GRP94, an ER chaperone with protein and peptide binding properties

Seminars in Cell and Developmental Biology

Volumn 10, Issue 5, 1999, Pages 495-505

  Argon, Yair ^a   Simen, Birgitte B ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Antigen presentation; HSP90; Peptide binding; Protein folding; Secretory pathway

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM; CANCER VACCINE; CHAPERONE; GLUCOSE REGULATED PROTEINS; GLUCOSE-REGULATED PROTEINS; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; MEMBRANE PROTEIN; PEPTIDE;

AMINO ACID SEQUENCE; ANIMAL; ANTIGEN PRESENTATION; CHEMISTRY; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; METABOLISM; MOLECULAR GENETICS; MOUSE; PHYSIOLOGY; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN PROCESSING; REVIEW; SEQUENCE HOMOLOGY;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; ANIMALS; ANTIGEN PRESENTATION; CALCIUM; CANCER VACCINES; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; HSP70 HEAT-SHOCK PROTEINS; HSP90 HEAT-SHOCK PROTEINS; MEMBRANE PROTEINS; MICE; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 0033210210     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1006/scdb.1999.0320     Document Type: Article

References (91)

1. Koch G, Smith M, Macer D, Webster P, Mortara R. Endoplasmic reticulum contains a common, abundant calcium-binding glycoprotein, endoplasmin. J Cell Sci. 86:1986;217-232.
2. Shiu RP, Pouyssegur J, Pastan I. Glucose depletion accounts for the induction of two transformation-sensitive membrane proteins in Rous sarcoma virus-transformed chick embryo fibroblasts. Proc Natl Acad Sci USA. 74:1977;3840-3844.
3. Van PN, Peter F, Soling HD. Four intracisternal calcium-binding glycoproteins from rat liver microsomes with high affinity for calcium. No indication for calsequestrin-like proteins in inositol 1,4,5-trisphosphate-sensitive calcium sequestering rat liver vesicles. J Biol Chem. 264:1989;17494-17501.
4. 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.
5. Kulomaa MS, Weigel NL, Kleinsek DA, Beattie WG, Conneely OM, March C, Zarucki-Schulz T, Schrader WT, O'Malley BW. Amino acid sequence of a chicken heat shock protein derived from the complementary DNA nucleotide sequence. Biochem. 25:1986;6244-6251.
6. Sargan DR, Tsai M-J, O'Malley BW. hsp108, a novel heat shock inducible protein of chicken. Biochemistry. 25:1986;6252-6258.
7. Srivastava PK, DeLeo AB, Old LJ. Tumor rejection antigens of chemically-induced sarcomas of inbred mice. Proc Natl Acad Sci USA. 83:1986;3407-3411.
8. Maki RG, Eddy RL Jr, Byers M, Shows TB, Srivastava PK. Mapping of the genes for human endoplasmic reticular heat shock protein gp96/grp94. Somatic Cell Mol Gen. 19:1993;73-81.
9. Dechert U, Weber P, Konig B, Ortwein C, Nilson I, Linxweiler W, Wollny E, Gassen HG. A protein kinase isolated from porcine brain microvessels is similar to a class of heat-shock proteins. Eur J Immunol. 225:1994;805-809.
10. Gupta RS. Phylogenetic analysis of the 90-kD heat shock family of protein sequences and an examination of the relationship among animals, plants, and fungi species. Mol Biol Evol. 12:1995;1063-1073.
11. Kozutsumi Y, Segal M, Normington K, Gething MJ, Sambrook J. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature. 332:1988;462-464.
12. Maki RG, Old LJ, Srivastava PK. Human homologue of murine tumor rejection antigen gp96: 5'-regulatory and coding regions and relationship to stress-induced proteins. Proc Natl Acad Sci USA. 87:1990;5658-5662.
13. Mori K, Sant A, Kohno K, Normington K, Gething MJ, Sambrook JF. A 22 bp cis -acting element is necessary and sufficient for the induction of the yeast KAR2 (BiP) gene by unfolded proteins. EMBO J. 11:1992;2583-2593.
14. Mori K, Ogawa N, Kawahara T, Yanagi H, Yura T. Palindrome with spacer of one nucleotide is characteristic of the cis -acting unfolded protein response element in Saccharomyces cerevisiae. J Biol Chem. 273:1998;9912-9920.
15. Cox JS, Shamu CE, Walter P. Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell. 73:1993;1197-1206.
16. Mori K, Ma W, Gething MJ, Sambrook J. A transmembrane protein with a cdc2+/CDC28-related kinase activity is required for signalling from the ER to the nucleus. Cell. 74:1993;743-756.
17. Shamu CE, Walter P. Oligomerization and phosphorylation of the Ire1p kinase during intracellular signaling from the endoplasmic reticulum to the nucleus. EMBO J. 15:1996;3028-3039.
18. Sidrauski C, Walter P. The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell. 90:1997;1031-1039.
19. Kawahara T, Yanagi H, Yura T, Mori K. Unconventional splicing of HAC1/ERN4 mRNA required for the unfolded protein response. Sequence-specific and non-sequential cleavage of the splice sites. J Biol Chem. 273:1998;1802-1807.
20. Liu ES, Lee AS. Common sets of nuclear factors binding to the conserved promoter sequence motif of two coordinately regulated ER protein genes, GRP78 and GRP94. Nucleic Acids Res. 19:1991;5425-5431.
21. Wooden SK, Li L-J, Navarro D, Qadri I, Pereira L, Lee AS. Transactivation of the grp78 promoter by malfolded proteins, glycosylation block, and calcium ionophore is mediated through a proximal region containing a CCAAT motif which interacts with CTF/NF-I. Mol Cell Biol. 11:1991;5612-5623.
22. Roy B, Lee AS. Transduction of calcium stress through interaction of the human transcription factor CBF with the proximal CCAAT regulatory element of the grp78/BiP promoter. Mol Cell Biol. 15:1995;2263-2274.
23. 2+depletion and formation of aberrant proteins: activation of the conserved stress-inducible grp core promoter element by the human nuclear factor YY1. Mol Cell Biol. 17:1997;54-60.
24. Yoshida H, Haze K, Yanagi H, Yura T, Mori K. Identification of the cis -acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins. Involvement of basic leucine zipper transcription factors. J Biol Chem. 273:1998;33741-33749.
25. Realini C, Rogers SW, Rechsteiner M. KEKE motifs. Proposed roles in protein-protein association and presentation of peptides by MHC class I receptors. FEBS Lett. 348:1994;109-113.
26. Wearsch PA, Nicchitta CV. Purification and partial molecular characterization of GRP94, an ER resident chaperone. Prot Expr Pur. 7:1996;114-121.
27. Wearsch PA, Nicchitta CV. Endoplasmic reticulum chaperone GRP94 subunit assembly is regulated through a defined oligomerization domain. Biochemistry. 35:1996;16760-16769.
28. Nemoto T, Matsusaka T, Ota M, Takagi T, Collinge DB, Walther-Larsen H. Dimerization characteristics of the 94-kDa glucose-regulated protein. J Biochem (Tokyo). 120:1996;249-256.
29. Koch GL, Macer DR, Wooding FB. Endoplasmin is a reticuloplasmin. J Cell Sci. 90:1988;485-491.
30. Cala SE, Jones LR. GRP94 resides within cardiac sarcoplasmic reticulum vesicles and is phosphorylated by casein kinase II. J Biol Chem. 269:1994;5926-5931.
31. Munro S, Pelham HR. A C-terminal signal prevents secretion of luminal ER proteins. Cell. 48:1987;899-907.
32. Peter F, Nguyen Van P, Soling HD. Different sorting of Lys-Asp-Glu-Leu proteins in rat liver. J Biol Chem. 267:1992;10631-10637.
33. Altmeyer A, Maki RG, Feldweg AM, Heike M, Protopopov VP, Masur SK, Srivastava PK. Tumor-specific cell surface expression of the KDEL containing, endoplasmic reticular heat shock protein gp96. Int J Can. 69:1996;340-349.
34. Wiest DL, Burgess WH, McKean D, Kearse KP, Singer A. The molecular chaperone calnexin is expressed on the surface of immature thymocytes in association with clonotype-independent CD3 complexes. EMBO J. 14:1995;3425-3433.
35. Bruneau N, Lombardo D, Bendayan M. Participation of GRP94-related protein in secretion of pancreatic bile salt-dependent lipase and in its internalization by the intestinal epithelium. J Cell Sci. 111:1998;2665-2679.
36. Qu D, Mazzarella RA, Green M. Analysis of the structure and synth esis of GRP94, an abundant stress protein of the endoplasmic reticulum. DNA Cell Biol. 13:1994;117-124.
37. Lenny N, Green M. Regulation of endoplasmic reticulum stress proteins in COS cells transfected with immunoglobulin u heavy chain cDNA. J Biol Chem. 266:1991;20532-20537.
38. Melnick, J, 1995, Duke Univ
39. Csermely P, Miyata Y, Schnaider T, Yahara I. Autophosphorylation of grp94 (endoplasmin). J Biol Chem. 270:1995;6381-6388.
40. 2+and GRP78/BiP. J Cell Physiol. 170:1997;115-129.
41. Trujillo R, Miro F, Plana M, Jose M, Bollen M, Stalmans W, Itarte E. Substrates for protein kinase CK2 in insulin receptor preparations from rat liver membranes: identification of a 210-kDa protein substrate as the dimeric form of endoplasmin. Arch Biochem Biophys. 344:1997;18-28.
42. Freiden PJ, Gaut JR, Hendershot LM. Interconversion of three differentially modified and assembled forms of BiP. EMBO J. 11:1992;63-70.
43. Ou WJ, Thomas DY, Bell AW, Bergeron JJM. Casein kinase II phosphorylation of signal sequence receptor α and the associated membrane chaperone calnexin. J Biol Chem. 267:1992;23789-23796.
44. 2+-calmodulin-regulated actin-binding protein. J Biol Chem. 264:1989;15083-15087.
45. Stebbins CE, Russo AA, Schneider C, Rosen N, Hartl FU, Pavletich NP. Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent. Cell. 89:1997;239-250.
46. Prodromou C, Roe SM, Piper PW, Pearl LH. A molecular clamp in the crystal structure of the N-terminal domain of the yeast Hsp90 chaperone. Nat Struct Biol 4:477-482@2r47.@xChavany C, Mimnaugh E, Miller P, Bitton R, Nguyen P, Trepel J, Whitesell L, Schnur R, Moyer J, Neckers L (1996) p185erbB2 binds to GRP94 in vivo. Dissociation of the p185erbB2/GRP94 heterocomplex by benzoquinone ansamycins precedes depletion of p185erbB2. J Biol Chem. 271:1997;4974-4977.
47. Mimnaugh EG, Chavany C, Neckers L. Polyubiquitination and proteasomal degradation of the p185c-erbB-2 receptor protein-tyrosine kinase induced by geldanamycin. J Biol Chem. 271:1996;22796-22801.
48. Melnick J, Aviel S, Argon Y. The endoplasmic reticulum stress protein GRP94, in addition to BiP, associates with unassembled immunoglobulin chains. J Biol Chem. 267:1992;21303-21306.
49. Schaiff WT, Hruska KA Jr, McCourt DW, Green M, Schwartz BD. HLA-DR associates with specific stress proteins and is retained in the endoplasmic reticulum in invariant chain negative cells. J Exp Med. 176:1992;657-666.
50. Kuznetsov G, Chen LB, Nigam SK. Several endoplasmic reticulum stress proteins, including ERp72, interact with thyroglobulin during its maturation. J Biol Chem. 269:1994;22990-22995.
51. Ramakrishnan M, Tugizov S, Pereira L, Lee AS. Conformation-defective herpes simplex virus 1 glycoprotein B activates the promoter of the grp94 gene that codes for the 94-kD stress protein in the endoplasmic reticulum. DNA Cell Biol. 14:1995;373-384.
52. Linnik KM, Herscovitz H. Multiple molecular chaperones interact with apolipoprotein B during its maturation. The network of endoplasmic reticulum-resident chaperones (ERp72, GRP94, calreticulin, and BiP) interacts with apolipoprotein b regardless of its lipidation state. J Biol Chem. 273:1998;21368-21373.
53. Ferreira LR, Norris K, Smith T, Hebert C, Sauk JJ. Association of Hsp47, Grp78, and Grp94 with procollagen supports the successive or coupled action of molecular chaperones. J Cell Biochem. 56:1994;518-526.
54. 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.
55. Melnick J, Argon Y. Molecular chaperones and the biosynthesis of antigen receptors. Immunol Today. 16:1995;243-250.
56. Wiech H, Buchner J, Zimmermann R, Jakob U. Hsp90 chaperones protein folding in vitro. Nature. 358:1992;169-170.
57. Jakob U, Lilie H, Meyer I, Buchner J. Transient interaction of Hsp90 with early unfolding intermediates of citrate synthase. Implications for heat shockin vivo. J Biol Chem. 270:1995;7288-7294.
58. Freeman BC, Morimoto RI. The human cytosolic molecular chaperones hsp90, hsp70 (hsc70) and hdj-1 have distinct roles in recognition of a non-native protein and protein refolding. Embo J. 15:1996;2969-2979.
59. Ferreira LR, Norris K, Smith T, Hebert C, Sauk JJ. Hsp47 and other ER-resident molecular chaperones form heterocomplexes with each other and with collagen type IV chains. Connect Tissue Res. 33:1996;265-273.
60. Johnson JL, Toft DO. A novel chaperone complex for steroid receptors involving heat shock proteins, immunophilins, and p23. J Biol Chem. 269:1994;24989-24993.
61. Chen S, Sullivan WP, Toft DO, Smith DF. Differential interactions of p23 and the TPR-containing proteins Hop, Cyp40, FKBP52 and FKBP51 with Hsp90 mutants. Cell Stress Chaperones. 3:1998;118-129.
62. Suto R, Srivastava PK. A mechanism for the specific immunogenicity of heat shock protein-chaperoned peptides. Science. 269:1995;1585-1588.
63. Arnold D, Faath S, Rammensee H, Schild H. Cross-priming of minor histocompatibility antigen-specific cytotoxic T cells upon immunization with the heat shock protein gp96. J Exp Med. 182:1995;885-889.
64. Nieland TJ, Tan MC, Monne-van Muijen M, Koning F, Kruisbeek AM, van Bleek GM. Isolation of an immunodominant viral peptide that is endogenously bound to the stress protein GP96/GRP94. Proc Natl Acad Sci USA. 93:1996;6135-6139.
65. Lammert E, Arnold D, Nijenhuis M, Momburg F, Hammerling GJ, Brunner J, Stevanovic S, Rammensee HG, Schild H. The endoplasmic reticulum-resident stress protein gp96 binds peptides translocated by TAP. Eur J Immunol. 27:1997;923-927.
66. Spee P, Neefjes J. TAP-translocated peptides specifically bind proteins in the endoplasmic reticulum, including gp96, protein disulfide isomerase and calreticulin. Eur J Immunol. 27:1997;2441-2449.
67. Arnold D, Wahl C, Faath S, Rammensee HG, Schild H. Influences of transporter associated with antigen processing (TAP) on the repertoire of peptides associated with the endoplasmic reticulum-resident stress protein gp96. J Exp Med. 186:1997;461-466.
68. Lammert E, Arnold D, Rammensee HG, Schild H. Expression levels of stress protein gp96 are not limiting for major histocompatibility complex class I-restricted antigen presentation. Eur J Immunol. 26:1996;875-879.
69. Wearsch PA, Voglino L, Nicchitta CV. Structural transitions accompanying the activation of peptide binding to the endoplasmic reticulum Hsp90 chaperone GRP94. Biochemistry. 37:1998;5709-5719.
70. Blachere NE, Li Z, Chandawarkar RY, Suto R, Jaikaria NS, Basu S, Udono H, Srivastava PK. Heat shock protein-peptide complexes, reconstituted in vitro, elicit peptide-specific cytotoxic T lymphocyte response and tumor immunity. J Exp Med. 186:1997;1315-1322.
71. Scheibel T, Weikl T, Buchner J. Two chaperone sites in Hsp90 differing in substrate specificity and ATP dependence. Proc Natl Acad Sci USA. 95:1998;1495-1499.
72. Young JC, Schneider C, Hartl FU. in vitro evidence that hsp90 contains two independent chaperone sites. FEBS Lett. 418:1997;139-143.
73. Young JC, Obermann WM, Hartl FU. Specific binding of tetratricopeptide repeat proteins to the C-terminal 12-kDa domain of hsp90. J Biol Chem. 273:1998;18007-18010.
74. 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 (GRP 78) and GRP 94. J Biol Chem. 267:1992;3983-3990.
75. 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.
76. Li Z, Srivastava PK. Tumor rejection antigen gp96/grp94 is an ATPase: implications for protein folding and antigen presentation. EMBO J. 12:1993;3143-3151.
77. Wearsch PA, Nicchitta CV. Interaction of endoplasmic reticulum chaperone GRP94 with peptide substrates is adenine nucleotide-independent. J Biol Chem. 272:1997;5152-5156.
78. Tamura Y, Peng P, Liu K, Daou M, Srivastava PK. Immunotherapy of tumors with autologous tumor-derived heat shock protein preparations. Science. 278:1997;117-120.
79. Srivastava PK, Maki RG. Stress-induced proteins in immune response to cancer. Curr Topics Microbiol Immunol. 167:1991;109-123.
80. Li Z. Priming of T cells by heat shock protein-peptide complexes as the basis of tumor vaccines. Semin Immunol. 9:1997;315-322.
81. Day PM, Yewdell JW, Porgador A, Germain RN, Bennink JR. Direct delivery of exogenous MHC class I molecule-binding oligopeptides to the endoplasmic reticulum of viable cells. Proc Natl Acad Sci USA. 94:1997;8064-8069.
82. Ljunggren HG, Stam NJ, Ohlen C, Neefjes JJ, Hoglund P, Heemels MT, Bast in J, Schumacher TN, Townsend A, Karre K, Ploegh HL. Empty MHC class I molecules come out in the cold. Nature. 346:1990;476-480.
83. Ortmann B, Androlewicz MJ, Cresswell P. MHC class I/β2-microglobulin complexes associate with TAP transporters before peptide bind ing. Nature. 368:1994;864-867.
84. Udono H, Srivastava PK. Heat shock protein 70-associated peptides elicit specific cancer immunity. J Exp Med. 178:1993;1391-1396.
85. Udono H, Srivastava PK. Comparison of tumor-specific immunogenicities of stress-induced proteins gp96, hsp90, and hsp70. J Immunol. 152:1994;5398-5403.
86. Csermely P, Schnaider T, Soti C, Prohaszka Z, Nardai G. The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review. Pharmacol Ther. 79:1998;129-168.
87. Cuervo AM, Knecht E, Terlecky SR, Dice JF. Activation of a selective pathway of lysosomal proteolysis in rat liver by prolonged starvation. Am J Physiol. 269:1995;1200-1208.
88. Katsumi A, Senda T, Yamashita Y, Yamazaki T, Hamaguchi M, Kojima T, Kobayashi S, Saito H. Protein C Nagoya, an elongated mutant of protein C, is retained within the endoplasmic reticulum and is associated with GRP78 and GRP94. Blood. 87:1996;4164-4175.
89. Schulte TW, Akinaga S, Murakata T, Agatsuma T, Sugimoto S, Nakano H, Lee YS, Simen BB, Argon Y, Felts S, Toft DO, Neckers LM, Sharma SV. Interaction of radicicol with members of the HSP90 family of molecular chaperones. Mol Endocrinol, 1999.
90. Wassenberg JJ, Dezfulian C, Nicchitta CV. Receptor mediated and fluid phase pathway for internalization of the ER HSP90 chaperone GRP94 in murine macrophages. J Cell Sci. 112:1999;2167-2175.
91. Arnold-Schild D, Hanau D, Spehner D, Schmid C, Rammensee HG, de la Salle H, Schild H. Cutting Edge: receptor-mediated endocytosis of heat shock proteins by pro- fessional antigen-presenting cells. J Immunol. 162:1999;3757-3760.