The peptide-binding activity of GRP94 is regulated by calcium

Biochemical Journal

Volumn 405, Issue 2, 2007, Pages 233-241

  Biswas, Chhanda ^a,b   Ostrovsky, Olga ^a   Makarewich, Catherine A ^a   Wanderling, Sherry ^b   Gidalevitz, Tali ^b,c   Argon, Yair ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Calcium store; Chaperone; Endoplasmic reticulum (ER); Glucose regulated protein of 94 kDa (GRP94); Heat shock protein (HSP)

Indexed keywords

CALCIUM STORE; CHAPERONE; ENDOPLASMIC RETICULUM (ER); GLUCOSE-REGULATED PROTEIN OF 94 KDA (GRP94); HEAT SHOCK PROTEIN (HSP);

BINDING SITES; CALCIUM COMPOUNDS; GLUCOSE; PERTURBATION TECHNIQUES;

PEPTIDES;

CALCIUM; CELL PROTEIN; GLUCOSE REGULATED PROTEIN 94; PEPTIDE; CALCIUM BINDING PROTEIN; ENDOPLASMIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING ASSAY; BINDING SITE; CALCIUM BINDING; CALCIUM CELL LEVEL; CONFORMATIONAL TRANSITION; ENDOPLASMIC RETICULUM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; AMINO ACID SEQUENCE; ANIMAL; ARMYWORM; CELL LINE; METABOLISM; PHYSIOLOGY;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CALCIUM; CALCIUM-BINDING PROTEINS; CELL LINE; MEMBRANE GLYCOPROTEINS; MICE; PEPTIDES; SPODOPTERA;

EID: 34447132178     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20061867     Document Type: Article

References (37)

1. Melnick, J., Dul, J. L. and Argon, Y. (1994) Sequential interaction of the chaperones BiP and GRP94 with immunoglobulin chains in the endoplasmic reticulum. Nature 370, 373-375
2. Randow, F. and Seed, B. (2001) Endoplasmic reticulum chaperone gp96 is required for innate immunity but not cell viability. Nat. Cell Biol. 3, 891-896
3. Argon, Y. and Simen, B. B. (1999) GRP94, an ER chaperone with protein and peptide binding properties. Semin. Cell Dev. Biol. 10, 495-505
4. Schulte, T. W., Akinaga, S., Murakata, T., Agatsuma, T., Sugimoto, S., Nakano, H., Lee, Y. S., Simen, B. B., 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
5. Srivastava, P. K. and Udono, H. (1994) Heat shock protein-peptide complexes in cancer immunotherapy. Curr. Opin. Immunol. 6, 728-732
6. Blachere, N. E., Li, Z., Chandawarkar, R. Y., Suto, R., Jaikaria, N. S., Basu, S., Udono, H. and Srivastava, P. K. (1997) Heat shock protein-peptide complexes, reconstituted in vitro, elicit peptide-specific cytotoxic T lymphocyte response and tumor immunity. J. Exp. Med. 186, 1315-1322
7. Suto, R. and Srivastava, P. K. (1995) A mechanism for the specific immunogenicity of heat shock protein-chaperoned peptides. Science 269, 1585-1588
8. Berwin, B., Rosser, M. F., Brinker, K. G. and Nicchitta, C. V. (2002) Transfer of GRP94(Gp96)-associated peptides onto endosomal MHC class I molecules. Traffic 3, 358-366
9. Li, H. T., Yan, J. B., Li, J., Zhou, M. H., Zhu, X. D., Zhang, Y. X. and Tien, P. (2005) Enhancement of humoral immune responses to HBsAg by heat shock protein gp96 and its N-terminal fragment in mice. World J. Gastroenterol. 11, 2858-2863
10. Vogen, S. M., Gidalevitz, T., Biswas, C., Simen, B. B., Stein, E., Gulmen, F. and Argon, Y. (2002) Radicicol-sensitive peptide binding to the N-terminal portion of GRP94. J. Biol. Chem. 277, 40742-40750
11. Gidalevitz, T., Biswas, C., Ding, H., Schneidman-Duhovny, D., Wolfson, H. J., Stevens, F., Radford, S. and Argon, Y. (2004) Identification of the N-terminal peptide binding site of glucose-regulated protein 94. J. Biol. Chem. 279, 16543-16552
12. Biswas, C., Sriram, U., Ciric, B., Ostrovsky, O., Gallucci, S. and Argon, Y. (2006) The N-terminal fragment of GRP94 is sufficient for peptide presentation via professional antigen presenting cells. Int. Immunol. 18, 1147-1157
13. Macer, D. and Koch, G. L. R. (1988) Identification of a set of calcium-binding protein in reticuloplasm, the luminal content of the endoplasmic reticulum. J. Cell Sci. 91, 61-70
14. Little, E., Ramakrishnan, M., Roy, B., Gazit, G. and Lee, A. S. (1994) The glucose-regulated proteins (GRP78 and GRP94): functions, gene regulation, and applications. Crit. Rev. Eukaryot Gene Expr. 4, 1-18
15. Lee, A. S. (1987) Coordinated regulation of a set of genes by glucose and calcium ionophores in mammalian cells. Trends Biochem. Sci. 12, 20-23
16. Drummond, I. A., Lee, A. S., Resendez, Jr, E. and Steinhardt, R. A. (1987) Depletion of intracellular calcium stores by calcium ionophore A23187 induces the genes for glucose-regulated proteins in hamster fibroblasts. J. Biol. Chem. 262, 12801-12805
17. 2+-binding proteins and members of the thioredoxin superfamily. J. Biol. Chem. 269, 1744-1749
18. Cala, S. E. and Jones, L. R. (1994) GRP94 resides within cardiac sarcoplasmic reticulum vesicles and is phosphorylated by casein kinase II. J. Biol. Chem. 269, 5926-5931
19. Van, P. N., Peter, F. and Soling, H. D. (1989) 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, 17494-17501
20. 2+ binding domains. J. Biol. Chem. 266, 21458-21465
21. Vassilakos, A., Michalak, M., Lehrman, M. A. and Williams, D. B. (1998) Oligosaccharide binding characteristics of the molecular chaperones calnexin and calreticulin. Biochemistry 37, 3480-3490
22. 2+ store: a view from the lumen. Trends Biochem. Sci. 23, 10-14
23. Nakamura, K., Zuppini, A., Arnaudeau, S., Lynch, J., Ahsan, I., Krause, R., Papp, S., De Smedt, H., Parys, J. B., Muller-Esterl, W. et al. (2001) Functional specialization of calreticulin domains. J. Cell Biol. 154, 961-972
24. Soldano, K. L., Jivan, A., Nicchitta, C. V. and Gewirth, D. T. (2003) Structure of the N-terminal domain of GRP94: Basis for ligand specificity and regulation. J. Biol. Chem. 278, 48330-48338
25. Edwards, D. P., Weigel, N. L., Schrader, W. T., O'Malley, B. W. and McGuire, W. L. (1984) Structural analysis of chicken oviduct progesterone receptor using monoclonal antibodies to the subunit B protein. Biochemistry 23, 4427-4435
26. 2+. FEBS J. 273, 513-522
27. Nakamura, K., Bossy-Wetzel, E., Burns, K., Fadel, M. P., Lozyk, M., Goping, I. S., Opas, M., Bleackley, R. C., Green, D. R. and Michalak, M. (2000) Changes in endoplasmic reticulum luminal environment affect cell sensitivity to apoptosis. J. Cell Biol. 150, 731-740
28. Corbett, E. F., Michalak, K. M., Oikawa, K., Johnson, S., Campbell, I. D., Eggleton, P., Kay, C. and Michalak, M. (2000) The conformation of calreticulin is influenced by the endoplasmic reticulum luminal environment. J. Biol. Chem. 275, 27177-27185
29. 2+ regulation of interactions between endoplasmic reticulum chaperones. J. Biol. Chem. 274, 6203-6211
30. 2+ from the endoplasmic reticulum. Biochem. J. 370, 449-458
31. 2+ and receptor-associated protein are independently required for proper folding and disulfide bond formation of the low density lipoprotein receptor-related protein. J. Biol. Chem. 273, 22374-22381
32. Wileman, T., Kane, L. P., Carson, G. R. and Terhorst, C. (1991) Depletion of cellular calcium accelerates protein degradation in the endoplasmic reticulum. J. Biol. Chem. 266, 4500-4507
33. Arnaudeau, S., Frieden, M., Nakamura, K., Castelbou, C., Michalak, M. and Demaurex, N. (2002) Calreticulin differentially modulates calcium uptake and release in the endoplasmic reticulum and mitochondria. J. Biol. Chem. 277, 46696-46705
34. 2+-handling proteins. J. Cell Biol. 160, 475-479
35. Vitadello, M., Penzo, D., Petronilli, V., Michieli, G., Gomirato, S., Menabo, R., Di Lisa, F. and Gorza, L. (2003) Overexpression of the stress protein Grp94 reduces cardiomyocyte necrosis due to calcium overload and simulated ischemia. FASEB J. 17, 923-925
36. Gorza, L. and Vitadello, M. (2000) Reduced amount of the glucose-regulated protein GRP94 in skeletal myoblasts results in loss of fusion competence. FASEB J. 14, 461-475
37. Ishii, T., Udono, H., Yamano, T., Ohta, H., Uenaka, A., Ono, T., Hizuta, A., Tanaka, N., Srivastava, P. K. and Nakayama, E. (1999) Isolation of MHC class I-restricted tumor antigen peptide and its precursors associated with heat shock proteins hsp70, hsp90, and gp96. J. Immunol. 162, 1303-1309