Setting the standards: quality control in the secretory pathway.

A variety of quality control mechanisms operate in the endoplasmic reticulum and in downstream compartments of the secretory pathway to ensure the fidelity and regulation of protein expression during cell life and differentiation. As a rule, only proteins that pass a stringent selection process are transported to their target organelles and compartments. If proper maturation fails, the aberrant products are degraded. Quality control improves folding efficiency by retaining proteins in the special folding environment of the endoplasmic reticulum, and it prevents harmful effects that could be caused by the deployment of incompletely folded or assembled proteins.

[1]  A. Helenius,et al.  Glycoproteins form mixed disulphides with oxidoreductases during folding in living cells , 1999, Nature.

[2]  H. Andersson,et al.  The lectin ERGIC-53 is a cargo transport receptor for glycoproteins , 1999, Nature Cell Biology.

[3]  Y. Ihara,et al.  Calnexin discriminates between protein conformational states and functions as a molecular chaperone in vitro. , 1999, Molecular cell.

[4]  D. Y. Thomas,et al.  Protein folding in a specialized compartment: the endoplasmic reticulum. , 1999, Structure.

[5]  S. High,et al.  ERp57 functions as a subunit of specific complexes formed with the ER lectins calreticulin and calnexin. , 1999, Molecular biology of the cell.

[6]  I. Mellman,et al.  Bulk Flow Redux? , 1999, Cell.

[7]  T. Rapoport,et al.  Interaction of BiP with the J-domain of the Sec63p Component of the Endoplasmic Reticulum Protein Translocation Complex* , 1999, The Journal of Biological Chemistry.

[8]  R. Dwek,et al.  Glycoproteins: glycan presentation and protein-fold stability. , 1999, Structure.

[9]  M. Totsuka,et al.  Accelerated secretion of mutant beta-lactoglobulin in Saccharomyces cerevisiae resulting from a single amino acid substitution. , 1999, Biochimica et biophysica acta.

[10]  J. Slot,et al.  Vesicular Tubular Clusters between the ER and Golgi Mediate Concentration of Soluble Secretory Proteins by Exclusion from COPI-Coated Vesicles , 1999, Cell.

[11]  J. Riordan,et al.  Removal of multiple arginine-framed trafficking signals overcomes misprocessing of delta F508 CFTR present in most patients with cystic fibrosis. , 1999, Molecular cell.

[12]  R. Plemper,et al.  Retrograde protein translocation: ERADication of secretory proteins in health and disease. , 1999, Trends in biochemical sciences.

[13]  William E. Balch,et al.  Integration of endoplasmic reticulum signaling in health and disease , 1999, Nature Medicine.

[14]  M. Carlson,et al.  Efficient export of the glucose transporter Hxt1p from the endoplasmic reticulum requires Gsf2p. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[15]  A. Helenius,et al.  Glycoprotein reglucosylation and nucleotide sugar utilization in the secretory pathway: identification of a nucleoside diphosphatase in the endoplasmic reticulum , 1999, The EMBO journal.

[16]  Á. Durán,et al.  Chs7p, a New Protein Involved in the Control of Protein Export from the Endoplasmic Reticulum that Is Specifically Engaged in the Regulation of Chitin Synthesis in Saccharomyces cerevisiae , 1999, The Journal of cell biology.

[17]  I. Greenwald,et al.  p24 Proteins and Quality Control of LIN-12 and GLP-1 Trafficking in Caenorhabditis elegans , 1999, The Journal of cell biology.

[18]  M. Marzioch,et al.  Erp1p and Erp2p, partners for Emp24p and Erv25p in a yeast p24 complex. , 1999, Molecular biology of the cell.

[19]  N. Bulleid,et al.  Intracellular Retention of Procollagen within the Endoplasmic Reticulum Is Mediated by Prolyl 4-Hydroxylase* , 1999, The Journal of Biological Chemistry.

[20]  H. Andersson,et al.  Protein Targeting to Endoplasmic Reticulum by Dilysine Signals Involves Direct Retention in Addition to Retrieval* , 1999, The Journal of Biological Chemistry.

[21]  C. Kaiser,et al.  LST1 Is a SEC24 Homologue Used for Selective Export of the Plasma Membrane ATPase from the Endoplasmic Reticulum , 1999, The Journal of cell biology.

[22]  Christopher H. Tipper,et al.  Yeast Mutants Affecting Possible Quality Control of Plasma Membrane Proteins , 1999, Molecular and Cellular Biology.

[23]  Roger A. Davis,et al.  Chinese Hamster Ovary Cells Require the Coexpression of Microsomal Triglyceride Transfer Protein and Cholesterol 7α-Hydroxylase for the Assembly and Secretion of Apolipoprotein B-containing Lipoproteins* , 1999, The Journal of Biological Chemistry.

[24]  P. Walter,et al.  Two endoplasmic reticulum (ER) membrane proteins that facilitate ER-to-Golgi transport of glycosylphosphatidylinositol-anchored proteins. , 1999, Molecular biology of the cell.

[25]  F. Melchers Fit for life in the immune system? Surrogate L chain tests H chains that test L chains. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[26]  D. Cyr,et al.  The Hdj‐2/Hsc70 chaperone pair facilitates early steps in CFTR biogenesis , 1999, The EMBO journal.

[27]  A. Helenius,et al.  Trimming and Readdition of Glucose to N-Linked Oligosaccharides Determines Calnexin Association of a Substrate Glycoprotein in Living Cells* , 1999, The Journal of Biological Chemistry.

[28]  Y. Jan,et al.  A New ER Trafficking Signal Regulates the Subunit Stoichiometry of Plasma Membrane KATP Channels , 1999, Neuron.

[29]  S. Emr,et al.  Ligand recognition and domain structure of Vps10p, a vacuolar protein sorting receptor in Saccharomyces cerevisiae. , 1999, European journal of biochemistry.

[30]  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.

[31]  Yih-Tai Chen,et al.  Coupling Assembly of the E-Cadherin/β-Catenin Complex to Efficient Endoplasmic Reticulum Exit and Basal-lateral Membrane Targeting of E-Cadherin in Polarized MDCK Cells , 1999, The Journal of cell biology.

[32]  J. Brodsky,et al.  The Requirement for Molecular Chaperones during Endoplasmic Reticulum-associated Protein Degradation Demonstrates That Protein Export and Import Are Mechanistically Distinct* , 1999, The Journal of Biological Chemistry.

[33]  A. J. Parodi,et al.  Reglucosylation of glycoproteins and quality control of glycoprotein folding in the endoplasmic reticulum of yeast cells. , 1999, Biochimica et biophysica acta.

[34]  J. Riordan,et al.  Perturbation of Hsp90 interaction with nascent CFTR prevents its maturation and accelerates its degradation by the proteasome , 1998, The EMBO journal.

[35]  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.

[36]  C. Barlowe,et al.  Transport of Axl2p Depends on Erv14p, an ER–Vesicle Protein Related to the Drosophila cornichon Gene Product , 1998, The Journal of cell biology.

[37]  K D Wittrup,et al.  Protein Folding Stability Can Determine the Efficiency of Escape from Endoplasmic Reticulum Quality Control* , 1998, The Journal of Biological Chemistry.

[38]  T. Stevens,et al.  Assembly of the Yeast Vacuolar H+-ATPase Occurs in the Endoplasmic Reticulum and Requires a Vma12p/Vma22p Assembly Complex , 1998, The Journal of cell biology.

[39]  A. Gilbert,et al.  Delta F508 CFTR localizes in the endoplasmic reticulum-Golgi intermediate compartment in cystic fibrosis cells. , 1998, Experimental cell research.

[40]  R B Corley,et al.  Assembly, sorting, and exit of oligomeric proteins from the endoplasmic reticulum , 1998, BioEssays : news and reviews in molecular, cellular and developmental biology.

[41]  A. C. van der Spoel,et al.  Transport of human lysosomal neuraminidase to mature lysosomes requires protective protein/cathepsin A , 1998, The EMBO journal.

[42]  K D Wittrup,et al.  Secretion efficiency in Saccharomyces cerevisiae of bovine pancreatic trypsin inhibitor mutants lacking disulfide bonds is correlated with thermodynamic stability. , 1998, Biochemistry.

[43]  K. Nagata Expression and function of heat shock protein 47: a collagen-specific molecular chaperone in the endoplasmic reticulum. , 1998, Matrix biology : journal of the International Society for Matrix Biology.

[44]  W. Annaert,et al.  Export of Cellubrevin from the Endoplasmic Reticulum Is Controlled by BAP31 , 1997, The Journal of cell biology.

[45]  A. Helenius,et al.  Quality control in the secretory pathway: the role of calreticulin, calnexin and BiP in the retention of glycoproteins with C-terminal truncations. , 1997, Molecular biology of the cell.

[46]  R. Tampé,et al.  A critical role for tapasin in the assembly and function of multimeric MHC class I-TAP complexes. , 1997, Science.

[47]  R. Plemper,et al.  Mutant analysis links the translocon and BiP to retrograde protein transport for ER degradation , 1997, Nature.

[48]  R. Schekman,et al.  Sec61p mediates export of a misfolded secretory protein from the endoplasmic reticulum to the cytosol for degradation , 1997, The EMBO journal.

[49]  R. Schekman,et al.  COPII and secretory cargo capture into transport vesicles. , 1997, Current opinion in cell biology.

[50]  J. Brodsky,et al.  ER-associated and proteasomemediated protein degradation: how two topologically restricted events came together. , 1997, Trends in cell biology.

[51]  R. Kopito ER Quality Control: The Cytoplasmic Connection , 1997, Cell.

[52]  A. Helenius,et al.  Interactions between Newly Synthesized Glycoproteins, Calnexin and a Network of Resident Chaperones in the Endoplasmic Reticulum , 1997, The Journal of cell biology.

[53]  S. Kellokumpu,et al.  Protein Disulfide Isomerase and Newly Synthesized Procollagen Chains form Higher-order Structures in the Lumen of the Endoplasmic Reticulum* , 1997, The Journal of Biological Chemistry.

[54]  T. Rapoport,et al.  Sec6l-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction , 1996, Nature.

[55]  C. Kaiser,et al.  A pathway for targeting soluble misfolded proteins to the yeast vacuole , 1996, The Journal of cell biology.

[56]  D. Perlmutter Alpha-1-antitrypsin deficiency: biochemistry and clinical manifestations. , 1996, Annals of medicine.

[57]  M. Knop,et al.  N‐glycosylation affects endoplasmic reticulum degradation of a mutated derivative of carboxypeptidase yscY in yeast , 1996, Yeast.

[58]  F. Koning,et al.  Isolation of an immunodominant viral peptide that is endogenously bound to the stress protein GP96/GRP94. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[59]  T. Stevens,et al.  Vps10p cycles between the late-Golgi and prevacuolar compartments in its function as the sorting receptor for multiple yeast vacuolar hydrolases , 1996, The Journal of cell biology.

[60]  P. Cresswell Invariant Chain Structure and MHC Class II Function , 1996, Cell.

[61]  M. Sousa,et al.  The molecular basis for the recognition of misfolded glycoproteins by the UDP‐Glc:glycoprotein glucosyltransferase. , 1995, The EMBO journal.

[62]  R. Swank,et al.  The -Glucuronidase Propeptide Contains a Serpin-related Octamer Necessary for Complex Formation with Egasyn Esterase and for Retention within the Endoplasmic Reticulum (*) , 1995, The Journal of Biological Chemistry.

[63]  J. Bonifacino,et al.  Transient Aggregation of Major Histocompatibility Complex Class II Chains during Assembly in Normal Spleen Cells (*) , 1995, The Journal of Biological Chemistry.

[64]  P. Cosson,et al.  Steric masking of a dilysine endoplasmic reticulum retention motif during assembly of the human high affinity receptor for immunoglobulin E , 1995, The Journal of cell biology.

[65]  H. Geuze,et al.  39 kDa receptor‐associated protein is an ER resident protein and molecular chaperone for LDL receptor‐related protein. , 1995, The EMBO journal.

[66]  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.

[67]  M. Knittler,et al.  Molecular chaperones involved in protein degradation in the endoplasmic reticulum: quantitative interaction of the heat shock cognate protein BiP with partially folded immunoglobulin light chains that are degraded in the endoplasmic reticulum. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[68]  W. Diekmann,et al.  Retention and retrieval: both mechanisms cooperate to maintain calreticulin in the endoplasmic reticulum. , 1994, Journal of cell science.

[69]  C. Zuker,et al.  The cyclophilin homolog NinaA functions as a chaperone, forming a stable complex in vivo with its protein target rhodopsin. , 1994, The EMBO journal.

[70]  D. Samols,et al.  Two carboxylesterases bind C-reactive protein within the endoplasmic reticulum and regulate its secretion during the acute phase response. , 1994, The Journal of biological chemistry.

[71]  T Nilsson,et al.  Retention and retrieval in the endoplasmic reticulum and the Golgi apparatus , 1994, Current Opinion in Cell Biology.

[72]  A. Helenius,et al.  Quality control in the secretory pathway: retention of a misfolded viral membrane glycoprotein involves cycling between the ER, intermediate compartment, and Golgi apparatus , 1994, The Journal of cell biology.

[73]  S. Emr,et al.  The sorting receptor for yeast vacuolar carboxypeptidase Y is encoded by the VPS10 gene , 1994, Cell.

[74]  L. Matsuuchi,et al.  A mutation of the mu transmembrane that disrupts endoplasmic reticulum retention. Effects on association with accessory proteins and signal transduction. , 1994, Journal of immunology.

[75]  J. Riordan,et al.  Participation of the endoplasmic reticulum chaperone calnexin (p88, IP90) in the biogenesis of the cystic fibrosis transmembrane conductance regulator. , 1994, The Journal of biological chemistry.

[76]  W. Balch,et al.  Vesicular stomatitis virus glycoprotein is sorted and concentrated during export from the endoplasmic reticulum , 1994, Cell.

[77]  H. Gilbert,et al.  Protein disulfide isomerase exhibits chaperone and anti-chaperone activity in the oxidative refolding of lysozyme. , 1994, The Journal of biological chemistry.

[78]  A Helenius,et al.  How N-linked oligosaccharides affect glycoprotein folding in the endoplasmic reticulum. , 1994, Molecular biology of the cell.

[79]  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.

[80]  S. Sprang,et al.  Affinity panning of a library of peptides displayed on bacteriophages reveals the binding specificity of BiP , 1993, Cell.

[81]  J. Wilson,et al.  The common variant of cystic fibrosis transmembrane conductance regulator is recognized by hsp70 and degraded in a pre-Golgi nonlysosomal compartment. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[82]  R. Green,et al.  Pre-Golgi degradation of yeast prepro-alpha-factor expressed in a mammalian cell. Influence of cell type-specific oligosaccharide processing on intracellular fate. , 1993, The Journal of biological chemistry.

[83]  A. Shafferman,et al.  Interrelations between assembly and secretion of recombinant human acetylcholinesterase. , 1993, The Journal of biological chemistry.

[84]  G. Fink,et al.  SHR3: A novel component of the secretory pathway specifically required for localization of amino acid permeases in yeast , 1992, Cell.

[85]  P. Arvan,et al.  Transient aggregation of nascent thyroglobulin in the endoplasmic reticulum: relationship to the molecular chaperone, BiP , 1992, The Journal of cell biology.

[86]  A. Parodi,et al.  Purification to apparent homogeneity and partial characterization of rat liver UDP-glucose:glycoprotein glucosyltransferase. , 1992, The Journal of biological chemistry.

[87]  Seng H. Cheng,et al.  Intracellular protein trafficking defects in human disease. , 1992, Trends in cell biology.

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

[89]  S. Pillai,et al.  Distinct intracellular fates of membrane and secretory immunoglobulin heavy chains in a pre-B cell line , 1991, The Journal of cell biology.

[90]  J. Rothman,et al.  Peptide-binding specificity of the molecular chaperone BiP , 1991, Nature.

[91]  J. Bonifacino,et al.  Colocalized transmembrane determinants for ER degradation and subunit assembly explain the intracellular fate of TCR chains , 1990, Cell.

[92]  R. Klausner,et al.  Protein degradation in the endoplasmic reticulum , 1990, Cell.

[93]  J. Sambrook The involvement of calcium in transport of secretory proteins from the endoplasmic reticulum , 1990, Cell.

[94]  C. Alberini,et al.  Developmental regulation of IgM secretion: The role of the carboxy-terminal cysteine , 1990, Cell.

[95]  G. Koch,et al.  Perturbation of cellular calcium induces secretion of luminal ER proteins , 1989, Cell.

[96]  T. Creighton Disulphide bonds and protein stability , 1988, BioEssays : news and reviews in molecular, cellular and developmental biology.

[97]  J. Rothman,et al.  The rate of bulk flow from the endoplasmic reticulum to the cell surface , 1987, Cell.

[98]  P. Robbins,et al.  Substrate specificities of rat liver microsomal glucosidases which process glycoproteins. , 1980, The Journal of biological chemistry.

[99]  G. Kreibich,et al.  Proteins of rough microsomal membranes related to ribosome binding. I. Identification of ribophorins I and II, membrane proteins characteristics of rough microsomes , 1978, The Journal of cell biology.

[100]  C. Anfinsen Principles that govern the folding of protein chains. , 1973, Science.

[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]  P. Cresswell,et al.  Mechanisms of MHC class I--restricted antigen processing. , 1998, Annual review of immunology.

[103]  A. Helenius Calnexin, calreticulin and the folding of glycoproteins , 1997 .

[104]  H. Pelham Control of protein exit from the endoplasmic reticulum. , 1989, Annual review of cell biology.

[105]  I. Mellman,et al.  The biogenesis of lysosomes. , 1989, Annual review of cell biology.

[106]  A. Helenius,et al.  Protein oligomerization in the endoplasmic reticulum. , 1989, Annual review of cell biology.

[107]  J. Rothman,et al.  Biosynthetic protein transport and sorting by the endoplasmic reticulum and Golgi. , 1987, Annual review of biochemistry.