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Abstract:

Here we report for the first time the three-dimensional structure of a mannose 6-phosphate receptor homology (MRH) domain present in a protein with enzymatic activity, glucosidase II (GII). GII is involved in glycoprotein folding in the endoplasmic reticulum. GII removes the two innermost glucose residues from the Glc3Man9GlcNAc2 transferred to nascent proteins and the glucose added by UDP-Glc:glycoprotein glucosyltransferase. GII is composed of a catalytic GIIα subunit and a regulatory GIIβ subunit. GIIβ participates in the endoplasmic reticulum localization of GIIβ and mediates in vivo enhancement of N-glycan trimming by GII through its C-terminal MRH domain. We determined the structure of a functional GIIβ MRH domain by NMR spectroscopy. It adopts a β-barrel fold similar to that of other MRH domains, but its binding pocket is the most shallow known to date as it accommodates a single mannose residue. In addition, we identified a conserved residue outside the binding pocket (Trp-409) present in GIIβ but not in other MRHs that influences GII glucose trimming activity. © 2013 by The American Society for Biochemistry and Molecular Biology, Inc.

Registro:

Documento: Artículo
Título:Structure of the lectin mannose 6-phosphate receptor homology (MRH) domain of glucosidase II, an enzyme that regulates glycoprotein folding quality control in the endoplasmic reticulum
Autor:Olson, L.J.; Orsi, R.; Alculumbre, S.G.; Peterson, F.C.; Stigliano, I.D.; Parodi, A.J.; D'Alessio, C.; Dahms, N.M.
Filiación:Dept. of Biochemistry, Medical College of Wisconsin, 8701 Watertown Plank Rd., Milwaukee, WI 53226, United States
Laboratory of Glycobiology, Fundación Inst. Leloir-Inst. de Investigaciones Bioquímicas de Buenos Aires, CONICET, Av. Patricias Argentinas 435, C1405BWE Buenos Aires, Argentina
School of Sciences, University of Buenos Aires, C1428EHA Buenos Aires, Argentina
Palabras clave:Binding pockets; Conserved residues; Endoplasmic reticulum; Enzymatic activities; Glucose residues; Glucosyltransferases; Nascent protein; Three-dimensional structure; Cell membranes; Glucose; Glycoproteins; Nuclear magnetic resonance spectroscopy; Trimming; Proteins; alpha glucosidase ab; glucosidase; glucosidase II alpha; glucosidase II beta; glycan; glycoprotein; glycosidase; lectin; mannose; mannose 6 phosphatase receptor homology; n glycan; somatomedin B receptor; unclassified drug; uridine diphosphate; article; binding affinity; binding site; carboxy terminal sequence; controlled study; endoplasmic reticulum; enzyme active site; enzyme activity; enzyme assay; enzyme localization; enzyme regulation; Escherichia coli; in vivo study; molecular dynamics; nonhuman; nuclear magnetic resonance spectroscopy; priority journal; protein binding; protein domain; protein expression; protein folding; protein protein interaction; quality control; residue analysis; Schizosaccharomyces pombe; Endoplasmic Reticulum (ER); Glucosidase II β; Glycobiology; Glycoprotein; MRH Domain; N-Glycan; NMR; Structural Biology; alpha-Glucosidases; Crystallography, X-Ray; Endoplasmic Reticulum; Glycoproteins; Mannose; Protein Folding; Protein Structure, Secondary; Protein Structure, Tertiary; Schizosaccharomyces; Schizosaccharomyces pombe Proteins
Año:2013
Volumen:288
Número:23
Página de inicio:16460
Página de fin:16475
DOI: http://dx.doi.org/10.1074/jbc.M113.450239
Título revista:Journal of Biological Chemistry
Título revista abreviado:J. Biol. Chem.
ISSN:00219258
CODEN:JBCHA
CAS:glucosidase, 9033-06-1; glycosidase, 9032-92-2; mannose, 31103-86-3, 3458-28-4; uridine diphosphate, 58-98-0; 4-nitrophenyl-alpha-glucosidase, 3.2.1.-; Glycoproteins; Mannose, 31103-86-3; Schizosaccharomyces pombe Proteins; alpha-Glucosidases, 3.2.1.20
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00219258_v288_n23_p16460_Olson

Referencias:

  • Castonguay, A.C., Olson, L.J., Dahms, N.M., Mannose 6-phosphate receptor homology (MRH) domain-containing lectins in the secretory pathway (2011) Biochim. Biophys. Acta, 1810, pp. 815-826
  • Munro, S., The MRH domain suggests a shared ancestry for the mannose 6-phosphate receptors and other N-glycan-recognising proteins (2001) Curr. Biol., 11, pp. R499-R501
  • Hammond, C., Braakman, I., Helenius, A., Role of N-linked oligosaccharide recognition, glucose trimming, and calnexin in glycoprotein folding and quality control (1994) Proceedings of the National Academy of Sciences of the United States of America, 91 (3), pp. 913-917
  • D'Alessio, C., Caramelo, J.J., Parodi, A.J., UDP-GlC:glycoprotein glucosyltransferase-glucosidase II, the ying-yang of the ER quality control (2010) Semin. Cell Dev. Biol., 21, pp. 491-499
  • Hosokawa, N., Kamiya, Y., Kamiya, D., Kato, K., Nagata, K., Human OS-9, a lectin required for glycoprotein endoplasmic reticulum-associated degradation, recognizes mannose-trimmed N-glycans (2009) J. Biol. Chem., 284, pp. 17061-17068
  • Quan, E.M., Kamiya, Y., Kamiya, D., Denic, V., Weibezahn, J., Kato, K., Weissman, J.S., Defining the glycan destruction signal for endoplasmic reticulum-associated degradation (2008) Mol. Cell, 32, pp. 870-877
  • Satoh, T., Chen, Y., Hu, D., Hanashima, S., Yamamoto, K., Yamaguchi, Y., Structural basis for oligosaccharide recognition of misfolded glycoproteins by OS-9 in ER-associated degradation (2010) Mol. Cell, 40, pp. 905-916
  • Fujimori, T., Kamiya, Y., Nagata, K., Kato, K., Hosokawa, N., Endoplasmic reticulum lectin XTP3-B inhibits endoplasmic reticulumassociated degradation of a misfolded α1-antitrypsin variant (2013) FEBS J., 280, pp. 1563-1575
  • Trombetta, E.S., Simons, J.F., Helenius, A., Endoplasmic reticulum glucosidase II is composed of a catalytic subunit, conserved from yeast to mammals, and a tightly bound noncatalytic HDEL- containing subunit (1996) Journal of Biological Chemistry, 271 (44), pp. 27509-27516. , DOI 10.1074/jbc.271.44.27509
  • D'Alessio, C., Fernández, F., Trombetta, E.S., Parodi, A.J., Genetic evidence for the heterodimeric structure of glucosidase II. The effect of disrupting the subunit-encoding genes on glycoprotein folding (1999) J. Biol. Chem., 274, pp. 25899-25905
  • Grinna, L.S., Robbins, P.W., Substrate specificities of rat liver microsomal glucosidases which process glycoproteins (1980) J. Biol. Chem., 255, pp. 2255-2258
  • Totani, K., Ihara, Y., Matsuo, I., Ito, Y., Substrate specificity analysis of endoplasmic reticulum glucosidase II using synthetic high mannose-type glycans (2006) Journal of Biological Chemistry, 281 (42), pp. 31502-31508. , http://www.jbc.org/cgi/reprint/281/42/31502, DOI 10.1074/jbc.M605457200
  • Hu, D., Kamiya, Y., Totani, K., Kamiya, D., Kawasaki, N., Yamaguchi, D., Matsuo, I., Yamamoto, K., Sugar-binding activity of the MRH domain in the ER α-glucosidase II β subunit is important for efficient glucose trimming (2009) Glycobiology, 19, pp. 1127-1135
  • Stigliano, I.D., Caramelo, J.J., Labriola, C.A., Parodi, A.J., D'Alessio, C., Glucosidase II β subunit modulates N-glycan trimming in fission yeasts and mammals (2009) Mol. Biol. Cell, 20, pp. 3974-3984
  • Stigliano, I.D., Alculumbre, S.G., Labriola, C.A., Parodi, A.J., D'Alessio, C., Glucosidase II and N-glycan mannose content regulate the half-lives of monoglucosylated species in vivo (2011) Mol. Biol. Cell, 22, pp. 1810-1823
  • Quinn, R.P., Mahoney, S.J., Wilkinson, B.M., Thornton, D.J., Stirling, C.J., A novel role for Gtb1p in glucose trimming of N-linked glycans (2009) Glycobiology, 19, pp. 1408-1416
  • Moreno, S., Klar, A., Nurse, P., Molecular genetic analysis of fission yeast Schizosaccharomyces pombe (1991) Methods Enzymol., 194, pp. 795-823
  • Alfa, C., Fantes, P., Hyams, J., McLeod, M., Wabrik, E., (1993) Experiments with Fission Yeast: A Laboratory Manual, pp. 133-136. , Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
  • Jannatipour, M., Rokeach, L.A., The Schizosaccharomyces pombe homologue of the chaperone calnexin is essential for viability (1995) J. Biol. Chem., 270, pp. 4845-4853
  • Matsuyama, A., Arai, R., Yashiroda, Y., Shirai, A., Kamata, A., Sekido, S., Kobayashi, Y., Yoshida, M., ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe (2006) Nature Biotechnology, 24 (7), pp. 841-847. , DOI 10.1038/nbt1222, PII NBT1222
  • Wright, A., Dankert, M., Robbins, P.W., Evidence for an intermediate stage in the biosynthesis of the Salmonella O-antigen (1965) Proc. Natl. Acad. Sci. U.S.A., 54, pp. 235-241
  • Trombetta, S.E., Bosch, M., Parodi, A.J., Glucosylation of glycoproteins by mammalian, plant, fungal, and trypanosomatid protozoa microsomal membranes (1989) Biochemistry, 28 (20), pp. 8108-8116
  • Allen, H.J., Johnson, E.A., The isolation of lectins on acid-treated agarose (1976) Carbohydr. Res., 50, pp. 121-131
  • Walker, J.M., (2002) The Protein Protocols Handbook, pp. 803-804. , 2nd Ed., Humana Press Inc., Totowa, NJ
  • Fernandez, F.S., Trombetta, S.E., Hellman, U., Parodi, A.J., Purification to homogeneity of UDP-glucose:glycoprotein glucosyltransferase from Schizosaccharomyces pombe and apparent absence of the enzyme from Saccharomyces cerevisiae (1994) Journal of Biological Chemistry, 269 (48), pp. 30701-30706
  • Bohnsack, R.N., Song, X., Olson, L.J., Kudo, M., Gotschall, R.R., Canfield, W.M., Cummings, R.D., Dahms, N.M., Cation-independent mannose 6-phosphate receptor: A composite of distinct phosphomannosyl binding sites (2009) J. Biol. Chem., 284, pp. 35215-35226
  • Myszka, D.G., Kinetic, equilibrium, and thermodynamic analysis of macromolecular interactions with BIACORE (2000) Methods Enzymol., 323, pp. 325-340
  • Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J., Bax, A., NMRPipe: A multidimensional spectral processing system based on UNIX pipes (1995) J. Biomol. NMR, 6, pp. 277-293
  • Bartels, C., Xia, T.H., Billeter, M., Güntert, P., Wüthrich, K., The program XEASY for computer-supported NMR spectral analysis of biological macromolecules (1995) J. Biomol. NMR, 6, pp. 1-10
  • Bartels, C., Billeter, M., Guntert, P., Wuthrich, K., Automated sequence-specific NMR assignment of homologous proteins using the program GARANT (1996) Journal of Biomolecular NMR, 7 (3), pp. 207-213
  • Shen, Y., Delaglio, F., Cornilescu, G., Bax, A., TALOS+: A hybrid method for predicting protein backbone torsion angles from NMR chemical shifts (2009) J. Biomol. NMR, 44, pp. 213-223
  • Herrmann, T., Guntert, P., Wuthrich, K., Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA (2002) Journal of Molecular Biology, 319 (1), pp. 209-227. , DOI 10.1016/S0022-2836(02)00241-3
  • Schwieters, C.D., Kuszewski, J.J., Tjandra, N., Clore, G.M., The Xplor-NIH NMR molecular structure determination package (2003) J. Magn. Reson., 160, pp. 65-73
  • Linge, J.P., Williams, M.A., Spronk, C.A.E.M., Bonvin, A.M.J.J., Nilges, M., Refinement of protein structures in explicit solvent (2003) Proteins: Structure, Function and Genetics, 50 (3), pp. 496-506. , DOI 10.1002/prot.10299
  • Olson, L.J., Peterson, F.C., Castonguay, A., Bohnsack, R.N., Kudo, M., Gotschall, R.R., Canfield, W.M., Dahms, N.M., Structural basis for recognition of phosphodiester-containing lysosomal enzymes by the cation-independent mannose 6-phosphate receptor (2010) Proc. Natl. Acad. Sci. U.S.A., 107, pp. 12493-12498
  • Chavez, C.A., Bohnsack, R.N., Kudo, M., Gotschall, R.R., Canfield, W.M., Dahms, N.M., Domain 5 of the cation-independent mannose 6-phosphate receptor preferentially binds phosphodiesters (mannose 6-phosphate N-acetylglucosamine ester) (2007) Biochemistry, 46 (44), pp. 12604-12617. , DOI 10.1021/bi7011806
  • Kim, J.J., Olson, L.J., Dahms, N.M., Carbohydrate recognition by the mannose-6-phosphate receptors (2009) Curr. Opin. Struct. Biol., 19, pp. 534-542
  • Watanabe, T., Totani, K., Matsuo, I., Maruyama, J., Kitamoto, K., Ito, Y., Genetic analysis of glucosidase II β-subunit in trimming of high-mannose-type glycans (2009) Glycobiology, 19, pp. 834-840
  • Olson, L.J., Yammani, R.D., Dahms, N.M., Kim, J.-J.P., Structure of uPAR, plasminogen, and sugar-binding sites of the 300 kDa mannose 6-phosphate receptor (2004) EMBO Journal, 23 (10), pp. 2019-2028. , DOI 10.1038/sj.emboj.7600215
  • Uson, I., Schmidt, B., Von Bulow, R., Grimme, S., Von Figura, K., Dauter, M., Rajashankar, K.R., Sheldrick, G.M., Locating the anomalous scatterer substructures in halide and sulfur phasing (2003) Acta Crystallographica Section D: Biological Crystallography, 59 (1), pp. 57-66. , DOI 10.1107/S090744490201884X
  • Brown, J., Delaine, C., Zaccheo, O.J., Siebold, C., Gilbert, R.J., Van Boxel, G., Denley, A., Jones, E.Y., Structure and functional analysis of the IGF-II/IGF2R interaction (2008) EMBO J., 27, pp. 265-276
  • Roberts, D.L., Weix, D.J., Dahms, N.M., Kim, J.-J.P., Molecular basis of lysosomal enzyme recognition: Three-dimensional structure of the cation-dependent mannose 6-phosphate receptor (1998) Cell, 93 (4), pp. 639-648. , DOI 10.1016/S0092-8674(00)81192-7
  • Mikami, K., Yamaguchi, D., Tateno, H., Hu, D., Qin, S.Y., Kawasaki, N., Yamada, M., Yamamoto, K., The sugar-binding ability of human OS-9 and its involvement in ER-associated degradation (2010) Glycobiology, 20, pp. 310-321
  • Totani, K., Ihara, Y., Matsuo, I., Ito, Y., Effects of macromolecular crowding on glycoprotein processing enzymes (2008) Journal of the American Chemical Society, 130 (6), pp. 2101-2107. , DOI 10.1021/ja077570k
  • Kamiya, Y., Satoh, T., Kato, K., Molecular and structural basis for N-glycan-dependent determination of glycoprotein fates in cells (2012) Biochim. Biophys. Acta, 1820, pp. 1327-1337
  • Fernandez, F., D'Alessio, C., Fanchiotti, S., Parodi, A.J., A misfolded protein conformation is not a sufficient condition for in vivo glucosylation by the UDP-Glc:glycoprotein glucosyltransferase (1998) EMBO Journal, 17 (20), pp. 5877-5886. , DOI 10.1093/emboj/17.20.5877
  • Olson, L.J., Dahms, N.M., Kim, J.-J.P., The N-terminal carbohydrate recognition site of the cation-independent mannose 6-phosphate receptor (2004) Journal of Biological Chemistry, 279 (32), pp. 34000-34009. , DOI 10.1074/jbc.M404588200
  • Woods, R.J., Pathiaseril, A., Wormald, M.R., Edge, C.J., Dwek, R.A., The high degree of internal flexibility observed for an oligomannose oligosaccharide does not alter the overall topology of the molecule (1998) European Journal of Biochemistry, 258 (2), pp. 372-386. , DOI 10.1046/j.1432-1327.1998.2580372.x
  • Kumari, M., Balaji, P.V., Sunoj, R.B., Quantification of binding affinities of essential sugars with a tryptophan analogue and the ubiquitous role of C-H⋯π interactions (2011) Phys. Chem. Chem. Phys., 13, pp. 6517-6530
  • Stenmark, P., Dupuy, J., Imamura, A., Kiso, M., Stevens, R.C., Crystal structure of botulinum neurotoxin type A in complex with the cell surface co-receptor GT1b-insight into the toxin-neuron interaction (2008) PLoS Pathog., 4, pp. e1000129
  • Schallus, T., Jaeckh, C., Fehér, K., Palma, A.S., Liu, Y., Simpson, J.C., Mackeen, M., Muhle-Goll, C., Malectin: A novel carbohydrate-binding protein of the endoplasmic reticulum and a candidate player in the early steps of protein N-glycosylation (2008) Mol. Biol. Cell, 19, pp. 3404-3414
  • Hancock, M.K., Yammani, R.D., Dahms, N.M., Localization of the carbohydrate recognition sites of the insulinlike growth factor II/mannose 6-phosphate receptor to domains 3 and 9 of the extracytoplasmic region (2002) Journal of Biological Chemistry, 277 (49), pp. 47205-47212. , DOI 10.1074/jbc.M208534200
  • Schrag, J.D., Bergeron, J.J.M., Li, Y., Borisova, S., Hahn, M., Thomas, D.Y., Cygler, M., The structure of calnexin, an ER chaperone involved in quality control of protein folding (2001) Molecular Cell, 8 (3), pp. 633-644. , DOI 10.1016/S1097-2765(01)00318-5
  • DeLano, W.L., (2002) The PyMOL Molecular Graphics System, , Schrödinger, LLC, New York

Citas:

---------- APA ----------
Olson, L.J., Orsi, R., Alculumbre, S.G., Peterson, F.C., Stigliano, I.D., Parodi, A.J., D'Alessio, C.,..., Dahms, N.M. (2013) . Structure of the lectin mannose 6-phosphate receptor homology (MRH) domain of glucosidase II, an enzyme that regulates glycoprotein folding quality control in the endoplasmic reticulum. Journal of Biological Chemistry, 288(23), 16460-16475.
http://dx.doi.org/10.1074/jbc.M113.450239
---------- CHICAGO ----------
Olson, L.J., Orsi, R., Alculumbre, S.G., Peterson, F.C., Stigliano, I.D., Parodi, A.J., et al. "Structure of the lectin mannose 6-phosphate receptor homology (MRH) domain of glucosidase II, an enzyme that regulates glycoprotein folding quality control in the endoplasmic reticulum" . Journal of Biological Chemistry 288, no. 23 (2013) : 16460-16475.
http://dx.doi.org/10.1074/jbc.M113.450239
---------- MLA ----------
Olson, L.J., Orsi, R., Alculumbre, S.G., Peterson, F.C., Stigliano, I.D., Parodi, A.J., et al. "Structure of the lectin mannose 6-phosphate receptor homology (MRH) domain of glucosidase II, an enzyme that regulates glycoprotein folding quality control in the endoplasmic reticulum" . Journal of Biological Chemistry, vol. 288, no. 23, 2013, pp. 16460-16475.
http://dx.doi.org/10.1074/jbc.M113.450239
---------- VANCOUVER ----------
Olson, L.J., Orsi, R., Alculumbre, S.G., Peterson, F.C., Stigliano, I.D., Parodi, A.J., et al. Structure of the lectin mannose 6-phosphate receptor homology (MRH) domain of glucosidase II, an enzyme that regulates glycoprotein folding quality control in the endoplasmic reticulum. J. Biol. Chem. 2013;288(23):16460-16475.
http://dx.doi.org/10.1074/jbc.M113.450239