BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

Characterization of nucleotide-induced changes on the quaternary structure of human 70 kDa heat shock protein Hsp70.1 by analytical ultracentrifugation

  • Borges, Julio C. (Depto. de Quimica e Fisica Molecular, Instituto de Quimica de Sao Carlos, USP) ;
  • Ramos, Carlos H.I. (Institute of Chemistry, University of Campinas-UNICAMP)
  • Published : 2009.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

Hsp70s assist in the process of protein folding through nucleotide-controlled cycles of substrate binding and release by alternating from an ATP-bound state in which the affinity for substrate is low to an ADP-bound state in which the affinity for substrate is high. It has been long recognized that the two-domain structure of Hsp70 is critical for these regulated interactions. Therefore, it is important to obtain information about conformational changes in the relative positions of Hsp70 domains caused by nucleotide binding. In this study, analytical ultracentrifugation and dynamic light scattering were used to evaluate the effect of ADP and ATP binding on the conformation of the human stress-induced Hsp70.1 protein. The results of these experiments showed that ATP had a larger effect on the conformation of Hsp70 than ADP. In agreement with previous biochemical experiments, our results suggest that conformational changes caused by nucleotide binding are a consequence of the movement in position of both nucleotide- and substrate-binding domains.

Keywords

References

  1. Wegele, H., M$\ddot{u}$ller, L. and Buchner, J. (2004) Hsp70 and Hsp90-a relay team for protein folding. Rev. Physiol. Biochem. Pharmacol. 151, 1-44 https://doi.org/10.1007/s10254-003-0021-1
  2. Borges, J.C. and Ramos, C.H.I. (2005) Protein folding assisted by chaperones. Protein Pept. Lett. 12, 256-261
  3. Lee, S. and Tsai, F.T.F. (2005) Molecular chaperones in protein quality control. J. Biochem. Mol Biol. 38, 259- 265 https://doi.org/10.5483/BMBRep.2005.38.3.259
  4. Craig, E.A. (1989) Essential roles of 70kDa heat inducible proteins. Bioessays 11, 48-52 https://doi.org/10.1002/bies.950110203
  5. Daugaard, M., Rohde, M. and J$\ddot{a}$$\ddot{a}$ttel$\ddot{a}$, M. (2007) The heat shock protein 70 family: highly homologous proteins with overlapping and distinct functions. FEBS Lett. 581, 3702-3710 https://doi.org/10.1016/j.febslet.2007.05.039
  6. Szabo, A., Langer, T., Schroder, H., Flanagan, J., Flanagan, J., Bukau, B. and Hartl, F.-U. (1994) The ATP hydrolysis-dependent reaction cycle of the Escherichia coli Hsp70 system - DnaK, DnaJ and GrpE. Proc. Natl. Acad. Sci. 91, 10345-10349 https://doi.org/10.1073/pnas.91.22.10345
  7. Russell, R., Karzai, A.W., Mehl, A.F. and McMacken, R. (1999) DnaJ dramatically stimulates ATP hydrolysis by DnaK: insight into targeting of Hsp70 proteins to polypeptide substrates. Biochemistry 38, 4165-4176 https://doi.org/10.1021/bi9824036
  8. Bukau, B. and Horwich, A.L. (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92, 351-366 https://doi.org/10.1016/S0092-8674(00)80928-9
  9. Buchberger, A., Theyssen, H., Schroder, H., McCarty, J.S., Virgallita, G., Milkereit, P., Reinstein, J. and Bukau, B. (1995) Nucleotide-induced conformational changes in the ATPase and substrate binding domains of the DnaK chaperone provide evidence for interdomain communication. J. Biol. Chem. 270, 16903-16910 https://doi.org/10.1074/jbc.270.28.16903
  10. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606-1619 https://doi.org/10.1016/S0006-3495(00)76713-0
  11. Schuck, P., Perugini, M.A., Gonzales, N.R., Howlett, G.J. and Schubert, D. (2002) Size-distribution analysis of proteins by analytical ultracentrifugation: strategies and application to model systems. Biophys. J. 82, 1096-1111 https://doi.org/10.1016/S0006-3495(02)75469-6
  12. Laue, T.M. (2001) Biophysical studies by ultracentrifugation. Curr. Opin. Struct. Biol. 11, 579-583 https://doi.org/10.1016/S0959-440X(00)00250-5
  13. Borges, J.C. and Ramos, C.H.I. (2006) Spectroscopic and thermodynamic measurements of nucleotide-induced changes in the human 70-kDa heat shock cognate protein. Arch. Biochem. Biophys. 452, 46-54 https://doi.org/10.1016/j.abb.2006.05.006
  14. Cantor, C. R. and Schimmel, P. R. (1980) Size and shape of macromolecules. In Biophysical Chemistry, Part II: Techniques for the Study of Biological Structure and Function (pg. 539-590). L.W. McCombs (ed.). W. H. Freeman and Company, New York
  15. Tanford, C. (1961) Physical Chemistry of Macromolecules. John Wiley & Sons, New York
  16. Hokputsa, S., Jumel, K., Alexander, C. and Harding, S.E. (2003) Hydrodynamic characterisation of chemically degraded hyaluronic acid. Carbohydrate Polymers 52, 111- 117 https://doi.org/10.1016/S0144-8617(02)00298-9
  17. Jiang, J., Prasad, K., Lafer, E.M. and Sousa, R. (2005) Structural basis of interdomain communication in the Hsc70 chaperone. Mol. Cell 20, 513-524 https://doi.org/10.1016/j.molcel.2005.09.028
  18. Sriram M., Osipiuk J., Freeman B., Morimoto R. and Joachimiak A. (1997) Human Hsp70 molecular chaperone binds two calcium ions within the ATPase domain. Structure 5, 403-414 https://doi.org/10.1016/S0969-2126(97)00197-4
  19. Osipiuk J., Walsh M.A., Freeman B.C., Morimoto R.I. and Joachimiak A. (1999) Structure of a new crystal form of human Hsp70 ATPase domain. Acta. Crystallogr. D. Biol. Crystallogr. 55, 1105-1107
  20. Morshauser R.C., Hu W., Wang H., Pang Y., Flynn G.C. and Zuiderweg ER. (1999) High-resolution solution structure of the 18 kDa substrate-binding domain of the mammalian chaperone protein Hsc70. J. Mol. Biol. 289, 1387- 1403 https://doi.org/10.1006/jmbi.1999.2776
  21. Worrall L.J. and Walkinshaw M.D. (2007) Crystal structure of the C-terminal three-helix bundle subdomain of C. elegans Hsp70. Biochem. Biophys. Res. Comun. 357, 105-110 https://doi.org/10.1016/j.bbrc.2007.03.107
  22. Revington, M., Zhang, Y., Yip, G.N., Kurochkin, A.V. and Zuiderweg, E.R. (2005) NMR investigations of allosteric processes in a two-domain thermus thermophilus Hsp70 molecular chaperone. J. Mol. Biol. 349,163-183 https://doi.org/10.1016/j.jmb.2005.03.033
  23. Fung, K.L., Hilgenberg, L., Wang, N.M. and Chirico, W.J. (1996) Conformations of the nucleotide and polypeptide binding domains of a cytosolic Hsp70 molecular chaperone are coupled. J. Biol. Chem. 271, 21559-21565 https://doi.org/10.1074/jbc.271.35.21559
  24. Revington, M., Holder, T.M. and Zuiderweg, E.R. (2004) NMR study of nucleotide-induced changes in the nucleotide binding domain of thermus thermophilus Hsp70 chaperone DnaK: implications for the allosteric mechanism. J. Biol. Chem. 279, 33958-33967 https://doi.org/10.1074/jbc.M313967200
  25. Borges, J.C., Fischer, H., Craievich, A.F., Hansen, L.D. and Ramos, C.H.I. (2003) Free human mitochondrial GrpE is a symmetric dimer in solution. J. Biol. Chem. 278, 35337-35344 https://doi.org/10.1074/jbc.M305083200
  26. Oliveira, C.L.P., Borges, J.C., Torriani, I. and Ramos, C.H.I. (2006) Low resolution structure and stability studies of human GrpE#2, a mitochondrial nucleotide exchange factor. Arch. Biochem. Biophys. 449, 77-86 https://doi.org/10.1016/j.abb.2006.02.015
  27. Ramos, C.H.I., Oliveira, C.L.P., Fan, C-Y, Torriani, I., and Cyr, D.M. (2008) Biophysical studies of chimeric type i and type II Hsp40s reveal that conserved central modules control the quaternary structure of Hsp40 family members. J. Mol. Biol. 383, 155-166 https://doi.org/10.1016/j.jmb.2008.08.019
  28. Johnson, M.L., Correia, J.J., Yphantis, D.A. and Halvorson, H.R. (1981) Analysis of data from the analytical ultracentrifuge by nonlinear least-squares techniques. Biophys. J. 36, 575-588 https://doi.org/10.1016/S0006-3495(81)84753-4
  29. Ralston, G. (1993) Introduction to analytical ultracentrifugation. Beckman Instruments Inc, Fullerton
  30. Lebowitz, J., Lewis, M.S. and Schuck, P. (2002) Modern analytical ultracentrifugation in protein science: a tutorial review. Protein Sci. 11, 2067-2079 https://doi.org/10.1110/ps.0207702
  31. Zhu, X., Zhao, X., Burkholder, W.F., Gragerov, A., Ogata, C.M., Gottesman, M.E. and Hendrickson, W.A. (1996) Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272, 1606-1614 https://doi.org/10.1126/science.272.5268.1606

Cited by

  1. Structural and functional characterization of the chaperone Hsp70 from sugarcane. Insights into conformational changes during cycling from cross-linking/mass spectrometry assays vol.104, 2014, https://doi.org/10.1016/j.jprot.2014.02.004
  2. Stoichiometry and thermodynamics of the interaction between the C-terminus of human 90kDa heat shock protein Hsp90 and the mitochondrial translocase of outer membrane Tom70 vol.513, pp.2, 2011, https://doi.org/10.1016/j.abb.2011.06.015
  3. Heat causes oligomeric disassembly and increases the chaperone activity of small heat shock proteins from sugarcane vol.48, pp.2-3, 2010, https://doi.org/10.1016/j.plaphy.2010.01.001
  4. Human Mitochondrial Hsp70 (Mortalin): Shedding Light on ATPase Activity, Interaction with Adenosine Nucleotides, Solution Structure and Domain Organization vol.10, pp.1, 2015, https://doi.org/10.1371/journal.pone.0117170
  5. Effects of transport distance, lairage time and stunning efficiency on cortisol, glucose, HSPA1A and how they relate with meat quality in cattle vol.117, 2016, https://doi.org/10.1016/j.meatsci.2016.03.001
  6. Structural and functional studies of the Leishmania braziliensis mitochondrial Hsp70: Similarities and dissimilarities to human orthologues vol.613, 2017, https://doi.org/10.1016/j.abb.2016.11.004
  7. Conformational Changes in Human Hsp70 Induced by High Hydrostatic Pressure Produce Oligomers with ATPase Activity but without Chaperone Activity vol.53, pp.18, 2014, https://doi.org/10.1021/bi500004q
  8. Molecular chaperones and heat shock proteins in atherosclerosis vol.302, pp.3, 2012, https://doi.org/10.1152/ajpheart.00646.2011