Protein folding in the ER

Seminars in Cell and Developmental Biology

Volumn 10, Issue 5, 1999, Pages 443-454

  Stevens, Fred J ^a   Argon, Yair ^b  

^a ARGONNE NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Chaperones; Cooperativity; ER quality control; Thermodynamics

Indexed keywords

CALCIUM; CHAPERONE; SIGNAL PEPTIDE;

CHEMICAL STRUCTURE; CHEMISTRY; ENDOPLASMIC RETICULUM; GENE TRANSLOCATION; GENETICS; GLYCOSYLATION; HUMAN; METABOLISM; OXIDATION REDUCTION REACTION; PROTEIN FOLDING; REVIEW; THERMODYNAMICS;

CALCIUM; ENDOPLASMIC RETICULUM; GLYCOSYLATION; HUMANS; MODELS, MOLECULAR; MOLECULAR CHAPERONES; OXIDATION-REDUCTION; PROTEIN FOLDING; PROTEIN SORTING SIGNALS; THERMODYNAMICS; TRANSLOCATION, GENETIC;

EID: 0033210208     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1006/scdb.1999.0315     Document Type: Article

References (106)

1. Anfinsen CB, Haber E, Sela M, White FHJ. The kinetics of formation of native ribonuclease during oxidation of the reduced polypeptide chain. Proc Natl Acad Sci USA. 47:1961;1309-1314.
2. Levinthal C. Are there pathways for protein folding? J Chim Physique. 65:1968;44-45.
3. Levinthal C. How to fold graciously. Debrunner, P, Tsibris JCM, Muck. E. Mossbauer Spectroscopy in Biological Systems. 67:1969;Univ of Illinois Press, Urbana, IL:
4. Jaenicke R. Protein folding: local structures, domains, subunits and assemblies. Biochemistry. 30:1991;3147-3161.
5. Ramakrishnan C, Ramachandran GN. Stereochemical criteria for polypeptide and protein chain conformations. II. Allowed conformations for a pair of peptide units. Biophys J. 5:1965;909-933.
6. Creighton TE, Darby NJ, Kemmink J. The roles of partly folded intermediates in protein folding. FASEB J. 10:1996;110-108.
7. Ptitsyn OB, Pain RH, Semisotnov GV, Zerovnik E, Razgulyaev OI. Evidence for a molten globule state as a general intermediate in protein folding. FEBS Lett. 262:1990;20-24.
8. Wu LC, Kim PS. Hydrophobic sequence minimization of the alpha-lactalbumin molten globule. Proc Natl Acad Sci USA. 94:1997;14314-14319.
9. Buchner J, Renner M, Lilie H, Hinz HJ, Jaenicke R, Kiefhabel T, Rudolph R. Alternatively folded states of an immunoglobulin. Biochemistry. 30:1991;6922-6929.
10. Goto Y, Hamaguchi K. Unfolding and refolding of the constant fragment of the immunoglobulin light chain. J Mol Biol. 156:1982;891-910.
11. Dul JL, Aviel S, Melnick J, Argon Y. Ig light chains are secreted predominantly as monomers. J Immunol. 157:1996;2969-2975.
12. Aviel, S, Melnick, J, Gidalevitz, T, Stevens, FJ, Dul, JL, Argon, Y, 1999, Folding of immunoblobulin chains in vivo: chaperone governed delayed folding of the variable domain and coupling of folding to chain assembly.
13. Weissman JS, Kim PS. A kinetic explanation for the rearrangement pathway of BPTI folding. Nat Struct Biol. 2:1995;1123-1130.
14. Creighton TE. How important is the molten globule for correct protein folding? Trends Biochem Sci. 22:1997;6-10.
15. Anderson RGW, Falck JR, Goldstein JL, Brown MS. Visualization of acidic organelles in intact cells by electron microscopy. Proc Natl Acad Sci USA. 81:1984;4838-4842.
16. Wiest DL, Burkhardt JK, Hester S, Hortsch M, Meyer DI, Argon Y. Membrane biogenesis during B cell differentiation: most endoplasmic reticulum proteins are expressed coordinately. J Cell Biol. 110:1990;1501-1511.
17. Sanders SL, Whitfield KM, Vogel JP, Rose MD, Schekman RW. Sec61p and BiP directly facilitate polypeptide translocation into the ER. Cell. 69:1992;353-365.
18. Braakman I, Helenius J, Helenius A. Role of ATP and disulphide bonds during protein folding in the endoplasmic reticulum. Nature. 356:1992;260-262.
19. Doms RW, Keller DS, Helenius A, Balch WE. Role for adenosine triphosphate in regulating the assembly and transport of vesicular stomatitis virus G protein trimers. J Cell Biol. 105:1987;1957-1969.
20. Levy F, Gabathuler R, Larsson R, Kvist S. ATP is required for in vitro assembly of MHC class I antigens but not for transfer of peptides across the ER membrane. Cell. 67:1991;265-274.
21. Blond-Elguindi S, Fourie AM, Sambrook JF, Gething MJ. Peptide-dependent stimulation of the ATPase activity of the molecular chaperone BiP is the result of conversion of oligomers to active monomers. J Biol Chem. 268:1993;12730-12735.
22. Csermely P, Miyata Y, Schnaider T, Yahara I. Autophosphorylation of grp94 (endoplasmin). J Biol Chem. 270:1995;6381-6388.
23. Dierks T, Volkmer J, Schlenstedt G, Jung C, Sandholzer U, Zachmann K, Schlotterhose P, Neifer K, Schmidt B, Zimmermann R. A microsomal ATP-binding protein involved in efficient protein transport into the mammalian endoplasmic reticulum. EMBO J. 15:1996;6931-6942.
24. Clairmont CA, De Maio A, Hirschberg CB. Translocation of ATP into the lumen of rough endoplasmic reticulum-derived vesicles and its binding to luminal proteins including BiP (GRP78) and GRP94. J Biol Chem. 267:1992;3983-3990.
25. Kim SH, Shin SJ, Park JS. Identification of the ATP transporter of rat liver rough endoplasmic reticulum via photoaffinity labeling and partial purification. Biochemistry. 35:1996;5418-5425.
26. Hwang C, Sinskey AJ, Lodish HF. Oxidized redox state of glutathione in the endoplasmic reticulum. Science. 257:1992;1496-1502.
27. 2+concentration in the endoplasmic reticulum of intact cells. EMBO J. 14:1995;5467-5475.
28. Li Y, Bergeron JJ, Luo L, Ou WJ, Thomas DY, Kang CY. 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 USA. 93:1996;9606-9611.
29. Horst M, Oppliger W, Rospert S, Schonfeld HJ, Schatz G, Azem A. Sequential action of two hsp70 complexes during protein import into mitochondria. EMBO J. 16:1997;1842-1849.
30. Randall LL, Hardy SJ. Correlation of competence for export with lack of tertiary structure of the mature species: a study in vivo of maltose-binding protein in E. coli. Cell. 46:1986;921-928.
31. Josefsson LG, Randall LL. Processing in vivo of precursor maltose-binding protein in Escherichia coli occurs post-translationally as well as co-translationally. J Biol Chem. 256:1981;2504-2507.
32. Josefsson LG, Randall LL. Different exported proteins in E. coli show differences in the temporal mode of processing in vivo. Cell. 25:1981;151-157.
33. Cover WH, Ryan JP, Bassford PJ Jr, Walsh KA, Bollinger J, Randall LL. Suppression of a signal sequence mutation by an amino acid substitution in the mature portion of the maltose-binding protein. J Bacteriol. 169:1987;1794-1800.
34. Liu GP, Topping TB, Cover WH, Randall LL. Retardation of folding as a possible means of suppression of a mutation in the leader sequence of an exported protein. J Biol Chem. 263:1988;14790-14793.
35. Bergman LW, Kuehl WM. Temporal relationship of translation and glycosylation of immunoglobulin heavy and light chains. Biochemistry. 17:1978;5174-5180.
36. Bergman LW, Kuehl WM. Formation of intermolecular disulfide bonds on nascent immunoglobulin polypeptides. J Biol Chem. 254:1979;5690-5694.
37. Landry SJ, Jordan R, McMacken R, Gierasch LM. Different conformations for the same polypeptide bound to chaperones DnaK and GroEL. Nature. 355:1992;455-457.
38. Ryabova LA, Desplancq D, Spirin AS, Pluckthun A. Functional antibody production using cell-free translation: effects of protein disulfide isomerase and chaperones. Nat Biotechnol. 15:1997;79-84.
39. Worn A, Pluckthun A. An intrinsically stable antibody scFv fragment can tolerate the loss of both disulfide bonds and fold correctly. FEBS Lett. 427:1998;357-361.
40. Ruddon RW, Sherman SA, Bedows E. Protein folding in the endoplasmic reticulum: lessons from the human chorionic gonadotropin beta subunit. Protein Sci. 5:1996;1443-1452.
41. Segal MS, Bye JM, Sambrook JF, Gething MJ. Disulfide bond formation during the folding of influenza virus hemagglutinin. J Cell Biol. 118:1992;227-244.
42. Hendershot L, Wei J, Gaut J, Melnick J, Aviel S, Argon Y. Inhibition of immunoglobulin folding and secretion by dominant negative BiP ATPase mutants. Proc Natl Acad Sci USA. 93:1996;5269-5274.
43. Machamer CE, Florkiewicz RZ, Rose JK. A single N-linked oligosaccharide at either of the two normal sites is sufficient for transport of vesicular stomatitis virus G protein to the cell surface. Mol Cell Biol. 5:1985;3074-3083.
44. Gallagher PJ, Henneberry JM, Sambrook JF, Gething MJ. Glycosylation requirements for intracellular transport and function of the hemagglutinin of influenza virus. J Virol. 66:1992;7136-7145.
45. Cresswell P, Blum JS, Kelner DN, Marks MS. Biosynthesis and processing of class II histocompatibility antigens. CRC Crit Rev Immunol. 7:1987;31-53.
46. Jost CR, Kurucz I, Jacobus CM, Titus JA, George AJ, Segal DM. Mammalian expression and secretion of functional single-chain Fv molecules. J Biol Chem. 269:1994;26267-26273.
47. Frand AR, Kaiser CA. The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol Cell. 1:1998;161-170.
48. Bardwell JC, McGovern K, Beckwith J. Identification of a protein required for disulfide bond formation in vivo. Cell. 67:1991;581-589.
49. Creighton TE. Protein folding coupled to disulphide bond formation. Biol Chem. 378:1997;731-744.
50. Marquardt T, Helenius A. Misfolding and aggregation of newly synthesized proteins in the endoplasmic reticulum. J Cell Biol. 117:1992;505-513.
51. Braakman I, Helenius J, Helenius A. Manipulating disulfide bond formation and protein folding in the endoplasmic reticulum. EMBO J. 11:1992;1717-1722.
52. Lodish HF, Kong N, Wikstrom L. Calcium is required for folding of newly made subunits of the asialoglycoprotein receptor within the endoplasmic reticulum. J Biol Chem. 267:1992;12753-12760.
53. Taniyama Y, Ogasahara K, Yutani K, Kikuchi M. Folding mechanism of mutant human lysozyme C77/95A with increased secretion efficiency in yeast. J Biol Chem. 267:1992;4619-4624.
54. Darby NJ, Creighton TE. Functional properties of the individual thioredoxin-like domains of protein disulfide isomerase. Biochemistry. 34:1995;11725-11735.
55. Fullekrug J, Sonnichsen B, Wunsch U, Arseven K, Nguyen Van P, Soling HD, Mieskes G. CaBP1, a calcium binding protein of the thioredoxin family, is a resident KDEL protein of the ER and not of the intermediate compartment. J Cell Sci. 107:1994;2719-2727.
56. Kuznetsov G, Chen LB, Nigam SK. Multiple molecular chaperones complex with misfolded large oligomeric glycoproteins in the endoplasmic reticulum. J Biol Chem. 272:1997;3057-3063.
57. Wu YS, Bevilacqua VL, Berg JM. Fibrillin domain folding and calcium binding: significance to Marfan syndrome. Chem Biol. 2:1995;91-97.
58. Wetmore DR, Hardman KD. Roles of the propeptide and metal ions in the folding and stability of the catalytic domain of stromelysin (matrix metalloproteinase 3). Biochemistry. 35:1996;6549-6558.
59. Okazaki A, Ikura T, Nikaido K, Kuwajima K. The chaperonin GroEL does not recognize apo-alpha-lactalbumin in the molten globule state. Nat Struct Biol. 1:1994;439-446.
60. Li LJ, Li X, Ferrario A, Rucker N, Liu ES, Wong S, Gomer CJ, Lee AS. Establishment of a Chinese hamster ovary cell line that expresses grp78 antisense transcripts and suppresses A23187 induction of both GRP78 and GRP94. J Cell Physiol. 153:1992;575-582.
61. 2+-dependent association with BiP. J Cell Biol. 114:1991;189-205.
62. Zhang JX, Braakman I, Matlack KE, Helenius A. Quality control in the secretory pathway: the role of calreticulin, calnexin and BiP in the retention of glycoproteins with C-terminal truncations. Mol Biol Cell. 8:1997;1943-1954.
63. 2+regulation of interactions between endoplasmic reticulum chaperones. J Biol Chem. 274:1999;6203-6211.
64. Machamer CE, Doms RW, Bole DG, Helenius A, Rose JK. Heavy chain binding protein recognizes incompletely disulfide-bonded forms of vesicular stomatitis virus G protein. J Biol Chem. 265:1990;6879-6883.
65. Melnick J, Dul JL, Argon Y. Sequential interaction of the chaperones BiP and GRP94 with immunoglobulin chains in the endoplasmic reticulum. Nature. 370:1994;373-375.
66. Flynn GC, Pohl J, Flocco MT, Rothman JE. Peptide-binding specificity of the molecular chaperone BiP. Nature. 353:1991;726-730.
67. Gething MJ, Blond-Elguindi S, Buchner J, Fourie A, Knarr G, Modrow S, Nanu L, Segal M, Sambrook J. Binding sites for Hsp70 molecular chaperones in natural proteins. Cold Spring Harbor Sym Quan Biol. 60:1995;417-428.
68. Lin HY, Masso-Welch P, Di YP, Cai JW, Shen JW, Subjeck JR. The 170-kDa glucose-regulated stress protein is an endoplasmic reticulum protein that binds immunoglobulin. Mol Biol Cell. 4:1993;1109-1119.
69. Saris N, Makarow M. Transient ER retention as stress response: conformational repair of heat-damaged proteins to secretion-competent structures. J Cell Sci. 111:1998;1575-1582.
70. Feldheim D, Rothblatt J, Schekman R. Topology and functional domains of Sec63p, an endoplasmic reticulum membrane protein required for secretory protein translocation. Mol Cell Biol. 12:1992;3288-3296.
71. Scidmore MA, Okamura HH, Rose MD. Genetic interactions between KAR2 and SEC63, encoding eukaryotic homologues of DnaK and DnaJ in the endoplasmic reticulum. Mol Biol Cell. 4:1993;1145-1159.
72. Silberstein S, Schlenstedt G, Silver PA, Gilmore R. A role for the DnaJ homologue Scj1p in protein folding in the yeast endoplasmic reticulum. J Cell Biol. 143:1998;921-933.
73. Zeng B, MacDonald JR, Bann JG, Beck K, Gambee JE, Boswell BA, Bachinger HP. Chicken FK506-binding protein, FKBP65, a member of the FKBP family of peptidylprolyl cis-trans isomerases, is only partially inhibited by FK506. Biochem J. 330:1998;109-114.
74. Lodish HF, Kong N. Cyclosporin A inhibits an initial step in folding of transferrin within the endoplasmic reticulum. J Biol Chem. 266:1991;14835-14838.
75. Ellis RJ, Hartl FU. Protein folding in the cell: competing models of chaperonin function. FASEB J. 10:1996;20-26.
76. Rupp K, Birnbach U, Lundstrom J, Van PN, Soling HD. Effects of CaBP2, the rat analog of ERp72, and of CaBP1 on the refolding of denatured reduced proteins. Comparison with protein disulfide isomerase. J Biol Chem. 269:1994;2501-2507.
77. Ellis RJ, Hartl FU. Principles of protein folding in the cellular environment. Curr Opin Struct Biol. 9:1999;102-110.
78. Dorner AJ, Wasley LC, Kaufman RJ. Overexpression of GRP78 mitigates stress induction of glucose regulated proteins and blocks secretion of selective proteins in Chinese hamster ovary cells. EMBO J. 11:1992;1563-1571.
79. Knittler MR, Dirks S, Haas IG. 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. Proc Natl Acad Sci USA. 92:1995;1764-1768.
80. Hamman BD, Hendershot LM, Johnson AE. BiP maintains the permeability barrier of the ER membrane by sealing the lumenal end of the translocon pore before and early in translocation. Cell. 92:1998;747-758.
81. Sousa MC, Ferrero-Garcia MA, Parodi AJ. Recognition of the oligosaccharide and protein moieties of glycoproteins by the UDP-Glc:glycoprotein glucosyltransferase. Biochemistry. 31:1992;97-105.
82. Jethmalani SM, Henle KJ. Calreticulin associates with stress proteins: implications for chaperone function during heat stress. J Cell Biochem. 69:1998;30-43.
83. Hebert DN, Simons JF, Peterson JR, Helenius A. Calnexin, calreticulin, and Bip/Kar2p in protein folding. Cold Spring Harbor Sym Quan Biol. 60:1995;405-415.
84. Kornfeld S, Mellman I. The biogenesis of lysosomes. Ann Rev Cell Biol. 5:1989;483-525.
85. Baranski TJ, Koelsch G, Hartsuck JA, Kornfeld S. Mapping and molecular modeling of a recognition domain for lysosomal enzyme targeting. J Biol Chem. 266:1991;23365-23372.
86. Tikkanen R, Peltola M, Oinonen C, Rouvinen J, Peltonen L. Severa l cooperating binding sites mediate the interaction of a lysosomal enzyme with phosphotransferase. EMBO J. 16:1997;6684-6693.
87. Munro S, Pelham HR. A C-terminal signal prevents secretion of luminal ER proteins. Cell. 48:1987;899-907.
88. Deretic D, Schmerl S, Hargrave PA, Arendt A, McDowell JH. Regulation of sorting and post-Golgi trafficking of rhodopsin by its C-terminal sequence QVS(A)PA. Proc Natl Acad Sci USA. 95:1998;10620-10625.
89. Hurtley SM, Helenius A. Protein oligomerization in the endoplasmic reticulum. Ann Rev Cell Biol. 5:1989;277-307.
90. Copeland CS, Zimmer KP, Wagner KR, Healey GA, Mellman I, Helenius A. Folding, trimerization, and transport are sequential events in the biogenesis of influenza virus hemagglutinin. Cell. 53:1988;197-209.
91. Shin J, Lee S, Strominger JL. Translocation of TCRa chains into the lumen of the endoplasmic reticulum and their degradation. Science. 259:1993;1901-1904.
92. Campbell JL, Schekman R. Selective packaging of cargo molecules into endoplasmic reticulum-derived COPII vesicles. Proc Natl Acad Sci USA. 94:1997;837-842.
93. Zhang C, DeLisi C. Estimating the number of protein folds. J Mol Biol. 284:1998;1301-1305.
94. Ward CL, Omura S, Kopito, RR. Degradation of CFTR by the ubiquitin-proteasome pathway. Cell. 83:1995;121-127.
95. Freedman RB. Protein disulfide isomerase: multiple roles in the modification of nascent secretory proteins. Cell. 57:1989;1069-1072.
96. Lewis MJ, Mazzarella RA, Green M. Structure and assembly of the endoplasmic reticulum. The synthesis of three major endoplasmic reticulum proteins during lipopolysaccharide-induced differentiation of murine lymphocytes. J Biol Chem. 260:1985;3050-3057.
97. Lewis MJ, Mazzarella RA, Green M. Structure and assembly of the endoplasmic reticulum: Biosynthesis and intracellular sorting of Erp61, ERp59, and ERp49, three protein components of murine endoplasmic reticulum. Arch Biochem Biophys. 245:1986;389-403.
98. Bush KT, Hendrickson BA, Nigam SK. Induction of the FK506-binding protein, FKBP13, under conditions which misfold proteins in the endoplasmic reticulum. Biochem J. 303:1994;705-708.
99. Coss MC, Winterstein D, Sowder II RC, Simek SL. Molecular cloning, DNA sequence analysis, and biochemical characterization of a novel 65-kDa FK506-binding protein (FKBP65). J Biol Chem. 270:1995;29336-29341.
100. Caroni P, Rothenfluh A, McGlynn E, Schneider C. S-Cyclophilin: new member of the cyclophilin family associated with the secretory pathway. J Biol Chem. 266:1991;10739-10742.
101. Spik G, Haendler B, Delmas O, Mariller C, Chamoux M, Maes P, Tartar A, Montreuil J, Stedman K, Kocher HP, Keller R, Hiestand PC, Movva NR. A novel secreted cyclophilin-like protein (SCYLP). J Biol Chem. 266:1991;10735-10738.
102. Price ER, Zydowsky LD, Jin M, Baker CH, McKeon FD, Walsh CT. Hu man cyclophilin B: a second cyclophilin gene encodes a peptidyl-prolyl isomerase with a signal sequence. Proc Natl Acad Sci USA. 88:1991;1903-1907.
103. Haas IG, Wabl M. Immunoglobulin heavy chain binding protein. Nature. 306:1983;387-389.
104. Lee AS, Bell J, Ting J. Biochemical characterization of the 94- and 78-kilodalton glucose-regulated proteins in hamster fibroblasts. J Biol Chem. 259:1984;4616-4621.
105. Ahluwalia N, Bergeron JJM, Wada I, Degen E, Williams DB. The p88 molecular chaperone is identical to the endoplasmic reticulum membrane protein, calnexin. J Biol Chem. 267:1992;10914-10918.
106. Galvin K, Krishna S, Ponchel F, Frohlich M, Cummings DE, Carlson R, Wands JR, Isselbacher KJ, Pillai S, Ozturk M. The major histocompatibility complex class I antigen-binding protein p88 is the product of the calnexin gene. Proc Natl Acad Sci USA. 89:1992;8452-8456.