Protein folding in the endoplasmic reticulum

Cold Spring Harbor Perspectives in Biology

Volumn 5, Issue 5, 2013, Pages

  Braakman, Ineke ^a   Hebert, Daniel N ^b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE;

BIOLOGICAL MODEL; ENDOPLASMIC RETICULUM; GLYCOSYLATION; METABOLISM; PHYSIOLOGY; PROTEIN FOLDING; PROTEIN PROCESSING; REVIEW;

ENDOPLASMIC RETICULUM; GLYCOSYLATION; MODELS, BIOLOGICAL; MOLECULAR CHAPERONES; PROTEIN FOLDING; PROTEIN MODIFICATION, TRANSLATIONAL; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84870733168     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a013201     Document Type: Article

References (141)

1. Aldag I., Bockau U, Rossdorf J, Laarmann S, Raaben W, Herrmann L., Weide T, Hartmann MW. 2011. Expression, secretion and surface display of a human alkaline phosphatase by the ciliate Tetrahymena thermophila. BMC Biotechnol 11: 11.
2. Alder N.N., Shen Y, Brodsky JL, Hendershot LM, Johnson AE. 2005. The molecular mechanisms underlying BiPmediated gating of the Sec61 translocon of the endoplasmic reticulum. J Cell Biol 168: 389-399.
3. Allen S., Naim HY, Bulleid NJ. 1995. Intracellular folding of tissue-type plasminogen activator. Effects of disulfide bond formation on N-linked glycosylation and secretion. J Biol Chem 270: 4797-4804.
4. Anttonen A.K., Mahjneh I, Hamalainen RH, Lagier-Tourenne C, Kopra O, Waris L, Anttonen M, Joensuu T, Kalimo H., Paetau A, et al. 2005. The gene disrupted in Marinesco-Sjogren syndrome encodes SIL1, an HSPA5 cochaperone. Nat Genet 37: 1309-1311.
5. Arnold S.M., Kaufman RJ. 2003. The noncatalytic portion of human UDP-glucose: Glycoprotein glucosyltransferase I confers UDP-glucose binding and transferase function to the catalytic domain. J Biol Chem 278: 43320-43328.
6. Barile M., Pisitkun T, Yu MJ, Chou CL, Verbalis MJ, Shen RF, Knepper MA. 2005. Large scale protein identification in intracellular aquaporin-2 vesicles from renal inner medullary collecting duct. Mol Cell Proteomics 4: 1095-1106.
7. Baviskar S.N., Shields MS. 2010. RNAi silenced Dd-grp94 (Dictyostelium discoideum glucose-regulated protein 94 kDa) cell lines in Dictyostelium exhibit marked reduction in growth rate and delay in development. Gene Expr 15: 75-87.
8. Berwin B., Hart JP, Rice S, Gass C, Pizzo SV, Post SR, Nicchitta CV. 2003. Scavenger receptor-A mediates gp96/GRP94 and calreticulin internalization by antigen-presenting cells. EMBO J 22: 6127-6136.
9. Bird C., Burke J, Gleeson PA, McCluskey J. 1990. Expression of human immunodeficiency virus 1 (HIV-1) envelope gene products transcribed froma heterologous promoter. Kinetics of HIV-1 envelope processing in transfected cells. J Biol Chem 265: 19151-19157.
10. Blond-Elguindi S, Cwirla SE, Dower WJ, Lipshutz RJ, Sprang S.R., Sambrook JF, Gething M-JH. 1993. Affinity panning of a library of peptides displayed on bacteriophages reveals the binding specificity of BiP. Cell 75: 717-728.
11. Bonfanti R., Colombo C, Nocerino V, Massa O, Lampasona V, Iafusco D, Viscardi M, Chiumello G, Meschi F, Barbetti F. 2009. Insulin gene mutations as cause of diabetes in children negative for five type 1 diabetes autoantibodies. Diabetes Care 32: 123-125.
12. Braakman I., Bulleid NJ. 2011. Protein folding and modification in the mammalian endoplasmic reticulum. Annu Rev Biochem 80: 71-99.
13. Braakman I., Hoover-Litty H, Wagner KR, Helenius A. 1991. Folding of influenza hemagglutinin in the endoplasmic reticulum. J Cell Biol 114: 401-411.
14. Braakman I., Helenius J, Helenius A. 1992a. Manipulating disulfide bond formation and protein folding in the endoplasmic reticulum. EMBO J 11: 1717-1722.
15. Braakman I., Helenius J, Helenius A. 1992b. Role of ATPand disulphide bonds during protein folding in the endoplasmic reticulum. Nature 356: 260-262.
16. Brandts J.F., Brennan M, Lung-Nan L. 1977. Unfolding and refolding occur much faster for a proline-free proteins than for most proline-containing proteins. Proc Natl Acad Sci 74: 4178-4181.
17. Bulleid NJ. 2012. Disulfide bond formation in the mammalian endoplasmic reticulum. Cold Spring Harb Perspect Biol 4: a013219.
18. Caramelo J.J., Parodi AJ. 2008. Getting in and out from calnexin/ calreticulin cycles. J Biol Chem 283: 10221-10225.
19. Caramelo J.J., Castro OA, Alonso LG, de Prat-Gay G, Parodi AJ. 2003. UDP-Glc:glycoprotein glucosyltransferase recognizes structured and solvent accessible hydrophobic patches in molten globule-like folding intermediates. Proc Natl Acad Sci 100: 86-91.
20. Caramelo J.J., Castro OA, de Prat-Gay G, Parodi AJ. 2004. The endoplasmic reticulumglucosyltransferase recognizes nearly native glycoprotein folding intermediates. J Biol Chem 279: 46280-46285.
21. Chen Y., Hu D, Yabe R, Tateno H, Qin SY, Matsumoto N, Hirabayashi J., Yamamoto K. 2011. Role of malectin in Glc(2)Man(9)GlcNAc(2)-dependent quality control of a1-antitrypsin. Mol Biol Cell 22: 3559-3570.
22. Christianson J.C., Shaler TA, Tyler RE, Kopito RR. 2008. OS-9 and GRP94 deliver mutant a1-antitrypsin to the Hrd1-SEL1L ubiquitin ligase complex for ERAD. Nat Cell Biol 10: 272-282.
23. Chung K.T., Shen Y, Hendershot LM. 2002. BAP, a mammalian BiP-associated protein, is a nucleotide exchange factor that regulates the ATPase activity of BiP. J Biol Chem 277: 47557-47563.
24. Daniels R., Kurowski B, Johnson AE, Hebert DN. 2003. Nlinked glycans direct the cotranslational folding pathway of influenza hemagglutinin. Mol Cell 11: 79-90.
25. Ding B., Kull B, Liu Z, Mottagui-Tabar S, Thonberg H, Gu H.F., Brookes AJ, Grundemar L, Karlsson C, Hamsten A, et al. 2005. Human neuropeptide Y signal peptide gain-of-function polymorphism is associated with increased body mass index: Possible mode of function. Regul Pept 127(1-3): 45-53.
26. Doms R.W., Ruusala A, Machamer C, Helenius J, Helenius A, Rose JK. 1988. Differential effects of mutations in three domains on folding, quaternary structure, and intracellular transport of vesicular stomatitis virus G protein. J Cell Biol 107: 89-99.
27. Duga S., Montefusco MC, Asselta R, Malcovati M, Peyvandi F, Santagostino E, Mannucci PM, Tenchini ML. 2003. Arg2074Cys missense mutation in the C2 domain of factor V causing moderately severe factor V deficiency:Molecular characterization by expression of the recombinant protein. Blood 101: 173-177.
28. Dutta R., Inouye M. 2000. GHKL, an emergent ATPase/kinase superfamily. Trends Biochem Sci 25: 24-28.
29. Earl P.L., Moss B, Doms RW. 1991. Folding, interaction with GRP78-BiP, assembly and transport of the human immunodeficiency virus type1 envelope protein. J Virol 65: 2047-2055.
30. Ellgaard L., Ruddock LW. 2005. The human protein disulphide isomerase family: Substrate interactions and functional properties. EMBO Rep 6: 28-32.
31. Ellis R.J., Hartl FU. 1999. Principles of protein folding in the cellular environment. Curr Opin Struct Biol 9: 102-110.
32. Ellis R.J., Van derVies SM. 1991. Molecular chaperones. Annu Rev Biochem 60: 321-347.
33. Flynn G.C., Pohl J, Flocco MT, Rothman JE. 1991. Peptidebinding specificity of the molecular chaperone BiP. Nature 353: 726-730.
34. Frickel E.M., Riek R, Jelesarov I, Helenius A, Wuthrich K, Ellgaard L. 2002. TROSY-NMR reveals interaction between ERp57 and the tip of the calreticulin P-domain. Proc Natl Acad Sci 99: 1954-1959.
35. Galli C., Bernasconi R, Solda T, Calanca V, Molinari M. 2011. Malectin participates in a backup glycoprotein quality control pathway in the mammalian ER. PLoS ONE 6: e16304.
36. Gamou S., Shimagaki M, Minoshima S, Kobayashi S, Shimizu N. 1989. Subcellular localization of the EGF receptor maturation process. Exp Cell Res 183: 197-206.
37. Geiger R., Gautschi M, Thor F, Hayer A, Helenius A. 2011. Folding, quality control, and secretion of pancreatic ribonuclease in live cells. J Biol Chem 286: 5813-5822.
38. Guerin M., Parodi AJ. 2003. The UDP-glucose:Glycoprotein glucosyltransferase is organized in at least two tightly bound domains from yeast to mammals. J Biol Chem 278: 20540-20546.
39. Hainzl O., Lapina MC, Buchner J, Richter K. 2009. The charged linker region is an important regulator of Hsp90 function. J Biol Chem 284: 22559-22567.
40. Hammond C., Braakman I, Helenius A. 1994. Role of Nlinked oligosaccharides, glucose trimming and calnexin during glycoprotein folding in the endoplasmic reticulum. Proc Natl Acad Sci 91: 913-917.
41. Hanson S.R., Culyba EK, Hsu TL, Wong CH, Kelly JW, Powers ET. 2009. The core trisaccharide of an N-linked glycoprotein intrinsically accelerates folding and enhances stability. Proc Natl Acad Sci 106: 3131-3136.
42. Hebert D.N., Foellmer B, Helenius A. 1995. Glucose trimming and reglucosylation determine glycoprotein association with calnexin in the endoplasmic reticulum. Cell 81: 425-433.
43. Hebert D.N., Foellmer B, Helenius A. 1996. Calnexin and calreticulin promote folding, delay oligomerization and suppress degradation of influenza hemagglutinin in microsomes. EMBO J 15: 2961-2968.
44. Hebert D.N., Zhang JX, Chen W, Foellmer B, Helenius A. 1997. The number and location of glycans on influenza hemagglutinin determine folding and association with calnexin and calreticulin. J Cell Biol 139: 613-623.
45. Hebert D.N., Garman SC, Molinari M. 2005. The glycan code of the endoplasmic reticulum: Asparagine-linked carbohydrates as protein maturation and quality-control tags. Trends Cell Biol 15: 364-370.
46. Hegde R.S., Bernstein HD. 2006. The surprising complexity of signal sequences. Trends Biochem Sci 31: 563-571.
47. Helenius A., Aebi M. 2004. Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev Biochem 73: 1019-1049.
48. Hendershot LM. 2004. The ER function BiP is a master regulator of ER function. Mt Sinai J Med 71: 289-297.
49. Hendershot L., Bole D, Köhler G, Kearney JF. 1987. Assembly and secretion of heavy chains that do not associate posttranslationally with immunoglobulin heavy chain binding protein. J Cell Biol 104: 761-767.
50. Hendriks G., Koudijs M, van Balkom BW, Oorschot V, Klumperman J., Deen PM, van der Sluijs P. 2004. Glycosylation is important for cell surface expression of the water channel aquaporin-2 but is not essential for tetramerization in the endoplasmic reticulum. J Biol Chem 279: 2975-2983.
51. Hoelen H., Kleizen B, Schmidt A, Richardson J, Charitou P, Thomas P.J., Braakman I. 2010. The primary folding defect and rescue of DF508 CFTRemerge during translation of the mutant domain. PLoS ONE 5: e15458.
52. Hogue B.G., Nayak DP. 1992. Synthesis and processing of the influenza virus neuraminidase, a type II transmembrane glycoprotein. Virology 188: 510-517.
53. Hubbard S.C., Robbins PW. 1979. Synthesis and processing of protein-linked oligosaccharides in vivo. J Biol Chem 254: 4568-4576.
54. Ishiguro S., Watanabe Y, Ito N, Nonaka H, Takeda N, Sakai T, Kanaya H., Okada K. 2002. SHEPHERD is the Arabidopsis GRP94 responsible for the formation of functional CLAVATA proteins. EMBO J 21: 898-908.
55. Jakob R.P., Schmid FX. 2009. Molecular determinants of a native-state prolyl isomerization. J Mol Biol 387: 1017-1031.
56. Jansen G., Maattanen P, Denisov AY, Scarffe L, Schade B, Balghi H., Dejgaard K, Chen LY, Muller WJ, Gehring K, et al. 2012. An interaction map of ER chaperones and foldases. Mol Cell Proteomics 11: 710-723.
57. Jansens A., van Duijn E, Braakman I. 2002. Coordinated nonvectorial folding in a newly synthesized multidomain protein. Science 298: 2401-2403.
58. Jitsuhara Y., Toyoda T, Itai T, Yamaguchi H. 2002. Chaperone-like functions of high-mannose type and complextype N-glycans and their molecular basis. J Biochem 132: 803-811.
59. Khanna R., Myers MP, Laine M, Papazian DM. 2001. Glycosylation increases potassium channel stability and surface expression in mammalian cells. J Biol Chem 276: 34028-34034.
60. Kim P.S., Arvan P. 1991. Folding and assembly of newly synthesized thyroglobulin occurs in a pre-Golgi compartment. J Biol Chem 266: 12412-12418.
61. Klappa P., Freedman RB, Zimmerman R. 1995. Protein disulfide isomerase and a lumenal cylcophilin-type peptidyl prolyl cis-trans isomerase are in transient contact with secretory proteins during late stages of translocation. Eur J Biochem 232: 755-764.
62. Kleizen B., Braakman I. 2004. Protein folding and quality control in the endoplasmic reticulum. Curr Opin Cell Biol 16: 343-349.
63. Knappe T.A., Eckert B, Schaarschmidt P, Scholz C, Schmid FX. 2007. Insertion of a chaperone domain converts FKBP12 into a powerful catalyst of protein folding. J Mol Biol 368: 1458-1468.
64. Kozlov G., Bastos-Aristizabal S, Maattanen P, Rosenauer A, Zheng F., Killikelly A, Trempe JF, Thomas DY, Gehring K. 2010. Structural basis of cyclophilin B binding by the calnexin/ calreticulin P-domain. J Biol Chem 285: 35551-35557.
65. Kundra R., Kornfeld S. 1999. Asparagine-linked oligosaccharides protect Lamp-1 and Lamp-2 from intracellular proteolysis. J Biol Chem 274: 31039-31046.
66. Labriola C., Cazzulo JJ, Parodi AJ. 1995. Retention of glucose units added by the UDP-GLC:glycoprotein glucosyltransferase delays exit of glycoproteins from the endoplasmic reticulum. J Cell Biol 130: 771-779.
67. Lambert G., Becker B, Schreiber R, Boucherot A, Reth M, Kunzelmann K. 2001. Control of cystic fibrosis transmembrane conductance regulator expression by BAP31. J Biol Chem 276: 20340-20345.
68. Land A., Zonneveld D, Braakman I. 2003. Folding of HIV-1 envelope glycoprotein involves extensive isomerization of disulfide bonds and conformation-dependent leader peptide cleavage. FASEB J 17: 1058-1067.
69. Lang K., Schmid FX, Fischer G. 1987. Catalysis of protein folding by prolyl isomerase. Nature 329: 268-270.
70. Lehrman MA. 2001. Oligosaccharide-based information in the endoplasmic reticulum quality control and other biological systems. J Biol Chem 276: 8623-8626.
71. Li Y., Bergeron JJ, Luo L, Ou WJ, Thomas DY, Kang CY. 1996. Effects of inefficient cleavage of the signal sequence of HIV-1 gp 120 on its association with calnexin, folding, and intracellular transport. Proc Natl Acad Sci 93: 9606-9611.
72. Lin Y., Lee H, Berg AH, Lisanti MP, Shapiro L, Scherer PE. 2000. The lipopolysaccharide-activated toll-like receptor (TLR)-4 induces synthesis of the closely related receptor TLR-2 in adipocytes. J Biol Chem 275: 24255-24263.
73. Lizak C., Fan YY, Weber TC, Aebi M. 2011. N-Linked glycosylation of antibody fragments in Escherichia coli. Bioconjug Chem 22: 488-496.
74. Lodish H.F., Kong N. 1984. Glucose removal from N-linked oligosaccharides is required for efficient maturation of certain secretory glycoproteins from the rough endoplasmic reticulum to the Golgi complex. J Cell Biol 98: 1720-1729.
75. Lodish H.F., Kong N, Snider M, Strous GA.M. 1983. Hepatoma secretory proteins migrate from the endoplasmic reticulum to Golgi at characteristic rates. Nature 304: 80-83.
76. Maynard J.C., Pham T, Zheng T, Jockheck-Clark A, Rankin HB, Newgard CB, Spana EP, Nicchitta CV. 2010. Gp93, the Drosophila GRP94 ortholog, is required for gut epithelial homeostasis and nutrient assimilationcoupled growth control. Dev Biol 339: 295-306.
77. Melnick J., Dul JL, Argon Y. 1994. Sequential interaction of the chaperones BiP and GRP94 with immunoglobulin chains in the endoplasmic reticulum. Nature 370: 373-375.
78. Mendes F., Roxo Rosa M, Dragomir A, Farinha CM, Roomans G.M., Amaral MD, Penque D. 2003. Unusually common cystic fibrosis mutation in Portugal encodes a misprocessed protein. Biochem Biophys ResCommun 311: 665-671.
79. Merlie J.P., Lindstrom J. 1983. Assembly in vivo of mouse muscle acetylcholine receptor: Identification of an a subunit species that may be an assembly intermediate. Cell 34: 747-757.
80. Meunier L., Usherwood Y-K, Chung KT, Hendershot LM. 2002. A subset of chaperones and folding enzymes from multiprotein complexes in the endoplasmic reticulum to bind nascent proteins. Mol Biol Cell 13: 4456-4469.
81. Molinari M., Helenius A. 2000. Chaperone selection during glycoprotein translocation into the endoplasmic reticulum. Science 288: 331-333.
82. Molinari M., Galli C, Vanoni O, Arnold SM, Kaufman RJ. 2005. Persistent glycoprotein misfolding activates the glucosidase II/UGT1-driven calnexin cycle to delay aggregation and loss of folding competence. Mol Cell 20: 503-512.
83. Nicchitta C.V., Murphy EC, Haynes R, Shelness GS. 1995. Stage-and ribosome-specific alterations in nascent chain-Sec61p interactions accompany translocation across the ER membrane. J Cell Biol 129: 957-970.
84. Nilsson I., von Heijne G. 1993. Determination of the distance between oligosaccharyltranferase active site and the endoplasmic reticulum membrane. J Biol Chem 268: 5798-5801.
85. Oliver J.D., van der, Wal Fj, Bulleid NJ, High S. 1997. Interaction of the thiol-dependent reductase ERp57 with nascent glycoproteins. Science 275: 86-88.
86. Oliver J.D., Roderick HL, Llewellyn DH, High S. 1999. ERp57 functions as a subunit of specific complexes formed with the ER lectins calreticulin and calnexin. Mol Biol Cell 10: 2573-2582.
87. Ostrovsky O., Ahmed NT, Argon Y. 2009. The chaperone activity of GRP94 toward insulin-like growth factor II is necessary for the stress response to serum deprivation. Mol Biol Cell 20: 1855-1864.
88. Otero J.H., Lizak B, Hendershot LM. 2010. Life and death of a BiP substrate. Semin Cell Dev Biol 21: 472-478.
89. Pappenberger G., Aygun H, Engels JW, Reimer U, Fischer G, Kiefhaber T. 2001. Nonprolyl cis peptide bonds in unfolded proteins cause complex folding kinetics. Nat Struct Biol 8: 452-458.
90. Pearse B.R., Hebert DN. 2010. Lectin chaperones help direct the maturation of glycoproteins in the endoplasmic reticulum. Biochim Biophys Acta 1803: 684-693.
91. Pearse B.R., Gabriel L, Wang N, Hebert DN. 2008. A cellbased reglucosylation assay demonstrates the role of GT1 in the quality control of a maturing glycoprotein. J Cell Biol 181: 309-320.
92. Pearse B.R., Tamura T, Sunryd JC, Grabowski GA, Kaufman RJ, Hebert DN. 2010. The role of UDP-Glc:glycoprotein glucosyltransferase 1 in the maturation of an obligate substrate prosaposin. J Cell Biol 189: 829-841.
93. Pena F., Jansens A, van Zadelhoff G, Braakman I. 2010. Calcium as a crucial cofactor for low density lipoprotein receptor folding in the endoplasmic reticulum. J Biol Chem 285: 8656-8664.
94. Petersen T.N., Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat Methods 8: 785-786.
95. Peterson J.R., Ora A, Nguyen Van P, Helenius A. 1995. Transient, lectin-like association of calreticulin with folding intermediates of cellular and viral glycoproteins. Mol Biol Cell 6: 1173-1184.
96. Piersma D., Berns EM, Verhoef-Post M, Uitterlinden AG, Braakman I., Pols HA, Themmen AP. 2006. A common polymorphism renders the luteinizing hormone receptor protein more active by improving signal peptide function and predicts adverse outcome in breast cancer patients. J Clin Endocrinol Metab 91: 1470-1476.
97. Pollock S., Kozlov G, Pelletier MF, Trempe JF, Jansen G, Sitnikov D., Bergeron JJ, Gehring K, Ekiel I, Thomas DY. 2004. Specific interaction of ERp57 and calnexin determined by NMR spectroscopy and an ER two-hybrid system. EMBO J 23: 1020-1029.
98. Popescu C.I., Paduraru C, Dwek RA, Petrescu SM. 2005. Soluble tyrosinase is an endoplasmic reticulum (ER)-associated degradation substrate retained in the ER by calreticulin and BiP/GRP78 and not calnexin. J Biol Chem 280: 13833-13840.
99. Popp MW, Karssemeijer RA, Ploegh HL. 2012. Chemoenzymatic site-specific labeling of influenza glycoproteins as a tool to observe virus budding in real time. PLoS Pathog 8: e1002604.
100. Rajagopalan S., Xu Y, Brenner MB. 1994. Retention of unassembled components of integral membrane proteins by calnexin. Science 263: 387-390.
101. Randow F., Seed B. 2001. Endoplasmic reticulum chaperone gp96 is required for innate immunity but not cell viability. Nat Cell Biol 3: 891-896.
102. Rane N.S., Chakrabarti O, Feigenbaum L, Hegde RS. 2010. Signal sequence insufficiency contributes to neurodegeneration caused by transmembrane prion protein. J Cell Biol 188: 515-526.
103. Ruiz-Canada C, Kelleher DJ, Gilmore R. 2009. Cotranslational and posttranslational N-glycosylation of polypeptides by distinct mammalian OST isoforms. Cell 136: 272-283.
104. Rutkevich L.A., Cohen-Doyle MF, Brockmeier U, Williams DB. 2010. Functional relationship between protein disulfide isomerase family members during the oxidative folding of human secretory proteins. Mol Biol Cell 21: 3093-3105.
105. Schallus T., Jaeckh C, Feher K, Palma AS, Liu Y, Simpson JC, Mackeen M., Stier G, Gibson TJ, Feizi T, et al. 2008. Malectin: A novel carbohydrate-binding protein of the endoplasmic reticulum and a candidate player in the early steps of protein N-glycosylation. Mol Biol Cell 19: 3404-3414.
106. 2+ leakage from the ER. EMBO J 31: 3282-3296.
107. Schiene-Fischer C, Habazettl J, Schmid FX, Fischer G. 2002. The hsp70 chaperone DnaK is a secondary amide peptide bond cis-trans isomerase. Nat Struct Biol 9: 419-424.
108. Schrag J.D., Bergeron JJ, Li Y, Borisova S, Hahn M, Thomas D.Y., Cygler M. 2001. The structure of calnexin, an ER chaperone involved in quality control of protein folding. Mol Cell 8: 633-644.
109. Schulte T.W., Akinaga S, Murakata T, Agatsuma T, Sugimoto S, Nakano H, Lee YS, Simen BB, Argon Y, Felts S., et al. 1999. Interaction of radicicol with members of the heat shock protein 90 family of molecular chaperones. Mol Endocrinol 13: 1435-1448.
110. + channel are not linked by a disulfide bond. Biochemistry 34: 1725-1733.
111. Senderek J., Krieger M, Stendel C, Bergmann C, Moser M, Breitbach-Faller N, Rudnik-Schoneborn S, Blaschek A, Wolf N.I., Harting I, et al. 2005. Mutations in SIL1 cause Marinesco-Sjogren syndrome, a cerebellar ataxia with cataract and myopathy. Nat Genet 37: 1312-1314.
112. Shaffer K.L., Sharma A, Snapp EL, Hegde RS. 2005. Regulation of protein compartmentalization expands the diversity of protein function. Dev Cell 9: 545-554.
113. Shakin-Eshleman SH, Remaley AT, Eshleman JR, Wunner WH, Spitalnik SL. 1992. N-linked glycosylation of rabies virus glycoprotein. Individual sequons differ in their glycosylation efficiencies and influence on cell surface expression. J Biol Chem 267: 10690-10698.
114. Singh I., Doms RW, Wagner KR, Helenius A. 1990. Intracellular transport of soluble and membrane-bound glycoproteins: Folding, assembly and secretion of anchor-free influenza hemagglutinin. EMBO J 9: 631-639.
115. Skehel J.J., Stevens DJ, Daniels RS, Douglas AR, Knossow M, Wilson I.A., Wiley DC. 1984. A carbohydrate side chain on hemagglutinins of Hong Kong influenza viruses inhibits recognition by a monoclonal antibody. ProcNatl Acad Sci 81: 1779-1783.
116. Solda T., Garbi N, Hammerling GJ, Molinari M. 2006. Consequences of ERp57 deletion on oxidative folding of obligate and facultative clients of the calnexin cycle. J Biol Chem 281: 6219-6226.
117. Soldano K.L., Jivan A, Nicchitta CV, Gewirth DT. 2003. Structure of the N-terminal domain of GRP94. Basis for ligand specificity and regulation. J Biol Chem 278: 48330-48338.
118. Sousa M., Parodi AJ. 1995. The molecular basis for the recognition of misfolded glycoproteins by the UDP-Glc: Glycoprotein glucosyltransferase. EMBO J 14: 4196-4203.
119. Srivastava PK. 2006. Therapeutic cancer vaccines. Curr Opin Immunol 18: 201-205.
120. Straub S.G., Sharp GW. 2002. Glucose-stimulated signaling pathways in biphasic insulin secretion. Diabetes Metab Res Rev 18: 451-463.
121. Suh P., Bergmann JE, Gabel CA. 1989. Selective retention of monoglycosylated high mannose oligosaccarides by a class of mutant vesicular stomatitis virus G proteins. J Cell Biol 108: 811-819.
122. Swanton E., Bulleid NJ. 2003. Protein folding and translocation across the endoplasmic reticulum membrane. Mol Membr Biol 20: 99-104.
123. Tamura T., Cormier JH, Hebert DN. 2011. Characterization of early EDEM1 protein maturation events and their functional implications. J Biol Chem 286: 24906-24915.
124. Tatu U, Braakman I, Helenius A. 1993. Membrane glycoprotein folding, oligomerization and intracellular transport: Effects of dithiothreitol in living cells. EMBO J 12: 2151-2157.
125. Thor F., Gautschi M, Geiger R, Helenius A. 2009. Bulk flow revisited: Transport of a soluble protein in the secretory pathway. Traffic 10: 1819-1830.
126. van der Zand A, Gent J, Braakman I, Tabak HF. 2012. Biochemically distinct vesicles from the endoplasmic reticulum fuse to form peroxisomes. Cell 149: 397-409.
127. Van Leeuwen JEM, Kearse KP. 1997. Reglucosylation of Nlinked glycans is critical for calnexin assembly with T cell receptor (TCR) a proteins but not TCRb proteins. J Biol Chem 272: 4179-4186.
128. Vassilakos A., Cohen-Doyle MF, Peterson PA, Jackson MR, Williams DB. 1996. The molecular chaperone calnexin facilitates folding and assembly of class I histocompatibility molecules. EMBO J 15: 1495-1506.
129. Visintin A., Mazzoni A, Spitzer JA, Segal DM. 2001. Secreted MD-2 is a large polymeric protein that efficiently confers lipopolysaccharide sensitivity to Toll-like receptor 4. Proc Natl Acad Sci 98: 12156-12161.
130. Vogen S., Gidalevitz T, Biswas C, Simen BB, Stein E, Gulmen F, Argon Y. 2002. Radicicol-sensitive peptide binding to the N-terminal portion of GRP94. J Biol Chem 277: 40742-40750.
131. Wada I., Kai M, Imai S, Sakane F, Kanoh H. 1997. Promotion of transferrin folding by cyclic interactions with calnexin and calreticulin. EMBO J 16: 5420-5432.
132. Wallis A.K., Freedman RB. 2011. Assisting oxidative protein folding: How do protein disulphide-isomerases couple conformational and chemical processes in protein folding? Top Curr Chem doi: 10.1007/128_2011_171.
133. Wanderling S., Simen BB, Ostrovsky O, Ahmed NT, Vogen SM, Gidalevitz T, Argon Y. 2007. GRP94 is essential for mesoderm induction and muscle development because it regulates insulin-like growth factor secretion. Mol Biol Cell 18: 3764-3775.
134. Wang N., Daniels R, Hebert DN. 2005. The cotranslational maturation of the type I membrane glycoprotein tyrosinase: The heat shock protein 70 system hands off to the lectin-based chaperone system. Mol Biol Cell 16: 3740-3752.
135. Wang N., Glidden EJ, Murphy SR, Pearse BR, Hebert DN. 2008. The cotranslational maturation program for the type II membrane glycoprotein influenza neuraminidase. J Biol Chem 283: 33826-33837.
136. Wearsch P.A., Voglino L, Nicchitta CV. 1998. Structural transitions accompanying the activation of peptide binding to the endoplasmic reticulum Hsp90 chaperone GRP94. Biochemistry 37: 5709-5719.
137. Yamada S., Ono T, Mizuno A, Nemoto TK. 2003. A hydrophobic segment within the C-terminal domain is essential for both client-binding and dimer formation of the HSP90-family molecular chaperone. Eur J Biochem 270: 146-154.
138. Zapun A., Darby NJ, Tessier DC, Michalak M, Bergeron JJ, Thomas DY. 1998. Enhanced catalysis of ribonuclease B folding by the interaction of calnexin or calreticulin with ERp57. J Biol Chem 273: 6009-6012.
139. Zhang H., Peters KW, Sun F, Marino CR, Lang J, Burgoyne RD, Frizzell RA. 2002. Cysteine string protein interacts with and modulates the maturation of the cystic fibrosis transmembrane conductance regulator. J Biol Chem 277: 28948-28958.
140. Zhao L., Longo-Guess C, Harris BS, Lee JW, Ackerman SL. 2005. Protein accumulation and neurodegeneration in the woozy mutant mouse is caused by disruption of SIL1, a cochaperone of BiP. Nat Genet 37: 974-979.
141. Zielinska D.F., Gnad F, Wisniewski JR, Mann M. 2010. Precision mapping of an in vivo N-glycoproteome reveals rigid topological and sequence constraints. Cell 141: 897-907.