Action of the Hsp70 chaperone system observed with single proteins

Nature Communications

Volumn 6, Issue , 2015, Pages

  Nunes, João M ^a   Mayer Hartl, Manajit ^b   Hartl, F Ulrich ^b   Müller, Daniel J ^a  

^a ETH ZURICH   (Switzerland)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN 70; IMMUNOGLOBULIN; IMMUNOGLOBULIN 27; PROTEIN DNAJ; PROTEIN DNAK; PROTEIN GRPE; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; CONNECTIN; DNAJ PROTEIN, E COLI; DNAK PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; GOLD; GRPE PROTEIN, E COLI; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 40; PROTEIN BINDING; TTN PROTEIN, HUMAN;

ANTIBODY; COLIFORM BACTERIUM; GENE EXPRESSION; PEPTIDE; PROTEIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; BETA SHEET; CONFORMATIONAL TRANSITION; ESCHERICHIA COLI; MOLECULAR WEIGHT; NONHUMAN; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN HYDROLYSIS; PROTEIN REFOLDING; PROTEIN UNFOLDING; STEADY STATE; APOPTOSIS; BINDING SITE; CHEMISTRY; HUMAN; HYDROLYSIS; KINETICS; METABOLISM; PROTEIN MULTIMERIZATION;

ESCHERICHIA COLI;

ADENOSINE TRIPHOSPHATE; APOPTOSIS; BINDING SITES; CONNECTIN; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GOLD; HEAT-SHOCK PROTEINS; HSP40 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; HYDROLYSIS; KINETICS; MICROSCOPY, ATOMIC FORCE; MOLECULAR CHAPERONES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION;

EID: 84943453603     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7307     Document Type: Article

References (47)

1. Zimmerman, S. B. & Trach, S. O. Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli. J. Mol. Biol. 222, 599-620 (1991).
2. Hartl, F. U. & Hayer-Hartl, M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295, 1852-1858 (2002).
3. Langer, T., Lu, C., Echols, H., Flanagan, J., Hayer, M. K. & Hartl, F. U. Successive action of DnaK, DnaJ and GroEL along the pathway of chaperonemediated protein folding. Nature 356, 683-689 (1992).
4. Hendrick, J. P., Langer, T., Davis, T. A., Hartl, F. U. & Wiedmann, M. Control of folding and membrane translocation by binding of the chaperone DnaJ to nascent polypeptides. Proc. Natl Acad. Sci. USA 90, 10216-10220 (1993).
5. Szabo, A., Langer, T., Schroder, H., Flanagan, J., Bukau, B. & Hartl, F. U. The ATP hydrolysis-dependent reaction cycle of the Escherichia coli Hsp70 system DnaK, DnaJ, and GrpE. Proc. Natl Acad. Sci. USA 91, 10345-10349 (1994).
6. Liberek, K., Marszalek, J., Ang, D., Georgopoulos, C. & Zylicz, M. Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc. Natl Acad. Sci. USA 88, 2874-2878 (1991).
7. Laufen, T. et al. Mechanism of regulation of Hsp70 chaperones by DnaJ cochaperones. Proc. Natl Acad. Sci. USA 96, 5452-5457 (1999).
8. Siegenthaler, R. K. & Christen, P. Tuning of DnaK chaperone action by nonnative protein sensor DnaJ and thermosensor GrpE. J. Biol. Chem. 281, 34448-34456 (2006).
9. Szabo, A., Korszun, R., Hartl, F. U. & Flanagan, J. A zinc finger-like domain of the molecular chaperone DnaJ is involved in binding to denatured protein substrates. EMBO J. 15, 408-417 (1996).
10. Zylicz, M., Yamamoto, T., McKittrick, N., Sell, S. & Georgopoulos, C. Purification and properties of the DnaJ replication protein of Escherichia coli. J. Biol. Chem. 260, 7591-7598 (1985).
11. Schönfeld, H. J. & Behlke, J. Molecular chaperones and their interactions investigated by analytical ultracentrifugation and other methodologies. Meth. Enzymol. 290, 269-296 (1998).
12. Shi, Y. Y., Hong, X. G. & Wang, C. C. The C-terminal (331-376) sequence of Escherichia coli DnaJ is essential for dimerization and chaperone activity: a small angle X-ray scattering study in solution. J. Biol. Chem. 280, 22761-22768 (2005).
13. Gamer, J. et al. A cycle of binding and release of the DnaK, DnaJ and GrpE chaperones regulates activity of the Escherichia coli heat shock transcription factor sigma32. EMBO J. 15, 607-617 (1996).
14. Rudiger, S., Schneider-Mergener, J. & Bukau, B. Its substrate specificity characterizes the DnaJ co-chaperone as a scanning factor for the DnaK chaperone. EMBO J. 20, 1042-1050 (2001).
15. Schroder, H., Langer, T., Hartl, F. U. & Bukau, B. DnaK, DnaJ and GrpE form a cellular chaperone machinery capable of repairing heat-induced protein damage. EMBO J. 12, 4137-4144 (1993).
16. Horwich, A. L., Farr, G. W. & Fenton, W. A. GroEL-GroES-mediated protein folding. Chem. Rev. 106, 1917-1930 (2006).
17. Tskhovrebova, L. & Trinick, J. Properties of titin immunoglobulin and fibronectin-3 domains. J. Biol. Chem. 279, 46351-46354 (2004).
18. Rief, M., Gautel, M., Oesterhelt, F., Fernandez, J. M. & Gaub, H. E. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276, 1109-1112 (1997).
19. Nunes, J. M. et al. A 'force buffer' protecting immunoglobulin titin. Angew. Chem. Int. Ed. Engl. 49, 3528-3531 (2010).
20. Carrion-Vazquez, M. et al. Mechanical and chemical unfolding of a single protein: a comparison. Proc. Natl Acad. Sci. USA 96, 3694-3699 (1999).
21. Borgia, M. B. et al. Single-molecule fluorescence reveals sequence-specific misfolding in multidomain proteins. Nature 474, 662-665 (2011).
22. Wright, C. F., Teichmann, S. A., Clarke, J. & Dobson, C. M. The importance of sequence diversity in the aggregation and evolution of proteins. Nature 438, 878-881 (2005).
23. Kaiser, C. M. et al. Real-time observation of trigger factor function on translating ribosomes. Nature 444, 455-460 (2006).
24. Oberhauser, A. F., Marszalek, P. E., Carrion-Vazquez, M. & Fernandez, J. M. Single protein misfolding events captured by atomic force microscopy. Nature Struct. Biol. 6, 1025-1028 (1999).
25. Muchowski, P. J., Schaffar, G., Sittler, A., Wanker, E. E., Hayer-Hartl, M. K. & Hartl, F. U. Hsp70 and Hsp40 chaperones can inhibit self-assembly of polyglutamine proteins into amyloid-like fibrils. Proc. Natl Acad. Sci. USA 97, 7841-7846 (2000).
26. Mayer, M. P., Rudiger, S. & Bukau, B. Molecular basis for interactions of the DnaK chaperone with substrates. Biol. Chem. 381, 877-885 (2000).
27. Mayer, M. P., Schroder, H., Rudiger, S., Paal, K., Laufen, T. & Bukau, B. Multistep mechanism of substrate binding determines chaperone activity of Hsp70. Nature Struct. Biol. 7, 586-593 (2000).
28. Liu, X. Concentrations of the GroEL/GroES and DnaK/DnaJ/GrpE molecular chaperones in Escherichia coli under normal and heat shock conditions. PhD thesis. Universität Zürich (2002).
29. Grimshaw, J. P. et al. DsbL and DsbI form a specific dithiol oxidase system for periplasmic arylsulfate sulfotransferase in uropathogenic Escherichia coli. J. Mol. Biol. 380, 667-680 (2008).
30. Sugimoto, S., Saruwatari, K., Higashi, C. & Sonomoto, K. The proper ratio of GrpE to DnaK is important for protein quality control by the DnaK-DnaJGrpE chaperone system and for cell division. Microbiology 154, 1876-1885 (2008).
31. Zhu, X. et al. Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272, 1606-1614 (1996).
32. Rudiger, S., Germeroth, L., Schneider-Mergener, J. & Bukau, B. Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. EMBO J. 16, 1501-1507 (1997).
33. Wagner, P. Immobilization strategies for biological scanning probe microscopy. FEBS Lett. 430, 112-115 (1998).
34. Marck, C. 'DNA Strider': a 'C' program for the fast analysis of DNA and protein sequences on the Apple Macintosh family of computers. Nucleic Acids Res. 16, 1829-1836 (1988).
35. Steward, A., Toca-Herrera, J. L. & Clarke, J. Versatile cloning system for construction of multimeric proteins for use in atomic force microscopy. Protein Sci. 11, 2179-2183 (2002).
36. Palleros, D. R., Reid, K. L., McCarty, J. S., Walker, G. C. & Fink, A. L. DnaK, Hsp73, and their molten globules. Two different ways heat shock proteins respond to heat. J. Biol. Chem. 267, 5279-5285 (1992).
37. Zylicz, M., Ang, D. & Georgopoulos, C. The grpE protein of Escherichia coli. Purification and properties. J. Biol. Chem. 262, 17437-17442 (1987).
38. Schaffar, G. et al. Cellular toxicity of polyglutamine expansion proteins: mechanism of transcription factor deactivation. Mol. Cell 15, 95-105 (2004).
39. Dietz, H. et al. Cysteine engineering of polyproteins for single-molecule force spectroscopy. Nat. Protoc. 1, 80-84 (2006).
40. Struckmeier, J. et al. Fully automated single-molecule force spectroscopy for screening applications. Nanotechnology 19, 384020 (2008).
41. Hutter, J. L. & Bechhoefer, J. Calibration of atomic-force microscope tips. Rev. Sci. Instr. 64, 1868-1873 (1993).
42. te Riet, J. et al. Interlaboratory round robin on cantilever calibration for AFM force spectroscopy. Ultramicroscopy 111, 1659-1669 (2011).
43. Kleijn, J. M., Barten, D. & Stuart, M. A. Adsorption of charged macromolecules at a gold electrode. Langmuir. 20, 9703-9713 (2004).
44. Nezu, T., Masuyama, T., Sasaki, K., Saitoh, S., Taira, M. & Araki, Y. Effect of pH and addition of salt on the adsorption behavior of lysozyme on gold, silica, and titania surfaces observed by quartz crystal microbalance with dissipation monitoring. Dent. Mater. J. 27, 573-580 (2008).
45. Kratky, O. Röntgenuntersuchung gelöster Fadenmoleküle. Recl. Trav. Chim. Pays-Bas. 68, 1106-1122 (1949).
46. Shapiro, S. S. & Wilk, M. B. An analysis of variance test for normality. Biometrika 52, 591-611 (1965).
47. Fay, M. P. & Proschan, M. A. Wilcoxon-Mann-Whitney or t-test? On assumptions for hypothesis tests and multiple interpretations of decision rules. Stat. Surv. 4, 1-39 (2010).