HSP90 interacts with and regulates the activity of heat shock factor 1 in Xenopus oocytes

Molecular and Cellular Biology

Volumn 18, Issue 9, 1998, Pages 4949-4960

  Ali, Adnan ^a   Bharadwaj, Steven ^a   O'Carroll, Ruth ^a   Ovsenek, Nick ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE ACTIVATION; GENE EXPRESSION REGULATION; HEAT SHOCK; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; XENOPUS;

AMPHIBIA; ANIMALIA; REPTILIA; XENOPUS;

EID: 0031866191     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.18.9.4949     Document Type: Article

References (77)

1. Abravaya, K. A., M. Myers, S. P. Murphy, and R. I. Morimoto. 1992. The human heat shock protein hsp70 interacts with HSF, the transcription factor that regulates heat shock gene expression. Genes Dev. 6:1153-1164.
2. Ananthan, J., A. L. Golberg, and R. Voellmy. 1986. Abnormal proteins serve as eukaryotic stress signals and trigger the activation of heat shock genes. Science 232:522-525.
3. Baler, R., W. J. Welch, and R. Voellmy. 1992. Heat shock gene regulation by nascent polypeptides and denatured proteins: hsp70 as a potential autoregulatory factor. J. Cell Biol. 117:1151-1159.
4. Baler, R., G. Dahl, and R. Voellmy. 1993. Activation of human heat shock genes is accompanied by oligomerization, modification, and rapid translocation of heat shock transcription factor HSF1. Mol. Cell. Biol. 13:2486-2496.
5. Baler, R., J. Zou, and R. Voellmy. 1996. Evidence for a role of hsp70 in the regulation of the heat shock response of mammalian cells. Cell Stress Chaperones 1:33-39.
6. Bharadwaj, S., A. Hnatov, A. Ali, and N. Ovsenek. 1998. Regulation of the DNA-binding and transcriptional activities of heat shock factor 1 is uncoupled in Xenopus oocytes. Biochim. Biophys. Acta 1402:79-85.
7. Bohen, S. P., and K. R. Yamamoto. 1994. Modulation of steroid-receptor signal transduction by heat shock proteins. p. 313-334. In R. I. Mormoto, A. Tissiers, and C. Georgopoulos (ed.), The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
8. Bonner, J. J., S. Heyward, and D. L. Fackenthal. 1992. Temperature-dependent regulation of a heterologous transcriptional activation domain fused to yeast heat shock transcription factor. Mol. Cell. Biol. 12:1021-1030.
9. Boorstein, W. R., and E. A. Craig. 1990. Transcriptional regulation of SSA3, an hsp70 gene from Saccharomyces cerevisiae. Mol. Cell. Biol. 10:3262-3267.
10. Brugge, J. S., E. Erikson, and R. L. Erikson. 1981. The specific interaction of the Rous sarcoma virus transforming protein pp60src, with two cellular proteins. Cell 25:363-372.
11. Clos, J., J. T. Westwood, P. B. Becker, S. Wilson, K. Lambert, and C. Wu. 1990. Molecular cloning and expression of a hexameric Drosophila heat shock factor subject to negative regulation. Cell 63:1085-1097.
12. Cotto, J. J., M. Kline, and R. I. Morimoto. 1996. Activation of heat shock factor 1 DNA binding preceds stress-induced serine phosphorylation. J. Biol. Chem. 271:3355-3358.
13. DiDomenico, B. J., G. E. Bugaisky, and S. Lindquist. 1982. The heat shock response is self-regulated at both the transcriptional and posttranscriptional levels. Cell 31:593-603.
14. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
15. Dougherty, J. J., D. A. Rabideau, A. M. Iannoti, W. P. Sullivan, and D. O. Toft. 1987. Identification of the 90 kDa substrate of rat liver type II casein kinase with the heat shock protein which binds steroid receptors. Biochim. Biophys. Acta 927:74-80.
16. Farkas, T., Y. A. Kutskova, and V. Zimarino. 1998. Intramolecular repression of mouse heat shock factor 1. Mol. Cell. Biol. 18:906-918.
17. Firestone, G. L., and S. D. Winguth. 1990. Immunoprecipitation of proteins. Methods Enzymol. 182:688-700.
18. Georgopoulos, C. 1992. The emergence of chaperone machines. Trends Biochem. Sci. 17:295-299.
19. Gordon, S., S. Bharadwaj, A. Hnatov, A. Ali, and N. Ovsenek. 1997. Distinct stress-inducible and developmentally regulated heat shock transcription factors in Xenopus oocytes. Dev. Biol. 181:47-63.
20. Gradin, K., J. McGuire, R. H. Wenger, I. Kvietikova, M. L. Whitelaw, R. Toftgard, L. Tora, M. Gassmann, and L. Poellinger. 1996. Functional interference between hypoxia and dioxin signal transduction pathways: competition for recruitment of the Arnt transcription factor. Mol. Cell. Biol. 16:5221-5231.
21. Green, M., T. J. Schuetz, E. K. Sullivan, and R. E. Kingston. 1995. A heat shock-responsive domain of human HSF1 that regulates transcription activation domain function. Mol. Cell. Biol. 15:3354-3362.
22. Grenert, J. P., W. P. Sullivan, P. Fadden, T. A. J. Haystead, J. Clark, E. Mimnaugh, H. Krutzsch, H. J. Ochel, T. W. Schulte, E. Sausville, L. M. Neckers, and D. O. Toft. 1997. The amino-terminal domain of heat shock protein 90 (hsp90) that binds geldanamycin is an ATP/ADP switch domain that regulates hsp90 conformation. J. Biol. Chem. 272:23843-23850.
23. Hartson, S. D., E. A. Ottinger, W. Huang, G. Barany, P. Burn, and R. L. Matts. 1998. Modular folding and evidence for phosphorylation-induced stabilization of an Hsp90-dependent kinase. J. Biol. Chem. 273:8475-8452.
24. Hartson, S. D., D. J. Barrett, P. Burn, and R. L. Matts. 1996. Hsp90-mediated folding of the lymphoid cell kinase p56lck. Biochemistry 35:13451-1359.
25. Hendrick, J. P., and F. U. Hartl. 1993. Molecular chaperone functions of heat shock proteins. Annu. Rev. Biochem. 62:349-384.
26. Holmberg. C. I., S. Leppa, J. E. Eriksson, and L. Sistonen. 1997. The phorbol ester 12-O-tetradecanoylphorbol 13-acetate enhances the heat-induced stress response. J. Biol. Chem. 272:6792-6798.
27. Horrell, A., J. Shuttleworth, and A. Coleman. 1987. Transcript levels and translational control of hsp70 synthesis in Xenopus oocytes. Genes Dev. 1:433-444.
28. Jakob, U., and J. Buchner. 1994. Assisting spontaneity: the role of hsp90 and small hsps as molecular chaperones. Trends Biochem. Sci. 19:205-211.
29. Kim, J., A. Nueda, Y. H. Meng, W. S. Dynan, and N. F. Michevi. 1997. Analysis of phosphorylation of human heat shock transcription factor-1 by MARK family members. J. Cell. Biochem. 67:43-54.
30. Kline, M. P., and R. I. Morimoto. 1997. Repression of the heat shock factor 1 transcriptional activation domain is modulated by constitutive phosphorylation. Mol. Cell. Biol. 17:2107-2115.
31. Knauf, U., E. M. Newton, J. Kryiakis, and R. E. Kingston. 1996. Repression of human heat shock factor 1 activity at control temperature by phosphorylation. Genes Dev. 10:2782-2793.
32. Landsberger, N., M. Ranjan, G. Almouzni, D. Stump, and A. P. Wolffe. 1995. The heat shock response in Xenopus oocytes, embryos, and somatic cells: a regulatory role for chromatin. Dev. Biol. 170:62-74.
33. Lis, J., and C. Wu. 1993, Protein traffic on the heat shock promoter: parking, stalling, and trucking along. Cell 74:1-4.
34. Mager, W. H., and A. J. J. DeKruijff. 1995. Stress-induced transcriptional activation. Microbiol. Rev. 59:506-531.
35. Melnick, J., S. Aviel, and Y. Argon. 1992. The endoplasmic reticulum stress protein GRP94, in addition to BiP, associates with unassembled immunoglobulin chains. J. Biol. Chem. 267:21303-21306.
36. Mercier, P. A., J. Foksa, N. Ovsenek, and J. T. Westwood. 1997. Xenopus heat shock factor 1 is a nuclear protein before heat stress. J. Biol. Chem. 272:14147-14151.
37. a.Meyer, D., and N. Ovsenek. Unpublished results.
38. Mifflin, L. C., and R. E. Cohen. 1994. hsc70 moderates the heat shock (stress) response in Xenopus laevis oocytes and binds to denatured protein inducers. J. Biol. Chem. 269:15718-15723.
39. Minami, Y., H. Kawasaki, Y. Miyata, K. Suzuki, and I. Yahara. 1990 Analysis of native forms and isoform compositions of the mouse 90-kDa heat shock protein, HSP90. J. Biol. Chem. 266:10099-10103.
40. Morimoto, R. I. 1993. Cells in stress: transcriptional activation of heat shock genes. Science 259:1409-1410.
41. Morimoto, R. I., A. Tissiers, and C. Georgopoulos (ed.). 1994. The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
42. Mosser, D. D., J. Duchaine, and B. Massie. 1993. The DNA-binding activity of the human heat shock transcription factor is regulated in vivo by hsp70. Mol. Cell. Biol. 13:5427-5438.
43. Nadeau, K., A. Das, and C. T. Walsh. 1993. Hsp90 chaperonins possess ATPase activity and bind heat shock transcription factors and peptidyl prolyl isomerases. J. Biol Chem. 268:1479-1487.
44. Nair, S. C., E. J. Toran, R. A. Rimerman, S. Hjermstad, T. E. Smithgall, and D. F. Smith. 1996. A pathway of multi-chaperone interactions common to diverse regulatory proteins: estrogen receptor, Fes tyrosine kinase, heat shock transcription factor HSF1, and the aryl hydrocarbon receptor Cell Stress Chaperones 1:237-250.
45. Nakai, A., and R. I. Morimoto. 1993. Characterization of a novel chicken heat shock transcription factor, heat shock factor 3, suggests a new regulatory pathway. Mol. Cell. Biol 13:1983-1997.
46. Nemoto, T., Y. Ohara-Nemoto, M. Ota, T. Takagi, and K. Yokoyama. 1995. Mechanism of dimer formation of the 90-kDa heat-shock protein. Eur. J. Biochem. 233:1-8.
47. Newton, E. M., U. Knauf, M. Green, and R. E. Kinston. 1996. The regulatory domain of human heat shock factor 1 is sufficient to sense heat stress. Mol. Cell. Biol 16:839-846.
48. Nunes, S. L., and S. K. Calderwood. 1995. Heat shock factor 1 and the heat shock cognate 70 protein associate in high molecular weight complexes in the cytoplasm of NIH-3T3 cells. Biochem. Biophys. Res. Commun. 213:1-6.
49. Orosz, A., J. Wisniewski, and C. Wu. 1996. Regulation of Drosophila heat shock factor trimerization: global sequence requirements and independence of nuclear localization. Mol. Cell. Biol. 16:7018-7030.
50. Ovsenek, N., and J. J. Heikkila. 1990. DNA sequence specific binding activity of the Xenopus heat shock transcription factor is heat indueible before the midblastula transition. Development 110:427-433.
51. Pratt, W. B., and M. J. Welsh. 1994. Chaperone functions of the heat shock proteins associated with steroid receptors. Semin. Cell Biol. 5:83-93.
52. Prodromou, C., S. M. Roe, R. O'Brien, J. E. Ladbury, P. W. Piper, and L. H. Pearl. 1997. Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 90:65-75.
53. Rabindran, S. K., G. Giorgi, J. Clos, and C. Wu. 1991. Molecular cloning and expression of a human heat shock factor, HSF1. Proc. Natl. Acad. Sci. USA 88:6906-6910.
54. Rabindran, S. K., R. I. Haroun, J. Clos, J. Wisniewski, and C. Wu. 1993. Regulation of heat shock factor trimer formation: role of a conserved leucine zipper. Science 259:230-234.
55. Rabiudran, S. K., J. Wisniewski, I. Li, G. C. Li, and C. Wu. 1994. Interaction between heat shock factor and hsp70 is insufficient to supress induction of DNA-binding activity in vivo. Mol. Cell. Biol. 14:6552-6520.
56. Sarge, K. D., S. P. Murphy, and R. I. Morimuto. 1993. Activation of heat shock gene transcription by heat shock factor 1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress. Mol. Cell. Biol. 13:1392-1407.
57. Schneider, C., L. Sepp-Lorenzio, E. Nimmesgern, O. Ouerfelli, S. Danishefsky, R. Rosen, and F. U. Hartl. 1996. Pharmacologic shifting of a balance between protein refolding and degradation mediated by hsp90. Proc. Natl. Acad. Sci. USA 93:14536-14541.
58. Schulte, T. W., M. V. Blagosklonny, C. Ingui, and L. Neckers. 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.
59. Shakinovich, R., G. Shue, and D. S. Kohtz. 1992. Conformational activation of a basic helix-loop-helix protein (MyoD1) by the C-terminal region of murine HSP90 (HSP84). Mol. Cell. Biol. 12:5059-5068.
60. Shi, Y., P. E. Kroeger, and R. I. Morimoto. 1995. The carboxyl-terminal domain of heat shock factor 1 is negatively regulated and stress responsive. Mol. Cell. Biol. 15:4309-4318.
61. Shi, Y., J. S. Lee, and K. M. Gavin. 1997. Everything you have ever wanted to know about Yin Yang 1. Biochim. Biophys. Acta 1332:49-66.
62. Shi, Y., D. D. Mosser, and R. I. Morimoto. 1998. Molecular chaperones as HSF1-specific transcriptional repressers. Genes Dev. 12:654-666.
63. Shue, G., and D. S. Kohtz. 1994. Structural and functional aspects of basic helix-loop-helix protein folding by heat-shock protein 90. J. Biol. Chem. 269:2707-2711.
64. 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.
65. Smith, D. F., M. W. Albers, S. L. Schreiber, K. L. Leach, and M. R. Deibel. 1993. FKBP54, a novel FK506-binding protein in avian progesterone receptor complexes and HeLa extracts. J. Biol. Chem. 268:24270-24273.
66. Smith, D. F., L. Whitesell, S. Nair, S. Chen, V. Prapapanich, and R. A. Rimerman. 1995. Progesterone receptor structure and function altered by geldanamycin, an hsp90-binding agent. Mol. Cell. Biol. 15:6804-6812.
67. Sorger, P. K. 1990. Yeast heat shock factor contains separable transient and sustained response transcriptional activators. Cell 62:793-805.
68. Stebbins, C. E., A. A. Russo, C. Schneider, N. Rosen, F. U. Hartl, and N. P. Pavletich. 1997. Costal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent. Cell 18:239-250.
69. Thalasiraman. V., and R. L. Matts. 1996. Effect of geldanamycin on the kinetics of chaperone-mediated renaturation of firefly luciferase in rabbit reticulocyte lysate. Biochemistry 35:13443-13450.
70. Uma, S., S. D. Hartson, J. J. Chen, and R. L. Matts. 1997. Hsp90 is obligatory for the heme-regulaled eIF-2a kinase to acquire and maintain an activatable conformation. J. Biol. Chem. 272:11648-11656.
71. Westwood, J. T., and C. Wu. 1993. Activation of Drosophila heat shock factor: conformational change associated with a monomer-to-trimer transition. Mol. Cell Biol. 13:3481-3486.
72. v-src heteroprotein complex formation by bezoquinone ansamycins: essential role for stress proteins in oncogenic transformation. Proc. Natl. Acad. Sci. USA 91:8324-8328.
73. Winegarden, N. A., K. S. Wong, M. Sopta, and J. T. Westwood. 1996. Sodium salicylate decreases intracellular ATP, induces both heat shock factor binding and chromosomal puffing, but does not induce hsp70 gene transcription in Drosophila. J. Biol. Chem. 271:26971-26980.
74. Wu, C. 1995. Heat shock transcription factors: structure and regulation. Annu. Rev. Cell Dev. Biol. 11:441-469.
75. Xia, W., and R. Voellmy. 1997. Hyperphosphorylation of heat shock transcription factor 1 is correlated with transcriptional competence and slow dissociation of active factor trimers, J. Biol. Chem. 272:4094-4102.
76. Zou, J., R. Baler, G. Dahl, and R. Voellmy. 1994. Activation of the DNA-binding ability of human heat shock factor 1 may involve the transition from an intramolecular to an intermolecular triple-stranded coiled-coil structure. Mol. Cell. Biol. 14:7557-7568.
77. Zou, J., D. Rungger, and R. Voellmy. 1995. Multiple levels of regulation of human heat shock transcription factor 1. Mol. Cell. Biol. 15:4319-4330.