Endoplasmic reticulum stress-inducible protein GRP94 is associated with an Mg2+-dependent serine kinase activity modulated by Ca2+ and CRP78/BiP

Journal of Cellular Physiology

Volumn 170, Issue 2, 1997, Pages 115-129

  Ramakrishnan, Meera ^a   Schönthal, Axel H ^a   Lee, Amy S ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CASEIN KINASE II; CHAPERONE; GLUCOSE REGULATED PROTEIN; HEAT SHOCK PROTEIN; PROTEIN SERINE KINASE;

AMINO ACID SEQUENCE; ARTICLE; AUTOPHOSPHORYLATION; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME KINETICS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ANIMALS; BLOTTING, WESTERN; CALCIUM; CARRIER PROTEINS; CELL LINE; ENDOPLASMIC RETICULUM; HEAT-SHOCK PROTEINS; HELA CELLS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; KIDNEY; LEUKEMIA, MYELOID; MAGNESIUM; MEMBRANE PROTEINS; MOLECULAR CHAPERONES; PEPTIDE MAPPING; PHOSPHOPEPTIDES; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RATS; SUBCELLULAR FRACTIONS;

EID: 1842370906     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4652(199702)170:2<115::AID-JCP3>3.0.CO;2-R     Document Type: Article

References (54)

1. Bidwai, A.P., Hanna, D.E., and Glover, C.V.C. (1992) Purification and characterization of casein kinase II (CKII) from Δcka-1, Δcka-2 Saccharomyces cerevisiae rescued by Drosophila CKII subunit. J. Biol. Chem., 267:18790-18796.
2. Blond-Elguindi, S., Fourie, A.M., Sambrook, J.F., and Gething, M.-J.H. (1993) Peptide dependent stimulation of the ATPase activity of the molecular chaperone BiP is a result of conversion of oligomers to active monomers. J. Biol. Chem., 268:12730-12735.
3. Boyle, W.J., Vander-beer, P., and Hunter, T. (1991) Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on a thin-layer cellulose plate. Method Enzymol., 201:110-149.
4. Cala, S.E., and Jones, L.R. (1994) GRP94 residues within cardiac sarcoplasmic reticulum vesicles is phosphorylated by casein kinase II. J. Biol. Chem., 269:5926-5931.
5. Campbell, A.K. (1983) Intracellular Calcium: Its Universal Role as Regulator. John Wiley & Sons, Inc., New York.
6. Cao, X., Zhou, Y., and Lee, A.S. (1995) Requirement of tyrosine-and serine/threonine kinases in the transcriptional activation of the mammalian grp78/BiP promoter by thapsigargin. J. Biol. Chem., 270:494-502.
7. Chang, S.C., Erwin, A., and Lee, A.S. (1989) The glucose regulated protein (GRP94 and GRP78) genes share common regulatory domains and are coordinately regulated by common trans-acting factors. Mol. Cell. Biol., 9:2153-2162.
8. Cox, J.S., Shamu, C.E., and Walter, P. (1993) Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell, 73:1197-1206.
9. Crute, B.E., and Buskirk, R.G.V. (1992) A casein kinase-like kinase phosphorylates β-tubulin and may be a microtubule-associated protein. J. Neurochem., 59:2017-2023.
10. Csermely, P., and Kahn, R.C. (1991) The 90-kDa heat shock protein (hsp90) possesses an ATP binding site and autophosphorylating activity. J. Biol. Chem., 266:4943-4950.
11. Csermely, P., Miyata, Y., Schnaider, T., and Yahara, I. (1995) Auto-phosphorylation of grp94 (endoplasmin). J. Biol. Chem., 270:6381-6388.
12. Dechert, U., Weber, P., Konig, B., Ortwein, C., Nilson, I., Linxweiler, W., Wollny, E., and Gassen, H.G. (1994) A protein kinase isolated from porcine brain microvessels is similar to a class of heat shock proteins. Eur. J. Biochem., 225:805-809.
13. Drummond, I.A.S., Lee, A.S., Resendez, E., Jr., 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.
14. Flynn, G.C., Chappell, T.G., and Rothman, J.E. (1989) Peptide binding and release by proteins implicated as catalyst of protein assembly. Science, 245:385-390.
15. Freiden, P.J., Gaut, J.R., and Hendershot, L. (1992) Interconversion of three differentially modified and assembled forms of BiP. EMBO J., 11:63-70.
16. Gatica, M., Hinrichs, M.V., Jedilcki, A., Allende, C.C., and Allende, J.E. (1993) Effect of metal ions on the activity of casein kinase II from Xenopus laevis. FEBS Lett., 315:173-177.
17. Gaut, J.R., and Hendershot, L.M. (1993) The immunoglobulin-binding protein in vitro autophosphorylation site maps to a threonine within the ATP binding cleft but is not a detectable site of in vivo phosphorylation. J. Biol. Chem., 268:12691-12698.
18. Hendershot, L.M., Ting, J., and Lee, A.S. (1988) Identity of the immunoglobulin heavy chain binding protein with the 78,000 dalton glucose-regulated protein and the role of post-translational modifications in its binding function. Mol. Cell. Biol., 8:4250-4256.
19. Jarvis, D., Summers, M.D., Garcia, A., Jr., and Bohlmeyer, D.A. (1993) Influence of different signal peptides and prosequences on expression and secretion of human tissue plasminogen activator in the baculovirus system. J. Biol. Chem., 268:16754-16762.
20. Kang, H., and Welch, W.J. (1991) Characterization and purification of the 94 kDa glucose regulated protein. J. Biol. Chem., 266:5643-5649.
21. Koch, G., Smith, M., Macer, D., Webster, P., and Mortara, R. (1986) Endoplasmic reticulum contains a common, abundant calcium binding glycoprotein, endoplasmin. J. Cell. Sci., 86:217-232.
22. Kuenzel, E.A., and Krebs, E.G. (1985) A synthetic peptide substrate specific for casein kinase II. Proc. Natl. Acad. Sci. USA, 82:737-741.
23. Langer, T., Lu, C., Flanagan, J., Hayer, M.K., and Hartl, F.U. (1992) Successive action of DnaK, DnaJ and GroEL along the pathway of chaperone mediated protein folding. Nature, 356:683-689.
24. Lee, A.S. (1981) The accumulation of three specific proteins related to glucose-regulated proteins in a temperature-sensitive hamster mutant cell line. J. Cell. Physiol., 106:119-125.
25. Lee, A.S. (1987) Coordinated regulation of a set of genes by glucose and calcium ionophores in mammalian cells. Trends Biochem., 12:20-23.
26. Lee, A.S. (1992) Mammalian stress response: Induction of the glucose regulated protein family. Curr. Opin. Cell Biol., 4:267-273.
27. Lee, A.S., Delegeane, A.M., Baker, V., and Chow, P.C. (1983) Transcriptional regulation of two genes specifically induced by glucose starvation in a hamster mutant fibroblast cell line. J. Biol. Chem., 258:597-603.
28. Lee, A.S., Bell, J., and Ting, T. (1984) Biochemical characterization of two hamster glucose regulated proteins. J. Biol. Chem., 259:4616-4621.
29. Leustek, T., Toledo, H., Brot, N., and Weissbach, H. (1991) Calcium-dependent autophosphorylation of the glucose regulated-protein, Grp78. Arch. Biochem. Biophys., 289:256-261.
30. 2+ depletion. J. Biol. Chem., 268:12003-12009.
31. Li, Z., and Srivatsava, P.K. (1993) Tumor rejection antigen grp96/ grp94 is an ATPase: Implication for protein folding and antigen presentation. EMBO J., 12:3143-3151.
32. Little, E., and Lee, A.S. (1995) Generation of a mammalian cell line deficient in glucose regulated protein stress induction through targeted ribozyme driven by a stress-inducible promoter. J. Biol. Chem., 270:9526-9534.
33. Lodish, H.F., Kong, N., and Wikstroem, L. (1992) Calcium is required for folding of newly made subunits of the asialoglycoprotein receptor within the endoplasmic reticulum. J. Biol. Chem., 267:12753-12760.
34. Mazzarella, R.A., and Green, M. (1987) ERp99, an abundant, conserved glycoprotein of the endoplasmic reticulum is homologous to the 90 kDa heat shock protein (hsp90) and the 94 kDa glucose regulated protein (GRP94). J. Biol. Chem., 262:8875-8883.
35. Melnick, J., Aviel, S., and Argon, Y. (1992) The endoplasmic reticulum stress protein GRP94 in addition to BiP, associates with unassembled immunoglobulin chains. J. Biol. Chem., 267:21303-21306.
36. 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.
37. Menoret, A., Meflah, K., and Le-Pendu, J. (1994) Expression of the 100-kDa glucose regulated protein (GRP100/endoplasmin) is associated with tumorigenicity in a model of rat colon adenocarcinoma. Intl. J. Cancer, 56:400-405.
38. Mon, K., Ma, W., Gething, M.J., and Sambrook, J. ( 1993) A transmembrane protein with a cdc2/CDC28 related kinase activity is required for signalling from the ER to the nucleus. Cell, 73:1197-1206.
39. 2+ binding proteins and member of the thioredoxin superfamily. J. Biol. Chem., 269:1744-1749.
40. Ou, W.-J., Thomas, D.Y., Bell, A.W., and Bergeron, J.J.M. (1992) Casein kinase II phosphorylation of signal sequence receptor α and the associated membrane chaperone calnexin. J. Biol. Chem., 267:23789-23796.
41. Pinna, L.A. (1990) Casein kinase 2: 'An eminence grise' in cellular regulation? Biochem. Biophys. Acta., 1054:267-284.
42. Price, B.D., and Calderwood, S.K. (1992) Gadd45 and Gadd153 messenger RNA levels are increased during hypoxia and after exposure of cells to agents which elevate the levels of the glucose-regulated nroteins Cancer Res., 52:3814-3817.
43. Qu, D., Mazzarella, R.A., and Green, M. (1993) Analysis of the structure and synthesis of GRP94, an abundant stress protein of the endoplasmic reticulum. DNA and Cell Biol., 13:117-124
44. Ramakrishnan, M., Tugizov, S., Pereira, L., and Lee, A.S. (1995) Conformation defective herpes simplex virus 1 glycoprotein B activates the promoter of the grp94 gene that codes for the 94 kDa stress protein in the endoplasmic reticulum. DNA and Cell Biol., 14:373-384.
45. Resendez, E., Jr., Ting, J., Kim, K.S., Wooden, S.K., and Lee, A.S. (1986) Calcium ionophore A23187 as a regulator of gene expression in mammalian cells. J. Cell. Biol., 103:2145-2152.
46. Schaiff, W.T., Hruska., K.A., McCourt, W.D., Green, M., and Schwartz, B.D. (1992) HLA-DR associates with specific stress proteins and is retained in endoplasmic reticulum in invariant chain negative cells. J. Exp. Med., 176:657-666.
47. Shackelford D., and Zivin, J.A. (1993) Renaturation of the calcium/ calmodulin-dependent kinase activity after electrophoretic transfer from sodium dodecyl-sulfate-polyacrylamide gels to membrane. Anal. Biochem., 211:131-138.
48. Shi, Y., Brown, E.D., and Walsh, C.T. (1994) Expression of recombinant human casein kinase II and recombinant heat shock protein 90 in Escherichia coli and characterization of their interaction. Proc. Natl. Acad. Sci. USA, 91:2767-2771.
49. Shiu, R.P.C., Pouysségur, J., and Pastan, I. (1977) 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, 74:3840-3844.
50. Sugawara, S., Takeda, K., Lee, A., and Dennert, G. (1993) Suppression of stress protein GRP78 induction in tumor B/C10ME eliminates resistance to cell mediated toxicity. Cancer Res., 53:6001-6005.
51. Wang, J., Lee, A.S., and Ou, J.-H. (1991) Proteolytic conversion of hepatitis B virus antigen precursor to end-product occurs in a post-endoplasmic reticulum compartment. J. Virol., 65:5080-5083.
52. 2+-ionophore-regulated proteins. J. Biol. Chem., 258:7102-7111.
53. Wu, C.B., Pelech, S.L., and Veis, A. (1992) The in vitro phosphorylation of the native rat incisor dentin phosphoryns. J. Biol. Chem., 267:16588-16594.
54. Zandomeni, R., and Weinmann, R. (1984) Inhibitory effect of 5, 6-dichloro-1-β-D-ribofuranosylbenzimidazole on a protein kinase. J. Biol. Chem., 259:14804-14811.