. J. Am. Chem. Soc. 129, 2345-2354.
45. Burmeister, W. P., Cottaz, S., Rollin, P., Vasella, A., and Henrissat, B. (2000) High resolution X-ray crystallography shows that ascorbate is a cofactor for myrosinase and substitutes for the function of the catalytic base. J. Biol. Chem. 275, 39385-39393.
46. Elbein, A. D., Tropea, J. E., Mitchell, M., and Kaushal, G. P. (1990) Kifunensine, a potent inhibitor of the glycoprotein processing mannosidase I. J. Biol. Chem. 265, 15599-15605.
47. Vallee, F., Karaveg, K., Herscovics, A., Moremen, K. W., and Howell, P. L. (2000) Structural basis for catalysis and inhibition of N-glycan processing class I α 1,2-mannosidases. J. Biol. Chem. 275, 41287-41298.
48. Wicki, J., Williams, S. J., and Withers, S. G. (2007) Transition-state mimicry by glycosidase inhibitors: A critical kinetic analysis. J. Am. Chem. Soc. 129, 4530-4531.
49. Hrmova, M., Stretltsov, V. A., Smith, B. J., Vasella, A., Varghese, J. N., and Fincher, G. B. (2005) Structural rationale for low-nanomolar binding of transition state mimics to a Family GH3 β-D-glucan glucohydrolase from barley. Biochemistry 44, 16529-16539.
50. Gloster, T. M., Macdonald, J. M., Tarling, C. A., Stick, R. V., Withers, S. G., and Davies, G. J. (2004) Structural, thermodynamic, and kinetic analyses of tetrahydrooxazine-derived inhibitors bound to β-glucosidases. J. Biol. Chem. 279, 49236-49242.
51. Gartenmann Dickson, L., Emmanuel, L., and Reymond, J.-L. (2004) Structure-activity relationships in aminocyclopentitol glycosidase inhibitors. Org. Biomol. Chem. 2, 1217-1226.
52. Li, B., Kawatkar, S. P., George, S., Strachan, H., Woods, R. J., Siriwardena, A., Moremen, K. W., and Boons, G.-J. (2004) Inhibition of Golgi mannosidase II with mannostatin A analogues: synthesis, biological evaluation, and structure-activity relationship studies. ChemBioChem 5, 1220-1227.
53. Kawatkar, S. P., Kuntz, D. A., Woods, R. J., Rose, D. R., and Boons, G.-J. (2006) Structural basis of the inhibition of Golgi α-mannosidase II by mannostatin A and the role of the thiomethyl moiety in ligand-protein interactions. J. Am. Chem. Soc. 128, 8310-8319.
54. Shah, N., Kuntz, D. A., and Rose, D. R. (2008) Golgi α-mannosidase II cleaves two sugars sequentially in the same catalytic site. Proc. Natl. Acad. Sci. U.S.A. 105, 9570-9575.