Quantification of interaction strengths between chaperones and tetratricopeptide repeat domain-containing membrane proteins

Journal of Biological Chemistry

Volumn 288, Issue 42, 2013, Pages 30614-30625

  Schweiger, Regina ^a   Soll, Jürgen ^a   Jung, Kirsten ^a   Heermann, Ralf ^a   Schwenkert, Serena ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING AFFINITIES; ENDOPLASMIC RETICULUM; INTERACTION MAPS; INTERACTION STRENGTH; MEMBRANE PROTEINS; PREPROTEINS; SURFACE PLASMON RESONANCE SPECTROSCOPY; TETRATRICOPEPTIDE REPEATS;

BINDING ENERGY; CELL MEMBRANES;

PROTEINS;

CHAPERONE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70.1; HEAT SHOCK PROTEIN 90.1; HEAT SHOCK PROTEIN 90.2; HEAT SHOCK PROTEIN 90.3; HEAT SHOCK PROTEIN 90.4; MEMBRANE PROTEIN; PROTEIN OM64; PROTEIN TOC64; PROTEIN TPR7; TETRATRICOPEPTIDE REPEAT PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARABIDOPSIS THALIANA; ARTICLE; BINDING AFFINITY; BIOCHEMISTRY; BIOPHYSICS; CONTROLLED STUDY; MOLECULAR DOCKING; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN IMMOBILIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; SURFACE PLASMON RESONANCE;

ARABIDOPSIS; CHLOROPLAST; ENDOPLASMIC RETICULUM(ER); INTERACTION MAP ANALYSIS; MICROSCALE THERMOPHORESIS; MITOCHONDRIA; SURFACE PLASMON RESONANCE (SPR);

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPLAST PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HSP90 HEAT-SHOCK PROTEINS; MEMBRANE PROTEINS; MITOCHONDRIAL PROTEINS; PROTEIN BINDING;

EID: 84886920674     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.493015     Document Type: Article

References (37)

1. Zimmermann, R., Eyrisch, S., Ahmad, M., and Helms, V. (2011) Protein translocation across the ER membrane. Biochim. Biophys. Acta 1808, 912-924
2. Schleiff, E., and Becker, T. (2011) Common ground for protein translocation: access control for mitochondria and chloroplasts. Nat. Rev. Mol. Cell Biol. 12, 48-59
3. Ast, T., Cohen, G., and Schuldiner, M. (2013) A network of cytosolic factors targets SRP-independent proteins to the endoplasmic reticulum. Cell 152, 1134-1145
4. Schlegel, T., Mirus, O., von Haeseler, A., and Schleiff, E. (2007) The tetratricopeptide repeats of receptors involved in protein translocation across membranes. Mol. Biol. Evol. 24, 2763-2774
5. Sommer, M., Rudolf, M., Tillmann, B., Tripp, J., Sommer, M. S., and Schleiff, E. (2013) Toc33 and Toc64-III cooperate in precursor protein import into the chloroplasts of Arabidopsis thaliana. Plant Cell Environ. 36, 970-983
6. Young, J. C., Hoogenraad, N. J., and Hartl, F. U. (2003) Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 112, 41-50
7. Lister, R., Carrie, C., Duncan, O., Ho, L. H., Howell, K. A., Murcha, M. W., and Whelan, J. (2007) Functional definition of outer membrane proteins involved in preprotein import into mitochondria. Plant Cell 19, 3739-3759
8. Scheufler, C., Brinker, A., Bourenkov, G., Pegoraro, S., Moroder, L., Bartunik, H., Hartl, F. U., and Moarefi, I. (2000) Structure of TPR domainpeptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101, 199-210
9. Fan, A. C., Bhangoo, M. K., and Young, J. C. (2006) Hsp90 functions in the targeting and outer membrane translocation steps of Tom70-mediated mitochondrial import. J. Biol. Chem. 281, 33313-33324
10. Faou, P., and Hoogenraad, N. J. (2012) Tom34: a cytosolic cochaperone of the Hsp90/Hsp70 protein complex involved in mitochondrial protein import. Biochim. Biophys. Acta 1823, 348-357
11. Bhangoo, M. K., Tzankov, S., Fan, A. C., Dejgaard, K., Thomas, D. Y., and Young, J. C. (2007) Multiple 40-kDa heat-shock protein chaperones function in Tom70-dependent mitochondrial import. Mol. Biol. Cell 18, 3414-3428
12. Chan, N. C., Likić, V. A., Waller, R. F., Mulhern, T. D., and Lithgow, T. (2006) The C-terminal TPR domain of Tom70 defines a family of mitochondrial protein import receptors found only in animals and fungi. J. Mol. Biol. 358, 1010-1022
13. Feldheim, D., and Schekman, R. (1994) Sec72p contributes to the selective recognition of signal peptides by the secretory polypeptide translocation complex. J. Cell Biol. 126, 935-943
14. Qbadou, S., Becker, T., Mirus, O., Tews, I., Soll, J., and Schleiff, E. (2006) The molecular chaperone Hsp90 delivers precursor proteins to the chloroplast import receptor Toc64. EMBO J. 25, 1836-1847
15. Qbadou, S., Becker, T., Bionda, T., Reger, K., Ruprecht, M., Soll, J., and Schleiff, E. (2007) Toc64-a preprotein-receptor at the outer membrane with bipartide function. J. Mol. Biol. 367, 1330-1346
16. Sohrt, K., and Soll, J. (2000) Toc64, a new component of the protein translocon of chloroplasts. J. Cell Biol. 148, 1213-1221
17. Carrie, C., Murcha, M. W., and Whelan, J. (2010) An in silico analysis of the mitochondrial protein import apparatus of plants.BMCPlant Biol. 10, 249
18. Chew, O., Lister, R., Qbadou, S., Heazlewood, J. L., Soll, J., Schleiff, E., Millar, A. H., and Whelan, J. (2004) A plant outer mitochondrial membrane protein with high amino acid sequence identity to a chloroplast protein import receptor. FEBS Lett. 557, 109-114
19. Schweiger, R., Müller, N. C., Schmitt, M. J., Soll, J., and Schwenkert, S. (2012) AtTPR7 is a chaperone-docking protein of the Sec translocon in Arabidopsis. J. Cell Sci. 125, 5196-5207
20. Schweiger, R., and Schwenkert, S. (2013) AtTPR7 as part of the Arabidopsis Sec post-translocon. Plant Signal. Behav. 8, doi 10.4161/psb.25286
21. Sung, D. Y., Vierling, E., and Guy, C. L. (2001) Comprehensive expression profile analysis of the Arabidopsis Hsp70 gene family. Plant Physiol. 126, 789-800
22. Krishna, P., and Gloor, G. (2001) The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperones 6, 238-246
23. Schmid, A. B., Lagleder, S., Gräwert, M. A., Rähl, A., Hagn, F., Wandinger, S. K., Cox, M. B., Demmer, O., Richter, K., Groll, M., Kessler, H., and Buchner, J. (2012) The architecture of functional modules in the Hsp90 co-chaperone Sti1/Hop. EMBO J. 31, 1506-1517
24. Lamberti, G., Gügel, I. L., Meurer, J., Soll, J., and Schwenkert, S. (2011) The cytosolic kinases STY8, STY17, and STY46 are involved in chloroplast differentiation in Arabidopsis. Plant Physiol. 157, 70-85
25. Fellerer, C., Schweiger, R., Schöngruber, K., Soll, J., and Schwenkert, S. (2011) Cytosolic HSP90 cochaperones HOP and FKBP interact with freshly synthesized chloroplast preproteins of Arabidopsis. Mol. Plant 4, 1133-1145
26. Zhang, X. P., and Glaser, E. (2002) Interaction of plant mitochondrial and chloroplast signal peptides with the Hsp70 molecular chaperone. Trends Plant Sci. 7, 14-21
27. Thompson, A. D., Bernard, S. M., Skiniotis, G., and Gestwicki, J. E. (2012) Visualization and functional analysis of the oligomeric states of Escherichia coli heat shock protein 70 (Hsp70/DnaK). Cell Stress Chaperones 17, 313-327
28. Kadota, Y., and Shirasu, K. (2012) The HSP90 complex of plants. Biochim. Biophys. Acta 1823, 689-697
29. Nemoto, T., and Sato, N. (1998) Oligomeric forms of the 90-kDa heat shock protein. Biochem. J. 330, 989-995
30. Aprile, F.A., Dhulesia, A., Stengel, F., Roodveldt, C., Benesch, J. L., Tortora, P., Robinson, C. V., Salvatella, X., Dobson, C. M., and Cremades, N. (2013)Hsp70 oligomerization is mediated by an interaction between the interdomain linker and the substrate-binding domain. PLoS One 8, e67961
31. Barta, P., Björkelund, H., and Andersson, K. (2011) Circumventing the requirement of binding saturation for receptor quantification using interaction kinetic extrapolation. Nucl. Med. Commun. 32, 863-867
32. Altschuh, D., Björkelund, H., Strandgard, J., Choulier, L., Malmqvist, M., and Andersson, K. (2012) Deciphering complex protein interaction kinetics using Interaction Map. Biochem. Biophys. Res. Commun. 428, 74-79
33. Seidel, S. A., Dijkman, P. M., Lea, W. A., van den Bogaart, G., Jerabek-Willemsen, M., Lazic, A., Joseph, J. S., Srinivasan, P., Baaske, P., Simeonov, A., Katritch, I., Melo, F. A., Ladbury, J. E., Schreiber, G., Watts, A., Braun, D., and Duhr, S. (2013) Microscale thermophoresis quantifies biomolecular interactions under previously challenging conditions. Methods 59, 301-315
34. Carrigan, P. E., Nelson, G. M., Roberts, P. J., Stoffer, J., Riggs, D. L., and Smith, D. F. (2004) Multiple domains of the co-chaperone Hop are important for Hsp70 binding. J. Biol. Chem. 279, 16185-16193
35. Brinker, A., Scheufler, C., Von Der Mulbe, F., Fleckenstein, B., Herrmann, C., Jung, G., Moarefi, I., and Hartl, F. U. (2002) Ligand discrimination by TPR domains. Relevance and selectivity of EEVD-recognition in Hsp70-Hop-Hsp90 complexes. J. Biol. Chem. 277, 19265-19275
36. Kriechbaumer, V., Tsargorodskaya, A., Mustafa, M. K., Vinogradova, T., Lacey, J., Smith, D. P., Abell, B. M., and Nabok, A. (2011) Study of receptorchaperone interactions using the optical technique of spectroscopic ellipsometry. Biophys. J. 101, 504-511
37. von Loeffelholz, O., Kriechbaumer, V., Ewan, R. A., Jonczyk, R., Lehmann, S., Young, J. C., and Abell, B. M. (2011) OEP61 is a chaperone receptor at the plastid outer envelope. Biochem. J. 438, 143-153