GrpE N-terminal Domain Contributes to the Interaction with DnaK and Modulates the Dynamics of the Chaperone Substrate Binding Domain

Journal of Molecular Biology

Volumn 374, Issue 4, 2007, Pages 1054-1064

  Moro, Fernando ^a   Taneva, Stefka G ^a   Velázquez Campoy, Adrián ^b   Muga, Arturo ^a  

^a CSIC UPV Unidad de Biofisica UBF   (Spain)

^b UNIVERSITY OF ZARAGOZA   (Spain)

Author keywords

binding thermodynamics; DnaK; GrpE; ITC; protein protein interaction

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CHAPERONE; PROTEIN DNAK; PROTEIN GRPE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING KINETICS; COMPLEX FORMATION; DISSOCIATION CONSTANT; MOLECULAR STABILITY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; THERMODYNAMICS;

EID: 35748955787     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.10.002     Document Type: Article

References (41)

1. Hartl F.U., and Hayer-Hartl M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295 (2002) 1852-1885
2. Mayer M.P., and Bukau B. Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol. Life Sci. 62 (2005) 670-684
3. Bukau B., Weissman J., and Horwich A. Molecular chaperones and protein quality control. Cell 125 (2006) 443-451
4. Schröder H., Langer T., Hartl F.U., and Bukau B. DnaK, DnaJ and GrpE form a cellular chaperone machinery capable of repairing heat-induced protein damage. EMBO J. 12 (1993) 4137-4144
5. Cyr D.M., Langer T., and Douglas M.G. DnaJ-like proteins: molecular chaperones and specific regulators of Hsp70. Trends Biochem. Sci. 19 (1994) 176-181
6. Packschies L., Theyssen H., Buchberger A., Bukau B., Goody R.S., and Reinstein J. GrpE accelerates nucleotide exchange of the molecular chaperone DnaK with an associative displacement mechanism. Biochemistry 36 (1997) 3417-3422
7. Hohfeld J., and Jentsch S. GrpE-like regulation of the hsc70 chaperone by the anti-apoptotic protein BAG-1. EMBO J. 16 (1997) 6209-6216
8. Groemping Y., Klostermeier D., Herrmann C., Veit T., Seidel R., and Reinstein J. Regulation of ATPase and chaperone cycle of DnaK from Thermus thermophilus by the nucleotide exchange factor GrpE. J. Mol. Biol. 305 (2001) 1173-1183
9. Miao B., Davis J.E., and Craig E.A. Mge1 functions as a nucleotide release factor for Ssc1, a mitochondrial Hsp70 of Saccharomyces cerevisiae. J. Mol. Biol. 265 (1997) 541-552
10. Schroda M., Vallon O., Whitelegge J.P., Beck C.F., and Wollman F.A. The chloroplastic GrpE homolog of Chlamydomonas: two isoforms generated by differential splicing. Plant Cell 13 (2001) 2823-2829
11. Harrison C.J., Hayer-Hartl M., Di Liberto M., Hartl F.U., and Kuriyan J. Crystal structure of the nucleotide exchange factor GrpE bound to the ATPase domain of the molecular chaperone DnaK. Science 276 (1997) 431-435
12. Grimshaw J.P., Siegenthaler R.K., Züger S., Schönfeld H.J., Z'graggen B.R., and Christen P. The heat-sensitive Escherichia coli grpE280 phenotype: impaired interaction of GrpE(G122D) with DnaK. J. Mol. Biol. 353 (2005) 888-896
13. Grimshaw J.P., Jelesarov I., Schönfeld H.J., and Christen P. Reversible thermal transition in GrpE, the nucleotide exchange factor of the DnaK heat-shock system. J. Biol. Chem. 276 (2001) 6098-6104
14. Groemping Y., and Reinstein J. Folding properties of the nucleotide exchange factor GrpE from Thermus thermophilus: GrpE is a thermosensor that mediates heat shock response. J. Mol. Biol. 314 (2001) 167-178
15. Moro F., and Muga A. Thermal adaptation of the yeast mitochondrial Hsp70 system is regulated by the reversible unfolding of its nucleotide exchange factor. J. Mol. Biol. 358 (2006) 1367-1377
16. Mally A., and Witt S.N. GrpE accelerates peptide binding and release from the high affinity state of DnaK. Nat. Struct. Biol. 8 (2001) 254-257
17. Han W., and Christen P. Interdomain communication in the molecular chaperone DnaK. Biochem. J. 369 (2003) 627-634
18. Mehl A.F., Heskett L.D., and Neal K.M. A GrpE mutant containing the NH(2)-terminal "tail" region is able to displace bound polypeptide substrate from DnaK. Biochem. Biophys. Res. Commun. 282 (2001) 562-569
19. Brehmer D., Gässler C., Rist W., Mayer M.P., and Bukau B. Influence of GrpE on DnaK-substrate interactions. J. Biol. Chem. 279 (2004) 27957-27964
20. Chesnokova L.S., Slepenkov S.V., Protasevich I.I., Sehorn M.G., Brouillette C.G., and Witt S.N. Deletion of DnaK's lid strengthens binding to the nucleotide exchange factor. GrpE: a kinetic and thermodynamic analysis. Biochemistry 42 (2003) 9028-9040
21. Gelinas A.D., Toth J., Bethoney K.A., Stafford W.F., and Harrison C.J. Mutational analysis of the energetics of the GrpE.DnaK binding interface: equilibrium association constants by sedimentation velocity analytical ultracentrifugation. J. Mol. Biol. 339 (2004) 447-458
22. Fukada H., and Takahashi K. Enthalpy and heat capacity changes for the proton dissociation of various buffer components in 0.1 M potassium chloride. Proteins 33 (1998) 159-166
23. Gelinas A.D., Langsetmo K., Toth J., Bethoney K.A., Stafford W.F., and Harrison C.J. A structure-based interpretation of E. coli GrpE thermodynamic properties. J. Mol. Biol. 323 (2002) 131-142
24. Moro F., Fernández-Sáiz V., and Muga A. The lid subdomain of DnaK is required for the stabilization of the substrate-binding site. J. Biol. Chem. 279 (2004) 19600-19606
25. Murphy K.P., and Freire E. Thermodynamics of structural stability and cooperative folding behaviour in proteins. Adv. Protein Chem. 43 (1992) 313-361
26. Murphy K.P., Xie D., Thompson K.S., Amzel L.M., and Freire E. Entropy in biological binding processes: estimation of translational entropy loss. Science 247 (1990) 559-561
27. Luque I., and Freire E. Structure-based prediction of binding affinities and molecular design of peptide ligands. Methods Enzymol. 295 (1998) 100-127
28. Karzai A.W., and McMacken R. A bipartite signaling mechanism involved in DnaJ-mediated activation of the Escherichia coli DnaK protein. J. Biol. Chem. 271 (1996) 11236-11246
29. Montgomery D., Jordan R., McMacken R., and Freire E. Thermodynamic and structural analysis of the folding/unfolding transitions of the Escherichia coli molecular chaperone DnaK. J. Mol. Biol. 232 (1993) 680-692
30. Neidhart F.C., and VanBogelen R.A. In: Neidherdt F.C. (Ed). Escherichia coli and Salmonella typhimurium (1987), American Society for Microbiology, Washington, DC 1334-1345
31. Gelinas A.D., Toth J., Bethoney K.A., Langsetmo K., Stafford W.F., and Harrison C.J. Thermodynamic linkage in the GrpE nucleotide exchange factor, a molecular thermosensor. Biochemistry 42 (2003) 9050-9059
32. Doig A.J., and Sternberg M.J.E. Side-chain conformational entropy in protein folding. Protein Sci. 4 (1995) 2247-2251
33. Horst M., Oppliger W., Feifel B., Schatz G., and Glick B.S. The mitochondrial protein import motor: dissociation of mitochondrial hsp70 from its membrane anchor requires ATP binding rather than ATP hydrolysis. Protein Sci. 5 (1996) 759-767
34. Rist W., Graf C., Bukau B., and Mayer M.P. Amide hydrogen exchange reveals conformational changes in hsp70 chaperones important for allosteric regulation. J. Biol. Chem. 281 (2006) 16493-16501
35. Swain J.F., Dinler G., Sivendran R., Montgomery D.L., Stotz M., and Gierasch L.M. Hsp70 chaperone ligands control domain association via an allosteric mechanism mediated by the interdomain linker. Mol. Cell 26 (2007) 27-39
36. Moro F., Fernández V., and Muga A. Interdomain interaction through helices A and B of DnaK peptide binding domain. FEBS Lett. 533 (2003) 119-123
37. Drees B.L., Grotkopp E.K., and Nelson H.C. The GCN4 leucine zipper can functionally substitute for the heat shock transcription factor's trimerization domain. J. Mol. Biol. 273 (1997) 61-74
38. Weissenhorn W., Calder L.J., Dessen A., Laue T., Skehel J.J., and Wiley D.C. Assembly of a rod-shaped chimera of a trimeric GCN4 zipper and the HIV-1 gp41 ectodomain expressed in Escherichia coli. Proc. Natl. Acad. Sci. USA 94 (1997) 6065-6069
39. Grimshaw J.P., Jelesarov I., Siegenthaler R.K., and Christen P. Thermosensor action of GrpE. The DnaK chaperone system at heat shock temperatures. J. Biol. Chem. 278 (2003) 19048-19053
40. Buchberger A., Schröder H., Büttner M., Valencia A., and Bukau B. A conserved loop in the ATPase domain of the DnaK chaperone is essential for stable binding of GrpE. Nat. Struct. Biol. 1 (1994) 95-101
41. 2-terminal domain of the chloroplast GrpE homolog CGE1 is required for dimerization and cochaperone function in vivo. J. Biol. Chem. 13 (2007) 11317-11328