DnaK prevents human insulin amyloid fiber formation on hydrophobic surfaces

Biochemistry

Volumn 51, Issue 11, 2012, Pages 2172-2180

  Ballet, Thomas ^a,b   Brukert, Franz ^a   Mangiagalli, Paolo ^b   Bureau, Christophe ^b   Boulangé, Laurence ^b,c   Nault, Laurent ^a   Perret, Thomas ^a   Weidenhaupt, Marianne ^a  

^a LABORATOIRE DES MATÉRIAUX ET DU GÉNIE PHYSIQUE   (France)

^b Becton Dickinson Pharmaceutical Systems   (France)

^c EKFB)   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATION KINETICS; AMYLOID FIBERS; GROWTH PHASE; HYDROPHOBIC SURFACES; LAG PHASE; MATERIAL SURFACE; MOLECULAR MECHANISM; PH-DEPENDENT; PROTEIN AGGREGATION; PROTEIN-SURFACE INTERACTIONS;

ADSORPTION; GLYCOPROTEINS; HYDROPHOBICITY; PEPTIDES; SURFACE CHEMISTRY;

INSULIN;

ADENOSINE TRIPHOSPHATE; AMYLOID; INSULIN; LEUCYLVALYLGLUTAMYLALANYLLEUCYLTYROSYLLEUCINE; NUCLEOTIDE; PEPTIDE; PROTEIN CLPB; PROTEIN DNAJ; PROTEIN DNAK; UNCLASSIFIED DRUG;

ADSORPTION; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; HORMONE PROTEIN COMPLEX; HYDROPHOBICITY; INSULIN BINDING; MOLECULAR DYNAMICS; PH; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN INTERACTION; SURFACE PROPERTY;

ADENOSINE TRIPHOSPHATE; AMYLOID; BACTERIAL PROTEINS; HEAT-SHOCK PROTEINS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; INSULIN; KINETICS; MOLECULAR CHAPERONES; PROTEIN RENATURATION; SURFACE PROPERTIES;

BACTERIA (MICROORGANISMS);

EID: 84858693441     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201457u     Document Type: Article

References (33)

1. Ellis, R. J. and van der Vies, S. M. (1991) Molecular chaperones Annu. Rev. Biochem. 60, 321-347
2. Ellis, R. J., van der Vies, S. M., and Hemmingsen, S. M. (1989) The molecular chaperone concept Biochem. Soc. Symp. 55, 145-153 (Pubitemid 19111028)
3. Ellis, R. J. and Hemmingsen, S. M. (1989) Molecular chaperones: Proteins essential for the biogenesis of some macromolecular structures Trends Biochem. Sci. 14, 339-342 (Pubitemid 19191344)
4. Mogk, A., Tomoyasu, T., Goloubinoff, P., Rudiger, S., Roder, D., Langen, H., and Bukau, B. (1999) Identification of thermolabile Escherichia coli proteins: Prevention and reversion of aggregation by DnaK and ClpB EMBO J. 18, 6934-6949 (Pubitemid 30000447)
5. Bukau, B. and Horwich, A. L. (1998) The Hsp70 and Hsp60 chaperone machines Cell 92, 351-366 (Pubitemid 28093013)
6. Goloubinoff, P., Mogk, A., Zvi, A. P., Tomoyasu, T., and Bukau, B. (1999) Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network Proc. Natl. Acad. Sci. U.S.A. 96, 13732-13737
7. Diamant, S., Ben-Zvi, A. P., Bukau, B., and Goloubinoff, P. (2000) Size-dependent disaggregation of stable protein aggregates by the DnaK chaperone machinery J. Biol. Chem. 275, 21107-21113 (Pubitemid 30481803)
8. Sluzky, V., Tamada, J. A., Klibanov, A. M., and Langer, R. (1991) Kinetics of insulin aggregation in aqueous solutions upon agitation in the presence of hydrophobic surfaces Proc. Natl. Acad. Sci. U.S.A. 88, 9377-9381 (Pubitemid 21915634)
9. Sluzky, V., Klibanov, A. M., and Langer, R. (1992) Mechanism of insulin aggregation and stabilization in agitated aqueous solutions Biotechnol. Bioeng. 40, 895-903
10. Brange, J., Andersen, L., Laursen, E. D., Meyn, G., and Rasmussen, E. (1997) Toward understanding insulin fibrillation J. Pharm. Sci. 86, 517-525 (Pubitemid 27203397)
11. Sharp, J. S., Forrest, J. A., and Jones, R. A. (2002) Surface denaturation and amyloid fibril formation of insulin at model lipid-water interfaces Biochemistry 41, 15810-15819 (Pubitemid 36062486)
12. Rüdiger, S., Germeroth, L., Schneider-Mergener, J., and Bukau, B. (1997) Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries, EMBO J 16, 1507 - 582.
13. Ivanova, M. I., Sievers, S. A., Sawaya, M. R., Wall, J. S., and Eisenberg, D. (2009) Molecular basis for insulin fibril assembly Proc. Natl. Acad. Sci. U.S.A. 106, 18990-18995
14. Cegielska, A. and Georgopoulos, C. (1989) Functional domains of the Escherichia coli dnaK heat shock protein as revealed by mutational analysis J. Biol. Chem. 264, 21122-21130 (Pubitemid 20017927)
15. 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. U.S.A. 88, 9513-9517 (Pubitemid 21915661)
16. Buchberger, A., Schroder, H., Buttner, M., Valencia, A., and Bukau, B. (1994) A conserved loop in the ATPase domain of the DnaK chaperone is essential for stable binding of GrpE Nat. Struct. Biol. 1, 95-101 (Pubitemid 24974821)
17. Veinger, L., Diamant, S., Buchner, J., and Goloubinoff, P. (1998) The small heat-shock protein IbpB from Escherichia coli stabilizes stress-denatured proteins for subsequent refolding by a multichaperone network J. Biol. Chem. 273, 11032-11037 (Pubitemid 28204946)
18. Olson, B. J. and Markwell, J. (2007) Assays for determination of protein concentration. Current Protocols in Protein Science, Chapter 3, Unit 3, 4, Wiley, New York.
19. Smith, D. A. and Radford, S. E. (2000) Protein folding: Pulling back the frontiers Curr. Biol. 10, R662-R664
20. Wiechelman, K. J., Braun, R. D., and Fitzpatrick, J. D. (1988) Investigation of the bicinchoninic acid protein assay: Identification of the groups responsible for color formation Anal. Biochem. 175, 231-237
21. Stoscheck, C. M. (1990) Quantitation of protein Methods Enzymol. 182, 50-68 (Pubitemid 20154379)
22. LeVine, H., III (1999) Quantification of β-sheet amyloid fibril structures with thioflavin T Methods Enzymol. 309, 274-284
23. Blundell, T. L., Cutfield, J. F., Dodson, G. G., Dodson, E., Hodgkin, D. C., and Mercola, D. (1971) The structure and biology of insulin Biochem. J. 125, 50P-51P
24. Burke, M. J. and Rougvie, M. A. (1972) Cross-β protein structures. I. Insulin fibrils Biochemistry 11, 2435-2439
25. Garriques, L. N., Frokjaer, S., Carpenter, J. F., and Brange, J. (2002) The effect of mutations on the structure of insulin fibrils studied by Fourier transform infrared (FTIR) spectroscopy and electron microscopy J. Pharm. Sci. 91, 2473-2480 (Pubitemid 35379405)
26. Theyssen, H., Schuster, H. P., Packschies, L., Bukau, B., and Reinstein, J. (1996) The second step of ATP binding to DnaK induces peptide release J. Mol. Biol. 263, 657-670 (Pubitemid 26395058)
27. McCarty, J. S., Buchberger, A., Reinstein, J., and Bukau, B. (1995) The role of ATP in the functional cycle of the DnaK chaperone system J. Mol. Biol. 249, 126-137
28. Skowyra, D. and Wickner, S. (1995) GrpE Alters the Affinity of DnaK for ATP and Mg J. Biol. Chem. 270, 26282-26285
29. Suh, W.-C., Burkholder, W. F., Lu, C. Z., Zhao, X., Gottesman, M. E., and Gross, C. A. (1998) Interaction of the Hsp70 molecular chaperone, DnaK, with its cochaperone DnaJ Proc. Natl. Acad. Sci. U.S.A. 95, 15223-15228 (Pubitemid 29018680)
30. Liberek, K., Wall, D., and Georgopoulos, C. (1995) The DnaJ chaperone catalytically activates the DnaK chaperone to preferentially bind the sigma 32 heat shock transcriptional regulator Proc. Natl. Acad. Sci. U.S.A. 92, 6224-6228
31. Rasmussen, T., Kasimova, M. R., Jiskoot, W., and van de Weert, M. (2009) The Chaperone-like Protein β-Crystallin Dissociates Insulin Dimers and Hexamers, Biochemistry 48, 9313-9320.
32. Rasmussen, T., Tantipolphan, R., van de Weert, M., and Jiskoot, W. (2010) The molecular chaperone alpha-crystallin as an excipient in an insulin formulation. Pharm Res 27, 1337-1347.
33. Nolan, A., Weiden, M. D., Hoshino, Y., and Gold, J. A. (2004) Cd40 but not CD154 knockout mice have reduced inflammatory response in polymicrobial sepsis: A potential role for Escherichia coli heat shock protein 70 in CD40-mediated inflammation in vivo Shock 22, 538-542 (Pubitemid 39576581)