Quality control of glycoprotein folding and ERAD: the role of N-glycan handling, EDEM1 and OS-9

Protein N-glycosylation and quality control of protein folding as well as the connected ER-associated degradation of misfolded glycoproteins (ERAD) are not only evolutionary highly conserved but also functionally linked. It is now established that particular N-glycan structures which result from processing reactions by exo-glycosidases in the ER are of importance for glycoprotein folding and for ERAD. Thus, mono-glucosylated N-glycan intermediates harbor structural information which is important for promoting glycoprotein folding. On the other hand, specific mannose-trimmed N-glycans harbor structural information for routing misfolded glycoproteins to ERAD. In this review, we summarize current knowledge concerning the role played by glucosidases I and II, in concert with the bifunctional glucosyltransferase and calnexin/calreticulin in glycoprotein folding, the role of conventional ER mannosidase I in concert with the mannosidase EDEM1 in handling and routing of misfolded glycoproteins, and how the bifunctional OS-9 provides a link to the ER dislocon for degradation.

[1]  Ari Helenius,et al.  Glucose trimming and reglucosylation determine glycoprotein association with calnexin in the endoplasmic reticulum , 1995, Cell.

[2]  J. Roth.  Protein N-glycosylation along the secretory pathway: relationship to organelle topography and function, protein quality control, and cell interactions. , 2002, Chemical reviews.

[3]  Maurizio Molinari,et al.  Role of EDEM in the Release of Misfolded Glycoproteins from the Calnexin Cycle , 2003, Science.

[4]  T. Shaler,et al.  OS-9 and GRP94 deliver mutant α1-antitrypsin to the Hrd1–SEL1L ubiquitin ligase complex for ERAD , 2008, Nature Cell Biology.

[5]  M. R. Leach,et al.  Localization of the Lectin, ERp57 Binding, and Polypeptide Binding Sites of Calnexin and Calreticulin* , 2002, The Journal of Biological Chemistry.

[6]  Thomas Sommer,et al.  A complex of Yos9p and the HRD ligase integrates endoplasmic reticulum quality control into the degradation machinery , 2006, Nature Cell Biology.

[7]  L. Leloir,et al.  The role of polyprenol-bound saccharides as intermediates in glycoprotein synthesis in liver. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

[8]  W. Balch,et al.  Expanding proteostasis by membrane trafficking networks. , 2013, Cold Spring Harbor perspectives in biology.

[9]  M. Aebi,et al.  The dolichol pathway of N-linked glycosylation. , 1999, Biochimica et biophysica acta.

[10]  J. Roth,et al.  Basal autophagy is involved in the degradation of the ERAD component EDEM1 , 2009, Cellular and Molecular Life Sciences.

[11]  Jeffrey L. Brodsky,et al.  One step at a time: endoplasmic reticulum-associated degradation , 2008, Nature Reviews Molecular Cell Biology.

[12]  R. Gilmore,et al.  Cotranslational and posttranslocational N-glycosylation of proteins in the endoplasmic reticulum. , 2015, Seminars in cell & developmental biology.

[13]  T. Boller,et al.  CNE1, a Saccharomyces cerevisiae Homologue of the Genes Encoding Mammalian Calnexin and Calreticulin , 1993, Yeast.

[14]  P. Robbins,et al.  Glycoprotein biosynthesis. Rat liver microsomal glucosidases which process oligosaccharides. , 1979, The Journal of biological chemistry.

[15]  J. Weissman,et al.  Defining the glycan destruction signal for endoplasmic reticulum-associated degradation. , 2008, Molecular cell.

[16]  D. Y. Thomas,et al.  Saccharomyces cerevisiae CNE1 Encodes an Endoplasmic Reticulum (ER) Membrane Protein with Sequence Similarity to Calnexin and Calreticulin and Functions as a Constituent of the ER Quality Control Apparatus (*) , 1995, The Journal of Biological Chemistry.

[17]  D. Wolf,et al.  Ubiquitylation in the ERAD Pathway. , 2010, Sub-cellular biochemistry.

[18]  David B. Williams.  Beyond lectins: the calnexin/calreticulin chaperone system of the endoplasmic reticulum , 2006, Journal of Cell Science.

[19]  Jonathan S. Weissman,et al.  A Luminal Surveillance Complex that Selects Misfolded Glycoproteins for ER-Associated Degradation , 2006, Cell.

[20]  Zehavit Frenkel,et al.  Endoplasmic Reticulum-associated Degradation of Mammalian Glycoproteins Involves Sugar Chain Trimming to Man6–5GlcNAc2* , 2003, Journal of Biological Chemistry.

[21]  I. Wada,et al.  A novel ER α‐mannosidase‐like protein accelerates ER‐associated degradation , 2001 .

[22]  Xiaohua Xu,et al.  Expression and characterization of Saccharomyces cerevisiae Cne1p, a calnexin homologue. , 2004, Journal of biochemistry.

[23]  E. Bause,et al.  Purification and characterization of trimming glucosidase I from pig liver. , 1989, European journal of biochemistry.

[24]  S. Kornfeld,et al.  Assembly of asparagine-linked oligosaccharides. , 1985, Annual review of biochemistry.

[25]  D. Tessier,et al.  Cloning and characterization of mammalian UDP-glucose glycoprotein: glucosyltransferase and the development of a specific substrate for this enzyme. , 2000, Glycobiology.

[26]  Koichi Kato,et al.  The role of MRH domain-containing lectins in ERAD. , 2010, Glycobiology.

[27]  David Balchin,et al.  In vivo aspects of protein folding and quality control , 2016, Science.

[28]  N. Matsumoto,et al.  Human XTP3-B binds to alpha1-antitrypsin variant null(Hong Kong) via the C-terminal MRH domain in a glycan-dependent manner. , 2010, Glycobiology.

[29]  D. Hebert,et al.  EDEM1 recognition and delivery of misfolded proteins to the SEL1L-containing ERAD complex. , 2009, Molecular cell.

[30]  P. H. Cameron,et al.  Association of folding intermediates of glycoproteins with calnexin during protein maturation , 1993, Nature.

[31]  W. Balch,et al.  Expanding proteostasis by membrane trafficking networks. , 2013, Cold Spring Harbor perspectives in medicine.

[32]  J. Caramelo,et al.  Glucosidase II beta subunit modulates N-glycan trimming in fission yeasts and mammals. , 2009, Molecular biology of the cell.

[33]  D. Wirth,et al.  Proposal for a common oligosaccharide intermediate in the synthesis of membrane glycoproteins , 1977, Cell.

[34]  Aaron Ciechanover,et al.  The ubiquitin–proteasome pathway: on protein death and cell life , 1998, The EMBO journal.

[35]  M. Sousa,et al.  Recognition of the oligosaccharide and protein moieties of glycoproteins by the UDP-Glc:glycoprotein glucosyltransferase. , 1992, Biochemistry.

[36]  Koichi Kato,et al.  Endoplasmic reticulum lectin XTP3‐B inhibits endoplasmic reticulum‐associated degradation of a misfolded α1‐antitrypsin variant , 2013, The FEBS journal.

[37]  M. Brenner,et al.  Endoplasmic reticulum resident protein of 90 kilodaltons associates with the T- and B-cell antigen receptors and major histocompatibility complex antigens during their assembly. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[38]  S. Nishikawa,et al.  Roles of Protein-disulfide Isomerase-mediated Disulfide Bond Formation of Yeast Mnl1p in Endoplasmic Reticulum-associated Degradation , 2009, Journal of Biological Chemistry.

[39]  E. Bieberich,et al.  Cloning and expression of glucosidase I from human hippocampus. , 1995, European journal of biochemistry.

[40]  R. Sternglanz,et al.  PNG1, a Yeast Gene Encoding a Highly Conserved Peptide:N-Glycanase , 2000, The Journal of cell biology.

[41]  P. H. Cameron,et al.  SSR alpha and associated calnexin are major calcium binding proteins of the endoplasmic reticulum membrane. , 1991, The Journal of biological chemistry.

[42]  Wolfram Tempel,et al.  Mechanism of Class 1 (Glycosylhydrolase Family 47) α-Mannosidases Involved in N-Glycan Processing and Endoplasmic Reticulum Quality Control* , 2005, Journal of Biological Chemistry.

[43]  A. Helenius,et al.  Transient, lectin-like association of calreticulin with folding intermediates of cellular and viral glycoproteins. , 1995, Molecular biology of the cell.

[44]  K Burns,et al.  Molecular cloning of the high affinity calcium-binding protein (calreticulin) of skeletal muscle sarcoplasmic reticulum. , 1989, The Journal of biological chemistry.

[45]  S. Kornfeld,et al.  The synthesis of complex-type oligosaccharides. I. Structure of the lipid-linked oligosaccharide precursor of the complex-type oligosaccharides of the vesicular stomatitis virus G protein. , 1978, The Journal of biological chemistry.

[46]  R. Spiro,et al.  Lipid-saccharide intermediates in glycoprotein biosynthesis. I. Formation of an oligosaccharide-lipid by thyroid slices and evaluation of its role in protein glycosylation. , 1976, The Journal of biological chemistry.

[47]  R. Kornfeld,et al.  Evidence for an alpha-mannosidase in endoplasmic reticulum of rat liver. , 1983, The Journal of biological chemistry.

[48]  R. Ugalde,et al.  Microsomal glucosidases of rat liver. Partial purification and inhibition by disaccharides. , 2005, European journal of biochemistry.

[49]  U. Dubach,et al.  Isolation of a homogeneous glucosidase II from pig kidney microsomes. , 1984, European journal of biochemistry.

[50]  D. Wolf,et al.  A genome‐wide screen identifies Yos9p as essential for ER‐associated degradation of glycoproteins , 2004, FEBS letters.

[51]  M. Brenner,et al.  Retention of unassembled components of integral membrane proteins by calnexin. , 1994, Science.

[52]  J. Simons,et al.  Endoplasmic Reticulum Glucosidase II Is Composed of a Catalytic Subunit, Conserved from Yeast to Mammals, and a Tightly Bound Noncatalytic HDEL-containing Subunit* , 1996, The Journal of Biological Chemistry.

[53]  N. Kawasaki,et al.  The sugar-binding ability of human OS-9 and its involvement in ER-associated degradation. , 2010, Glycobiology.

[54]  I. Wada,et al.  SEL1L Protein Critically Determines the Stability of the HRD1-SEL1L Endoplasmic Reticulum-associated Degradation (ERAD) Complex to Optimize the Degradation Kinetics of ERAD Substrates* , 2011, The Journal of Biological Chemistry.

[55]  M. Molinari,et al.  EDEM1 regulates ER-associated degradation by accelerating de-mannosylation of folding-defective polypeptides and by inhibiting their covalent aggregation. , 2006, Biochemical and biophysical research communications.

[56]  H. Söling,et al.  Definition of the Lectin-like Properties of the Molecular Chaperone, Calreticulin, and Demonstration of Its Copurification with Endomannosidase from Rat Liver Golgi (*) , 1996, The Journal of Biological Chemistry.

[57]  Tom A. Rapoport,et al.  Distinct Ubiquitin-Ligase Complexes Define Convergent Pathways for the Degradation of ER Proteins , 2006, Cell.

[58]  A. Parodi,et al.  Immunolocalization of UDP-glucose:glycoprotein glucosyltransferase indicates involvement of pre-Golgi intermediates in protein quality control , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[59]  A. Helenius,et al.  Roles of N-linked glycans in the endoplasmic reticulum. , 2004, Annual review of biochemistry.

[60]  P. van Kerkhof,et al.  Glucosidase II, a protein of the endoplasmic reticulum with high mannose oligosaccharide chains and a rapid turnover. , 1987, The Journal of biological chemistry.

[61]  A. Herscovics,et al.  Characterization of a specific alpha-mannosidase involved in oligosaccharide processing in Saccharomyces cerevisiae. , 1985, The Journal of biological chemistry.

[62]  Koichi Kato,et al.  EDEM1 accelerates the trimming of alpha1,2-linked mannose on the C branch of N-glycans. , 2010, Glycobiology.

[63]  D. Wolf,et al.  ER Degradation of a Misfolded Luminal Protein by the Cytosolic Ubiquitin-Proteasome Pathway , 1996, Science.

[64]  U. Hellman,et al.  A new stress protein: synthesis of Schizosaccharomyces pombe UDP–Glc:glycoprotein glucosyltransferase mRNA is induced by stress conditions but the enzyme is not essential for cell viability. , 1996, The EMBO journal.

[65]  A. Parodi,et al.  Genetic Evidence for the Heterodimeric Structure of Glucosidase II , 1999, The Journal of Biological Chemistry.

[66]  R. Ménard,et al.  The heterodimeric structure of glucosidase II is required for its activity, solubility, and localization in vivo. , 2000, Glycobiology.

[67]  E. Bause,et al.  The α- and β-subunits are required for expression of catalytic activity in the hetero-dimeric glucosidase II complex from human liver , 2000 .

[68]  Woong Kim,et al.  Yos9p detects and targets misfolded glycoproteins for ER-associated degradation. , 2005, Molecular cell.

[69]  A. Herscovics,et al.  Inhibition of N-linked complex oligosaccharide formation by 1-deoxynojirimycin, an inhibitor of processing glucosidases. , 1982, The Journal of biological chemistry.

[70]  A. Parodi,et al.  Retention of glucose units added by the UDP-GLC:glycoprotein glucosyltransferase delays exit of glycoproteins from the endoplasmic reticulum , 1995, The Journal of cell biology.

[71]  M. Michalak,et al.  Oligosaccharide binding characteristics of the molecular chaperones calnexin and calreticulin. , 1998, Biochemistry.

[72]  Jennifer Apodaca,et al.  The Png1–Rad23 complex regulates glycoprotein turnover , 2006, The Journal of cell biology.

[73]  T. Rapoport,et al.  A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol , 2004, Nature.

[74]  A. Herscovics,et al.  Importance of glycosidases in mammalian glycoprotein biosynthesis. , 1999, Biochimica et biophysica acta.

[75]  E. Bause,et al.  Characterization of calf liver glucosidase I and its inhibition by basic sugar analogs. , 1986, Archives of biochemistry and biophysics.

[76]  P. Robbins,et al.  Effects of N-glycan precursor length diversity on quality control of protein folding and on protein glycosylation. , 2015, Seminars in cell & developmental biology.

[77]  M. Guerin,et al.  The UDP-glucose:Glycoprotein Glucosyltransferase Is Organized in at Least Two Tightly Bound Domains from Yeast to Mammals* , 2003, Journal of Biological Chemistry.

[78]  A. Herscovics,et al.  Glycosidases of the asparagine-linked oligosaccharide processing pathway. , 1994, Glycobiology.

[79]  P. Calvo,et al.  Glucosidase II from rat liver microsomes. Kinetic model for binding and hydrolysis. , 1991, The Biochemical journal.

[80]  L. Liscum,et al.  The use of 1-deoxymannojirimycin to evaluate the role of various alpha-mannosidases in oligosaccharide processing in intact cells. , 1986, The Journal of biological chemistry.

[81]  J. Elting,et al.  Characterization of a glucosidase involved in an initial step in the processing of oligosaccharide chains. , 1980, The Journal of biological chemistry.

[82]  S. Ōmura,et al.  Novel Aspects of Degradation of T Cell Receptor Subunits from the Endoplasmic Reticulum (ER) in T Cells: Importance of Oligosaccharide Processing, Ubiquitination, and Proteasome-dependent Removal from ER Membranes , 1998, The Journal of experimental medicine.

[83]  G. Lederkremer,et al.  Evidence that transient glucosylation of protein-linked Man9GlcNAc2, Man8GlcNAc2, and Man7GlcNAc2 occurs in rat liver and Phaseolus vulgaris cells. , 1984, The Journal of biological chemistry.

[84]  Yoshiki Yamaguchi,et al.  Structural basis for oligosaccharide recognition of misfolded glycoproteins by OS-9 in ER-associated degradation. , 2010, Molecular cell.

[85]  G. Lederkremer,et al.  Transient glucosylation of protein-bound Man9GlcNAc2, Man8GlcNAc2, and Man7GlcNAc2 in calf thyroid cells. A possible recognition signal in the processing of glycoproteins. , 1983, The Journal of biological chemistry.

[86]  K. Colley,et al.  Sialylation of N-glycans: mechanism, cellular compartmentalization and function , 2016, Histochemistry and Cell Biology.

[87]  A. Helenius,et al.  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.

[88]  M. Brenner,et al.  Interaction with newly synthesized and retained proteins in the endoplasmic reticulum suggests a chaperone function for human integral membrane protein IP90 (calnexin). , 1993, The Journal of biological chemistry.

[89]  W. Lennarz,et al.  The molecular basis of coupling of translocation and N-glycosylation. , 2006, Trends in biochemical sciences.

[90]  David Y. Thomas,et al.  Htm1p, a mannosidase‐like protein, is involved in glycoprotein degradation in yeast , 2001, EMBO reports.

[91]  Thomas Sommer,et al.  Htm1 protein generates the N-glycan signal for glycoprotein degradation in the endoplasmic reticulum , 2009, The Journal of cell biology.

[92]  J. Cho,et al.  ERADication of EDEM1 occurs by selective autophagy and requires deglycosylation by cytoplasmic peptide N-glycanase , 2014, Histochemistry and Cell Biology.

[93]  A. Imberty,et al.  Structure of Penicillium citrinum α1,2-Mannosidase Reveals the Basis for Differences in Specificity of the Endoplasmic Reticulum and Golgi Class I Enzymes* , 2002, The Journal of Biological Chemistry.

[94]  T. Sommer,et al.  ERAD: the long road to destruction , 2005, Nature Cell Biology.

[95]  J. Roth,et al.  Expression of a cDNA encoding the glucose trimming enzyme glucosidase II in CHO cells and molecular characterization of the enzyme deficiency in a mutant mouse lymphoma cell line. , 1997, Glycobiology.

[96]  H. Ploegh,et al.  Multiprotein complexes that link dislocation, ubiquitination, and extraction of misfolded proteins from the endoplasmic reticulum membrane. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[97]  R. Spiro,et al.  Endoplasmic reticulum kifunensine-resistant alpha-mannosidase is enzymatically and immunologically related to the cytosolic alpha-mannosidase. , 1996, Archives of biochemistry and biophysics.

[98]  C. Gabel,et al.  Selective retention of monoglucosylated high mannose oligosaccharides by a class of mutant vesicular stomatitis virus G proteins , 1989, The Journal of cell biology.

[99]  U. Hellman,et al.  Purification to homogeneity of UDP-glucose:glycoprotein glucosyltransferase from Schizosaccharomyces pombe and apparent absence of the enzyme fro Saccharomyces cerevisiae. , 1994, The Journal of biological chemistry.

[100]  G. Fink,et al.  Proteinase C (carboxypeptidase Y) mutant of yeast , 1975, Journal of bacteriology.

[101]  J. Bonifacino,et al.  Ubiquitin and the control of protein fate in the secretory and endocytic pathways. , 1998, Annual review of cell and developmental biology.

[102]  A. Parodi,et al.  The UDP-Glc:glycoprotein glucosyltransferase is a soluble protein of the endoplasmic reticulum. , 1991, Glycobiology.

[103]  V. Kidd,et al.  A frameshift mutation results in a truncated alpha 1-antitrypsin that is retained within the rough endoplasmic reticulum. , 1988, The Journal of biological chemistry.

[104]  R. Morimoto,et al.  The biology of proteostasis in aging and disease. , 2015, Annual review of biochemistry.

[105]  I. Wada,et al.  Enhancement of Endoplasmic Reticulum (ER) Degradation of Misfolded Null Hong Kong α1-Antitrypsin by Human ER Mannosidase I* , 2003, Journal of Biological Chemistry.

[106]  S. Kornfeld,et al.  Partial purification and characterization of the glucosidases involved in the processing of asparagine-linked oligosaccharides. , 1980, Archives of biochemistry and biophysics.

[107]  D. Wolf,et al.  CPY* and the power of yeast genetics in the elucidation of quality control and associated protein degradation of the endoplasmic reticulum. , 2005, Current topics in microbiology and immunology.

[108]  Koichi Kato,et al.  EDEM1 accelerates the trimming of alpha1,2-linked mannose on the C branch of N-glycans. , 2010, Glycobiology.

[109]  Pedro Carvalho,et al.  A complex of Pdi1p and the mannosidase Htm1p initiates clearance of unfolded glycoproteins from the endoplasmic reticulum. , 2011, Molecular cell.

[110]  R. Riek,et al.  NMR structure of the calreticulin P-domain , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[111]  M. Hagiwara,et al.  Posttranscriptional Regulation of Glycoprotein Quality Control in the Endoplasmic Reticulum Is Controlled by the E2 Ub-Conjugating Enzyme UBC6e. , 2016, Molecular cell.

[112]  S. Nishikawa,et al.  Mnl1p, an α-Mannosidase-like Protein in YeastSaccharomyces cerevisiae, Is Required for Endoplasmic Reticulum-associated Degradation of Glycoproteins* , 2001, The Journal of Biological Chemistry.

[113]  S. Baksh,et al.  Expression of calreticulin in Escherichia coli and identification of its Ca2+ binding domains. , 1991, The Journal of biological chemistry.

[114]  J. Roth,et al.  Two isoforms of trimming glucosidase II exist in mammalian tissues and cell lines but not in yeast and insect cells. , 2001, Biochemical and biophysical research communications.

[115]  Daniel J. Kelleher,et al.  The evolution of N-glycan-dependent endoplasmic reticulum quality control factors for glycoprotein folding and degradation , 2007, Proceedings of the National Academy of Sciences.

[116]  H. Ploegh,et al.  SEL1L nucleates a protein complex required for dislocation of misfolded glycoproteins , 2008, Proceedings of the National Academy of Sciences.

[117]  A. Parodi,et al.  Glucosylation of glycoproteins by mammalian, plant, fungal, and trypanosomatid protozoa microsomal membranes. , 1989, Biochemistry.

[118]  M. Aebi,et al.  Genetic tailoring of N-linked oligosaccharides: the role of glucose residues in glycoprotein processing of Saccharomyces cerevisiae in vivo. , 1998, Glycobiology.

[119]  Yan Liu,et al.  Oligosaccharide Modification in the Early Secretory Pathway Directs the Selection of a Misfolded Glycoprotein for Degradation by the Proteasome* , 1999, The Journal of Biological Chemistry.

[120]  J. Weissman,et al.  Exploration of the topological requirements of ERAD identifies Yos9p as a lectin sensor of misfolded glycoproteins in the ER lumen. , 2005, Molecular cell.

[121]  D. Hebert,et al.  EDEM1 reveals a quality control vesicular transport pathway out of the endoplasmic reticulum not involving the COPII exit sites , 2007, Proceedings of the National Academy of Sciences.

[122]  M. Nita-Lazar,et al.  Yos9 protein is essential for degradation of misfolded glycoproteins and may function as lectin in ERAD. , 2005, Molecular cell.

[123]  E. Bause,et al.  Affinity Purification and Characterization of Glucosidase II from Pig Liver , 1997, Biological chemistry.

[124]  R. Spiro,et al.  Endoplasmic Reticulum Kifunensine-Resistant α-Mannosidase Is Enzymatically and Immunologically Related to the Cytosolic α-Mannosidase , 1996 .

[125]  K. Moremen,et al.  Human EDEM2, a novel homolog of family 47 glycosidases, is involved in ER-associated degradation of glycoproteins. , 2005, Glycobiology.

[126]  M R Jackson,et al.  The Molecular Chaperone Calnexin Binds Glc1Man9GlcNAc2 Oligosaccharide as an Initial Step in Recognizing Unfolded Glycoproteins (*) , 1995, The Journal of Biological Chemistry.

[127]  J. Cho,et al.  Protein N-glycosylation, protein folding, and protein quality control , 2010, Molecules and cells.

[128]  Douglas,et al.  Purification and characterization of glucosidase II, an endoplasmic reticulum hydrolase involved in glycoprotein biosynthesis. , 1982, The Journal of biological chemistry.

[129]  Koichi Kato,et al.  EDEM2 initiates mammalian glycoprotein ERAD by catalyzing the first mannose trimming step , 2014, The Journal of cell biology.

[130]  A. Corfield,et al.  Eukaryotic protein glycosylation: a primer for histochemists and cell biologists , 2016, Histochemistry and Cell Biology.

[131]  K. Moremen,et al.  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 Biosynthesis* , 1999, The Journal of Biological Chemistry.

[132]  F. Martiniuk,et al.  Identity of neutral alpha-glucosidase AB and the glycoprotein processing enzyme glucosidase II. Biochemical and genetic studies. , 1985, The Journal of biological chemistry.

[133]  Maurizio Molinari,et al.  A Novel Stress-induced EDEM Variant Regulating Endoplasmic Reticulum-associated Glycoprotein Degradation* , 2005, Journal of Biological Chemistry.

[134]  Wei R. Chen,et al.  The Number and Location of Glycans on Influenza Hemagglutinin Determine Folding and Association with Calnexin and Calreticulin , 1997, The Journal of cell biology.

[135]  A. Herscovics.  Processing glycosidases of Saccharomyces cerevisiae. , 1999, Biochimica et biophysica acta.

[136]  The unfolded protein response in a dolichyl phosphate mannose-deficient Chinese hamster ovary cell line points out the key role of a demannosylation step in the quality-control mechanism of N-glycoproteins. , 2002 .

[137]  J. Roth,et al.  Immunolocalization of the oligosaccharide trimming enzyme glucosidase II , 1986, The Journal of cell biology.

[138]  A. Herscovics,et al.  Cloning and expression of a specific human alpha 1,2-mannosidase that trims Man9GlcNAc2 to Man8GlcNAc2 isomer B during N-glycan biosynthesis. , 1999, Glycobiology.

[139]  Koichi Kato,et al.  Human OS-9, a Lectin Required for Glycoprotein Endoplasmic Reticulum-associated Degradation, Recognizes Mannose-trimmed N-Glycans* , 2009, The Journal of Biological Chemistry.

[140]  J. Hoseki,et al.  Structural basis of an ERAD pathway mediated by the ER-resident protein disulfide reductase ERdj5. , 2011, Molecular cell.

[141]  E. Bause,et al.  Purification by affinity chromatography of glucosidase I, an endoplasmic reticulum hydrolase involved in the processing of asparagine-linked oligosaccharides. , 1984, European journal of biochemistry.

[142]  Hangil Park,et al.  Cytoplasmic peptide:N‐glycanase (PNGase) in eukaryotic cells: occurrence, primary structure, and potential functions , 2002, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[143]  Yan A. Su,et al.  Complete sequence analysis of a gene (OS‐9) ubiquitously expressed in human tissues and amplified in sarcomas , 1996, Molecular carcinogenesis.

[144]  P. Robbins,et al.  Synthesis and processing of protein-linked oligosaccharides in vivo. , 1979, The Journal of biological chemistry.

[145]  K. Mori,et al.  SEL1L is required for endoplasmic reticulum-associated degradation of misfolded luminal proteins but not transmembrane proteins in chicken DT40 cell line. , 2011, Cell structure and function.

[146]  J. Weissman,et al.  Road to Ruin: Targeting Proteins for Degradation in the Endoplasmic Reticulum , 2011, Science.

[147]  S. Kornfeld,et al.  The synthesis of complex-type oligosaccharides. II. Characterization of the processing intermediates in the synthesis of the complex oligosaccharide units of the vesicular stomatitis virus G protein. , 1978, The Journal of biological chemistry.

[148]  D. Y. Thomas,et al.  The Structure of calnexin, an ER chaperone involved in quality control of protein folding. , 2001, Molecular cell.

[149]  G. Kozlov,et al.  Structural basis of carbohydrate recognition by calreticulin , 2011 .

[150]  H. Ploegh,et al.  A membrane protein required for dislocation of misfolded proteins from the ER , 2004, Nature.

[151]  A. Mir,et al.  N-glycan structure of a short-lived variant of ribophorin I expressed in the MadIA214 glycosylation-defective cell line reveals the role of a mannosidase that is not ER mannosidase I in the process of glycoprotein degradation. , 2001, Glycobiology.

[152]  I. Wada,et al.  Human XTP3-B Forms an Endoplasmic Reticulum Quality Control Scaffold with the HRD1-SEL1L Ubiquitin Ligase Complex and BiP* , 2008, Journal of Biological Chemistry.

[153]  I. Wada,et al.  EDEM3, a Soluble EDEM Homolog, Enhances Glycoprotein Endoplasmic Reticulum-associated Degradation and Mannose Trimming* , 2006, Journal of Biological Chemistry.

[154]  M. Pavelka,et al.  Functional Ultrastructure: Atlas of Tissue Biology and Pathology , 2005 .

[155]  M. Yamada,et al.  Cloning and characterization of three isoforms of OS-9 cDNA and expression of the OS-9 gene in various human tumor cell lines. , 1998, Journal of biochemistry.

[156]  A. Helenius,et al.  Chaperone selection during glycoprotein translocation into the endoplasmic reticulum. , 2000, Science.

[157]  Kato,et al.  Sugar-binding activity of the MRH domain in the ER α-glucosidase II β subunit is important for efficient glucose trimming , 2009 .

[158]  L. Leloir,et al.  The role of lipid intermediates in the glycosylation of proteins in the eucaryotic cell. , 1979, Biochimica et biophysica acta.

[159]  F. Seela,et al.  By N-Glycosylation , 2004 .

[160]  Douglas J Taatjes,et al.  In focus in HCB , 2021, Histochemistry and Cell Biology.

[161]  L. Rizzolo,et al.  Post-translational protein modification in the endoplasmic reticulum. Demonstration of fatty acylase and deoxymannojirimycin-sensitive alpha-mannosidase activities. , 1988, The Journal of biological chemistry.

[162]  M. Aebi,et al.  Degradation of Misfolded Endoplasmic Reticulum Glycoproteins in Saccharomyces cerevisiae Is Determined by a Specific Oligosaccharide Structure , 1998, The Journal of cell biology.

[163]  I. Wada,et al.  EDEM As an Acceptor of Terminally Misfolded Glycoproteins Released from Calnexin , 2003, Science.

[164]  R. Spiro,et al.  Lipid-saccharide intermediates in glycoprotein biosynthesis. II. Studies on the structure of an oligosaccharide-lipid from thyroid. , 1976, The Journal of biological chemistry.

[165]  J. Hoseki,et al.  ERdj5 Is Required as a Disulfide Reductase for Degradation of Misfolded Proteins in the ER , 2008, Science.

[166]  W. Lennarz,et al.  The role of polyprenol-linked sugars in glycoprotein synthesis. , 1976, Annual review of biochemistry.

[167]  C. Parker,et al.  Drosophila UDP‐glucose:glycoprotein glucosyltransferase: sequence and characterization of an enzyme that distinguishes between denatured and native proteins. , 1995, The EMBO journal.

[168]  P. Howell,et al.  Crystal structure of a class I α1,2‐mannosidase involved in N‐glycan processing and endoplasmic reticulum quality control , 2000, The EMBO journal.

[169]  H. Ploegh,et al.  SEL1L, the homologue of yeast Hrd3p, is involved in protein dislocation from the mammalian ER , 2006, The Journal of cell biology.