Reappraisal of the role of heat shock proteins as regulators of steroid receptor activity

Critical Reviews in Biochemistry and Molecular Biology

Volumn 33, Issue 6, 1998, Pages 437-466

  Ylikomi, T ^a,b   Wurtz, J M ^c   Syvala H ^a,d   Passinen, S ^a   Pekki, A ^a   Haverinen, M ^a   Blauer M ^a   Tuohimaa, P ^a   Gronemeyer, H ^c  

^a TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^b TAMPERE UNIVERSITY HOSPITAL   (Finland)

^c INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^d UNIVERSITY OF TAMPERE   (Finland)

Author keywords

Chaperoning; Heat shock protein; Nuclear localization; Steroid receptor

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; OLIGOMER; STEROID RECEPTOR;

ANIMAL TISSUE; CHICKEN; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REVIEW;

ANIMALS; HEAT-SHOCK PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; RECEPTORS, STEROID;

EID: 0032408110     PISSN: 10409238     EISSN: None     Source Type: Journal    
DOI: 10.1080/10409239891204279     Document Type: Review

References (204)

1. Renaud, J. P., Rochel, N., Ruff, M., Vivat, V., Chambon, P., Gronemeyer, H., and Moras, D., Crystal structure of the RAR-gamma ligand-binding domain bound to all-trans retinoic acid, Nature, 378(6558), 681, 1995.
2. Wurtz, J. M., Bourguet, W., Renaud, J. P., Vivat, V., Chambon, P., Moras, D., and Gronemeyer, H., A canonical structure for the ligand-binding domain of nuclear receptors, Nat Struct Biol, 3(2), 206, 1996.
3. 2a. Moras, D. and Gronemeyer, H., The nuclear receptor ligand-binding domain: structure and function, Curr Opin Cell Biol, 10(3), 384, 1998.
4. 2b. Torchia, J., Glass, C., and Rosenfeld, M. G., Co-activators and co-repressors in the integration of transcriptional responses, Curr Opin Cell Biol, 10(3), 373, 1998.
5. Pazin, M. J. and Kadonaga, J. T., What's up and down with histone deacetylation and transcription?, Cell, 89(3), 325, 1997.
6. Wade, P. A., Pruss, D., and Wolffe, A. P., Histone acetylation: chromatin in action, Trends Biochem Sci, 22(4), 128, 1997.
7. Wolffe, A. P., Transcriptional control. Sinful repression, Nature, 387(6628), 16, 1997.
8. Horwitz, K. B., Jackson, T. A., Bain, D. L., Richer, J. K., Takimoto, G. S., and Tung, L., Nuclear receptor coactivators and corepressors, Mol Endocrinol, 10(10), 1167, 1996.
9. Glass, C. K., Rose, D. W., and Rosenfeld, M. G., Nuclear receptor coactivators, Curr Opin Cell Biol, 9(2), 222, 1997.
10. Bocquel, M. T., Kumar, V., Stricker, C., Chambon, P., and Gronemeyer, H., The contribution of the N- and C-terminal regions of steroid receptors to activation of transcription is both receptor and cell-specific, Nucleic Acids Res, 17(7), 2581, 1989.
11. Meyer, M. E., Gronemeyer, H., Turcotte, B., Bocquel, M. T., Tasset, D., and Chambon, P., Steroid hormone receptors compete for factors that mediate their enhancer function, Cell, 57(3), 433, 1989.
12. Tasset, D., Tora, L., Fromental, C., Scheer, E., and Chambon, P., Distinct classes of transcriptional activating domains function by different mechanisms, Cell, 62(6), 1177, 1990.
13. Toft, D. and Gorski, J., A receptor molecule for estrogens: isolation from the rat uterus and preliminary characterization, Proc Natl Acad Sci USA, 55(6), 1574, 1966.
14. Jensen, E. V., Suzuki, T., Kawashima, T., Stumpf, W. E., Jungblut, P. W., and DeSombre, E. R., A two-step mechanism for the interaction of estradiol with rat uterus, Proc Natl Acad Sci USA, 59(2), 632, 1968.
15. Grody, W. W., Schrader, W. T., and O'Malley, B. W., Activation, transformation, and subunit structure of steroid hormone receptors, Endocr Rev, 3(2), 141, 1982.
16. Dougherty, J. J., Puri, R. K., and Toft, D. O., Polypeptide components of two 8 S forms of chicken oviduct progesterone receptor, J Biol Chem, 259(12), 8004, 1984.
17. Kost, S. L., Smith, D. F., Sullivan, W. P., Welch, W. J., and Toft, D. O., Binding of heat shock proteins to the avian progesterone receptor, Mol Cell Biol, 9(9), 3829, 1989.
18. Onate, S. A., Estes, P. A., Welch, W. J., Nordeen, S. K., and Edwards, D. P., Evidence that heat shock protein-70 associated with progesterone receptors is not involved in receptor-DNA binding, Mol Endocrinol, 5(12), 1993, 1991.
19. Smith, D. F., Dynamics of heat shock protein 90-progesterone receptor binding and the disactivation loop model for steroid receptor complexes, Mol Endocrinol, 7(11), 1418, 1993.
20. Joab, I., Radanyi, C., Renoir, M., Buchou, T., Catelli, M. G., Binart, N., Mester, J., and Baulieu, E. E., Common non-hormone binding component in non-transformed chick oviduct receptors of four steroid hormones, Nature, 308(5962), 850, 1984.
21. Baulieu, E. E., Antihormone-steroid hormonal activity, heat-shock protein hsp90 and receptors, Horm Res, 28(2-4), 181, 1987.
22. Dalman, F. C., Koenig, R. J., Perdew, G. H., Massa, E., and Pratt, W. B., In contrast to the glucocorticoid receptor, the thyroid hormone receptor is translated in the DNA binding state and is not associated with hsp90, J Biol Chem, 265(7), 3615, 1990.
23. 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., Retinoic acid receptor belongs to a subclass of nuclear receptors that do not form "docking" complexes with hsp90, Biochemistry, 30(22), 5605, 1991.
24. Whitfield, G. K., Hsieh, J. C., Nakajima, S., MacDonald, P. N., Thompson, P. D., Jurutka, P. W., Haussler, C. A., and Haussler, M. R., A highly conserved region in the hormone-binding domain of the human vitamin D receptor contains residues vital for heterodimerization with retinoid X receptor and for transcriptional activation Nov;9(11):1509, Mol Endocrinol, 9(9), 1166, 1995.
25. Bardwell, J. C. and Craig, E. A., Major heat shock gene of Drosophila and the Escherichia coli heat-inducible dnaK gene are homologous, Proc Natl Acad Sci USA, 81(3), 848, 1984.
26. Hunt, C. and Morimoto, R. I., Conserved features of eukaryotic hsp70 genes revealed by comparison with the nucleotide sequence of human hsp70, Proc Natl Acad Sci USA, 82(19), 6455, 1985.
27. Kelley, P. M. and Schlesinger, M. J., Antibodies to two major chicken heat shock proteins cross-react with similar proteins in widely divergent species, Mol Cell Biol, 2(3), 267, 1982.
28. Welch, W. J. and Feramisco, J. R., Purification of the major mammalian heat shock proteins, J Biol Chem, 257(24), 14949, 1982.
29. Burdon, R. H., Heat shock and the heat shock proteins, Biochem J, 240(2), 313, 1986.
30. Gething, M. J. and Sambrook, J., Protein folding in the cell, Nature, 355(6355), 33, 1992.
31. Hemmingsen, S. M., Woolford, C., van der Vies, S. M., Tilly, K., Dennis, D. T., Georgopoulos, C. P., Hendrix, R. W., and Ellis, R. J., Homologous plant and bacterial proteins chaperone oligomeric protein assembly, Nature, 333(6171), 330, 1988.
32. Hartl, F. U., Molecular chaperones in cellular protein folding, Nature, 381(6583), 571, 1996.
33. Buchner, J., Supervising the fold: functional principles of molecular chaperones, Faseb J, 10(1), 10, 1996.
34. Jakob, U. and Buchner, J., Assisting spontaneity: the role of Hsp90 and small Hsps as molecular chaperones, Trends Biochem Sci, 19(5), 205, 1994.
35. Ellis, R. J. and van der Vies, S. M., Molecular chaperones, Annu Rev Biochem, 60, 321, 1991.
36. Picard, D., Khursheed, B., Garabedian, M. J., Fortin, M. G., Lindquist, S., and Yamamoto, K. R., Reduced levels of hsp90 compromise steroid receptor action in vivo, Nature, 348(6297), 166, 1990.
37. Pratt, W. B., The role of heat shock proteins in regulating the function, folding, and trafficking of the glucocorticoid receptor, J Biol Chem, 268(29), 21455, 1993.
38. Baulieu, E. E., Binart, N., Cadepond, F., Catelli, M. G., Chambraud, B., Garnier, J., Gasc, J. M., Groyer-Schweizer, G., Oblin, M. E., Radanyi, C., and et al., Receptor-associated nuclear proteins and steroid/antisteroid action, Ann NY Acad Sci, 595, 300, 1990.
39. Smith, D. F. and Toft, D. O., Steroid receptors and their associated proteins, Mol Endocrinol, 7(1), 4, 1993.
40. Pratt, W. B. and Toft, D. O., Steroid receptor interactions with heat shock protein and immunophilin chaperones, Endocr Rev, 18(3), 306, 1997.
41. Halachmi, S., Marden, E., Martin, G., MacKay, H., Abbondanza, C., and Brown, M., Estrogen receptor-associated proteins: possible mediators of hormone-induced transcription, Science, 264(5164), 1455, 1994.
42. Cavailles, V., Dauvois, S., Danielian, P. S., and Parker, M. G., Interaction of proteins with transcriptionally active estrogen receptors, Proc Natl Acad Sci USA, 91(21), 10009, 1994.
43. Cavailles, V., Dauvois, S., L'Horset, F., Lopez, G., Hoare, S., Kushner, P. J., and Parker, M. G., Nuclear factor RIP140 modulates transcriptional activation by the estrogen receptor, Embo J, 14(15), 3741, 1995.
44. Chen, J. D. and Evans, R. M., A transcriptional co-repressor that interacts with nuclear hormone receptors, Nature, 377(6548), 454, 1995.
45. Horlein, A. J., Naar, A. M., Heinzel, T., Torchia, J., Gloss, B., Kurokawa, R., Ryan, A., Kamei, Y., Soderstrom, M., Glass, C. K., and Rosenfeld, M. G., Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor, Nature, 377(6548), 397, 1995.
46. LeDouarin, B., Zechel, C., Garnier, J. M., Lutz, Y., Tora, L., Pierrat, P., Heery, D., Gronemeyer, H., Chambon, P., and Losson, R., The N-terminal part of TIF1, a putative mediator of the ligand-dependent activation function (AF-2) of nuclear receptors, is fused to B-raf in the oncogenic protein T18, Embo J, 14(9), 2020, 1995.
47. Voegel, J. J., Heine, M. J., Zechel, C., Chambon, P., and Gronemeyer, H., TIF2, a 160 kDa transcriptional mediator for the ligand-dependent activation function AF-2 of nuclear receptors, Embo J, 15(14), 3667, 1996.
48. vom Baur, E., Zechel, C., Heery, D., Heine, M. J., Garnier, J. M., Vivat, V., Le Douarin, B., Gronemeyer, H., Chambon, P., and Losson, R., Differential ligand-dependent interactions between the AF-2 activating domain of nuclear receptors and the putative transcriptional intermediary factors mSUG1 and TIF1, Embo J, 15(1), 110, 1996.
49. Renoir, J. M. and Mester, J., Chick oviduct progesterone receptor: structure, immunology, function, Mol Cell Endocrinol, 37(1), 1, 1984.
50. Catelli, M. G., Binart, N., Jung-Testas, I., Renoir, J. M., Baulieu, E. E., Feramisco, J. R., and Welch, W. J., The common 90-kd protein component of non-transformed '8S' steroid receptors is a heat-shock protein, Embo J, 4(12), 3131, 1985.
51. Schuh, S., Yonemoto, W., Brugge, J., Bauer, V. J., Riehl, R. M., Sullivan, W. P., and Toft, D. O., A 90,000-dalton binding protein common to both steroid receptors and the Rous sarcoma virus transforming protein, pp60v-src, J Biol Chem, 260(26), 14292, 1985.
52. Sanchez, E. R., Toft, D. O., Schlesinger, M. J., and Pratt, W. B., Evidence that the 90-kDa phosphoprotein associated with the untransformed L-cell glucocorticoid receptor is a murine heat shock protein, J Biol Chem, 260(23), 12398, 1985.
53. Prapapanich, V., Chen, S., Nair, S. C., Rimerman, R. A., and Smith, D. F., Molecular cloning of human p48, a transient component of progesterone receptor complexes and an Hsp70-binding protein, Mol Endocrinol, 10(4), 420, 1996.
54. Smith, D. F., Schowalter, D. B., Kost, S. L., and Toft, D. O., Reconstitution of progesterone receptor with heat shock proteins, Mol Endocrinol, 4(11), 1704, 1990.
55. Johnson, J. L., Beito, T. G., Krco, C. J., and Toft, D. O., Characterization of a novel 23-kilodalton protein of unactive progesterone receptor complexes, Mol Cell Biol, 14(3), 1956, 1994.
56. Ferris, D. K., Harel-Bellan, A., Morimoto, R. I., Welch, W. J., and Farrar, W. L., Mitogen and lymphokine stimulation of heat shock proteins in T lymphocytes, Proc Natl Acad Sci USA, 85(11), 3850, 1988.
57. Ramachandran, C., Catelli, M. G., Schneider, W., and Shyamala, G., Estrogenic regulation of uterine 90-kilodalton heat shock protein, Endocrinology, 123(2), 956, 1988.
58. Moore, S. K., Kozak, C., Robinson, E. A., Ullrich, S. J., and Appella, E., Murine 86- and 84-kDa heat shock proteins, cDNA sequences, chromosome assignments, and evolutionary origins, J Biol Chem, 264(10), 5343, 1989.
59. Minami, Y., Kawasaki, H., Miyata, Y., Suzuki, K and Yahara, I., Analysis of native forms and isoform compositions of the mouse 90-kDa heat shock protein, HSP90, J Biol Chem, 266(16), 10099, 1991.
60. Jerome, V., Vourc'h, C., Baulieu, E. E., and Catelli, M. G., Cell cycle regulation of the chicken hsp90 alpha expression, Exp Cell Res, 205(1), 44, 1993.
61. Meng, X., Jerome, V., Devin, J., Baulieu, E. E., and Catelli, M. G., Cloning of chicken hsp90 beta: the only vertebrate hsp90 insensitive to heat shock, Biochem Biophys Res Commun, 190(2), 630, 1993.
62. Radanyi, C., Renoir, J. M., Sabbah, M., and Baulieu, E. E., Chick heat-shock protein of Mr = 90,000, free or released from progesterone receptor, is in a dimeric form, J Biol Chem, 264(5), 2568, 1989.
63. Bresnick, E. H., Dalman, F. C., and Pratt, W. B., Direct stoichiometric evidence that the untransformed Mr 300,000, 9S, glucocorticoid receptor is a core unit derived from a larger heteromeric complex, Biochemistry, 29(2), 520, 1990.
64. Stancato, L. F., Chow, Y. H., Hutchison, K. A., Perdew, G. H., Jove, R., and Pratt, W. B., Raf exists in a native heterocomplex with hsp90 and p50 that can be reconstituted in a cell-free system, J Biol Chem, 268(29), 21711, 1993.
65. Hutchison, K. A., Brott, B. K., De Leon, J. H., Perdew, G. H., Jove, R., and Pratt, W. B., Reconstitution of the multiprotein complex of pp60src, hsp90, and p50 in a cell-free system, J Biol Chem, 267(5), 2902, 1992.
66. Miyata, Y. and Yahara, I., The 90-kDa heat shock protein, HSP90, binds and protects casein kinase II from self-aggregation and enhances its kinase activity, J Biol Chem, 267(10), 7042, 1992.
67. Matts, R. L. and Hurst, R., Evidence for the association of the heme-regulated eIF-2 alpha kinase with the 90-kDa heat shock protein in rabbit reticulocyte lysate in situ, J Biol Chem, 264(26), 15542, 1989.
68. Wright, L. S., Finn, K. A., and Siegel, F. L., Concomitant preparative isolation of calmodulin and heat shock protein (hsp90) from bovine testes, Protein Expr Purif, 4(5), 417, 1993.
69. Denis, M., Cuthill, S., Wikstrom, A. C., Poellinger, L., and Gustafsson, J. A., Association of the dioxin receptor with the Mr 90,000 heat shock protein: a structural kinship with the glucocorticoid receptor, Biochem Biophys Res Commun, 155(2), 801, 1988.
70. Nair, S. C., Toran, E. J., Rimerman, R. A., Hjermstad, S., Smithgall, T. E., and Smith, D. F., A pathway of multi-chaperone interactions common to diverse regulatory proteins: estrogen receptor, Fes tyrosine kinase, heat shock transcription factor Hsfl, and the aryl hydrocarbon receptor, Cell Stress Chaperones, 1(4), 237, 1996.
71. Cutforth, T. and Rubin, G. M., Mutations in Hsp83 and cdc37 impair signaling by the sevenless receptor tyrosine kinase in Drosophila, Cell, 77(7), 1027, 1994.
72. Xu, Y. and Lindquist, S., Heat-shock protein hsp90 governs the activity of pp60v-src kinase, Proc Natl Acad Sci USA, 90(15), 7074, 1993.
73. 70a. Rutherford, S. L. and Lindquist, S., Hsp90 as a capacitor for morphological evolution, Nature, 396, 336, 1998.
74. Ang, D., Liberek, K., Skowyra, D., Zylicz, M., and Georgopoulos, C., Biological role and regulation of the universally conserved heat shock proteins, J Biol Chem, 266(36), 24233, 1991.
75. Rothman, J. E., Polypeptide chain binding proteins: catalysts of protein folding and related processes in cells, Cell, 59(4), 591, 1989.
76. Craig, E. A. and Gross, C. A., Is hsp70 the cellular thermometer?, Trends Biochem Sci, 16(4), 135, 1991.
77. Hendrick, J. P. and Hartl, F. U., Molecular chaperone functions of heat-shock proteins, Annu Rev Biochem, 62, 349, 1993.
78. Smith, D. F., Sullivan, W. P., Marion, T. N., Zaitsu, K., Madden, B., McCormick, D. J., and Toft, D. O., Identification of a 60-kilodalton stress-related protein, p60, which interacts with hsp90 and hsp70, Mol Cell Biol, 13(2), 869, 1993.
79. Howard, K. J. and Distelhorst, C. W., Evidence for intracellular association of the glucocorticoid receptor with the 90-kDa heat shock protein, J Biol Chem, 263(7), 3474, 1988.
80. Smith, D. F., Stensgard, B. A., Welch, W. J., and Toft, D. O., Assembly of progesterone receptor with heat shock proteins and receptor activation are ATP mediated events, J Biol Chem, 267(2), 1350, 1992.
81. Honore, B., Leffers, H., Madsen, P., Rasmussen, H. H., Vandekerckhove, J., and Celis, J. E., Molecular cloning and expression of a transformation-sensitive human protein containing the TPR motif and sharing identity to the stress-inducible yeast protein STIl, J Biol Chem, 267(12), 8485, 1992.
82. Tai, P. K., Maeda, Y., Nakao, K., Wakim, N. G., Duhring, J. L., and Faber, L. E., A 59-kilodalton protein associated with progestin, estrogen, androgen, and glucocorticoid receptors, Biochemistry, 25(18), 5269, 1986.
83. Renoir, J. M., Radanyi, C., Faber, L. E., and Baulieu, E. E., The non-DNA-binding heterooligomeric form of mammalian steroid hormone receptors contains a hsp90-bound 59-kilodalton protein, J Biol Chem, 265(18), 10740, 1990.
84. Sanchez, E. R., Faber, L. E., Henzel, W. J., and Pratt, W. B., The 56-59-kilodalton protein identified in untransformed steroid receptor complexes is a unique protein that exists in cytosol in a complex with both the 70- and 90-kilodalton heat shock proteins, Biochemistry, 29(21), 5145, 1990.
85. Sanchez, E. R., Hsp56: a novel heat shock protein associated with untransformed steroid receptor complexes, J Biol Chem, 265(36), 22067, 1990.
86. Tai, P. K., Albers, M. W., Chang, H., Faber, L. E., and Schreiber, S. L., Association of a 59-kilodalton immunophilin with the glucocorticoid receptor complex, Science, 256(5061), 1315, 1992.
87. Peattie, D. A., Harding, M. W., Fleming, M. A., DeCenzo, M. T., Lippke, J. A., Livingston, D. J., and Benasutti, M., Expression and characterization of human FKBP52, an immunophilin that associates with the 90-kDa heat shock protein and is a component of steroid receptor complexes, Proc Natl Acad Sci USA, 89(22), 10974, 1992.
88. Wiederrecht, G., Hung, S., Chan, H. K., Marcy, A., Martin, M., Calaycay, J., Boulton, D., Sigal, N., Kincaid, R. L., and Siekierka, J. J., Characterization of high molecular weight FK-506 binding activities reveals a novel FK-506-binding protein as well as a protein complex, J Biol Chem, 267(30), 21753, 1992.
89. Callebaut, I., Renoir, J. M., Lebeau, M. C., Massol, N., Burny, A., Baulieu, E. E., and Mornon, J. P., An immunophilin that binds M(r) 90,000 heat shock protein: main structural features of a mammalian p59 protein, Proc Natl Acad Sci USA, 89(14), 6270, 1992.
90. Ratajczak, T., Carrello, A., Mark, P. J., Warner, B. J., Simpson, R. J., Moritz, R. L., and House, A. K., The cyclophilin component of the unactivated estrogen receptor contains a tetratricopeptide repeat domain and shares identity with p59 (FKBP59), J Biol Chem, 268(18), 13187, 1993.
91. Milad, M., Sullivan, W., Diehl, E., Altmann, M., Nordeen, S., Edwards, D. P., and Toft, D. O., Iteraction of the progesterone receptor with binding proteins for FK506 and cyclosporin A, Mol Endocrinol, 9(7), 838, 1995.
92. Owens-Grillo, J. K., Hoffmann, K., Hutchison, K. A., Yem, A. W., Deibel, M. R., Jr., Handschumacher, R. E., and Pratt, W. B., The cyclosporin A-binding immunophilin CyP-40 and the FK506-binding immunophilin hsp56 bind to a common site on hsp90 and exist in independent cytosolic heterocomplexes with the untransformed glucocorticoid receptor, J Biol Chem, 270(35), 20479, 1995.
93. Smith, D. F., Baggenstoss, B. A., Marion, T. N., and Rimerman, R. A., Two FKBP-related proteins are associated with progesterone receptor complexes, J Biol Chem, 268(24), 18365, 1993.
94. Rexin, M., Busch, W., and Gehring, U., Protein components of the nonactivated glucocorticoid receptor, J Biol Chem, 266(36), 24601, 1991.
95. Hutchison, K. A., Scherrer, L. C., Czar, M. J., Ning, Y., Sanchez, E. R., Leach, K. L., Deibel, M. R., Jr., and Pratt, W. B., FK506 binding to the 56-kilodalton immunophilin (Hsp56) in the glucocorticoid receptor heterocomplex has no effect on receptor folding or function, Biochemistry, 32(15), 3953, 1993.
96. Schreiber, S. L. and Crabtree, G. R., The mechanism of action of cyclosporin A and FK506, Immunol Today, 13(4), 136, 1992.
97. Hohfeld, J., Minami, Y., and Hartl, F. U., Hip, a novel cochaperone involved in the eukaryotic Hsc70/Hsp40 reaction cycle, Cell, 83(4), 589, 1995.
98. Caplan, A. J., Langley, E., Wilson, E. M., and Vidal, J., Hormone-dependent transactivation by the human androgen receptor is regulated by a dnaJ protein, J Biol Chem, 270(10), 5251, 1995.
99. Kimura, Y., Yahara, I., and Lindquist, S., Role of the protein chaperone YDJ1 in establishing Hsp90-mediated signal transduction pathways, Science, 268(5215), 1362, 1995.
100. Johnson, J. L. and Toft, D. O., A novel chaperone complex for steroid receptors involving heat shock proteins, immunophilins, and p23, J Biol Chem, 269(40), 24989, 1994.
101. Perdew, G. H. and Whitelaw, M. L., Evidence that the 90-kDa heat shock protein (HSP90) exists in cytosol in heteromeric complexes containing HSP70 and three other proteins with Mr of 63,000, 56,000, and 50,000, J Biol Chem, 266(11), 6708, 1991.
102. Sanchez, E. R., Meshinchi, S., Tienrungroj, W., Schlesinger, M. J., Toft, D. O., and Pratt, W. B., Relationship of the 90-kDa murine heat shock protein to the untransformed and transformed states of the L cell glucocorticoid receptor, J Biol Chem, 262(15), 6986, 1987.
103. Srinivasan, G., Patel, N. T., and Thompson, E. B., Heat shock protein is tightly associated with the recombinant human glucocorticoid receptor: glucocorticoid response element complex, Mol Endocrinol, 8(2), 189, 1994.
104. Scherrer, L. C., Dalman, F. C., Massa, E., Meshinchi, S., and Pratt, W. B., Structural and functional reconstitution of the glucocorticoid receptor-hsp90 complex, J Biol Chem, 265(35), 21397, 1990.
105. Sabbah, M., Radanyi, C., Redeuilh, G., and Baulieu, E. E., The 90 kDa heat shock protein (hsp90) modulates the binding of the estrogen receptor to its cognate DNA, Biochem J, 314(Pt 1), 205, 1996.
106. Pratt, W. B., Transformation of glucocorticoid and progesterone receptors to the DNA-binding state, J Cell Biochem, 35(1), 51, 1987.
107. Bagchi, M. K., Tsai, S. Y., Tsai, M. J., and O'Malley, B. W., Progesterone enhances target gene transcription by receptor free of heat shock proteins hsp90, hsp56, and hsp70, Mol Cell Biol, 11(10), 4998, 1991.
108. Wagner, R. L., Apriletti, J. W., McGrath, M. E., West, B. L., Baxter, J. D., and Fletterick, R. J., A structural role for hormone in the thyroid hormone receptor, Nature, 378(6558), 690, 1995.
109. Shaknovich, R., Shue, G., and Kohtz, D. S., Conformational activation of a basic helix-loop-helix protein (MyoD1) by the C-terminal region of murine HSP90 (HSP84), Mol Cell Biol, 12(11), 5059, 1992.
110. Inano, K., Curtis, S. W., Korach, K. S., Omata, S., and Horigome, T., Heat shock protein 90 strongly stimulates the binding of purified estrogen receptor to its responsive element, J Biochem (Tokyo), 116(4), 759, 1994.
111. Bresnick, E. H., Dalman, F. C., Sanchez, E. R., and Pratt, W. B., Evidence that the 90-kDa heat shock protein is necessary for the steroid binding conformation ofthe L cell glucocorticoid receptor, J Biol Chem, 264(9), 4992, 1989.
112. Ohara-Nemoto, Y., Stromstedt, P. E., Dahlman-Wright, K., Nemoto, T., Gustafsson, J. A., and Carlstedt-Duke, J., The steroid-binding properties of recombinant glucocorticoid receptor: a putative role for heat shock protein hsp90, J Steroid Biochem Mol Biol, 37(4), 481, 1990.
113. Nemoto, T., Ohara-Nemoto, Y., and Ota, M., Association of the 90-kDa heat shock protein does not affect the ligand-binding ability of androgen receptor, J Steroid Biochem Mol Biol, 42(8), 803, 1992.
114. Eul, J., Meyer, M. E., Tora, L., Bocquel, M. T., Quirin-Stricker, C., Chambon, P., and Gronemeyer, H., Expression of active hormone and DNA-binding domains of the chicken progesterone receptor in E. coli, Embo J, 8(1), 83, 1989.
115. Groyer, A., Schweizer-Groyer, G., Cadepond, F., Mariller, M., and Baulieu, E. E., Antiglucocorticosteroid effects suggest why steroid hormone is required for receptors to bind DNA in vivo but not in vitro, Nature, 328(6131), 624, 1987.
116. Renoir, J. M., Radanyi, C., and Baulieu, E. E., The antiprogesterone RU486 stabilizes the heterooligomeric, non-DNA-binding, 8S-form of the rabbit uterus cytosol progesterone receptor, Steroids, 53(1-2), 1, 1989.
117. Baulieu, E. E., Contragestion and other clinical applications of RU486, an antiprogesterone at the receptor, Science, 245(4924), 1351, 1989.
118. Meyer, M. E., Pornon, A., Ji, J. W., Bocquel, M. T., Chambon, P., and Gronemeyer, H., Agonistic and antagonistic activities of RU486 on the functions of the human progesterone receptor, Embo J, 9(12), 3923, 1990.
119. Klein-Hitpass, L., Cato, A. C., Henderson, D., and Ryffel, G. U., Two types of antiprogestins identified by their differential action in transcriptionally active extracts from T47D cells, Nucleic Acids Res, 19(6), 1227, 1991.
120. 116a. Becker, P. B., Gloss, B., Schmid, W., Strable, U., and Schutz, G., In vivo protein-DNA interactions in a glucocorticoid response element require the presence of the hormone, Nature, 324(6098), 686, 1986.
121. 116b. Truss, M., Bartsch, J., and Beato, M., Antiprogestins prevent progesterone receptor binding to hormone responsive elements in vivo, Proc Natl Acad Sci USA, 91(24), 11333, 1994.
122. Couette, B., Lombes, M., Baulieu, E. E., and Rafestin-Oblin, M. E., Aldosterone antagonists destabilize the mineralocorticosteroid receptor, Biochem., 282(Pt 3), 697, 1992.
123. Langer, T., Lu, C., Echols, H., Flanagan, J., Hayer, M. X., and Hartl, F. U., Successive action of DnaK, DnaJ and GroEL along the pathway of chaperone-mediated protein folding, Nature, 356(6371), 683, 1992.
124. Jakob, U., Lilie, H., Meyer, I., and Buchner, J., Transient interaction of Hsp90 with early unfolding intermediates of citrate synthase. Implications for heat shock in vivo, J Biol Chem, 270(13), 7288, 1995.
125. Skowyra, D., Georgopoulos, C., and Zylicz, M., The E. coli dnaK gene product, the hsp70 homolog, can reactivate heat-inactivated RNA polymerase in an ATP hydrolysis-dependent manner, Cell, 62(5), 939, 1990.
126. Hendrick, J. P., Langer, T., Davis, T. A., Hartl, F. U., and Wiedmann, M., Control of folding and membrane translocation by binding of the chaperone DnaJ to nascent polypeptides, Proc Natl Acad Sci USA, 90(21), 10216, 1993.
127. Freeman, B. C., Toft, D. O., and Morimoto, R. I., Molecular chaperone machines: chaperone activities of the cyclophilin Cyp-40 and the steroid aporeceptor-associated protein p23, Science, 274(5293), 1718, 1996.
128. Wiech, H., Buchner, J., Zimmermann, R., and Jakob, U., Hsp90 chaperones protein folding in vitro, Nature, 358 (6382), 169, 1992.
129. Smith, D. F. and Toft, D. O., Composition, assembly and activation of the avian progesterone receptor, J Steroid Biochem Mol Biol, 41(3-8), 201, 1992.
130. Hutchison, K. A., Czar, M. J., Scherrer, L. C., and Pratt, W. B., Monovalent cation selectivity for ATP-dependent association of the glucocorticoid receptor with hsp70 and hsp90, J Biol Chem, 267(20), 14047, 1992.
131. Kaufmann, S. H., Wright, W. W., Okret, S., Wikstrom, A. C., Gustafsson, J. A., Shaper, N. L., and Shaper, J. H., Evidence that rodent epididymal sperm contain the Mr approximately 94,000 glucocorticoid receptor but lack the Mr approximately 90,000 heat shock protein, Endocrinology, 130(5), 3074, 1992.
132. Bohen, S. P. and Yamamoto, K. R., Isolation of Hsp90 mutants by screening for decreased steroid receptor function, Proc Natl Acad Sci USA, 90(23), 11424, 1993.
133. Holley, S. J. and Yamamoto, K. R., A role for Hsp90 in retinoid receptor signal transduction, Mol Biol Cell, 6(12), 1833, 1995.
134. Ning, Y. M. and Sanchez, E. R., Potentiation of glucocorticoid receptor-mediated gene expression by the immunophilin ligands FK506 and rapamycin, J Biol Chem, 268(9), 6073, 1993.
135. Tai, P. K., Albers, M. W., McDonnell, D. P., Chang, H., Schreiber, S. L., and Faber, L. E., Potentiation of progesterone receptor-mediated transcription by the immunosuppressant FK506, Biochemistry, 33(35), 10666, 1994.
136. Jung-Testas, I., Delespierre, B., and Baulieu, E.-E., The immunosuppressant FK506 inhibits the antigluco-corticosteroid activity of RU486 on the growth of mouse fibroblasts in culture, C.R. Acad. Sci. Paris, 316, 1493, 1993.
137. Renoir, J. M., Le Bihan, S., Mercier-Bodard, C., Gold, A., Arjomandi, M., Radanyi, C., and Baulieu, E. E., Effects of immunosuppressants FK506 and rapamycin on the heterooligomeric form of the progesterone receptor, J Steroid Biochem Mol Biol, 48(1), 101, 1994.
138. Kralli, A. and Yamamoto, K. R., An FK506-sensitive transporter selectively decreases intracellular levels and potency of steroid hormones, J Biol Chem, 271(29), 17152, 1996.
139. Czar, M. J., Lyons, R. H., Welsh, M. J., Renoir, J. M., and Pratt, W. B., Evidence that the FK506-binding immunophilin heat shock protein 56 is required for trafficking of the glucocorticoid receptor from the cytoplasm to the nucleus, Mol Endocrinol, 9(11), 1549, 1995.
140. Deshaies, R. J., Koch, B. D., Werner-Washburne, M., Craig, E. A., and Schekman, R., A subfamily of stress proteins facilitates translocation of secretory and mitochondrial precursor polypeptides, Nature. 332(6167), 800, 1988.
141. Chirico, W. J., Waters, M. G., and Blobel, G., 70K heat shock related proteins stimulate protein translocation into microsomes, Nature, 332(6167), 805, 1988.
142. Powers, M. A. and Forbes, D. J., Cytosolic factors in nuclear transport: what's importin?, Cell, 79(6), 931, 1994.
143. Mandell, R. B. and Feldherr, C. M., Identification of two HSP70-related Xenopus oocyte proteins that are capable of recycling across the nuclear envelope, J Cell Biol, 111(5 Pt 1), 1775, 1990.
144. Imamoto, N., Matsuoka, Y., Kurihara, T., Kohno, K., Miyagi, M., Sakiyama, F., Okada, Y., Tsunasawa, S., and Yoneda, Y., Antibodies against 70-kD heat shock cognate protein inhibit mediated nuclear import of karyophilic proteins, J Cell Biol, 119(5), 1047, 1992.
145. Yang, J. and DeFranco, D. B., Differential roles of heat shock protein 70 in the in vitro nuclear import of glucocorticoid receptor and simian virus 40 large tumor antigen, Mol Cell Biol, 14(8), 5088, 1994.
146. Jeoung, D. I., Chen, S., Windsor, J., and Pollack, R. E., Human major HSP70 protein complements the localization and functional defects of cytoplasmic mutant SV40 T antigen in Swiss 3T3 mouse fibroblast cells, Genes Dev, 5(12A), 2235, 1991.
147. Yang, J. and DeFranco, D. B., Assessment of glucocorticoid receptor-heat shock protein 90 interactions in vivo during nucleocytoplasmic trafficking, Mol Endocrinol, 10(1), 3, 1996.
148. Goldstein, L., Localization of nucleus-specific protein as shown by transplantation experiments in Amoeba proteus, Exp Cell Res, 15, 635, 1958.
149. Goldstein, L. and Ko, C., Distribution of proteins between nucleus and cytoplasm of Amoeba proteus, J Cell Biol, 88(3), 516, 1981.
150. Guiochon-Mantel, A., Lescop, P., Christin-Maitre, S., Loosfelt, H., Perrot-Applanat, M., and Milgrom, E., Nucleocytoplasmic shuttling of the progesterone receptor, Embo J, 10(12), 3851, 1991.
151. Guiochon-Mantel, A., Delabre, K., Lescop, P., and Milgrom, E., Nuclear localization signals also mediate the outward movement of proteins from the nucleus, Proc Natl Acad Sci USA, 91(15), 7179, 1994.
152. Htun, H., Barsony, J., Renyi, I., Gould, D. L., and Hager, G. L., Visualization of glucocorticoid receptor translocation and intranuclear organization in living cells with a green fluorescent protein chimera, Proc Natl Acad Sci USA, 93(10), 4845, 1996.
153. Wikstrom, A. C., Bakke, O., Okret, S., Bronnegard, M., and Gustafsson, J. A., Intracellular localization of the glucocorticoid receptor: evidence for cytoplasmic and nuclear localization, Endocrinology, 120(4), 1232, 1987.
154. Gasc, J. M., Delahaye, F., and Baulieu, E. E., Compared intracellular localization of the glucocorticosteroid and progesterone receptors: an immunocytochemical study, Exp Cell Res, 181(2), 492, 1989.
155. Govindan, M. V., Immunofluorescence microscopy of the intracellular translocation of glucocorticoid-receptor complexes in rat hepatoma (HTC) cells, Exp Cell Res, 127(2), 293, 1980.
156. Pekki, A., Koistinaho, J., Ylikomi, T., Vilja, P., Westphal, H., and Touhimaa, P., Subcellular location of unoccupied and occupied glucocorticoid receptor by a new immunohistochemical technique, J Steroid Biochem Mol Biol, 41(3-8), 753, 1992.
157. Brink, M., Humbel, B. M., De Kloet, E. R., and Van Driel, R., The unliganded glucocorticoid receptor is localized in the nucleus, not in the cytoplasm, Endocrinology, 130(6), 3575, 1992.
158. Ylikomi, T., Bocquel, M. T., Berry, M., Gronemeyer, H., and Chambon, P., Cooperation of proto-signals for nuclear accumulation of estrogen and progesterone receptors, Embo J, 11(10), 3681, 1992.
159. Picard, D. and Yamamoto, K. R., Two signals mediate hormone-dependent nuclear localization of the glucocorticoid receptor, Embo J, 6(11), 3333, 1987.
160. Verdi, J. M. and Campagnoni, A. T., Translational regulation by steroids. Identification of a steroid modulatory element in the 5′-untranslated region of the myelin basic protein messenger RNA, J Biol Chem, 265(33), 20314, 1990.
161. Migliaccio, A., Di Domenico, M., Castoria, G., de Falco, A., Bontempo, P., Nola, E., and Auricchio, F., Tyrosine kinase/p21ras/MAP-kinase pathway activation by estradiol-receptor complex in MCF-7 cells, Embo J, 15(6), 1292, 1996.
162. Wen, W., Meinkoth, J. L., Tsien, R. Y., and Taylor, S. S., Identification of a signal for rapid export of proteins from the nucleus, Cell, 82(3), 463, 1995.
163. Schowalter, D. B., Sullivan, W. P., Maihle, N. J., Dobson, A. D., Conneely, O. M., O'Malley, B. W., and Toft, D. O., Characterization of progesterone receptor binding to the 90- and 70-kDa heat shock proteins, J Biol Chem, 266(31), 21165, 1991.
164. Dalman, F. C., Scherrer, L. C., Taylor, L. P., Akil, H., and Pratt, W. B., Localization of the 90-kDa heat shock protein-binding site within the hormone-binding domain of the glucocorticoid receptor by peptide competition, J Biol Chem, 266(6), 3482, 1991.
165. Marivoet, S., Van Dijck, P., Verhoeven, G., and Heyns, W., Interaction of the 90-kDa heat shock protein with native and in vitro translated androgen receptor and receptor fragments, Mol Cell Endocrinol, 88(1-3), 165, 1992.
166. Chambraud, B., Berry, M., Redeuilh, G., Chambon, P., and Baulieu, E. E., Several regions of human estrogen receptor are involved in the formation of receptor-heat shock protein 90 complexes, J Biol Chem, 265(33), 20686, 1990.
167. Carson-Jurica, M. A., Lee, A. T., Dobson, A. W., Conneely, O. M., Schrader, W. T., and O'Malley, B. W., Iteraction of the chicken progesterone receptor with heat shock protein (HSP) 90, J Steroid Biochem, 34(1-6), 1, 1989.
168. Schlatter, L. K., Howard, K. J., Parker, M. G., and Distelhorst, C. W., Comparison of the 90-kilodalton heat shock protein interaction with in vitro translated glucocorticoid and estrogen receptors, Mol Endocrinol, 6(1), 132, 1992.
169. Bourguet, W., Ruff, M., Chambon, P., Gronemeyer, H., and Moras, D., Crystal structure of the ligand-binding domain of the human nuclear receptor RXR-alpha, Nature, 375(6530), 377, 1995.
170. 164a. Brzozowski, A. M., Pike, A. C., Dauter, Z., Hubbard, R. E., Bonn, T., Engstrom, O., Ohman, L., Greene, G. L., Gustafsson, J. A., and Carlquist, M., Molecular basis of agonism and antagonism in the estrogen receptor, Nature, 389(6652), 753, 1997.
171. 164b. Williams, S. P. and Sigler, P. B., Atomic structure of progesterone complexed with its receptor, Nature, 393(6683), 392, 1998.
172. 164c. Tanenbaum, D. M., Wang, Y., Williams, S. P., and Sigler, P. B., Crystallographic comparison of the estrogen and progesterone receptor's ligand binding domains, Proc Natl Acad Sci USA, 95(11), 5998, 1998.
173. Iwasaki, M., Saito, H., Yamamoto, M., Korach, K. S., Hirogome, T., and Sugano, H., Purification of heat shock protein 90 from calf uterus and rat liver and characterization of the highly hydrophobic region, Biochim Biophys Acta, 992(1), 1, 1989.
174. Hansen, J. C. and Gorski, J., Conformational and electrostatic properties of unoccupied and liganded estrogen receptors determined by aqueous two-phase partitioning, Biochemistry, 24(22), 6078, 1985.
175. Fritsch, M., Leary, C. M., Furlow, J. D., Ahrens, H., Schuh, T. J., Mueller, G. C., and Gorski, J., A ligand-induced conformational change in the estrogen receptor is localized in the steroid binding domain, Biochemistry, 31(23), 5303, 1992.
176. Alnemri, E. S. and Litwack, G., The steroid binding domain influences intracellular solubility of the baculovirus overexpressed glucocorticoid and mineralocorticoid receptors, Biochemistry, 32(20), 5387, 1993.
177. Hansen, J. C. and Gorski, J., Conformational transitions of the estrogen receptor monomer. Effects of estrogens, antiestrogen, and temperature, J Biol Chem, 261(30), 13990, 1986.
178. Tuohimaa, P., Pekki, A., Blauer, M., Joensuu, T., Vilja, P., and Ylikomi, T., Nuclear progesterone receptor is mainly heat shock protein 90-free in vivo, Proc Natl Acad Sci USA, 90(12), 5848, 1993.
179. Denis, M. and Gustafsson, J. A., Translation of glucocorticoid receptor mRNA in vitro yields a nonactivated protein, J Biol Chem, 264(11), 6005, 1989.
180. Pekki, A. K., Different immunoelectron microscopic locations of progesterone receptor and HSP90 in chick oviduct epithelial cells, J Histochem Cytochem, 39(8), 1095, 1991.
181. Gasc, J. M., Renoir, J. M., Faber, L. E., Delahaye, F., and Baulieu, E. E., Nuclear localization of two steroid receptor-associated proteins, hsp90 and p59, Exp Cell Res, 186(2), 362, 1990.
182. Rexin, M., Busch, W., Segnitz, B., and Gehring, U., Structure of the glucocorticoid receptor in intact cells in the absence of hormone, J Biol Chem, 267(14), 9619, 1992.
183. Alexis, M. N., Mavridou, I., and Mitsiou, D. J., Subunit composition of the untransformed glucocorticoid receptor in the cytosol and in the cell, Eur J Biochem, 204(1), 75, 1992.
184. Kang, K. I., Devin, J., Cadepond, F., Jibard, N., Guiochon-Mantel, A., Baulieu, E. E., and Catelli, M. G., In vivo functional protein-protein-interaction: nuclear targeted hsp90 shifts cytoplasmic steroid receptor mutants into the nucleus, Proc Natl Acad Sci USA, 91(1), 340, 1994.
185. Pekki, A., Ylikomi, T., Syvala, H., and Tuohimaa, P., Progesterone receptor does not form oligomeric (8S), non-DNA-binding complex in intact cell nuclei, J Cell Biochem, 58(1), 95, 1995.
186. Passinen, S., Haverinen, M., Pekki, A., Rauta, J., Paranko, J., Syvälä, H., Tuohimaa, P., and Ylikomi, T., Only a small portion of cytoplasmic progesterone receptors is associated with hsp90 in vivo, Submitted, for publication.
187. Rossini, G. P. and Camellini, L., Oligomeric structures of cytosoluble estrogen receptor complexes as studied by anti-estrogen receptor antibodies and chemical crosslinking of intact cells, J Steroid Biochem Mol Biol, 50(5-6), 241, 1994.
188. Rossini, G. P., The quaternary structures of untransformed steroid hormone receptors: an open issue, J Theor Biol, 166(3), 339, 1994.
189. Segnitz, B. and Gehring, U., Subunit structure of the nonactivated human estrogen receptor, Proc Natl Acad Sci USA, 92(6), 2179, 1995.
190. Adam, S. A., Marr, R. S., and Gerace, L., Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors, J Cell Biol, 111(3), 807, 1990.
191. Markland, W., Smith, A. E., and Roberts, B. L., Signal-dependent translocation of simian virus 40 large-T antigen into rat liver nuclei in a cell-free system, Mol Cell Biol, 7(12), 4255, 1987.
192. Haverinen, M., Syvälä, H., Passinen, S., Tuohimaa, P., and Ylikomi, T., Progesterone receptor but not hsp90 is transported into the nucleus in in vitro nuclear transport assays with the receptor-hsp90 heterooligomer, manuscript.
193. Stancato, L. F., Hutchison, K. A., Krishna, P., and Pratt, W. B., Animal and plant cell lysates share a conserved chaperone system that assembles the glucocorticoid receptor into a functional heterocomplex with hsp90, Biochemistry, 35(2), 554, 1996.
194. Picard, D., Salser, S. J., and Yamamoto, K. R., A movable and regulable inactivation function within the steroid binding domain of the glucocorticoid receptor, Cell, 54(7), 1073, 1988.
195. Picard, D., Regulation of protein function through expression of chimaeric proteins, Curr Opin Biotechnol, 5(5), 511, 1994.
196. Cadepond, F., Schweizer-Groyer, G., Segard-Maurel, I., Jibard, N., Hollenberg, S. M., Giguere, V., Evans, R. M., and Baulieu, E. E., Heat shock protein 90 as a critical factor in maintaining glucocortico-steroid receptor in a nonfunctional state, J Biol Chem, 266(9), 5834, 1991.
197. Scherrer, L. C., Picard, D., Massa, E., Harmon, J. M., Simons, S. S., Jr., Yamamoto, K. R., and Pratt, W. B., Evidence that the hormone binding domain of steroid receptors confers hormonal control on chimeric proteins by determining their hormone-regulated binding to heat-shock protein 90, Biochemistry, 32(20), 5381, 1993.
198. Bunone, G., Briand, P. A., Miksicek, R. J., and Picard, D., Activation of the unliganded estrogen receptor by EGF involves the MAP kinase pathway and direct phosphorylation, Embo J, 15(9), 2174, 1996.
199. Lee, H. S., Aumais, J., and White, J. H., Hormone-dependent transactivation by estrogen receptor chimeras that do not interact with hsp90. Evidence for transcriptional repressors, J Biol Chem, 271(42), 25727, 1996.
200. White, R., Sjoberg, M., Kalkhoven, E., and Parker, M. G., Ligand-independent activation of the estrogen receptor by mutation of a conserved tyrosine, Embo J, 16(6), 1427, 1997.
201. Gorski, J. and Hansen, J. C., The "one and only" step model of estrogen action, Steroids, 49(6), 461, 1987.
202. Wrenn, C. K. and Katzenellenbogen, B. S., Cross-linking of estrogen receptor to chromatin in intact MCF-7 human breast cancer cells: optimization and effect of ligand, Mol Endocrinol, 4(11), 1647, 1990.
203. Nicholls, A., Sharp, K. A., and Honig, B., Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons, Proteins, 11(4), 281, 1991.
204. Pekki, A. and Tuohimaa, P., New freeze-dry and vapor fixation method for immunohistochemistry of soluble proteins: subcellular location of the progesterone receptor, J Histochem Cytochem, 37(8), 1207, 1989.