Geldanamycin, an hsp90/GRP94-binding drug, induces increased transcription of endoplasmic reticulum (ER) chaperones via the ER stress pathway

Journal of Cellular Physiology

Volumn 174, Issue 2, 1998, Pages 170-179

  Lawson, Beth ^a   Brewer, Joseph W ^a   Hendershot, Linda M ^a,b  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANSAMYCIN DERIVATIVE; BENZOQUINONE DERIVATIVE; CHAPERONE; GELDANAMYCIN; HEAT SHOCK PROTEIN 90; SECRETORY PROTEIN; TRANSCRIPTION FACTOR; TUNICAMYCIN;

ANIMAL CELL; ARTICLE; CELL STRAIN 3T3; CELL STRAIN COS1; CHO CELL; CONTROLLED STUDY; DRUG PROTEIN BINDING; ENDOPLASMIC RETICULUM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FOLDING; STRESS; TRANSCRIPTION REGULATION;

ANIMALIA;

EID: 0031891726     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4652(199802)174:2<170::AID-JCP4>3.0.CO;2-L     Document Type: Article

References (43)

1. Barone, M.V., Crozat, A., Tabaee, A., Philipson, L., and Ron, D. (1994) CHOP (GADD153) and its oncogenic variant, TLS-CHOP, have opposing effects on the induction of G1/S arrest. Genes Dev., 8:453-464.
2. Blagosklonny, M.V., Toretsky, J., Bohen, S., and Neckers, L. (1996) Mutant conformation of p53 translated in vitro or in vivo requires functional HSP90. Proc. Natl. Acad. Sci. USA, 93:8379-8383.
3. Bole, D.G., Hendershot, L.M., and Kearney, J.F. (1986) Posttranslational association of immunoglobulin heavy chain binding protein with nascent heavy chains in nonsecreting and secreting hybridomas. J. Cell Biol., 102:1558-1566.
4. Burnette, W.N. (1981) "Western blotting": Electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal. Biochem., 112:195-203.
5. Carlson, S.G., Fawcett, T.W., Bartlett, J.D., Bernier, M., and Holbrook, N.J. (1993) Regulation of the C/EBP-related gene gadd153 by glucose deprivation. Mol. Cell. Biol., 13:4736-4744.
6. Chang, H.C., and Lindquist, S. (1994) Conservation of Hsp90 macromolecular complexes in Saccharomyces cerevisiae. J. Biol. Chem., 269:24983-24988.
7. Chavany, C., Mimnaugh, E., Miller, P., Bitton, R., Nguyen, P., Trepel, J., Whitesell, L., Schnur, R., Moyer, J., and 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., 271:4974-4977.
8. Dalman, F.C., Sturzenbecker, L.J., Levin, A.A., Lucas, D.A., Perdew, G.H., Petkovitch, M., Chambon, P., Grippo, J.F., and Pratt, W.B. (1991) Retinoic acid receptor belongs to a subclass of nuclear receptors that do not form "docking" complexes with hsp90. Biochemistry, 30:5605-5608.
9. DeBoer, C., Meulman, P.A., Wnuk, R.J., and Peterson, D.H. (1970) Geldanamycin, a new antibiotic. J. Antibiot. (Tokyo), 23:442-447.
10. Dorner, A.J., Wasley, L.C., Raney, P., Haugejorden, S., Green, M., and Kaufman, R.J. (1990) The stress response in Chinese hamster ovary cells. Regulation of ERp72 and protein disulfide isomerase expression and secretion. J. Biol. Chem., 265:22029-22034.
11. 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.
12. Ferreira, L.R., Norris, K., Smith, T., Hebert, C., and Sauk, J.J. (1994) Association of Hsp47, Grp78, and Grp94 with procollagen supports the successive or coupled action of molecular chaperones. J. Cell. Biochem., 56:518-526.
13. Gluzman, Y. (1981) SV40-transformed simian cells support the replication of early SV40 mutants. Cell, 23:175-182.
14. 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.
15. Hendrick, J.P., and Hartl, F.U. (1993) Molecular chaperone functions of heat-shock proteins. Annu. Rev. Immunol., 62:349-384.
16. Hutchison, K.A., Brott, B.K., De Leon, J.H., Perdew, G.H., Jove, R., and Pratt, W.B. (1992) Reconstitution of the multiprotein complex of pp60src, hsp90, and p50 in a cell-free system. J. Biol. Chem., 267:2902-2908.
17. 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.
18. Lindquist, S., and Craig, E.A. (1988) The heat-shock proteins. Annu. Rev. Genet., 22:631-677.
19. Luethy, J.D., Fargnoli, J., Park, J.S., Fornace, A.J., Jr., and Holbrook, N.J. (1990) Isolation and characterization of the hamster gadd153 gene. Activation of promoter activity by agents that damage DNA. J. Biol. Chem., 265:16521-16526.
20. 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.
21. 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.
22. 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.
23. Miller, P., DiOrio, C., Moyer, M., Schnur, R.C., Bruskin, A., Cullen, W., and Mover, J.D. (1994) Depletion of the erbB-2 gene product p185 by benzoquinoid ansamycins. Cancer Res., 54:2724-2730.
24. Mimnaugh, E.G., Chavany, C., and Neckers, L. (1996) Polyubiquitination and proteasomal degradation of the p185c-erbB-2 receptor protein-tyrosine kinase induced by geldanamycin. J. Biol. Chem., 271:22796-22801.
25. Morris, J.A., Dorner, A.J., Edwards, C.A., Hendershot, L.M., and Kaufman, R.J. (1997) 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.
26. Murakami, Y., Mizuno, S., Hori, M., and Uehara, Y. (1988) Reversal of transformed phenotypes by herbimycin A in src oncogene expressed rat fibroblasts. Cancer Res., 48:1587-1590.
27. Murakami, Y., Uehara, Y., Yamamoto, C., Fukazawa, H., and Mizuno, S. (1991) Induction of hsp 72/73 by herbimycin A, an inhibitor of transformation by tyrosine kinase oncogenes. Exp. Cell Res., 195:338-344.
28. Murakami, Y., Fukazawa, H., Mizuno, S., and Uehara, Y. (1994a) Conversion of epidermal growth factor (EGF) into a stimulatory ligand for A431-cell growth by herbimycin A by decreasing the level of expression of EGF receptor. Biochem. J., 301:57-62.
29. Murakami, Y., Mizuno, S., and Uehara, Y. (1994b) Accelerated degradation of 160 kDa epidermal growth factor (EGF) receptor precursor by the tyrosine kinase inhibitor herbimycin A in the endoplasmic reticulum of A431 human epidermoid carcinoma cells. Biochem. J., 301:63-68.
30. Oi, V.T., Morrison, S.L., Herzenberg, L.A., and Berg, P. (1983) Immunoglobulin gene expression in transformed lymphoid cells. Proc. Natl. Acad. Sci. USA, 80:825-829.
31. Picard, D., Khursheed, B., Garabedian, M.J., Fortin, M.G., Lindquist, S., and Yamamoto, K.R. (1990) Reduced levels of hsp90 compromise steroid receptor action in vivo. Nature, 348:166-168.
32. Ron, D., and Habener, J.F. (1992) CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant-negative inhibitor of gene transcription. Genes Dev., 6:439-453.
33. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratories, Cold Spring Harbor, New York.
34. Scherrer, L.C., Dalman, F.C., Massa, E., Meshinchi, S., and Pratt, W.B. (1990) Structural and functional reconstitution of the glucocorticoid receptor-hsp90 complex. J. Biol. Chem., 265:21397-21400.
35. Schulte, T.W., Blagosklonny, M.V., Ingui, C., and Neckers, L. (1995) Disruption of the Raf-1-Hsp90 molecular complex results in destabilization of Raf-1 and loss of Raf-1-Ras association. J. Biol. Chem., 270:24585-24588.
36. Smith, D.F. (1993) Dynamics of heat shock protein 90-progesterone receptor binding and the disactivation loop model for steroid receptor complexes. Mol. Endocrinol., 7:1418-1429.
37. Smith, D.F., Schowalter, D.B., Kost, S.L., and Toft, D.O. (1990) Reconstitution of progesterone receptor with heat shock proteins. Mol. Endocrinol., 4:1704-1711.
38. Smith, D.F., Whitesell, L., Nair, S.C., Chen, S., Prapapanich, V., and Rimerman, R.A. (1995) Progesterone receptor structure and function altered by geldanamycin, an hsp90-binding agent. Mol. Cell. Biol., 15:6804-6812.
39. Uehara, Y., Murakami, Y., Mizuno, S., and Kawai, S. (1988) Inhibition of transforming activity of tyrosine kinase oncogenes by herbimycin A. Virology, 164:294-298.
40. Uehara, Y., Murakami, Y., Sugimoto, Y., and Mizuno, S. (1989) Mechanism of reversion of Rous sarcoma virus transformation by herbimycin A: Reduction of total phosphotyrosine levels due to reduced kinase activity and increased turnover of p60v-src1. Cancer Res., 49:780-785.
41. Wang, X.-Z., Lawson, B., Brewer, J.W., Zinszner, H., Sanjay, A., Mi, L.-J., Boorstein, R., Kreibich, G., Hendershot, L.M., and Ron, D. (1996) Signals from the stressed endoplasmic reticulum induce C/ EBP-homologous protein (CHOP/GADD153). Mol. Cell. Biol., 16:4273-4280.
42. Whitesell, L., and Cook, P. (1996) Stable and specific binding of heat shock protein 90 by geldanamycin disrupts glucocorticoid receptor function in intact cells. Mol. Endocrinol., 10:705-712.
43. Whitesell, L., Mimnaugh, E.G., De Costa, B., Myers, C.E., and Neckers, L.M. (1994) Inhibition of heat shock protein HSP90-pp60 v-src heteroprotein complex formation by benzoquinone ansamycins: Essential role for stress proteins in oncogenic transformation. Proc. Natl. Acad. Sci. USA, 91:8324-8328.