ATPase Subdomain IA Is a Mediator of Interdomain Allostery in Hsp70 Molecular Chaperones

PLoS Computational Biology

Volumn 10, Issue 5, 2014, Pages

  General, Ignacio J ^a   Liu, Ying ^a   Blackburn, Mandy E ^b   Mao, Wenzhi ^a,c   Gierasch, Lila M ^b   Bahar, Ivet ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

^c TSINGHUA UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOPHAGES; BINDING SITES; NUCLEOTIDES; STRUCTURAL DYNAMICS;

ALLOSTERY; ATPASES; COVARIANCE DATA; HEAT SHOCK PROTEIN 70; INTER-DOMAIN; MOLECULAR CHAPERONES; NUCLEOTIDE BINDING; RATIONAL DESIGN; SUBDOMAIN; SUBSTRATE BINDING DOMAIN;

SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATASE; HEAT SHOCK PROTEIN 70; PROTEIN DNAJ; CHAPERONE; PROTEIN BINDING;

ALLOSTERISM; ALPHA HELIX; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SUBSTRATE COMPLEX; IN VIVO STUDY; MOLECULAR RECOGNITION; NUCLEOTIDE BINDING SITE; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN FOLDING; SIGNAL TRANSDUCTION; BINDING SITE; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; ULTRASTRUCTURE;

ADENOSINE TRIPHOSPHATASES; BINDING SITES; COMPUTER SIMULATION; HSP70 HEAT-SHOCK PROTEINS; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR CHAPERONES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY;

EID: 84901650125     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003624     Document Type: Article

References (65)

1. Hartl FU, Hayer-Hartl M, (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295: 1852-1858.
2. Hartl FU, Hayer-Hartl M, (2009) Converging concepts of protein folding in vitro and in vivo. Nat Struct Mol Biol 16: 574-581.
3. Bukau B, Horwich AL, (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92: 351-366.
4. Walerych D, Olszewski MB, Gutkowska M, Helwak A, Zylicz M, et al. (2009) Hsp70 molecular chaperones are required to support p53 tumor suppressor activity under stress conditions. Oncogene 28: 4284-4294.
5. Broer L, Ikram MA, Schuur M, DeStefano AL, Bis JC, et al. (2011) Association of HSP70 and its co-chaperones with Alzheimer's disease. J Alzheimers Dis 25: 93-102.
6. Flaherty KM, Luca-Flaherty C, McKay DB, (1990) Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein. Nature 346: 623-628.
7. Zhu X, Zhao X, Burkholder WF, Gragerov A, Ogata CM, et al. (1996) Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272: 1606-1614.
8. Zhuravleva A, Clerico EM, Gierasch LM, (2012) An interdomain energetic tug-of-war creates the allosterically active state in Hsp70 molecular chaperones. Cell 151: 1296-1307.
9. Mayer MP, (2013) Hsp70 chaperone dynamics and molecular mechanism. Trends Biochem Sci 38: 507-14.
10. Wu CC, Naveen V, Chien CH, Chang YW, Hsiao CD, (2012) Crystal structure of DnaK protein complexed with nucleotide exchange factor GrpE in DnaK chaperone system: insight into intermolecular communication. J Biol Chem 287: 21461-21470.
11. Changeux JP, Edelstein SJ, (1998) Allosteric receptors after 30 years. Neuron 21: 959-980.
12. Changeux JP, Edelstein SJ, (2005) Allosteric mechanisms of signal transduction. Science 308: 1424-1428.
13. Kovbasyuk L, Kramer R, (2004) Allosteric supramolecular receptors and catalysts. Chem Rev 104: 3161-3187.
14. Gunasekaran K, Ma B, Nussinov R, (2004) Is allostery an intrinsic property of all dynamic proteins? Proteins 57: 433-443.
15. Revington M, Zhang Y, Yip GN, Kurochkin AV, Zuiderweg ER, (2005) NMR investigations of allosteric processes in a two-domain Thermus thermophilus Hsp70 molecular chaperone. J Mol Biol 349: 163-183.
16. Bertelsen EB, Chang L, Gestwicki JE, Zuiderweg ER, (2009) Solution conformation of wild-type E. coli Hsp70 (DnaK) chaperone complexed with ADP and substrate. Proc Natl Acad Sci U S A 106: 8471-8476.
17. Zhuravleva A, Gierasch LM, (2011) Allosteric signal transmission in the nucleotide-binding domain of 70-kDa heat shock protein (Hsp70) molecular chaperones. Proc Natl Acad Sci U S A 108: 6987-6992.
18. Arakawa A, Handa N, Shirouzu M, Yokoyama S, (2011) Biochemical and structural studies on the high affinity of Hsp70 for ADP. Protein Sci 20: 1367-1379.
19. Smock RG, Rivoire O, Russ WP, Swain JF, Leibler S, et al. (2010) An interdomain sector mediating allostery in Hsp70 molecular chaperones. Mol Syst Biol 6: 414.
20. Smock RG, Blackburn ME, Gierasch LM, (2011) Conserved, disordered C terminus of DnaK enhances cellular survival upon stress and DnaK in vitro chaperone activity. J Biol Chem 286: 31821-31829.
21. Woo HJ, Jiang J, Lafer EM, Sousa R, (2009) ATP-induced conformational changes in Hsp70: molecular dynamics and experimental validation of an in silico predicted conformation. Biochemistry 48: 11470-11477.
22. Golas E, Maisuradze GG, Senet P, Oldziej S, Czaplewski C, et al. (2012) Simulation of the opening and closing of Hsp70 chaperones by coarse-grained molecular dynamics. J Chem Theory Comput 8: 1750-1764.
23. Liu Y, Gierasch LM, Bahar I (2010) Role of Hsp70 ATPase domain intrinsic dynamics and sequence evolution in enabling its functional interactions with NEFs. PLoS Comput Biol 6: pii: e1000931. doi: 10.1371/journal.pcbi.1000931.
24. Chiappori F, Merelli I, Colombo G, Milanesi L, Morra G, (2012) Molecular mechanism of allosteric communication in Hsp70 revealed by molecular dynamics simulations. PLoS Comput Biol 8: e1002844.
25. Kityk R, Kopp J, Sinning I, Mayer MP, (2012) Structure and dynamics of the ATP-bound open conformation of Hsp70 chaperones. Mol Cell 48: 863-874.
26. Qi R, Sarbeng EB, Liu Q, Le KQ, Xu X, et al. (2013) Allosteric opening of the polypeptide-binding site when an Hsp70 binds ATP. Nat Struct Mol Biol 20: 900-907.
27. Bahar I, Lezon TR, Yang LW, Eyal E, (2010) Global dynamics of proteins: bridging between structure and function. Annu Rev Biophys 39: 23-42.
28. Atilgan C, Atilgan AR, (2009) Perturbation-response scanning reveals ligand entry-exit mechanisms of ferric binding protein. PLoS Comput Biol 5: e1000544.
29. Liu Y, Bahar I, (2012) Sequence evolution correlates with structural dynamics. Mol Biol Evol 29: 2253-2263.
30. Bahar I, Atilgan AR, Erman B, (1997) Direct evaluation of thermal fluctuations in proteins using a single-parameter harmonic potential. Fold Des 2: 173-181.
31. Haliloglu T, Bahar I, Erman B, (1997) Gaussian dynamics of folded proteins. Phys Rev Lett 79: 3090-3093.
32. Bahar I, Chennubhotla C, Tobi D, (2007) Intrinsic dynamics of enzymes in the unbound state and relation to allosteric regulation. Curr Opin Struct Biol 17: 633-640.
33. Laufen T, Mayer MP, Beisel C, Klostermeier D, Mogk A, et al. (1999) Mechanism of regulation of hsp70 chaperones by DnaJ cochaperones. Proc Natl Acad Sci U S A 96: 5452-5457.
34. Vogel M, Mayer MP, Bukau B, (2006) Allosteric regulation of Hsp70 chaperones involves a conserved interdomain linker. J Biol Chem 281: 38705-38711.
35. Swain JF, Dinler G, Sivendran R, Montgomery DL, Stotz M, et al. (2007) Hsp70 chaperone ligands control domain association via an allosteric mechanism mediated by the interdomain linker. Mol Cell 26: 27-39.
36. Pellecchia M, Montgomery DL, Stevens SY, Vander Kooi CW, Feng HP, et al. (2000) Structural insights into substrate binding by the molecular chaperone DnaK. Nat Struct Biol 7: 298-303.
37. Liu Q, Hendrickson WA, (2007) Insights into Hsp70 chaperone activity from a crystal structure of the yeast Hsp110 Sse1. Cell 131: 106-120.
38. Davis JE, Voisine C, Craig EA, (1999) Intragenic suppressors of Hsp70 mutants: interplay between the ATPase- and peptide-binding domains. Proc Natl Acad Sci U S A 96: 9269-9276.
39. Montgomery DL, Morimoto RI, Gierasch LM, (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.
40. Liebscher M, Roujeinikova A, (2009) Allosteric coupling between the lid and interdomain linker in DnaK revealed by inhibitor binding studies. J Bacteriol 191: 1456-1462.
41. Moro F, Fernandez V, Muga A, (2003) Interdomain interaction through helices A and B of DnaK peptide binding domain. FEBS Lett 533: 119-123.
42. Suh WC, Burkholder WF, Lu CZ, Zhao X, Gottesman ME, et al. (1998) Interaction of the Hsp70 molecular chaperone, DnaK, with its cochaperone DnaJ. Proc Natl Acad Sci U S A 95: 15223-15228.
43. Vogel M, Bukau B, Mayer MP, (2006) Allosteric regulation of Hsp70 chaperones by a proline switch. Mol Cell 21: 359-367.
44. Gassler CS, Buchberger A, Laufen T, Mayer MP, Schroder H, et al. (1998) Mutations in the DnaK chaperone affecting interaction with the DnaJ cochaperone. Proc Natl Acad Sci U S A 95: 15229-15234.
45. Lockless SW, Ranganathan R, (1999) Evolutionarily conserved pathways of energetic connectivity in protein families. Science 286: 295-299.
46. Halabi N, Rivoire O, Leibler S, Ranganathan R, (2009) Protein sectors: evolutionary units of three-dimensional structure. Cell 138: 774-786.
47. Dunn SD, Wahl LM, Gloor GB, (2008) Mutual information without the influence of phylogeny or entropy dramatically improves residue contact prediction. Bioinformatics 24: 333-340.
48. Fodor AA, Aldrich RW, (2004) Influence of conservation on calculations of amino acid covariance in multiple sequence alignments. Proteins 56: 211-221.
49. Weigt M, White RA, Szurmant H, Hoch JA, Hwa T, (2009) Identification of direct residue contacts in protein-protein interaction by message passing. Proc Natl Acad Sci U S A 106: 67-72.
50. Morcos F, Pagnani A, Lunt B, Bertolino A, Marks DS, et al. (2011) Direct-coupling analysis of residue coevolution captures native contacts across many protein families. Proc Natl Acad Sci U S A 108: E1293-E1301.
51. Jones DT, Buchan DW, Cozzetto D, Pontil M, (2012) PSICOV: precise structural contact prediction using sparse inverse covariance estimation on large multiple sequence alignments. Bioinformatics 28: 184-190.
52. Ahmad A, Bhattacharya A, McDonald RA, Cordes M, Ellington B, et al. (2011) Heat shock protein 70 kDa chaperone/DnaJ cochaperone complex employs an unusual dynamic interface. Proc Natl Acad Sci U S A 108: 18966-18971.
53. Sousa R, Jiang J, Lafer EM, Hinck AP, Wang L, et al. (2012) Evaluation of competing J domain:Hsp70 complex models in light of existing mutational and NMR data. Proc Natl Acad Sci U S A 109: E734.
54. Jiang J, Maes EG, Taylor AB, Wang L, Hinck AP, et al. (2007) Structural basis of J cochaperone binding and regulation of Hsp70. Mol Cell 28: 422-433.
55. Hu Z, Ma B, Wolfson H, Nussinov R, (2000) Conservation of polar residues as hot spots at protein interfaces. Proteins 39: 331-342.
56. Ma B, Elkayam T, Wolfson H, Nussinov R, (2003) Protein-protein interactions: structurally conserved residues distinguish between binding sites and exposed protein surfaces. Proc Natl Acad Sci U S A 100: 5772-5777.
57. Zheng W, Brooks B, (2005) Identification of dynamical correlations within the myosin motor domain by the normal mode analysis of an elastic network model. J Mol Biol 346: 745-759.
58. Chennubhotla C, Bahar I, (2006) Markov propagation of allosteric effects in biomolecular systems: application to GroEL-GroES. Mol Syst Biol 2: 36.
59. Chennubhotla C, Bahar I, (2007) Signal propagation in proteins and relation to equilibrium fluctuations. PLoS Comput Biol 3: 1716-1726.
60. Zheng W, Brooks BR, Doniach S, Thirumalai D, (2005) Network of dynamically important residues in the open/closed transition in polymerases is strongly conserved. Structure 13: 565-577.
61. Clerico EM, Zhuravleva A, Smock RG, Gierasch LM, (2010) Segmental isotopic labeling of the Hsp70 molecular chaperone DnaK using expressed protein ligation. Biopolymers 94: 742-752.
62. Jordan R, 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.
63. Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, et al. (2008) The Pfam protein families database. Nucleic Acids Res 36: D281-D288.
64. Yang LW, Rader AJ, Liu X, Jursa CJ, Chen SC, et al. (2006) oGNM: online computation of structural dynamics using the Gaussian Network Model. Nucleic Acids Res 34: W24-W31.
65. Harrison CJ, Hayer-Hartl M, Di LM, Hartl F, 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.