Combining crystallography and EPR: crystal and solution structures of the multidomain cochaperone DnaJ

The crystal structure of the N-terminal part of T. thermophilus DnaJ unexpectedly showed an ordered GF domain and guided the design of a construct enabling the first structure determination of a complete DnaJ cochaperone molecule. By combining the crystal structures with spin-labelling EPR and cross-linking in solution, a dynamic view of this flexible molecule was developed.

[1]  B. Bainbridge,et al.  Genetics , 1981, Experientia.

[2]  H. Steinhoff,et al.  Structural Analysis of a HAMP Domain , 2005, Journal of Biological Chemistry.

[3]  Randy J Read,et al.  Electronic Reprint Biological Crystallography Likelihood-enhanced Fast Translation Functions Biological Crystallography Likelihood-enhanced Fast Translation Functions , 2022 .

[4]  Jingzhi Li,et al.  Crystal structure of yeast Sis1 peptide-binding fragment and Hsp70 Ssa1 C-terminal complex. , 2006, The Biochemical journal.

[5]  N. Pannu,et al.  REFMAC5 for the refinement of macromolecular crystal structures , 2011, Acta crystallographica. Section D, Biological crystallography.

[6]  P. Christen,et al.  Mechanism of the Targeting Action of DnaJ in the DnaK Molecular Chaperone System* , 2003, Journal of Biological Chemistry.

[7]  J. Reinstein,et al.  Balance of ATPase stimulation and nucleotide exchange is not required for efficient refolding activity of the DnaK chaperone , 2005, FEBS letters.

[8]  H. Zimmermann,et al.  DeerAnalysis2006—a comprehensive software package for analyzing pulsed ELDOR data , 2006 .

[9]  G. G. Stokes "J." , 1890, The New Yale Book of Quotations.

[10]  A. N. Tikhonov,et al.  Solutions of ill-posed problems , 1977 .

[11]  S. Miao,et al.  The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones , 2006, Cellular and Molecular Life Sciences CMLS.

[12]  E. Craig,et al.  In Vivo Bipartite Interaction Between the Hsp40 Sis1 and Hsp70 in Saccharomyces cerevisiae , 2005, Genetics.

[13]  D. Cyr,et al.  Eukaryotic homologues of Escherichia coli dnaJ: a diverse protein family that functions with hsp70 stress proteins. , 1993, Molecular biology of the cell.

[14]  Hironori Suzuki,et al.  Peptide-binding sites as revealed by the crystal structures of the human Hsp40 Hdj1 C-terminal domain in complex with the octapeptide from human Hsp70. , 2010, Biochemistry.

[15]  Sean McSweeney,et al.  Specific radiation damage can be used to solve macromolecular crystal structures. , 2003, Structure.

[16]  C. Sander,et al.  A module of the DnaJ heat shock proteins found in malaria parasites. , 1992, Trends in biochemical sciences.

[17]  Radiation-damage-induced phasing with anomalous scattering: substructure solution and phasing. , 2004, Acta crystallographica. Section D, Biological crystallography.

[18]  Masasuke Yoshida,et al.  K+ is an indispensable cofactor for GrpE stimulation of ATPase activity of DnaK·DnaJ complex from Thermus thermophilus , 1997, FEBS letters.

[19]  F. Hartl,et al.  Control of folding and membrane translocation by binding of the chaperone DnaJ to nascent polypeptides. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[20]  良二 上田 J. Appl. Cryst.の発刊に際して , 1970 .

[21]  F. Young Biochemistry , 1955, The Indian Medical Gazette.

[22]  M. Sternberg,et al.  Left-handed polyproline II helices commonly occur in globular proteins. , 1993, Journal of molecular biology.

[23]  Zbigniew Dauter,et al.  Biological Crystallography Structural Effects of Radiation Damage and Its Potential for Phasing , 2022 .

[24]  A. Karzai,et al.  A Bipartite Signaling Mechanism Involved in DnaJ-mediated Activation of the Escherichia coli DnaK Protein (*) , 1996, The Journal of Biological Chemistry.

[25]  J. Reinstein,et al.  Mechanism of regulation of hsp70 chaperones by DnaJ cochaperones. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[26]  J. Reinstein,et al.  Regulation of ATPase and chaperone cycle of DnaK from Thermus thermophilus by the nucleotide exchange factor GrpE. , 2001, Journal of molecular biology.

[27]  T. Langer,et al.  DnaJ-like proteins: molecular chaperones and specific regulators of Hsp70. , 1994, Trends in biochemical sciences.

[28]  Kevin Cowtan,et al.  research papers Acta Crystallographica Section D Biological , 2005 .

[29]  G. Jeschke,et al.  Dead-time free measurement of dipole-dipole interactions between electron spins. , 2000, Journal of magnetic resonance.

[30]  A. Hinck,et al.  Structural basis of J cochaperone binding and regulation of Hsp70. , 2007, Molecular cell.

[31]  F. Hartl,et al.  Molecular chaperone functions of heat-shock proteins. , 1993, Annual review of biochemistry.

[32]  G. Jeschke,et al.  Distance measurements on spin-labelled biomacromolecules by pulsed electron paramagnetic resonance. , 2007, Physical chemistry chemical physics : PCCP.

[33]  Masasuke Yoshida,et al.  A Novel Factor Required for the Assembly of the DnaK and DnaJ Chaperones of Thermus thermophilus* , 1996, The Journal of Biological Chemistry.

[34]  George M Sheldrick,et al.  Substructure solution with SHELXD. , 2002, Acta crystallographica. Section D, Biological crystallography.

[35]  P. Christen,et al.  Control of the DnaK Chaperone Cycle by Substoichiometric Concentrations of the Co-chaperones DnaJ and GrpE* , 1998, The Journal of Biological Chemistry.

[36]  D E McRee,et al.  XtalView/Xfit--A versatile program for manipulating atomic coordinates and electron density. , 1999, Journal of structural biology.

[37]  R. McMacken,et al.  DnaJ dramatically stimulates ATP hydrolysis by DnaK: insight into targeting of Hsp70 proteins to polypeptide substrates. , 1999, Biochemistry.

[38]  J. Reinstein,et al.  Functional characterization of the DnaK chaperone system from the archaeon Methanothermobacter thermautotrophicus ΔH , 2009, FEBS letters.

[39]  E. Zuiderweg,et al.  Reply to Sousa et al.: Evaluation of competing J domain:Hsp70 complex models in light of methods used , 2012, Proceedings of the National Academy of Sciences.

[40]  J. Reinstein,et al.  Directed evolution of the DnaK chaperone: mutations in the lid domain result in enhanced chaperone activity. , 2010, Journal of molecular biology.

[41]  J. Reinstein,et al.  The N Terminus of ClpB from Thermus thermophilus Is Not Essential for the Chaperone Activity* , 2002, The Journal of Biological Chemistry.

[42]  Thomas Terwilliger,et al.  SOLVE and RESOLVE: automated structure solution, density modification and model building. , 2004, Journal of synchrotron radiation.

[43]  G. Sheldrick A short history of SHELX. , 2008, Acta crystallographica. Section A, Foundations of crystallography.

[44]  C. Georgopoulos,et al.  The NH2-terminal 108 amino acids of the Escherichia coli DnaJ protein stimulate the ATPase activity of DnaK and are sufficient for lambda replication. , 1994, The Journal of biological chemistry.

[45]  J. Prestegard,et al.  The influence of C‐terminal extension on the structure of the “J‐domain” in E. coli DnaJ , 2008, Protein science : a publication of the Protein Society.

[46]  Masasuke Yoshida,et al.  Trigonal DnaK-DnaJ Complex Versus Free DnaK and DnaJ , 2004, Journal of Biological Chemistry.

[47]  C. Levinthal,et al.  Site‐directed mutagenesis of colicin E1 provides specific attachment sites for spin labels whose spectra are sensitive to local conformation , 1989, Proteins.

[48]  R. Seidel,et al.  The functional cycle and regulation of the Thermus thermophilus DnaK chaperone system. , 1999, Journal of molecular biology.

[49]  K. Wüthrich,et al.  NMR structure determination of the Escherichia coli DnaJ molecular chaperone: secondary structure and backbone fold of the N-terminal region (residues 2-108) containing the highly conserved J domain. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[50]  T. Lithgow,et al.  The J‐protein family: modulating protein assembly, disassembly and translocation , 2004, EMBO reports.

[51]  Z. Otwinowski,et al.  [20] Processing of X-ray diffraction data collected in oscillation mode. , 1997, Methods in enzymology.

[52]  Thomas C Terwilliger,et al.  SOLVE and RESOLVE: automated structure solution and density modification. , 2003, Methods in enzymology.

[53]  S. Schlee,et al.  The DnaK/ClpB chaperone system from Thermus thermophilus , 2002, Cellular and Molecular Life Sciences CMLS.

[54]  M. Saraste,et al.  FEBS Lett , 2000 .

[55]  J. Guy,et al.  The Crystal Structure of the Human Co-Chaperone P58IPK , 2011, PloS one.

[56]  Wolfgang Kabsch,et al.  Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants , 1993 .

[57]  C. Georgopoulos,et al.  The Conserved G/F Motif of the DnaJ Chaperone Is Necessary for the Activation of the Substrate Binding Properties of the DnaK Chaperone (*) , 1995, The Journal of Biological Chemistry.

[58]  Eric Blanc,et al.  Automated structure solution with autoSHARP. , 2007, Methods in molecular biology.

[59]  K. Wüthrich,et al.  NMR structure of the J-domain and the Gly/Phe-rich region of the Escherichia coli DnaJ chaperone. , 1996, Journal of molecular biology.

[60]  Randy J. Read,et al.  Improved Fourier Coefficients for Maps Using Phases from Partial Structures with Errors , 1986 .

[61]  E. Zuiderweg,et al.  Heat shock protein 70 kDa chaperone/DnaJ cochaperone complex employs an unusual dynamic interface , 2011, Proceedings of the National Academy of Sciences.

[62]  R J Read,et al.  Crystallography & NMR system: A new software suite for macromolecular structure determination. , 1998, Acta crystallographica. Section D, Biological crystallography.

[63]  Arthur Schweiger,et al.  EasySpin, a comprehensive software package for spectral simulation and analysis in EPR. , 2006, Journal of magnetic resonance.

[64]  Steven Hayward,et al.  Improvements in the analysis of domain motions in proteins from conformational change: DynDom version 1.50. , 2002, Journal of molecular graphics & modelling.

[65]  P. Emsley,et al.  Features and development of Coot , 2010, Acta crystallographica. Section D, Biological crystallography.

[66]  D. Cyr,et al.  The crystal structure of the peptide-binding fragment from the yeast Hsp40 protein Sis1. , 2000, Structure.

[67]  J. Reinstein,et al.  DafA cycles between the DnaK chaperone system and translational machinery. , 2004, Journal of molecular biology.

[68]  H. Taguchi,et al.  Isolation of the stable hexameric DnaK.DnaJ complex from Thermus thermophilus. , 1994, The Journal of biological chemistry.

[69]  A. Hinck,et al.  Evaluation of competing J domain:Hsp70 complex models in light of existing mutational and NMR data , 2011, Proceedings of the National Academy of Sciences.

[70]  N. Pfanner,et al.  Partner proteins determine multiple functions of Hsp70. , 1995, Trends in cell biology.

[71]  Gunnar Jeschke,et al.  Rotamer libraries of spin labelled cysteines for protein studies. , 2011, Physical chemistry chemical physics : PCCP.

[72]  E. Fedorov,et al.  Radiation-induced site-specific damage of mercury derivatives: phasing and implications. , 2005, Acta crystallographica. Section D, Biological crystallography.

[73]  S. Doublié [29] Preparation of selenomethionyl proteins for phase determination. , 1997, Methods in enzymology.

[74]  J. Prestegard,et al.  Backbone dynamics of the N-terminal domain in E. coli DnaJ determined by 15N- and 13CO-relaxation measurements. , 1999, Biochemistry.

[75]  E. Craig,et al.  The Glycine-Phenylalanine-Rich Region Determines the Specificity of the Yeast Hsp40 Sis1 , 1999, Molecular and Cellular Biology.