Overexpression of BiP in tobacco alleviates endoplasmic reticulum stress

Plant Cell

Volumn 11, Issue 3, 1999, Pages 459-469

  Leborgne Castel, Nathalie ^a,c   Jelitto Van Dooren, Edith P W M ^a,b   Crofts, Andrew J ^a,d   Denecke, Jürgen ^a,c,d  

^a UNIVERSITY OF YORK   (United Kingdom)

^b TNO   (Netherlands)

^c UNIVERSITÉ DE BOURGOGNE   (France)

^d UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOPLASMIC RETICULUM; PROTEIN EXPRESSION;

EID: 0033101899     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.11.3.459     Document Type: Article

References (56)

1. Anderson, J.V., Li, Q.-B., Haskell, D.W., and Guy, C.L. (1994). Structural organization of the spinach endoplasmic reticulum-luminal 70-kilodalton heat-shock cognate gene and expression of 70-kilodalton heat-shock genes during cold acclimation. Plant Physiol. 104, 1359-1370.
2. Blond-Elguindi, S., Cwirla, C.E., Dower, W.J., Lipshutz, R.J., Sprang, S.R., Sambrook, J.F., and Gething, M.-J.H. (1993). Affinity panning of a library of peptides displayed on bacteriophages reveals the binding specificity of BiP. Cell 75, 717-728.
3. Boston, R.S., Gillikin, J.W., and Wrobel, R.L. (1995). Coordinate induction of three ER-luminal stress proteins in maize endosperm mutants. J. Cell. Biochem. 19A, 143.
4. Brodsky, J.L., Goeckeler, J., and Schekman, R. (1995). BiP and Sec63p are required for both co-and post-translational protein translocation into yeast endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 92, 9643-9646.
5. Casadaban, M.J., and Cohen, S. (1980). Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J. Mol. Biol. 138, 179-207.
6. Coleman, C.E., Lopes, M.A., Gillikin, J.W., Boston, R.S., and Larkins, B.A. (1995). A defective signal peptide in the maize high-lysine mutant floury2. Proc. Natl. Acad. Sci. USA 92, 6828-6831.
7. Coleman, C.E., Clore, A.M., Ranch, J.P., Higgins, R., Lopes, M.A., and Larkins, B.A. (1997). Expression of a mutant α-zein creates the floury2 phenotype in transgenic maize. Proc. Natl. Acad. Sci. USA 94, 7094-7097.
8. Cox, J., and Walter, P. (1996). A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87, 391-404.
9. Cox, J., Shamu, C., and Walter, P. (1993). Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane kinase. Cell 73, 1197-1206.
10. Crofts, A.J., and Denecke, J. (1998). Calreticulin and calnexin in plants. Trends Plant Sci. 3, 396-399.
11. Crofts, A.J., Leborgne-Castel, N., Pesca, M., Vitale, A., and Denecke, J. (1998). BiP and calreticulin form an abundant complex that is independent of endoplasmic reticulum stress. Plant Cell 10, 813-823.
12. D'Amico, L., Valsasina, B., Daminati, M.G., Fabbrini, M.S., Nitti, G., Bollini, R., Ceriotti, A., and Vitale, A. (1992). Bean homologs of the mammalian glucose-regulated proteins: Induction by tunicamycin and interaction with newly synthesized seed storage proteins in the endoplasmic reticulum. Plant J. 2, 443-445.
13. Deblaere, R., Bytebier, B., De Greve, H., Debroeck, F., Schell, J., Van Montagu, M., and Leemans, J. (1985). Efficient octopine Ti plasmid-derived vectors for Agrobacterium-mediated gene transfer to plants. Nucleic Acids Res. 13, 4777-4788.
14. Denecke, J. (1996). Soluble endoplasmic reticulum resident proteins and their function in protein synthesis and transport. Plant Physiol. Biochem. 34, 197-205.
15. Denecke, J., and Vitale, A. (1995). The use of plant protoplasts to study protein synthesis, quality control, protein modification and transport through the plant endomembrane system. In Methods in Cell Biology, Vol. 50, D.W. Galbraith, H.J. Bohnert, and D.P. Bourque, eds (San Diego, CA: Academic Press), pp. 335-348.
16. Denecke, J., Botterman, J., and Deblaere, R. (1990). Protein secretion in plant cells can occur via a default pathway. Plant Cell 2, 51-59.
17. Denecke, J., Goldman, M.H.S., Demolder, J., Seurinck, J., and Botterman, J. (1991). The tobacco luminal binding protein is encoded by a multigene family. Plant Cell 3, 1025-1035.
18. Denecke, J., De Rycke, R., and Botterman, J. (1992). Plant and mammalian sorting signals for protein retention in the endoplasmic reticulum contain a conserved epitope. EMBO J. 11, 2345-2355.
19. Denecke, J., Carlsson, L.E., Vidal, S., Höglund, A.-S., Ek, B., van Zeijl, M.J., Sinjorgo, K.M.C., and Palva, E.T. (1995). The tobacco homolog of mammalian calreticulin is present in protein complexes in vivo. Plant Cell 7, 391-406.
20. Dorner, A.J., Wasley, L.C., and Kaufman, R.J. (1992). Overexpression of GRP78 mitigates stress induction of glucose regulated proteins and blocks secretion of selective proteins in Chinese hamster ovary cells. EMBO J. 11, 1563-1571.
21. Faye, L., and Chrispeels, M.J. (1989). Apparent inhibition of β-fructosidase secretion by tunicamycin may be explained by breakdown of the unglycosylated protein during secretion. Plant Physiol. 89, 845-851.
22. Fontes, E.B.P., Shank, B.B., Wrobel, R.L., Moose, S.P., OBrian, G.R., Wurtzel, E.T., and Boston, R.S. (1991). Characterization of an immunoglobulin binding protein homolog in the maize floury-2 endosperm mutant. Plant Cell 3, 483-496.
23. Gething, M.-J., and Sambrook, J. (1992). Protein folding in the cell. Nature 355, 33-45.
24. Gething, M.-J., McCammon, K., and Sambrook, J. (1986). Expression of wild-type mutant forms of influenza haemagglutinin: The role of folding in intracellular transport. Cell 46, 939-950.
25. Gillikin, J.W., Zhang, F., Coleman, C.E., Bass, H.W., Larkins, B.A., and Boston, R.S. (1997). A defective signal peptide tethers the floury2 zein to the endoplasmic reticulum membrane. Plant Physiol. 114, 345-352.
26. Gomord, V., Fitchette-Laine, A.C., Denmat, L.A., Michaud, D., and Faye, L. (1998). Production of foreign proteins in tobacco cells. In Methods in Molecular Biotechnology, C. Cunningham and A.J. Porter, eds (Totowa, NJ: Humana Press Inc.), pp. 155-164.
27. Hamman, B.D., Hendershot, L.M., and Johnson, A.E. (1998). 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, 747-758.
28. Hammond, C., and Helenius, A. (1995). Quality control in the secretory pathway. Curr. Opin. Cell Biol. 7, 523-529.
29. Harmsen, M.M., Bruyne, M.I., Raué, H.A., and Maat, J. (1996). Overexpression of binding protein and disruption of the PMR1 gene synergically stimulate secretion of bovine prochymosin but not plant thaumatin in yeast. Appl. Microbiol. Biotechnol. 46, 365-370.
30. Hendershot, L., Wei, J., Gaut, J., Melnick, J., Aviel, S., and Argon, Y. (1996). Inhibition of immunoglobulin folding and secretion by dominant negative BiP ATPase mutants. Proc. Natl. Acad. Sci. USA 93, 5269-5274.
31. Hurtley, S., Bole, D., Hoover-Litty, H., Helenius, A., and Copeland, C. (1989). Interaction of misfolded influenza virus hemagglutinin with binding protein (BiP). J. Cell Biol. 108, 2117-2126.
32. Jefferson, R.A., Kavanagh, T.A., and Michael, W.B. (1987). GUS fusions: β-Glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901-3907.
33. Jones, R.L. (1985). Protein synthesis and secretion by the barley aleurone: A perspective. Israel J. Bot. 34, 377-395.
34. Kalinski, A., Rowley, D.L., Loer, D.S., Foley, C., Buta, G., and Herman, E. (1995). Binding-protein expression is subject to temporal, developmental and stress-induced regulation in terminally differentiated soybean organs. Planta 195, 611-621.
35. Kohno, K., Normington, K., Sambrook, J., Gething, M.-J., and Mori, K. (1993). The promoter region of the yeast KAR2 (BiP) gene contains a regulatory domain that responds to the presence of unfolded proteins in the endoplasmic reticulum. Mol. Cell. Biol. 13, 877-890.
36. Koizumi, N. (1996). Isolation and responses to stress of a gene that encodes a luminal binding protein in Arabidopsis thaliana. Plant Cell Physiol. 37, 862-865.
37. Li, L-J., Li, X., Ferrario, A., Rucker, N., Liu, E.S., Wong, S., Gomer, C.J., and Lee, A.S. (1992). 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, 575-582.
38. Lupattelli, F., Pedrazzini, E., Bollini, R., Vitale, A., and Ceriotti, A. (1997). The rate of phaseolin assembly is controlled by the glucosylation state of its N-linked oligosaccharide chains. Plant Cell 9, 597-609.
39. Lyman, S.K., and Schekman, R. (1997). Binding of secretory precursor polypeptide to a translocon subcomplex is regulated by BiP. Cell 88, 85-96.
40. Maliga, P., Breznowitz, A., and Marton, L. (1973). Streptomycin-resistant plants from callus culture of haploid tobacco. Nature 244, 29-30.
41. Mori, K., Sant, A., Khono, K., Normington, K., Gething, M.-J., and Sambrook, J. (1993). A transmembrane protein with a cdc2+/ CDC28 related kinase activity is required for signaling from the ER to the nucleus. Cell 74, 743-756.
42. Morris, J.A., Dorner, A.J., Edwards, C.A., Hendershot, L.M., and Kaufman, R.J. (1997). Immunoglobulin binding protein (BiP) function is required to protect cells from endoplasmic reticulum stress but is not required for the secretion of selective proteins. J. Biol. Chem. 272, 4327-4334.
43. Murashige, R., and Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15, 473-497.
44. Nagata, T., Nemoto, Y., and Hasezawa, S. (1992). Tobacco BY-2 cell line as the "HeLa" cell in the cell biology of higher plants. Int. Rev. Cytol. 132, 1-30.
45. Pedrazzini, E., Giovinazzo, G., Bollini, R., Ceriotti, A., and Vitale, A. (1994). Binding of BiP to an assembly-defective protein in plant cell. Plant J. 5, 103-110.
46. Pedrazzini, E., Giovinazzo, G., Bielli, A., de Virgilio, M., Frigerio, L., Pesca, M., Faoro, F., Bollini, R., Ceriotti, A., and Vitale, A. (1997). Protein quality control along the route to the plant vacuole. Plant Cell 9, 1869-1880.
47. Robinson, A.R., Bockhauss, J.A., Voegler, A.C., and Wittrup, K.D. (1996). Reduction of BiP levels decreases heterologous protein secretion in Saccharomyces cerevisiae. J. Biol. Chem. 271, 10017-10022.
48. Rogers, J. (1985). Two barley α-amylase gene families are regulated differently in barley aleurone cells. J. Biol. Chem. 260, 3731-3738.
49. Rose, M., Misra, L.M., and Vogel, J.P. (1989). KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene. Cell 57, 1211-1221.
50. Shamu, C.E. (1997). Signal transduction: Splicing together the unfolded-protein response. Curr. Biol. 7, R67-R70.
51. Sidrauski, C., and Walter, P. (1997). The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 90, 1031-1039.
52. Sidrauski, C., Chapman, R., and Walter, P. (1998). The unfolded protein response: An intracellular signalling pathway with many surprising features. Trends Cell Biol. 8, 245-249.
53. Simons, J.F., Ebersold, M., and Helenius, A. (1998). Cell wall 1,6-β-glucan synthesis in Saccharomyces cerevisiae depends on ER glucosidases I and II, and the molecular chaperone BiP/kar2p. EMBO J. 17, 396-405.
54. Vitale, A., Ceriotti, A., and Denecke, J. (1993). The role of the endoplasmic reticulum in protein synthesis, modification and intracellular transport. J. Exp. Bot. 44, 1417-1444.
55. Vitale, A., Bielli, A., and Ceriotti, A. (1995). The binding protein associates with monomeric phaseolin. Plant Physiol. 107, 1411-1418.
56. Vogel, J.P., Misra, L.M., and Rose, M.D. (1990). Loss of BiP/ GRP78 function blocks translocation of secretory proteins in yeast. J. Cell Biol. 110, 1885-1895.