How chaperones fold proteins

Biological Chemistry

Volumn 379, Issue 3, 1998, Pages 245-259

  Beissinger, Martina ^a   Buchner, Johannes ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

GroE; Hsp70; Hsp90; Molecular chaperones; Protein folding; sHsp

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CHAPERONE; CHAPERONIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; NUCLEOTIDE BINDING PROTEIN; PROTEIN;

CONFORMATIONAL TRANSITION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; REVIEW; STRESS;

MODELS, CHEMICAL; MOLECULAR CHAPERONES; PROTEIN FOLDING;

EID: 0031946770     PISSN: 14316730     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (163)

1. Aligue, R., Akhavan-Niak, H., and Russell, P. (1994). A role for hsp90 in the cell cycle control: Wee1 tyrosine kinase activity requires interaction with Hsp90. EMBO J. 13, 6099-6106.
2. Allen, S.P., Polazzi, J.O., Gierse, J.K., Easton, A.M. (1992). Two novel heat shock genes encoding proteins produced in response to heterologous protein expression in Escherichia coli. J. Bacteriol. 174, 6938-6947.
3. Anderson, C.M., Stenkamp, R.E., and Steitz, T.A. (1978). Sequencing a protein by X-ray crystallography. II. Refinement of yeast hexokinase B co-ordinates and sequence at 2.1 Å resolution. J. Mol. Biol. 123, 15-33.
4. Anfinsen, C.B. (1973). Principles that govern the folding of protein chains. Science 181, 223-230.
5. Anson, M.L. (1945). Protein denaturation and the properties of protein groups. Adv. Protein Chem. 2, 361-386.
6. Arrigo, A.-P., Suhan, J., and Welch, W.J. (1988). Dynamic changes in the structure and intracellular localization of the mammalian low-molecular weight heat shock protein. Mol. Cell. Biol. 8, 5059-5071.
7. Arrigo, A.-P., and Landry, J. (1994). Expression and function of the low molecular weight heat shock proteins. In: The Biology of Heat Shock Proteins and Molecular Chaperones. R.I. Morimoto, ed. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press), pp. 335-373.
8. 2 chaperonin hetero-oligomer. Nature 265, 653-656.
9. Behlke, J., Lutsch, G., Gaestel, M., Bielka, H. (1991). Supramolecular structure of the recombinant murine small heat shock protein hsp25. FEBS Lett. 288, 119-122.
10. Bockkareva, E.S., Lissin, N.M., Flynn, G.C., Rothman, J.E., Girshovich, A.S. (1992). Positive cooperativity in the functioning of molecular chaperone GroEL. J. Biol. Chem. 267, 6796-6800.
11. Bose, S., Weikl, T., Bügl, H., and Buchner, J. (1996). Chaperone function of Hsp90-associated proteins. Science 274, 1715-1717.
12. Brady, J.P., Garland, D., Duglas-Tabor, Y., Robinson, Jr., G., Groome, A., and Wawrousek, E.F. (1997). Targeted disruption of the mouse αA-crystallin gene induces cataract and cytoplasmic inclusion bodies containing the small heat shock protein αB-crystallin. Proc. Natl. Acad. Sci. USA 94, 884-889.
13. Braig, K., Otwinowski, Z., Hegde, R., Boisvert, D.C., Joachimiak, A., Horwich, A.L., and Sigler, P.B. (1994). The crystal structure of the bacterial chaperonin GrpEL at 2.8 Ä. Nature 371, 578-586.
14. Brunschier, R., Danner, M., and Seckler, R. (1993). Interaction of phage P22 tailspike protein with GroE molecular chaperones during refolding in vitro. J. Biol. Chem. 268, 2767-2772.
15. Buchberger, A., Theyssen, H., Schröder, H., McCarty, J.S., Virgallita, G., Milkereit, P., Reinstein, J., and Bukau, B. (1995). Nucleotide-induced conformational changes in the ATPase and substrate binding domains of the DnaK chaperone provide evidence for interdomain communication. J. Biol. Chem. 270, 16903-16910.
16. Buchberger, A., Schröder, H., Hesterkamp, T., Schönfeld, H.J., Bukau, B. (1996). Substrate shuttling between the DnaK and GroEL systems indicates a chaperone network promoting protein folding. J. Mol. Biol. 26, 328-333.
17. Buchner, J. (1996). Supervising the fold: functional principles of molecular chaperones. FASEB J. 10, 10-19.
18. Burston, S.G., Ranson, N. A., and Clarke, A.R. (1995). The origins and consequences of asymmetry in the chaperonin reaction cycle. J. Mol. Biol. 249, 138-152.
19. Carrell, R.W., and Lomas, D.A. (1997). Conformational disease. Lancet 350, 134-138.
20. 1H NMR spectroscopy of flexible C-terminal extensions in bovine lens α-crystallin. FEBS-Lett. 311, 143-149.
21. Carver, J.A., Guerreiro, N., Nicholls, K.A., Truscott, R.J. (1995). On the interaction of α-crystallin with unfolded proteins. Biochim. Biophys. Acta. 1252, 251-260.
22. Chen, S., Roseman, A.M., Hunter, A.S., Wood, S.P., Burston, S.G., Ranson, N.A., Clarke, A.R., and Saibil, H.R. (1994). Location of a folding protein and shape changes in GroEL-GroES complexes imaged by cryo-electron microscopy. Nature 371, 261-264.
23. Chen, S., Prappapanich, V., Rimerman, R.A., Honoré, B., and Smith, D.F. (1996). Interactions of p60, a mediator of progesterone receptor assembly, with heat shock proteins Hsp90 and Hsp70. Mol. Endocrinol. 10, 682-693.
24. Choudhury, P., Liu, Y., and Sifers, R.N. (1997). Qualitiy control of protein folding: Participation in Human Disease. News Physiol. Sci. 12, 162-166.
25. Clauwaert, J., Ellerton, H.D., Koretz, J.F., Thomson, K., Augusteyn, R.C. (1989). The effect of temperature on the renaturation of alpha-crystallin. Curr. Eye Res. 8, 397-403.
26. Collier, D.N. (1993). SecB: A molecular chaperone of Escherichia coli protein secretion pathway. Adv. Prot. Chem. 44, 151-193.
27. 2 complexes in molecular chaperone activity. Folding and Design 1, 265-273.
28. Csermely, P., Kajtár, J., Hollósi, M., Jalsovszky, G., Jolly, S., Kahn, C.R., Gergely, P., Jr., Söti, C., Mihály, K., and Somogy, J. (1993). ATP induces a conformational change in the 90-kDa heat shock protein (hsp90). J. Biol. Chem. 268, 1901-1907.
29. DeBoer, C., Meulman, P.A., Wnuk, R.J., and Peterson, D.H. (1970). Geldanamycin, a new antibiotic. J. Antibiot. (Tokyo) 23, 442-447.
30. De Jong, W.W., Leeunissen, J.A., and Voorter, C.E. (1993). Evolution of the alpha-crystallin/small heat-shock protein family. Mol. Biol. Evol. 10, 103-126.
31. Diamond, D.L., and Randall, L.L. (1997). Kinetic partitioning. J. Biol. Chem. 272, 28994-28998.
32. Ehrnsperger, M., Buchner, J., and Gaestel, M. (1997a). Structure and function of small heat-shock proteins. In: Molecular Chaperones in the Life Cycle of Proteins. A.L. Fink and Y. Goto, eds. (New York: Marcel Dekker), pp. 533-575.
33. Ehrnsperger, M., Gräber, S., Gaestel, M., and Buchner, J. (1997b). Binding of non-native protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation. EMBO J. 16, 221-229.
34. Engel, A., Hayer-Hartl, M.K., Goldie, K.N, Pfeifer, G., Hegerl, R., Müller, S., da Silva, A.C.R., Baumeister, W., and Hartl, F.-U. (1995). Functional significance of symmetrical versus asymmetrical GroEL-GroES chaperonin complexes. Science 269, 832-836.
35. Ewalt, K.L., Hendrick, J.P., Houry, W.A., and Hartl, F.-U. (1997). In vivo observation of polypeptide flux through the bacterial chaperonin system. Cell 90, 491-500.
36. Farahbakhsh, Z.T., Huang, Q.L., Ding, L.L., Altenbach, C., Steinhoff, H.J., Horwitz, J., Hubbell, W.L. (1995). Interaction of α-crystallin with spin-labeled peptides. Biochemistry 17, 509-516.
37. Fenton, W.A., Kashi, Y., Furtak, K., and Horwich, A.L. (1994). Residues in chaperonin GroEL required for polypeptide binding and release. Nature 371, 614-619.
38. Fenton, W.A., and Horwich, A.L. (1997). GroEL-mediated protein folding. Prot. Sci. 6, 743-760.
39. Flaherty, K.M., DeLuca-Flaherty, C., and McKay, D.B. (1990). Three-dimensional structure of the ATPase fragment of a 70 kilodalton heat shock cognate protein. Nature 346, 623-628.
40. Flynn, G.C., Chappel, T.G., and Rothman, J.E. (1989). Peptide binding and release by proteins implicated as catalysts of protein assembly. Science 245, 385-390.
41. Flynn, G.C., Pohl, J., Flocco, M.T., and Rothman, J.E. (1991). Peptide-binding specifity of the molecular chaperone Bip. Nature 353, 726-730.
42. Freeman, B.C., and Morimoto, R.I. (1996). The human cytosolic molecular chaperones Hsp90, Hsp70 (Hsc70), and Hdj1 have distinct roles in recognition of a non-native protein and protein refolding. EMBO J. 15, 2969-2979.
43. Gamer, J., Multhaup, G., Tomoyasu, T., McCarty, J.S., Rüdiger, S., Schönfeld, H.J., Schirra, C., Bujard, H., and Bukau, B. (1996). A cycle of binding and release of the DnaK, DnaJ and GrpE chaperones regulates activity of the E. coli heat shock transcription factor sigma32. EMBO J. 15, 607-617.
44. Gao, B., Eisenberg, E., and Greene, L. (1995). Interaction of nucleotide-free hsc70 with clathrin and peptide and effect of ATP analogues. Biochemistry34, 11882-11888.
45. Gervasoni, P., Staudemann, W., James, P., Gehrig, P., and Plückthun, A. (1996). β-lactamase binds to GroEL in a conformation highly protected against hydrogen/deuterium exchange. Proc. Natl. Acad. Sci. USA 93, 12189-12194.
46. Gething, M.J., and Sambrook, J. (1992). Protein folding in the cell. Nature 355, 33-45.
47. Gething, M.J., Blond-Elguindi, S., Mori, K., and Sambrook, J.F. (1994). Structure, function and regulation of the endoplasmic reticulum chaperone, Bip. In: The Biology of Heat Shock Proteins and Molecular Chaperones. R.I. Morimoto, A. Tissieres, and C. Georgopoulos, eds. (Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press), pp. 111-135.
48. Goloubinoff, P., Christeller, J.T., Gatenby, A.A., and Lorimer, G.H. (1989). Reconstitution of active dimeric ribulose bisphosphate carboxylase from an unfolded state depends on two chaperonin proteins an MgATP. Nature 342, 884-889.
49. Gorovits, B.M., Ybarra, J., Seale, J.W., and Horowitz, P.M. (1997). Conditions for nucleotide-dependent GroES-GroEL interactions. J. Biol. Chem. 272, 26999-27004.
50. Gragerov, A., Zeng, L., Zhao, X., Burkholder, W., and Gottesman, M.E. (1994). Specifity of DnaK-peptide binding. J. Mol. Biol. 235, 848-854.
51. Gray, T.E., and Fersht, A.R. (1991). Co-operativity in ATP hydrolysis by GroEL is increased by GroES. FEBS Lett. 292, 254-258.
52. Ha, J.H., and McKay, D.B. (1994). ATPase kinetics of recombinant bovine 70 kilodalton heat shock cognate protein and its amino-terminal ATPase domain. Biochemistry 33, 14625-14635.
53. Ha, J.H., and McKay, D.B. (1995). Kinetics of nucleotide-induced conformational changes in the tryptophan fluorescence of the molecular chaperone Hsc70 and its subfragments suggest the ATP-induced conformational change follows initial ATP binding. Biochemistry 34, 11635-11644.
54. Ha, J.-H., Johnson, E.R., McKay, D.B., Sousa, M.C., Takeda, S., and Wilbanks, S.M. (1997). Structure and properties of the 70-kilodalton heat-shock proteins. In: Molecular Chaperones in the Life Cycle of Proteins. A.L. Fink, and Y. Goto, eds. (New York: Marcel Dekker), pp. 95-122.
55. Hardy, S.J.S., and Randall, L.L. (1991). A kinetic partitioning model of selective binding of nonnative proteins by the bacterial chaperone SecB. Science 251, 439-443.
56. Harrison, C.J., Hayer-Hartl, M., Di Liberto, M., Hartl, F.-U., and Kuriyan, J. (1997). Crystal structure of the nucleotide exchange factor GrpE bound to the ATPase domain of the molecular chaperone DnaK. Science 276, 431-435.
57. Hartl, F.U. (1996). Molecular chaperones in cellular protein folding. Nature 381, 571-580.
58. Hayer-Hartl, M.K., Martiaanism of dimer formation of the 90-kDa heat-shock protein. Eur. J. Biochem. 233, 1-8.
59. Hayer-Hartl, M.K., Weber, F., and Hartl, F.-U. (1996). Mechanism of chaperonin action: GroES binding and release can drive GroEL-mediated protein folding in the absence of ATP hydrolysis. EMBO J. 15, 6111-6121.
60. Head, M.W., Corbin, E., Goldman, J.E. (1993). Overexpression and abnormal modification of the stress proteins αB-crystallin and HSP27 in Alexander disease. Am. J. Pathol. 143, 1743-1753.
61. Holmgren, A., and Bränden, C.I. (1989). Crystal structure of chaperone protein PapD reveals an immunoglobulin fold. Nature 342, 248-251.
62. Horwitz, J. (1992). Alpha-crystallin can function as a molecular chaperone. Proc. Natl. Acad. Sci. USA 89, 10449-10453.
63. Hoshino, M., Kawata, Y., and Goto, Y. (1996). Interaction of GroEL with conformational states of horse cytochrome c. J. Mol. Biol. 262, 575-587.
64. Hunt, J.F., van der Vies, S.M., Henry, L., and Deisenhofer, J. (1997). Structural adaptations in the specialized bacteriophage T4 co-chaperonin Gp31 expand the size of the Anfinsen cage. Cell 90, 361-371.
65. Iwaki, T., Iwaki, A., Tateishi, J., Sakaki, Y., Goldman, J.E. (1993). αB-crystallin and 27-kDa heat shock protein are regulated by stress conditions in the central nervous system and accumulate in Rosenthal fibers. Am. J. Pathol. 143, 487-495.
66. Jaenicke, R. (1987). Folding and association of proteins. Prog. Biophys. Mol. Biol. 49, 117-237.
67. Jaenicke, R., and Creighton, T.E. (1993). Junior Chaperones. Curr. Biol. 3, 234-235.
68. Jakob, U., Gaestel, M., Engel, K., Buchner, J. (1993). Small heat shock proteins are molecular chaperones. J. Biol. Chem. 268, 1517-1520.
69. Jakob, U., Lilie, H., Meyer, I., and Buchner, J. (1995). Transient interaction of Hsp90 with early unfolding intermediates of citrate synthase. Implications for heat shock in vivo. J. Biol. Chem. 270, 7288-7294.
70. Jakob, U., Scheibel, T., Bose, S., Reinstein, J., and Buchner, J. (1996). Assessment of the ATP binding properties of Hsp90. J. Biol. Chem. 271, 10035-10041.
71. Jordan, R., and McMacken, R. (1995). Modulation of the ATPase activity of the molecular chaperone DnaK by peptides and the DnaJ and GrpE heat shock proteins. J. Biol. Chem. 270, 4563-4569.
72. Kato, S., Hirano, A., Umahara, T., Llena, J.R, Herz, R, Ohama, E. (1992). Ultrastructural and immunohistochemical studies on ballooned cortical neurons in Creutzfeldt-Jakob disease: expression of αB-crystallin, ubiquitin and stress-response protein 27. Acta Neuropathol. 84, 443-448.
73. Kiefhaber, T., Rudolph, R., Kohler, H.-H., and Buchner, J. (1991). Protein aggregation in vitro and in vivo: A quantitative model of the kinetic competition between folding and aggregation. Bio/ Technology 9, 825-829.
74. Koyasu, S., Nishida, E., Kadowaki, T., Matsuzaki, F., Iida, K., Harada, F., Kasuga, M., Sakai, J., and Yahare, I. (1986). Two mammalian heat shock proteins, HSP90 and HSP100, are actin-binding proteins. Proc. Natl. Acad. Sci. USA 83, 8054-8058.
75. Lamba, O.P., Borchman, D., Sinha, S.K., Shah, J., Renugopalakrishnan, V., Yappert, M.C. (1993). Estimation of the secondary structure and conformation of bovine lens crystallins by infrared spectroscopy: quantitative analysis and resolution by Fourier self-deconvolution and curve fit. Biochim. Biophys. Acta. 1163, 113-123.
76. Landry, J., Chretien, P., Lambert, H., Mickey, E., Weber, L.A. (1989). Heat shock resistance conferred by expression of the human HSP27 gene in rodent cells. J. Cell Biol. 109, 7-15.
77. Landry, S.J., Jordan, R., McMacken, R., and Gierasch, L.M. (1992). Different conformations for the same polypeptide bound to chaperones DnaK and GroEL. Nature 355, 455-457.
78. Landry, S.J., Zeistraryalls, Fayet, O., Georgopoulos, C., and Gierasch, L.M. (1993). Characterisation of a functionally important mobile domain of GroES. Nature 364, 255-258.
79. Langer, T., Pfeifer, G., Martin, J., Baumeister, W., Haiti, F.-U. (1992a). Chaperonin-mediated protein folding: GroES binds to one end of the GroEL cylinder, which accommodates the protein substrate within its central cavity. EMBO J. 11, 4757-4765.
80. Langer, T., Lu, C., Echols, H., Flanagan, J., Hayer, M.K., and Haiti, F.-U. (1992b). Successive action of DnaK, DnaJ and GroEL along the pathway of chaperone-mediated protein folding. Nature 356, 683-689.
81. Lee, G.J., Pokala, N., and Vierling, E. (1995). Structure and in vitro molecular chaperone activity of cytosolic small heat shock proteins from pea. J. Biol. Chem. 270, 10432-10438.
82. Lee, G.J., Roseman, A.M., Saibil, H.R., and Vierling, E. (1997). A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding competent state. EMBO J. 16, 659-671.
83. Liberek, K. Marszalek, J., Ang, D., Georgopoulos, C., and Zylicz, M. (1991 ). Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc. Natl. Acad. Sci. USA 88, 2874-2878.
84. Lill, R., Cunningham, K., Brundage, L.A., Ito, K., Oliver, D., and Wickner, W. (1989). SecA protein hydrolyzes ATP and is an essential component of the protein translocation ATPase of Escherichia coli. EMBO J. 8, 961-966.
85. Lilie, H., and Buchner, J. (1995). Interaction of GroEL with a highly structured folding intermediate: Iterative binding cycles do not involve unfolding. J. Biol. Chem. 92, 8100-8104.
86. Llorca, O., Marco, S., Carrascosa, J.L., and Valpuesta, J.M. (1994). Symmetric GroEL-GroES complexes can contain substrate simultaneously in both GroEL rings. FEBS Lett. 345, 181-186.
87. Llorca, O., Carrascosa, J.L., Valpuesta, J.M. (1996). Biochemical characterization of symmetric GroEL-GroES complexes: Evidence for a role in protein folding. J. Biol. Chem. 271, 68-76.
88. Llorca, O., Marco, S., Carrascosa, J.L., and Valpuesta, J.M. (1997). Symmetric GroEL-GroES complexes can contain substrate simultaneously in both GroEL rings. FEBS Lett. 405, 195-199.
89. Lorimer, G.H. (1996). A quantitative assessment of the role of the chaperonin proteins in protein folding in vivo. FASEB J. 10, 5-9.
90. McCarty, J.S., Buchberger, A., Reinstein, J., and Bukau, B. (1995). The role of ATP in the functional cycle of the DnaK chaperone system. J. Mol. Biol. 249, 126-137.
91. Minami, Y., Kimura, Y., Kawasaki, H., Suzuki, K., and Yahara, I. (1994). The carboxy-terminal region of mammalian hsp90 is required for its dimerization and function in vivo. Mol. Cell. Biol. 14, 1459-1464.
92. Murai, N., Makino, Y., and Yoshida, M. (1996). GroEL locked in a closed conformation by an interdomain cross-link can bind ATP and polypeptide but cannot process further reaction steps. J. Biol. Chem. 271, 28229-28234.
93. Nathan, D.F., Vos, M.H., and Lindquist, S. (1997). In vivo functions of the Saccharomyces cerevisiae Hsp90 chaperone. Proc. Natl. Acad. Sci. USA 94, 12948-12956.
94. Nemoto, T., Ohara-Nemoto, Y., Ota, M., Takagi, T., and Yokoyama, K. (1995). Mechanism of dimer formation of the 90-kDa heat-shock protein. Eur. J. Biochem. 233, 1-8.
95. O'Brien, M.C., and McKay, D.B. (1995). How potassium affects the activity of the molecular chaperone Hsc70:1. Potassium is required for optimal ATPase activity. J. Biol. Chem. 270, 2247-2250.
96. + but not ATP hydrolysis. Nature 365, 664-666.
97. Pierpaoli, E.V., Sandmeier, E., Baici, A., Schönfeld, H.J., Gisler, S., and Christen, P. (1997). The Power stroke of the DnaK/DnaJ/ GrpE molecular chaperone system. J. Mol. Biol. 269, 757-768.
98. Plesofsky-Vig, N., Vig, J., and Brambl, R. (1992). Phylogeny of the alpha-crystallin-related heat-shock proteins. J. Mol. Evol. 35, 537-545.
99. Pratt, W.B., and Toft, D.O. (1997). Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocrine Reviews 18, 306-360.
100. Prodromou, C., Roe, S.M., O'Brien, R., Ladbury, J.E., Piper, P.W., and Pearl, L.H. (1997). Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 90, 65-75.
101. Raman, B., Ramakrishna, T., Rao, C.M. (1995). Temperature dependent chaperone-like activity of alpha-crystallin. FEBS Lett. 365, 133-136.
102. Randall, L.L. (1992). Peptide binding by chaperone SecB: Implications for recognition of nonnative structure. Science 257, 241-245.
103. Randall, L.L., and Hardy, S.J.S. (1995). High selectivity with low specificity: How SecB has solved the paradox of chaperone binding. Trends Biochem. Sci. 20, 65-69.
104. Roseman, A., Chen, S., White, H., Braig, K., and Saibil, H. (1996). The chaperonin ATPase cycle: Mechanism of allosteric switching and movements of substrate-binding domains in GroEL. Cell 87, 241-251.
105. Rüdiger, S., Germeroth, L., Schneider-Mergener, J., and Bukau, B. (1997). Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. EMBO J. 16, 1501-1507.
106. Rye, H.S., Burston, S.G., Fenton, W.A., Beechem, J.M., Xu, Z., Sigler, P.B., and Horwich, A.L. (1997). Distinct actions of cis and trans ATP within the double ring of the chaperonin GroEL. Nature 388, 792-798.
107. Scheibel, T., and Buchner, J. (1997). The Hsp90 family - an overview. In: Guidebook to Molecular Chaperones and Protein-Folding Catalysts. M.J. Gething, ed. (Oxford, England: Sambrook and Tooze Publications at Oxford University Press), pp. 147-151.
108. Scheibel, T., Neuhofen, S., Weikl, T., Mayr, C., Reinstein, J., Vogel, P.D., and Buchner, J. (1997). ATP-binding properties of human Hsp90. J. Biol. Chem. 272, 18608-18613.
109. Scheibel, T., Weikl, T., and Buchner, J. (1998). Two chaperone sites in Hsp90 differing in substrate specificity and ATP-dependence. Proc. Natl. Acad. Sci. USA95, in press.
110. Schmid, D., Baici, A., Gehring, H., and Christen, P. (1994). Kinetics of molecular chaperone action. Science 263, 971-973.
111. Schmidt, M., Buchner, J., Todd, M.J., Lorimer, G.H., and Viitanen, P.V. (1994a). On the role of GroES in the chaperonin-assisted folding reaction. Three case studies. J. Biol. Chem. 269, 10304-10311.
112. Schmidt, M., Rutkat, K., Rachel, R., Pfeifer, G., Jaenicke, R., Viitanen, P., Lorimer, G., and Buchner, J. (1994b). Symmetric complexes of GroE chaperonins as part of the functional cycle. Science 265, 656-659.
113. Schröder, H., Langer, T., Haitl, F-U., and Bukau, B. (1993). DnaK, DnaJ and GrpE form a cellular chaperone machinery capable of repairing heat-induced protein damage. EMBO J. 12, 4137-4144.
114. Shinohara, H., Inaguma, Y. Goto, S., Inagaki, T., Kato, K. (1993). αB crystallin and HSP28 are enhanced in the cerebral cortex of patients with Alzheimers disease. J. Neurol. Sci. 119, 203-208.
115. Siezen, R.J., and Argos, P. (1983). Structural homology of lens crystallins. III. Secondary structure estimation from circular dichroism and prediction from amino acid sequences. Biochim. Biophys. Acta. 748, 56-67.
116. Sifers, R.N. (1995). Defective protein folding as a cause of disease. Nat. Struct. Biol. 2, 355-357.
117. Singh, K., Groth-Vasselli, B., Kumosinski, T.F., Farnsworth, P.N. (1995). α-Crystallin quaternary structure: molecular basis for its chaperone activity. FEBS Lett. 372, 283-287.
118. Smith, D.F., and Toft, D. O. (1993). Steroid receptors and their associated proteins. Mol. Endocrinol. 7, 4-11.
119. Smith, D.F. (1996). Steroid receptors and molecular chaperones. Sci. Med. 2, 38-47.
120. Smith, V.F., Hardy, S.J.S., and Randall, L.L. (1997). Determination of the binding frame of the chaperone SecB within the physiological ligand oligopeptide-binding protein. Protein Sci. 6, 1746-1755.
121. Sparrer, H., Lilie, H., and Buchner, J. (1996). Dynamics of the GroEL-protein complex: Effects of nucleotides and folding mutants. J. Mol. Biol. 258, 74-87.
122. Sparrer, H., Rutkat, K., and Buchner, J. (1997). Catalysis of protein folding by symmetric chaperone complexes. Proc. Natl. Acad. Sci. USA 94, 1096-1100.
123. Sparrer, H., and Buchner, J. (1997). How GroES regulates binding of nonnative protein to GroEL. J. Biol. Chem. 272, 14080-14086.
124. Sriram, M., Osipiuk, J., Freeman, B., Morimoto, R., and Joachimiak, A. (1997). Human Hsp70 molecular chaperone binds two calciumions within the ATPase domain. Structure 15, 403-414.
125. Stebbins, C.E., Russo, A.A., Schneider, C., Rosen, N., Hartl, F.U., and Pavletich, N.P. (1997). Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent. Cell 89, 239-250.
126. Strepanova, L., Leng, X.-H., Parker, S.B., and Harper, J.W. (1996). Mammalian p50 (CDC37) is a protein kinase targeting subunit of Hsp90 that binds and stabilises CDK4. Genes Dev. 10, 1491-1502.
127. Sullivan, W., Stensgard, B., Caucutt, G., Bartha, B., McMahon, N., Alnemri, E.S., Litwack, G., and Toft, D.O. (1997). Nucleotides and two functional states of Hsp90. J. Biol. Chem. 272, 8007-8012.
128. Surewicz, W.K., Mantsch, H.H., Chapman, D. (1993). Determination of protein secondary structure by Fourier transform infrared spectroscopy: a critical assessment. Biochemistry 32, 389-394.
129. Szabo, A., Langer, T., Schröder, H., Flanagan, J., Bukau., B., and Hartl, F.-U. (1994). The ATP hydrolysis-dependent reaction cycle of the E.coli hsp70 system DnaK, DnaJ, and GrpE. Proc. Natl. Acad. Sci. USA 91, 10345-10349.
130. Szyperski, T., Pellecchia, M., Wall, D., Georgopoulos, C., and Wüthrich, K. (1994). NMR structure determination of the E. coli DnaJ molecular chaperone: Secondary structure and backbone fold of the N-terminal region (residues 2 - 108) containing the highly conserved J domain. Proc. Natl. Acad. Sci. USA 91, 11343-11347.
131. Tardieu, A., Laporte, D., Licinio, P., Kropp, B., and Delaye, M. (1986). Calflens α-crystallin quaternary structure: A three-lay tetrahedral model. J. Mol. Biol. 192, 711-724.
132. Tatzeit, J., Zuo, J., Voellmy, R., Scott, M., Hartl, U., Prusiner, S.B., and Welch, W.J. (1995). Scrapie prions selectively modify the stress response in neuroblastoma cells. Proc. Natl. Acad. USA 92, 2944-2948.
133. Tetu, B., Brisson, J., Landry, J., Huot, J. (1992). Prognostic significance of heat-shock protein-27 in node-positive breast carcinoma: an immunohistochemical study. Breast Cancer Res. Treat. 36, 93-97.
134. Theyssen, H., Schuster, H.P., Packschies, L., Bukau, B., and Reinstein, J. (1996). The second step of ATP binding to DnaK induces peptide release. J. Mol. Biol. 263, 657-670.
135. Thor, A., Benz, C., Moore, D., Goldman, E., Edgerton, S., Landry, J., Schwartz, L., Mayall, B., Hickey, E., Weber, L.A. (1991). Stress response protein (srp-27) determination in primary human breast carcinomas: clinical, histologic, and prognostic correlations. J. Natl. Cancer Inst. 83, 170-178.
136. Todd, M.J., Viitanen, P.V., and Lorimer, G.H. (1994). Dynamics of the chaperonin ATPase cycle: implications for facilitated protein folding. Science 265, 659-666.
137. Todd, M.J., Lorimer, G.H., and Thirumalai, D. (1996). Chaperonin-facilitated protein folding: Optimization of rate and yield by an iterative annealing mechanism. Proc. Natl. Adac. Sci. USA 93, 4030-4035.
138. Topping, T.B., and Randall, L.L. (1994). Determination of the binding frame within a physiological ligand for the chaperone SecB. Protein Sci. 3, 1395-1406.
139. Topping, T.B., and Randall, L.L. (1997). Chaperone SecB from Escherichia coli mediates kinetic partitioning via a dynamic equilibrium with its ligands. J. Biol. Chem. 272, 19314-19318.
140. Van den Ijssel, P.R., Overkamp, P., Knauf, U., Gaestel, M., de Jong, W.W. (1994). αA-crystallin confers cellular thermoresistance. FEBS Lett. 355, 54-56.
141. Van der Vies, S.M., Gatenby, A.A., and Georgopoulos, C. (1994). Bacteriophage T4 encodes a co-chaperonin that can substitute for Escherichia coli GroES in protein folding. Nature 368, 654-656.
142. Vierling, E. (1991). The role of heat shock proteins in plants. Annu. Rev. Plant Physiol. Plant Biol. 42, 579-620.
143. Viitanen, P.V., Gatenby, A.A., and Lorimer, G.H. (1992). Purified chaperonin 60 (groEL) interacts with the nonnative states of a multitude of Escherichia coli proteins. Protein Sci. 1, 363-369.
144. Wall, D., Zylicz, M., and Georgopoulos, C. (1995). The conserved G/F motif of the DnaJ chaperone is necessary for the activation of the substrate binding properties of the DnaK chaperone. J. Biol. Chem. 270, 2139-2144.
145. Waters, E.R. (1995). The molecular evolution of the small heat-shock proteins in plants. Genetics 141, 785-795.
146. Wawrzynow, A., Banecki, B., Wall, D., Liberek, K., Georgopoulos, C., and Zylicz, M. (1995). ATP hydrolysis is required for the DnaJ-dependent activation of DnaK chaperone for binding to both native and denatured protein substrates. J. Biol. Chem. 270, 19307-19311.
147. Wearsch, P.A., and Nicchitta, C.V. (1996). Endoplasmic reticulum chaperone GRP94 subunit assembly is regulated through a defined oligomerization domain. Biochemistry 35, 16760-16769.
148. Wei, J., Gaut, J.R., and Hendershot, L.M. (1995). In vitro dissociation of Bip-peptide complexes requires a conformational change in Bip after ATP binding but does not require ATP hydrolysis. J. Biol. Chem. 270, 26677-26682.
149. Weissman, J.S., Rye, H.S., Fenton, W.A., Beechem, J.M., and Norwich, A.L. (1996). Characterization of the active intermediate of a GroEL-GroES-mediated protein folding reaction. Cell 84, 481-490.
150. Whitesell, L., Mimnaugh, E.G., De Costa, B., Myers, C.E., and Neckers, L.M. (1994). Inhibition of heat shock protein HSP90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation. Proc. Natl. Acad. Sci. USA 97, 8324-8328.
151. Wiech, H., Buchner, J., Zimmermann, R., and Jakob, U. (1992). Hsp90 chaperones protein folding in vitro. Nature 358, 169-170.
152. Wigley, D.B., Davies, G.J., Dodson, E.J., Maxwell, A., and Dodson, G. (1991). Crystal structure of an N-terminal fragment of the DNA gyrase B protein. Nature 351, 624-629.
153. Wilbanks, S.M., Chen, L., Tsuruta, H., Hodgson, K.O., and McKay, D.B. (1995). Solution small-angle X-ray scattering study of the molecular chaperone Hsc70 and its subfragments. Biochemistry 34, 12095-12106.
154. Wilhelmson, A., Cuthill, S., Denis, M., Wikström, A.-C., Gustafsson, J.-Å, and Poellinger, L. (1990). The specific DNA binding activity of the dioxin receptor is modulated by the 90 kDa heatshock protein. EMBO J. 9, 69-76.
155. Wistow, G. (1985). Domain structure and evolution in alpha-crystallins and small heat-shock proteins. FEBS Lett. 181, 1-6.
156. Xu, Y., and Lindquist, S. (1993). Heat shock protein Hsp90 governs the activity of v-Src kinase. Proc. Natl. Acad. Sci. USA 90, 7074-7078.
157. 7 chaperonin complex. Nature 368, 741-750.
158. Yenari, M., Fink, S.L., Sun, G.H., Patel, M., Kunis, D., Onley, D., Sapolsky, R.M., and Steinberg, G.K. (1997). Overexpression of inducible HSP72 protein using herpes simplex viral vectors improves neuron survival in experimental stroke. Soc. Neurosci. Abs. 23, 1391.
159. Yifrach, O., and Horovitz, A. (1994). Two lines of allosteric communication in the oligomeric chaperonin GroEL are revealed by the single mutation Arg 196 → Ala. J. Mol. Biol. 243, 397-401.
160. Young, J.C., Schneider, C., and Hartl, F-U. (1997). In vitro evidence that hsp90 contains two independent chaperone sites. FEBS Lett. 418, 139-143.
161. Zahn, R., Spitzfaden, C., Ottiger, M., Wüthrich, K., and Plückthun, A. (1994). Destabilization of the complete protein secondary structure on binding to the chaperone GroEL. Nature 368, 261-265.
162. Zav'yalov, V.P., Zav'yalova, G.A., Denesyuk, A.I., Gaestel, M., and Korpela, T. (1995). Structural and functional homology between periplasmic bacterial molecular chaperones and small heat shock proteins. FEMS Immunol. Med. Microbiol. 11, 265-272.
163. Zhu, X., Zhao, X., Burkholder, W.F., Gragerov, A., Ogata, C.M., Gottesman, M., and Hendrickson, W.A. (1996). Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272, 1606-1614.