Crystal structure of a class I α1,2-mannosidase involved in N-glycan processing and endoplasmic reticulum quality control

EMBO Journal

Volumn 19, Issue 4, 2000, Pages 581-588

  Vallée, François ^a   Lipari, Francesco ^b   Yip, Patrick ^a   Sleno, Barry ^b   Herscovics, Annette ^b   Howell, P Lynne ^a,c  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Class I 1,2 mannosidase; Crystallography; Drug design; ER quality control; Processing glycosidase

Indexed keywords

ALPHA MANNOSIDASE; CALCIUM ION; GLYCAN; GLYCOPROTEIN;

ARTICLE; CRYSTAL STRUCTURE; ENDOPLASMIC RETICULUM; ENZYME SPECIFICITY; GENETIC DISORDER; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN SYNTHESIS; SACCHAROMYCES CEREVISIAE;

EUKARYOTA; MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 0034651605     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.4.581     Document Type: Article

References (50)

1. Aleshin, A., Golubev, A., Firsov, L.M. and Honzatko, R.B. (1992) Crystal structure of glucoamylase from Aspergillus awamori var. X100 to 2.2Å resolution. J. Biol. Chem., 267, 19291-19298.
2. Alzari, P.M. Souchon, H. and Dominguez, R. (1996) The crystal structure of endoglucanase CelA, a family 8 glycosyl hydrolase from Clostridium thermocellum. Structure, 4, 265-275.
3. Bischoff, J. and Kornfeld, R. (1983) Evidence for an α-mannosidase in endoplasmic reticulum of rat liver. J. Biol. Chem., 258, 7907-7910.
4. Bischoff, J., Liscum, L. and Kornfeld, R. (1986) The use of 1-deoxymannojirimycin to evaluate the role of various α-mannosidases in oligosaccharide processing in intact cells. J. Biol. Chem., 261, 4766-4774.
5. Brünger, A.T. et al. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D, 54, 905-921.
6. 2 as an essential intermediate in oligosaccharide processing. J. Biol. Chem., 257, 14657-14666.
7. Camirand, A., Heysen, A., Grondin, B. and Herscovics, A. (1991) Glycoprotein biosynthesis in Saccharomyces cerevisiae. J. Biol. Chem., 266, 15120-15127.
8. Dole, K., Lipari, F., Herscovics, A. and Howell, P.L. (1997) Crystallization and preliminary X-ray analysis of the class I α 1,2-mannosidase from Saccharomyces cerevisiae. J. Struct. Biol., 120, 69-72.
9. Frandsen, T.P., Dupont, C., Lehmbeck, J., Stoffer, B. Sierks, M.R., Hontzatko, R.B. and Svensson, B. (1994) Site-directed mutagenesis of the catalytic base glutamic acid 400 in glucoamylase from Aspergillus niger and of tyrosine 48 and glutamine 401, both hydrogen-bonded to the γ-carboxylate group of glutamic acid 400. Biochemistry, 33, 13808-13816.
10. Gonzalez, D.S., Karaveg, K., Vandersall-Nairn, A.S., Lal, A. and Moremen, K.W. (1999) Identification, expression and characterization of a cDNA encoding human endoplasmic reticulum mannosidase I, the enzyme that catalyzes the first mannose trimming step in mammalian Asn-linked oligosaccharide. J. Biol. Chem., 274, 21375-21386.
11. Grondin, B. and Herscovics, A. (1992) Topology of ER processing α-mannosidase of Saccharomyces cerevisiae. Glycobiology, 2, 369-372.
12. Hammond, C. and Helenius, A. (1995) Quality control in the secretory pathway. Curr. Opin. Cell Biol., 7, 523-529.
13. Henrissat, B. (1991) A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J., 280, 309-316.
14. Herscovics, A. (1999a) Processing glycosidases of Saccharomyces cerevisiae. Biochim. Biophvs. Acta, 1426, 275-285.
15. Herscovics, A. (1999b) Importance of glycosidases in mammalian glycoprotein biosynthesis. Biochim. Biophys. Acta, 1473, 96-107.
16. Herscovics, A. (1999c) Glycosidases of the asparagine-linked oligosaccharide processing pathway. In Pinto, B.M. (ed.), Comprehensive Natural Products Chemistry. Elsevier, New York, NY, Vol. 3, pp. 13-35.
17. Hutchinson, E.G. and Thornton, J.M. (1996) PROMOTIF: a program to identify and analyze structural motifs in proteins. Protein Sci., 5, 212-220.
18. Jakob, C.A., Burda, P., Roth, J. and Aebi, M. (1998) Degradation of misfolded endoplasmic reticulum glycoproteins in Saccharomyces cerevisiae is determined by a specific oligosaccharide structure. J. Cell Biol. 142, 1223-1233.
19. 2. J. Biol. Chem., 263, 14757-14763.
20. Jelinek-Kelly, S., Akiyama, T., Saunier, B., Tkacz, J.S. and Herscovics, A. (1985) Characterization of a specific α-mannosidase involved in oligosaccharide processing in Saccharomyces cerevisiae. J. Biol. Chem., 260, 2253-2257.
21. Knop, M., Hauser, N. and Wolf, D.H. (1996) N-Glycosylation affects endoplasmic reticulum degradation of a mutated derivative of carboxypeptidase yscY in yeast. Yeast, 12, 1229-1238.
22. Kopito, R.R. (1999) Biosynthesis and degradation of CFTR. Physiol. Rev., 79, S167-S173.
23. Kraulis, P. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr., 24, 946-950.
24. Lal, A., Pang, P., Kalelkar, S., Romero, P.A., Herscovics, A. and Moremen, K.W. (1998) Substrate specificities of recombinant murine Golgi α1,2-mannosidases IA and IB and comparison with endoplasmic reticulum and Golgi processing α1,2-mannosidases. Glycobiology, 8, 981-995.
25. Laskowski, R., MacArthur, M., Moss, D. and Thornton, J. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystatlogr., 26, 91-97.
26. Lipari, F. and Herscovics, A. (1994) Production, purification and characterization of recombinant yeast processing α1,2-mannosidase. Glycobiology, 4, 697-702.
27. Lipari, F. and Herscovics, A. (1996) Role of the cysteine residues in the α1,2-mannosidase involved in N-glycan biosynthesis in Saccharomyces cerevisiae. The conserved Cys340 and Cys385 residues form an essential disulfide bond. J. Biol. Chem., 271, 27615-27622.
28. Lipari, F. and Herscovics, A. (1999) Calcium binding to the class 1 α1,2-mannosidase from Saccharomyces cerevisiae occurs outside the EF hand motif. Biochemistry, 38, 1111-1118.
29. Lipari, F., Gour-Salin, B.J. and Herscovics, A. (1995) The Saccharomyces cerevisiae processing α1,2-mannosidase is an inverting glycosidase. Biochem. Biophys. Res. Commun., 209, 322-326.
30. Liu, Y., Choudhury, P., Cabral, C.M. and Sifers, R.N. (1997) Intracellular disposal of incompletely folded human α1-antitrypsin involves release from calnexin and post-translational trimming of asparagine-linked oligosaccharides. J. Biol Chem., 272, 7946-7951.
31. Liu, Y., Choudhury, P., Cabral, C.M. and Sifers, R.N. (1999) Oligosaccharide modification in the early secretory pathway directs the selection of a misfolded glycoprotein for degradation by the proteasome. J. Biol. Chem., 274, 5861-5867.
32. Ly, H.D. and Withers, S.G. (1999). Mutagenesis of glycosidases. Annu. Rev. Biochem., 68, 487-522.
33. Massaad, M.J., Franzusoff, A. and Herscovics, A. (1999) The processing α1,2-mannosidase of Saccharomyces cerevisiae depends on Rer1p for its localization in the endoplasmic reticulum. Eur. J. Cell Biol., 78, 435-440.
34. Merrit, E. and Murphy, M. (1994) RASTER3D: a program for photorealistic molecular graphics. Acta Crystallogr. D, 50, 869-873.
35. Moremen, K.W., Trimble, R.B. and Herscovics, A. (1994) Glycosidases of the asparagine-linked oligosaccharide processing pathway. Glycobiology, 4, 113-125.
36. Nagar, B., Jones, R.G., Diefenbach, R.J., Isenman, D.E. and Rini, J.M. (1998) X-ray crystal structure of C3d: a C3 fragment and ligand for complement receptor 2. Science, 280, 1277-1281.
37. Nicholls, A., Sharp, K.A. and Honig, B. (1991) Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbon. Proteins, 11, 281-296.
38. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol., 276, 307-326.
39. Park, H.W., Boduluri, S.R., Moomaw, J.F., Casey, P.J. and Beese, L.S. (1997) Crystal structure of protein farnesyltransferase at 2.25Å resolution. Science, 275, 1800-1804.
40. Parsiegla, G., Juy, M., Reverbel-Leroy, C., Tardif, C., Belaich, J.-P., Driguez, H. and Haser, R. (1998) The crystal structure of the processive endocellulase CelF of Clostridium cellulolyticum in complex with a thiooligosaccharide inhibitor at 2.0 Å resolution. EMBO J., 17, 5551-5562.
41. Petrescu, A.J., Petrescu, S.M., Dwek, R.A. and Wormald, M.R. (1999) A statistical analysis of N-and O-glycan linkage conformations from crystallographic data. Glycobiology, 9, 343-352.
42. Rizzolo, L.J. and Kornfeld, R. (1988) Post-translational protein modification in the endoplasmic reticulum. Demonstration of fatty acylase and deoxymannojirimycin-sensitive α-mannosidase activities. J. Biol. Chem., 263, 9520-9525.
43. Roussel, A. and Cambillau, C. (1991) The TURBO-FRODO graphics package. In Silicon Graphics Partners Geometry. Silicon Graphics Corporation, p. 81.
44. Schmidt, A., Schlacher, A., Steiner, W., Schwab, H. and Kratky, C. (1998) Structure of the xylanase from Penicillium simplicissimum. Protein Sci., 7, 2081-2088.
45. Sifers, R.N. (1995) Detective protein folding as a cause of disease. Nature Struct. Biol., 2, 355-357.
46. Su, K., Stoller, T., Rocco, J., Zemsky, J. and Green, R. (1993) Pre-Golgi degradation of yeast prepro-α-factor expressed in a mammalian cell. Influence of cell type-specific oligosaccharide processing on intracellular fate. J. Biol. Chem., 268, 14301-14309.
47. 2 isomer B during N-glycan biosynthesis. Glycobiology, 9, 1073-1078.
48. Varki, A. (1993) Biological roles of oligosaccharides: all of the theories are correct. Glycoblology, 3, 97-130.
49. Weng, S. and Spiro, R.G. (1993) Demonstration that a kifunensine-resistant α-mannosidase with a unique processing action on N-linked oligosaccharides occurs in rat liver endoplasmic reticulum and various cultured cells. J. Biol. Chem., 268, 25656-25663.
50. 9 processing α-mannosidase. Glycobiology, 1, 605-614.