Characterization of ATPase Cycles of Molecular Chaperones by Fluorescence and Transient Kinetic Methods

Protein Folding Handbook

Volumn 1, Issue , 2008, Pages 105-161

  Schlee, Sandra ^a   Reinstein, Jochen ^a  

^a NONE

Author keywords

Enzyme; Fluorescence; Kinetic methods; Molecular chaperones; Motion

Indexed keywords

EID: 84889806388     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9783527619498.ch37     Document Type: Chapter

References (106)

1. Buchberger, A., Theyssen, H., Schröder, H., McCarty, J. S., Virgallita, G., Milkereit, P., Reinstein, J., & 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.
2. McCarty, J. S., Buchberger, A., Reinstein, J., & Bukau, B. (1995). The Role of ATP in the Functional Cycle of the DnaK Chaperone System. J. Mol. Biol. 249, 126-137.
3. Vale, R. D. & Milligan, R. A. (2000). The way things move: looking under the hood of molecular motor proteins. Science 288, 88-95.
4. Bagshaw, C. R. (2001). ATP analogues at a glance. J. Cell Sci. 114, 459-460.
5. Jameson, D. M. & Eccleston, J. F. (1997). Fluorescent nucleotide analogues: synthesis and applications. Methods Enzymol. 278, 363-390.
6. Cross, R. A., Jackson, A. P., Citi, S., Kendrick-Jones, J., & Bagshaw, C. R. (1988). Active site trapping of nucleotide by smooth and non-muscle myosins. J. Mol. Biol. 203, 173-181.
7. Karlish, S. J., Yates, D. W., & Glynn, I. M. (1978). Conformational transitions between Na+-bound and K+-bound forms of (Na++K+)-ATPase, studied with formycin nucleotides. Biochim. Biophys. Acta 525, 252-264.
8. White, D. C., Zimmerman, R. W., & Trentham, D. R. (1986). The ATPase kinetics of insect fibrillar flight muscle myosin subfragment-1. J. Muscle Res. Cell Motil. 7, 179-192.
9. Klostermeier, D., Seidel, R., & Reinstein, J. (1998). Functional Properties of the Molecular Chaperone DnaK from Thermus thermophilus. J. Mol. Biol. 279, 841-853.
10. Packschies, L., Theyssen, H., Buchberger, A., Bukau, B., Goody, R. S., & Reinstein, J. (1997). GrpE Accelerates Nucleotide Exchange of the Molecular Chaperone DnaK with an Associative Displacement Mechanism. Biochemistry 36, 3417-3422.
11. Theyssen, H., Schuster, H.-P., Packschies, L., Bukau, B., & Reinstein, J. (1996). The Second Step of ATP Binding to DnaK Induces Peptide Release. J. Mol. Biol. 263, 657-670.
12. Leonard, N. J. (1993). Etheno-bridged nucleotides in enzyme reactions and protein binding. Chemtracts Biochem. Mol. Biol. 4, 251-284.
13. Yarbrough, L. R., Schlageck, J. G., & Baughman, M. (1979). Synthesis and properties of fluorescent nucleotide substrates for DNA-dependent RNA polymerases. J. Biol. Chem. 254, 12069-12073.
14. Weikl, T., Muschler, P., Richter, K., Veit, T., Reinstein, J., & Buchner, J. (2000). C-terminal regions of hsp90 are important for trapping the nucleotide during the ATPase cycle. J. Mol. Biol. 303, 583-592.
15. Rudolph, M. G., Veit, T. J. H., & Reinstein, J. (1999). The novel fluorescent CDP-analogue (Pb)MABACDP is a specific probe for the NMP binding site of UMP/CMP-kinase. Protein Science 8, 2697-2704.
16. Scheidig, A. J., Franken, S. M., Corrie, J. E. T., Reid, G. P., Wittinghofer, A., Pai, E. F., & Goody, R. S. (1995). X-ray crystalstructure analysis of the catalytic domain of the oncogene product p21(h-ras) complexed with caged gtp and mant dgppnhp. J. Mol. Biol. 253, 132-150.
17. Hiratsuka, T. & Uchida, K. (1973). Preparation and properties of 2' (or 3')-O-(2,4,6-trinitrophenyl) adenosine 5'-triphosphate, an analogue of adenosine triphosphate. Biochim. Biophys. Acta 320, 635-647.
18. Hiratsuka, T. (1983). New ribosemodified fluorescent analogues of adenine and guanine nucleotides available as substrates for various enzymes. Biochim. Biophys. Acta 734, 496-508.
19. Moore, K. J. M. & Lohman, T. M. (1994). Kinetic Mechanism of Adenine Nucleotide Binding to and Hydrolysis by the Escherichia coli Rep Monomer. 1. Use of Fluorescent Nucleotide Analogues. Biochemistry 33, 14550-14564.
20. Woodward, S. K., Eccleston, J. F., & Geeves, M. A. (1991). Kinetics of the interaction of 20(30)-O-(N-methylanthraniloyl)-ATP with myosin subfragment 1 and actomyosin subfragment 1: characterization of two acto-S1-ADP complexes. Biochemistry 30, 422-430.
21. Schlee, S., Groemping, Y., Herde, P., Seidel, R., & Reinstein, J. (2001). The Chaperone Function of ClpB from Thermus thermophilus Depends on Allosteric Interactions of its Two ATP-binding Sites. J. Mol. Biol. 306, 889-899.
22. Watanabe, Y. Y., Motohashi, K., & Yoshida, M. (2002). Roles of the Two ATP Binding Sites of ClpB from Thermus thermophilus. J. Biol. Chem. 277, 5804-5809.
23. Bujalowski, W. & Jezewska, M. J. (2000). Kinetic mechanism of nucleotide cofactor binding to Escherichia coli replicative helicase DnaB protein. stopped-flow kinetic studies using fluorescent, ribose-, and base-modified nucleotide analogues. Biochemistry 39, 2106-2122.
24. Witt, S. N. & Slepenkov, S. V. (1999). Unraveling the Kinetic Mechanism of the 70-kDa Molecular Chaperones Using Fluorescence Spectroscopic Methods. Journal of Fluorescence 9, 281-293.
25. Buchberger, A., Reinstein, J., & Bukau, B. (1999) in Molecular Chaperones and Folding Catalysts: Regulation, Cellular Functions and Mechanisms (Bukau, B., Ed.) pp 573-635, Harwood Academic Publishers, Amsterdam.
26. Bukau, B. & Horwich, A. L. (1998). The hsp70 and hsp60 chaperone machines. Cell 92, 351-366.
27. Schlee, S. & Reinstein, J. (2002). The DnaK/ClpB chaperone system from Thermus thermophilus. Cellular and Molecular Life Sciences 59, 1598-1606.
28. Pearl, L. H. & Prodromou, C. (2002). Structure, function, and mechanism of the Hsp90 molecular chaperone. Adv. Protein Chem. 59, 157-186.
29. Richter, K. & Buchner, J. (2001). Hsp90: chaperoning signal transduction. J. Cell Physiol 188, 281-290.
30. Mayer, M. P. & Bukau, B. (1999). Molecular chaperones: the busy life of Hsp90. Curr. Biol. 9, R322-R325.
31. Buchner, J. (1999). Hsp90 & Co. - a holding for folding. Trends Biochem. Sci. 24, 136-141.
32. Pratt, W. B. & Toft, D. O. (2003). Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp. Biol. Med. (Maywood.) 228, 111-133.
33. Csermely, P. & Kahn, C. R. (1991). The 90-kDa heat shock protein (hsp-90) possesses an ATP binding site and autophosphorylating activity. J. Biol. Chem. 266, 4943-4950.
34. Nadeau, K., Das, A., & Walsh, C. T. (1993). Hsp90 chaperonins possess ATPase activity and bind heat shock transcription factors and peptidyl prolyl isomerases. J. Biol. Chem. 268, 1479-1487.
35. Nadeau, K., Sullivan, M. A., Bradley, M., Engman, D. M., & Walsh, C. T. (1992). 83-kilodalton heat shock proteins of trypanosomes are potent peptide-stimulated ATPases. Protein Sci. 1, 970-979.
36. Csermely, P., Kajtar, J., Hollosi, M., Jalsovszky, G., Holly, S., Khan, C. R., Gergely, P., Söti, C., Mihaly, K., & Somogyi, J. (1993). ATP Induces a Conformational Change of the 90-kDa Heat Shock Protein (hsp90). J. Biol. Chem. 268, 1901-1907.
37. Jakob, U., Scheibel, T., Bose, S., Reinstein, J., & Buchner, J. (1996). Assessment of the ATP Binding Properties of Hsp90. J. Biol. Chem. 271, 10035-10041.
38. Scheibel, T., Neuhofen, S., Weikl, T., Mayr, C., Reinstein, J., Vogel, P. D., & Buchner, J. (1997). ATPbinding Properties of Human Hsp90. J. Biol. Chem. 272, 18608-18613.
39. Bauer, M., Baumann, J., & Trommer, W. E. (1992). ATP binding to bovine serum albumin. FEBS Lett. 313, 288-290.
40. Prodromou, C., Roe, S. M., O'Brien, R., Ladbury, J. E., Piper, P. W., & Pearl, L. H. (1997). Identification and Structural Characterization of the ATP/ADP-Binding Site in the HSP90 Molecular Chaperone. Cell 90, 65-75.
41. Stebbins, C. E., Russo, A. A., Schneider, C., Rosen, N., Hartl, F. U., & Pavletich, N. P. (1997). Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent. Cell 89, 239-250.
42. Buchner, J. (1996). Supervising the fold: functional principles of molecular chaperones. FASEB Journal 10, 10-19.
43. Wegele, H., Muschler, P., Bunck, M., Reinstein, J., & Buchner, J. (2003). Dissection of the contribution of individual domains to the ATPase mechanism of Hsp90. J. Biol. Chem. 78, 39303-39310.
44. Richter, K., Reinstein, J., & Buchner, J. (2002). N-terminal residues regulate the catalytic efficiency of the Hsp90 ATPase cycle. J. Biol. Chem. 277, 44905-44910.
45. Richter, K., Muschler, P., Hainzl, O., Reinstein, J., & Buchner, J. (2003). Sti1 Is a Non-competitive Inhibitor of the Hsp90 ATPase. Binding prevents the N-terminal dimerization reaction during the ATPase cycle. J. Biol. Chem. 278, 10328-10333.
46. Wegele, H., Haslbeck, M., Reinstein, J., & Buchner, J. (2003). Sti1 Is a Novel Activator of the Ssa Proteins. J. Biol. Chem. 278, 25970-25976.
47. Vale, R. D. (2000). AAA proteins. Lords of the ring. J. Cell Biol. 150, F13-F19.
48. Ogura, T. & Wilkinson, A. J. (2001). AAA+ superfamily ATPases: common structure-diverse function. Genes Cells 6, 575-597.
49. Neuwald, A. F., Aravind, L., Spouge, J. L., & Koonin, E. V. (1999). AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res. 9, 27-43.
50. Parsell, D. A., Kowal, A. S., & Lindquist, S. (1994). Saccharomyces cerevisiae Hsp104 Protein: Purification and characterization of ATP-induced structural changes. J. Biol. Chem. 269, 4480-4487.
51. Zolkiewski, M., Kessel, M., Ginsburg, A., & Maurizi, M. R. (1999). Nucleotide-dependent oligomerization of ClpB from Escherichia coli. Protein Sci. 8, 1899-1903.
52. Glover, J. R. & Lindquist, S. (1998). Hsp104, Hsp70, and Hsp40: A Novel Chaperone System that Rescues Previously Aggregated Proteins. Cell 94, 73-82.
53. Motohashi, K., Watanabe, Y., Yohda, M., & Yoshida, M. (1999). Heat-inactivated proteins are rescued by the DnaK·J-GrpE set and ClpB chaperones. Proc. Natl. Acad. Sci. U.S.A. 96, 7184-7189.
54. Parsell, D. A., Kowal, A. S., Singer, M. A., & Lindquist, S. (1994). Protein disaggregation mediated by heatshock protein Hsp104. Nature 372, 475-478.
55. Goloubinoff, P., Mogk, A., Zvi, A. P., Tomoyasu, T., & Bukau, B. (1999). Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc. Natl. Acad. Sci. U.S.A. 96, 13732-13737.
56. Mogk, A., Tomoyasu, T., Goloubinoff, P., Rüdiger, S., Röder, D., Langen, H., & Bukau, B. (1999). Identification of thermolabile Escherichia coli proteins: prevention and reversion of aggregation by DnaK and ClpB. EMBO J. 18, 6934-6949.
57. Zolkiewski, M. (1999). ClpB Cooperates with DnaK, DnaJ, and GrpE in Suppressing Protein Aggregation: A NOVEL MULTI-CHAPERONE SYSTEM FROM ESCHERICHIA COLI. J. Biol. Chem. 274, 28083-28086.
58. Mogk, A., Schlieker, C., Strub, C., Rist, W., Weibezahn, J., & Bukau, B. (2003). Roles of individual domains and conserved motifs of the AAA+ chaperone ClpB in oligomerization, ATP hydrolysis, and chaperone activity. J. Biol. Chem. 278, 17615-17624.
59. Hattendorf, D. A. & Lindquist, S. L. (2002). Analysis of the AAA sensor-2 motif in the C-terminal ATPase domain of Hsp104 with a site-specific fluorescent probe of nucleotide binding. Proc. Natl. Acad. Sci. U.S.A.
60. Kim, K. I., Woo, K. M., Seong, I. S., Lee, Z.-W., Baek, S. H., & Chung, C. H. (1998). Mutational analysis of the two ATP-binding sites in ClpB, a heat shock protein with proteinactivated ATPase activity in Escherichia coli. Biochem. J. 333, 671-676.
61. Schirmer, E. C., Queitsch, C., Kowal, A. S., Parsell, D. A., & Lindquist, S. (1998). The ATPase activity of Hsp104, effects of environmental conditions and mutations [published erratum appears in J Biol Chem 1998 Jul 31; 273(31):19922]. J. Biol. Chem. 273, 15546-15552.
62. Krzewska, J., Konopa, G., & Liberek, K. (2001). Importance of Two ATPbinding Sites for Oligomerization, ATPase Activity and Chaperone Function of Mitochondrial Hsp78 Protein. J. Mol. Biol. 314, 901-910.
63. Hattendorf, D. A. & Lindquist, S. L. (2002). Cooperative kinetics of both Hsp104 ATPase domains and interdomain communication revealed by AAA sensor-1 mutants. EMBO J. 21, 12-21.
64. Barker, R., Trayer, I. P., & Hill, R. L. (1974). Nucleoside Phosphates Attached to Agarose. Methods Enzymol. 34B, 479-491.
65. Lambrecht, W. & Trautschold, I. (1974) in Methoden der enzymatischen Analyse II (Anonymouspp 2151-2160, Verlag Chemie, Weinheim.
66. Gao, B., Emoto, Y., Greene, L., & Eisenberg, E. (1993). Nucleotide Binding Properties of Bovine Brain Uncoating ATPase. J. Biol. Chem. 268, 8507-8513.
67. Wilbanks, S. M. & McKay, D. B. (1995). How Potassium Affects the Activity of the Molecular Chaperone Hsc70: II. Potassium Binds Specifically In The AtPase Active Site. J. Biol. Chem. 270, 2251-2257.
68. Feifel, B., Sandmeier, E., Schönfeld, H.-J., & Christen, P. (1996). Potassium ions and the molecular-chaperone activity of DnaK. Eur. J. Biochem. 237, 318-321.
69. Gao, B., Greene, L., & Eisenberg, E. (1994). Characterization of Nucleotide-Free Uncoating ATPase and Its Binding to ATP, ADP, and ATP Analogues. Biochemistry 33, 2048-2054.
70. Russell, R., Jordan, R., & McMacken, R. (1998). Kinetic Characterization of the ATPase Cycle of the DnaK Molecular Chaperone. Biochemistry 37, 596-607.
71. Adam, H. (1962) in Methoden der enzymatischen Analyse (Bergmeyer, H. U., Ed.) pp 573-577, Verlag Chemie, Weinheim.
72. Buchberger, A., Valencia, A., McMacken, R., Sander, C., & Bukau, B. (1994). The chaperone function of DnaK requires the coupling of ATPase activity with substrate binding through residue E171. EMBO J. 13, 1687-1695.
73. Liberek, K., Marszalek, J., Ang, D., Georgopoulos, C., & Zylicz, M. (1991). Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc. Natl. Acad. Sci. U.S.A. 88, 2874-2878.
74. McCarty, J. S. & Walker, G. C. (1991). DnaK as a thermometer: Threonine-199 is site of autophosphorylation and is critical for ATPase activity. Proc. Natl. Acad. Sci. U.S.A. 88, 9513-9517.
75. O'Brien, M. C. & McKay, D. B. (1995). How Potassium Affects the Activity of the Molecular Chaperone Hsc70: I. Potassium is Required for Optimal Atpase Activity. J. Biol. Chem. 270, 2247-2250.
76. Chock, S. P., Chock, P. B., & Eisenberg, E. (1979). The mechanism of the skeletal muscle myosin ATPase. II. Relationship between the fluorescence enhancement induced by ATP and the initial Pi burst. J. Biol. Chem. 254, 3236-3243.
77. Brune, M., Hunter, J. L., Corrie, J. E. T., & Webb, M. R. (1994). Direct, Real-Time Measurement of Rapid Inorganic Phosphate Release Using a Novel Fluorescent Probe and Its Application to Actomyosin Subfragment 1 ATPase. Biochemistry 33, 8262-8271.
78. Karzai, A. W. & McMacken, R. (1996). A bipartite signaling mechanism involved in DnaJ-mediated activation of the Escherichia coli DnaK protein. J. Biol. Chem. 271, 11236-11246.
79. Laufen, T., Mayer, M. P., Beisel, C., Klostermeier, D., Mogk, A., Reinstein, J., & Bukau, B. (1999). Mechanism of regulation of Hsp70 chaperones by DnaJ cochaperones. Proc. Natl. Acad. Sci. U.S.A 96, 5452-5457.
80. Russell, R., Karzai, A. W., Mehl, A. F., & McMacken, R. (1999). DnaJ Dramatically Stimulates ATP Hydrolysis by DnaK: Insight into Targeting of Hsp70 Proteins to Polypeptide Substrates. Biochemistry 38, 4165-4176.
81. Garnier, C., Lafitte, D., Tsvetkov, P. O., Barbier, P., Leclerc-Devin, J., Millot, J. M., Briand, C., Makarov, A. A., Catelli, M. G., & Peyrot, V. (2002). Binding of ATP to heat shock protein 90: evidence for an ATPbinding site in the C-terminal domain. J. Biol. Chem. 277, 12208-12214.
82. Groemping, Y., Klostermeier, D., Herrmann, C., Veit, T., Seidel, R., & Reinstein, J. (2001). Regulation of ATPase and Chaperone Cycle of DnaK from Thermus thermophilus by the Nucleotide Exchange Factor GrpE. J. Mol. Biol. 305, 1173-1183.
83. Ha, J.-H. & McKay, D. B. (1994). ATPase Kinetics of Recombinant Bovine 70 kDa Heat Shock Cognate Protein and Its Amino-Terminal ATPase Domain. Biochemistry 33, 14625-14635.
84. Eftink, M. R. (1997). Fluorescence Methods for Studying Equilibrium Macromolecule-Ligand Interactions. Methods Enzymol. 278, 221-257.
85. Bartha, B. B., Ajtai, K., Toft, D. O., & Burghardt, T. P. (1998). ATP sensitive tryptophans of hsp90. Biophys. Chem. 72, 313-321.
86. Reinstein, J., Vetter, I. R., Schlichting, I., Rösch, P., Wittinghofer, A., & Goody, R. S. (1990). Fluorescence and NMR Investigations on the Ligand Binding Properties of Adenylate Kinases. Biochemistry 29, 7440-7450.
87. Klostermeier, D., Seidel, R., & Reinstein, J. (1999). The Functional Cycle and Regulation of the Thermus thermophilus DnaK Chaperone System. J. Mol. Biol. 287, 511-525.
88. Thrall, S. H., Reinstein, J., Wöhrl, B. M., & Goody, R. S. (1996). Evaluation of human immunodeficiency virus type 1 reverse transcriptase primer tRNA binding by fluorescence spectroscopy: specificity and comparison to primer/template binding. Biochemistry 35, 4609-4618.
89. Press, W. H., Flannery, B. P., Teukolsky, S. A., & Vetterling, W. T. (1989) in Numerical recipes in Pascal; The art of scientific computing, Cambridge University Press, Cambridge, USA.
90. Wang, Z. X. (1995). An exact mathematical expression for describing competitive binding of two different ligands to a protein molecule. FEBS Lett. 360, 111-114.
91. Fabiato, A. & Fabiato, F. (1987). Multiligand program and constants. Eur. J. Biochem. 162, 357-363.
92. Brehmer, D., Rüdiger, S., Gassler, C. S., Klostermeier, D., Packschies, L., Reinstein, J., Mayer, M. P., & Bukau, B. (2001). Tuning of chaperone activity of Hsp70 proteins by modulation of nucleotide exchange. Nat. Struct. Biol. 8, 427-432.
93. Steinfeld, J. I., Francisco, J. S., & Hase, W. L. (1989) in Chemical Kinetics and Dynamics, Prentice-Hall, Inc., New Jersey 07632.
94. Roberts, D. V. (1977) in Enzyme kinetics, Cambridge University Press, Cambridge.
95. Gutfreund, H. (1995) in Kinetics for the Life Sciences: Receptors, transmitters and catalysts, University Press, Cambridge.
96. Bernasconi, C. F. (1976) in Relaxation kinetics, AcademicPress, New York.
97. Schlee, S., Beinker, P., Akhrymuk, A., & Reinstein, J. (2004). A chaperone network for the resolubilization of protein aggregates: direct interaction of ClpB and DnaK. J. Mol. Biol. 336, 275-285.
98. Wu, X., Gutfreund, H., & Chock, P. B. (1992). Kinetic Method for Differentiating Mechanisms for Ligand Exchange Reactions: Application To Test for Substrate Channeling in Glycolysis. Biochemistry 31, 2123-2128.
99. Johnson, K. A. (2003) in Kinetic Analysis of Macromolecules, Oxford University Press.
100. Bagshaw, C. R., Eccleston, J. F., Eckstein, F., Goody, R. S., Gutfreund, H., & Trentham, D. R. (1974). The Magnesium Ion-Dependent Adenosine Triphosphatase of Myosin: Two-Step processes of adenosine triphospahte association and adenosine dophosphate dissociation. Biochem. J. 141, 351-364.
101. Nowak, E., Strzelecka-Golaszewska, H., & Goody, R. S. (1988). Kinetics of Nucleotide and Metal Ion Interaction with G-Actin. Biochemistry 27, 1785-1792.
102. Geeves, M. A., Branson, J. P., & Attwood, P. V. (1995). Kinetics of nucleotide binding to pyruvate carboxylase. Biochemistry 34, 11846-11854.
103. Trentham, D. R., Eccleston, J. F., & Bagshaw, C. R. (1976). Kinetic analysis of ATPase mechanisms. Q. Rev. Biophys. 9, 217-281.
104. Eccleston, J. F. & Trentham, D. R. (1979). Magnesium ion dependent rabbit skeletal muscle myosin guanosine and thioguanosine triphosphatase mechanism and a novel guanosine diphosphatase reaction. Biochemistry 18, 2896-2904.
105. Ha, J.-H. & McKay, D. B. (1995). Kinetics of Nucleotide-Induced 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.
106. Ehresmann, B., Imbault, P., & Weil, J. H. (1973). Spectrophotometric Determination of Protein Concentration in Cell Extracts Containing tRNA's and rRNA's. Anal. Biochem. 54, 454-463.