An interdomain energetic tug-of-war creates the allosterically active state in Hsp70 molecular chaperones

Cell

Volumn 151, Issue 6, 2012, Pages 1296-1307

  Zhuravleva, Anastasia ^a   Clerico, Eugenia M ^a   Gierasch, Lila M ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CHAPERONE; HEAT SHOCK PROTEIN 70; PROTEIN DNAK;

ALLOSTERISM; ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; ENERGY TRANSFER; ENZYME ACTIVITY; ESCHERICHIA COLI; HYDROLYSIS; HYDROPHOBICITY; LIGAND BINDING; MOLECULAR DOCKING; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

EID: 84870916379     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2012.11.002     Document Type: Article

References (78)

1. A. Ahmad, A. Bhattacharya, R.A. McDonald, M. Cordes, B. Ellington, E.B. Bertelsen, and E.R.P. Zuiderweg Heat shock protein 70 kDa chaperone/DnaJ cochaperone complex employs an unusual dynamic interface Proc. Natl. Acad. Sci. USA 108 2011 18966 18971
2. E.B. Bertelsen, L. Chang, J.E. Gestwicki, and E.R.P. Zuiderweg Solution conformation of wild-type E. coli Hsp70 (DnaK) chaperone complexed with ADP and substrate Proc. Natl. Acad. Sci. USA 106 2009 8471 8476
3. A. Bhattacharya, A.V. Kurochkin, G.N.B. Yip, Y. Zhang, E.B. Bertelsen, and E.R.P. Zuiderweg Allostery in Hsp70 chaperones is transduced by subdomain rotations J. Mol. Biol. 388 2009 475 490
4. A. Buchberger, H. Theyssen, H. Schröder, J.S. McCarty, G. Virgallita, P. Milkereit, J. Reinstein, and B. Bukau Nucleotide-induced conformational changes in the ATPase and substrate binding domains of the DnaK chaperone provide evidence for interdomain communication J. Biol. Chem. 270 1995 16903 16910
5. B. Bukau, and G.C. Walker Mutations altering heat shock specific subunit of RNA polymerase suppress major cellular defects of E. coli mutants lacking the DnaK chaperone EMBO J. 9 1990 4027 4036
6. G. Calloni, T. Chen, S.M. Schermann, H.C. Chang, P. Genevaux, F. Agostini, G.G. Tartaglia, M. Hayer-Hartl, and F.U. Hartl DnaK functions as a central hub in the E. coli chaperone network Cell Rep. 1 2012 251 264
7. L. Chang, E.B. Bertelsen, S. Wisén, E.M. Larsen, E.R. Zuiderweg, and J.E. Gestwicki High-throughput screen for small molecules that modulate the ATPase activity of the molecular chaperone DnaK Anal. Biochem. 372 2008 167 176
8. L. Chang, Y. Miyata, P.M.U. Ung, E.B. Bertelsen, T.J. McQuade, H.A. Carlson, E.R.P. Zuiderweg, and J.E. Gestwicki Chemical screens against a reconstituted multiprotein complex: myricetin blocks DnaJ regulation of DnaK through an allosteric mechanism Chem. Biol. 18 2011 210 221
9. E.M. Clerico, A. Zhuravleva, R.G. Smock, and L.M. Gierasch Segmental isotopic labeling of the Hsp70 molecular chaperone DnaK using expressed protein ligation Biopolymers 94 2010 742 752
10. P. Csermely, R. Palotai, and R. Nussinov Induced fit, conformational selection and independent dynamic segments: an extended view of binding events Trends Biochem. Sci. 35 2010 539 546
11. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
12. A. del Sol, C.-J. Tsai, B. Ma, and R. Nussinov The origin of allosteric functional modulation: multiple pre-existing pathways Structure 17 2009 1042 1050
13. V. Fernández-Sáiz, F. Moro, J.M. Arizmendi, S.P. Acebrón, and A. Muga Ionic contacts at DnaK substrate binding domain involved in the allosteric regulation of lid dynamics J. Biol. Chem. 281 2006 7479 7488
14. K.M. Flaherty, C. DeLuca-Flaherty, and D.B. McKay Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein Nature 346 1990 623 628
15. I. Gelis, A.M.J.J. Bonvin, D. Keramisanou, M. Koukaki, G. Gouridis, S. Karamanou, A. Economou, and C.G. Kalodimos Structural basis for signal-sequence recognition by the translocase motor SecA as determined by NMR Cell 131 2007 756 769
16. F. Glaser, T. Pupko, I. Paz, R.E. Bell, D. Bechor-Shental, E. Martz, and N. Ben-Tal ConSurf: identification of functional regions in proteins by surface-mapping of phylogenetic information Bioinformatics 19 2003 163 164
17. N. Halabi, O. Rivoire, S. Leibler, and R. Ranganathan Protein sectors: evolutionary units of three-dimensional structure Cell 138 2009 774 786
18. F.U. Hartl, A. Bracher, and M. Hayer-Hartl Molecular chaperones in protein folding and proteostasis Nature 475 2011 324 332
19. J. Jiang, E.G. Maes, A.B. Taylor, L. Wang, A.P. Hinck, E.M. Lafer, and R. Sousa Structural basis of J cochaperone binding and regulation of Hsp70 Mol. Cell 28 2007 422 433
20. H.H. Kampinga, and E.A. Craig The HSP70 chaperone machinery: J proteins as drivers of functional specificity Nat. Rev. Mol. Cell Biol. 11 2010 579 592
21. Keller, R. (2004). Optimizing the process of nuclear magnetic resonance spectrum analysis and computer aided resonance assignment. PhD thesis, ETH, Zurich.
22. D.P. Kumar, C. Vorvis, E.B. Sarbeng, V.C. Cabra Ledesma, J.E. Willis, and Q. Liu The four hydrophobic residues on the Hsp70 inter-domain linker have two distinct roles J. Mol. Biol. 411 2011 1099 1113
23. Q. Liu, and W.A. Hendrickson Insights into Hsp70 chaperone activity from a crystal structure of the yeast Hsp110 Sse1 Cell 131 2007 106 120
24. G. Manley, and J.P. Loria NMR insights into protein allostery Arch. Biochem. Biophys. 519 2012 223 231
25. K. Mapa, M. Sikor, V. Kudryavtsev, K. Waegemann, S. Kalinin, C.A.M. Seidel, W. Neupert, D.C. Lamb, and D. Mokranjac The conformational dynamics of the mitochondrial Hsp70 chaperone Mol. Cell 38 2010 89 100
26. M. Marcinowski, M. Höller, M.J. Feige, D. Baerend, D.C. Lamb, and J. Buchner Substrate discrimination of the chaperone BiP by autonomous and cochaperone-regulated conformational transitions Nat. Struct. Mol. Biol. 18 2011 150 158
27. M.P. Mayer, and B. Bukau Hsp70 chaperones: cellular functions and molecular mechanism Cell. Mol. Life Sci. 62 2005 670 684
28. M.P. Mayer, H. Schröder, S. Rüdiger, K. Paal, T. Laufen, and B. Bukau Multistep mechanism of substrate binding determines chaperone activity of Hsp70 Nat. Struct. Biol. 7 2000 586 593
29. M.P. Mayer, D. Brehmer, C.S. Gässler, and B. Bukau Hsp70 chaperone machines Adv. Protein Chem. 59 2001 1 44
30. J.S. McCarty, and G.C. Walker DnaK as a thermometer: threonine-199 is site of autophosphorylation and is critical for ATPase activity Proc. Natl. Acad. Sci. USA 88 1991 9513 9517
31. D.L. Montgomery, R.I. Morimoto, and L.M. Gierasch Mutations in the substrate binding domain of the Escherichia coli 70 kDa molecular chaperone, DnaK, which alter substrate affinity or interdomain coupling J. Mol. Biol. 286 1999 915 932
32. F. Moro, V. Fernández, and A. Muga Interdomain interaction through helices A and B of DnaK peptide binding domain FEBS Lett. 533 2003 119 123
33. F. Moro, V. Fernández-Sáiz, and A. Muga The lid subdomain of DnaK is required for the stabilization of the substrate-binding site J. Biol. Chem. 279 2004 19600 19606
34. M. Revington, T.M. Holder, and E.R.P. Zuiderweg NMR study of nucleotide-induced changes in the nucleotide binding domain of Thermus thermophilus Hsp70 chaperone DnaK: implications for the allosteric mechanism J. Biol. Chem. 279 2004 33958 33967
35. W. Rist, C. Graf, B. Bukau, and M.P. Mayer Amide hydrogen exchange reveals conformational changes in hsp70 chaperones important for allosteric regulation J. Biol. Chem. 281 2006 16493 16501
36. A. Rousaki, Y. Miyata, U.K. Jinwal, C.A. Dickey, J.E. Gestwicki, and E.R.P. Zuiderweg Allosteric drugs: the interaction of antitumor compound MKT-077 with human Hsp70 chaperones J. Mol. Biol. 411 2011 614 632
37. A.M. Ruschak, and L.E. Kay Methyl groups as probes of supra-molecular structure, dynamics and function J. Biomol. NMR 46 2010 75 87
38. R. Schlecht, A.H. Erbse, B. Bukau, and M.P. Mayer Mechanics of Hsp70 chaperones enables differential interaction with client proteins Nat. Struct. Mol. Biol. 18 2011 345 351
39. D. Sharma, and D.C. Masison Single methyl group determines prion propagation and protein degradation activities of yeast heat shock protein (Hsp)-70 chaperones Ssa1p and Ssa2p Proc. Natl. Acad. Sci. USA 108 2011 13665 13670
40. R.G. Smock, and L.M. Gierasch Sending signals dynamically Science 324 2009 198 203
41. R.G. Smock, O. Rivoire, W.P. Russ, J.F. Swain, S. Leibler, R. Ranganathan, and L.M. Gierasch An interdomain sector mediating allostery in Hsp70 molecular chaperones Mol. Syst. Biol. 6 2010 414
42. J.F. Swain, E.G. Schulz, and L.M. Gierasch Direct comparison of a stable isolated Hsp70 substrate-binding domain in the empty and substrate-bound states J. Biol. Chem. 281 2006 1605 1611
43. J.F. Swain, G. Dinler, R. Sivendran, D.L. Montgomery, M. Stotz, and L.M. Gierasch Hsp70 chaperone ligands control domain association via an allosteric mechanism mediated by the interdomain linker Mol. Cell 26 2007 27 39
44. H. Theyssen, H.P. Schuster, L. Packschies, B. Bukau, and J. Reinstein The second step of ATP binding to DnaK induces peptide release J. Mol. Biol. 263 1996 657 670
45. V. Tugarinov, and L.E. Kay Ile, Leu, and Val methyl assignments of the 723-residue malate synthase G using a new labeling strategy and novel NMR methods J. Am. Chem. Soc. 125 2003 13868 13878
46. V. Tugarinov, and L.E. Kay Methyl groups as probes of structure and dynamics in NMR studies of high-molecular-weight proteins ChemBioChem 6 2005 1567 1577
47. V. Tugarinov, P.M. Hwang, J.E. Ollerenshaw, and L.E. Kay Cross-correlated relaxation enhanced 1H-13C NMR spectroscopy of methyl groups in very high molecular weight proteins and protein complexes J. Am. Chem. Soc. 125 2003 10420 10428
48. V. Tugarinov, V. Kanelis, and L.E. Kay Isotope labeling strategies for the study of high-molecular-weight proteins by solution NMR spectroscopy Nat. Protoc. 1 2006 749 754
49. S.R. Tzeng, and C.G. Kalodimos Protein dynamics and allostery: an NMR view Curr. Opin. Struct. Biol. 21 2011 62 67
50. M. Vogel, M.P. Mayer, and B. Bukau Allosteric regulation of Hsp70 chaperones involves a conserved interdomain linker J. Biol. Chem. 281 2006 38705 38711
51. J. Weigelt Single scan, sensitivity- and gradient-enhanced TROSY for multidimensional NMR experiments J. Am. Chem. Soc. 120 1998 10778 10779
52. S.M. Wilbanks, L. Chen, H. Tsuruta, K.O. Hodgson, and D.B. McKay Solution small-angle X-ray scattering study of the molecular chaperone Hsc70 and its subfragments Biochemistry 34 1995 12095 12106
53. X.T. Zhu, X. Zhao, W.F. Burkholder, A. Gragerov, C.M. Ogata, M.E. Gottesman, and W.A. Hendrickson Structural analysis of substrate binding by the molecular chaperone DnaK Science 272 1996 1606 1614
54. A. Zhuravleva, and L.M. Gierasch Allosteric signal transmission in the nucleotide-binding domain of 70-kDa heat shock protein (Hsp70) molecular chaperones Proc. Natl. Acad. Sci. USA 108 2011 6987 6992
55. Bukau, B.; and Walker, G.C. (1990). Mutations altering heat shock specific subunit of RNA polymerase suppress major cellular defects of E. coli mutants lacking the DnaK chaperone. EMBO J. 9, 4027-4036.
56. Clerico, E.M.; Zhuravleva, A.; Smock, R.G.; and Gierasch, L.M. (2010). Segmental isotopic labeling of the Hsp70 molecular chaperone DnaK using expressed protein ligation. Biopolymers 94, 742-752.
57. Gelis, I.; Bonvin, A.M.J.J.; Keramisanou, D.; Koukaki, M.; Gouridis, G.; Karamanou, S.; Economou, A.; and Kalodimos, C.G. (2007). Structural basis for signal-sequence recognition by the translocase motor SecA as determined by NMR. Cell 131, 756-769.
58. Chang, L.; Bertelsen, E.B.; Wisén, S.; Larsen, E.M.; Zuiderweg, E.R.; and Gestwicki, J.E. (2008). High-throughput screen for small molecules that modulate the ATPase activity of the molecular chaperone DnaK. Anal. Biochem. 372, 167-176.
59. Ghosh, K.; and Dill, K.A. (2009). Computing protein stabilities from their chain lengths. Proc. Natl. Acad. Sci. USA 106, 10649-10654.
60. Henikoff, S.; and Henikoff, J.G. (1992). Amino acid substitution matrices from protein blocks. Proc. Natl. Acad. Sci. USA 89, 10915-10919.
61. Humphrey, W.; Dalke, A.; and Schulten, K. (1996). VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38, 27-28.
62. McCarty, J.S.; and Walker, G.C. (1991). DnaK as a thermometer: threonine-199 is site of autophosphorylation and is critical for ATPase activity. Proc. Natl. Acad. Sci. USA 88, 9513-9517.
63. Montgomery, D.L.; Morimoto, R.I.; and Gierasch, L.M. (1999). Mutations in the substrate binding domain of the Escherichia coli 70 kDa molecular chaperone, DnaK, which alter substrate affinity or interdomain coupling. J. Mol. Biol. 286, 915-932.
64. Moro, F.; Fernández, V.; and Muga, A. (2003). Interdomain interaction through helices A and B of DnaK peptide binding domain. FEBS Lett. 533, 119-123.
65. Pellecchia, M.; Montgomery, D.L.; Stevens, S.Y.; Vander Kooi, C.W.; Feng, H.P.; Gierasch, L.M.; and Zuiderweg, E.R.P. (2000). Structural insights into substrate binding by the molecular chaperone DnaK. Nat. Struct. Biol. 7, 298-303.
66. Pierpaoli, E.V.; Gisler, S.M.; and Christen, P. (1998). Sequence-specific rates of interaction of target peptides with the molecular chaperones DnaK and DnaJ. Biochemistry 37, 16741-16748.
67. Roberts, E.; Eargle, J.; Wright, D.; and Luthey-Schulten, Z. (2006). MultiSeq: unifying sequence and structure data for evolutionary analysis. BMC Bioinformatics 7, 382.
68. Ruschak, A.M.; and Kay, L.E. (2010). Methyl groups as probes of supra-molecular structure, dynamics and function. J. Biomol. NMR 46, 75-87.
69. Shepard, L.A.; Heuck, A.P.; Hamman, B.D.; Rossjohn, J.; Parker, M.W.; Ryan, K.R.; Johnson, A.E.; and Tweten, R.K. (1998). Identification of a membrane-spanning domain of the thiol-activated pore-forming toxin Clostridium perfringens perfringolysin O: an α-helical to beta-sheet transition identified by fluorescence spectroscopy. Biochemistry 37, 14563-14574.
70. Smock, R.G.; Rivoire, O.; Russ, W.P.; Swain, J.F.; Leibler, S.; Ranganathan, R.; and Gierasch, L.M. (2010). An interdomain sector mediating allostery in Hsp70 molecular chaperones. Mol. Syst. Biol. 6, 414.
71. Swain, J.F.; Schulz, E.G.; and Gierasch, L.M. (2006). Direct comparison of a stable isolated Hsp70 substrate-binding domain in the empty and substrate-bound states. J. Biol. Chem. 281, 1605-1611.
72. Swain, J.F.; Dinler, G.; Sivendran, R.; Montgomery, D.L.; Stotz, M.; and Gierasch, L.M. (2007). Hsp70 chaperone ligands control domain association via an allosteric mechanism mediated by the interdomain linker. Mol. Cell 26, 27-39.
73. Tugarinov, V.; and Kay, L.E. (2003). Ile, Leu, and Val methyl assignments of the 723-residue malate synthase G using a new labeling strategy and novel NMR methods. J. Am. Chem. Soc. 125, 13868-13878.
74. Tugarinov, V.; Kanelis, V.; and Kay, L.E. (2006). Isotope labeling strategies for the study of high-molecular-weight proteins by solution NMR spectroscopy. Nat. Protoc. 1, 749-754.
75. Weigelt, J. (1998). Single scan, sensitivity- and gradient-enhanced TROSY for multidimensional NMR experiments. J. Am. Chem. Soc. 120, 10778-10779.
76. 13C chemical-shift data. J. Biomol. NMR 4, 171-180.
77. Zhou, H.X.; and Dill, K.A. (2001). Stabilization of proteins in confined spaces. Biochemistry 40, 11289-11293.
78. Zhuravleva, A.; and Gierasch, L.M. (2011). Allosteric signal transmission in the nucleotide-binding domain of 70-kDa heat shock protein (Hsp70) molecular chaperones. Proc. Natl. Acad. Sci. USA 108, 6987-6992.