Structural basis for the antifolding activity of a molecular chaperone

Nature

Volumn 537, Issue 7619, 2016, Pages 202-206

  Huang, Chengdong ^a   Rossi, Paolo ^a   Saio, Tomohide ^a   Kalodimos, Charalampos G ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; MALTOSE BINDING PROTEIN; PROTEIN SECB; BACTERIAL PROTEIN; CHAPERONE; ESCHERICHIA COLI PROTEIN; PHOA PROTEIN, E COLI; PROTEIN AGGREGATE; PROTEIN BINDING; SECB PROTEIN, BACTERIA;

CHEMICAL BINDING; CHEMICAL REACTION; HYDROPHOBICITY; MOLECULAR ANALYSIS; PHOSPHATASE; PROTEIN; REACTION KINETICS; SOLUTION;

ARTICLE; CONTROLLED STUDY; ESCHERICHIA COLI; HETERONUCLEAR MULTIPLE QUANTUM COHERENCE; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HYDROPHOBICITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN UNFOLDING; SURFACE PLASMON RESONANCE; CHEMICAL PHENOMENA; CHEMISTRY; ENZYME SPECIFICITY; KINETICS; METABOLISM; MOLECULAR MODEL;

ALKALINE PHOSPHATASE; BACTERIAL PROTEINS; ESCHERICHIA COLI PROTEINS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; KINETICS; MALTOSE-BINDING PROTEINS; MODELS, MOLECULAR; MOLECULAR CHAPERONES; PROTEIN AGGREGATES; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN UNFOLDING; SUBSTRATE SPECIFICITY;

EID: 84984661295     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature18965     Document Type: Article

References (42)

1. Bukau, B., Weissman, J., Horwich, A. Molecular chaperones and protein quality control. Cell 125, 443-451 (2006).
2. Kim, Y. E., Hipp, M. S., Bracher, A., Hayer-Hartl, M., Hartl, F. U. Molecular chaperone functions in protein folding and proteostasis. Annu. Rev. Biochem. 82, 323-355 (2013).
3. Saibil, H. Chaperone machines for protein folding, unfolding and disaggregation. Nature Rev. Mol. Cell Biol. 14, 630-642 (2013).
4. Horwich, A. L. Molecular chaperones in cellular protein folding: the birth of a field. Cell 157, 285-288 (2014).
5. Mattoo, R. U. H., Goloubinoff, P. Molecular chaperones are nanomachines that catalytically unfold misfolded and alternatively folded proteins. Cell. Mol. Life Sci. 71, 3311-3325 (2014).
6. Sala, A., Bordes, P., Genevaux, P. Multitasking SecB chaperones in bacteria. Front. Microbiol. 5, 666 (2014).
7. Hartl, F. U., Lecker, S., Schiebel, E., Hendrick, J. P., Wickner, W. The binding cascade of SecB to SecA to SecY/E mediates preprotein targeting to the E. coli plasma membrane. Cell 63, 269-279 (1990).
8. Hardy, S. J., Randall, L. L. A kinetic partitioning model of selective binding of nonnative proteins by the bacterial chaperone SecB. Science 251, 439-443 (1991).
9. Wolff, N., Sapriel, G., Bodenreider, C., Chaffotte, A., Delepelaire, P. Antifolding activity of the SecB chaperone is essential for secretion of HasA, a quickly folding ABC pathway substrate. J. Biol. Chem. 278, 38247-38253 (2003).
10. Bechtluft, P. et al. Direct observation of chaperone-induced changes in a protein folding pathway. Science 318, 1458-1461 (2007).
11. Zhou, J., Xu, Z. Structural determinants of SecB recognition by SecA in bacterial protein translocation. Nature Struct. Biol. 10, 942-947 (2003).
12. Ullers, R. S. et al. SecB is a bona fide generalized chaperone in Escherichia coli. Proc. Natl Acad. Sci. USA 101, 7583-7588 (2004).
13. Knoblauch, N. T. et al. Substrate specificity of the SecB chaperone. J. Biol. Chem. 274, 34219-34225 (1999).
14. Ullers, R. S., Ang, D., Schwager, F., Georgopoulos, C., Genevaux, P. Trigger factor can antagonize both SecB and DnaK/DnaJ chaperone functions in Escherichia coli. Proc. Natl Acad. Sci. USA 104, 3101-3106 (2007).
15. Sakr, S. et al. Lon protease quality control of presecretory proteins in Escherichia coli and its dependence on the SecB and DnaJ (Hsp40) chaperones. J. Biol. Chem. 285, 23506-23514 (2010).
16. Calloni, G. et al. DnaK functions as a central hub in the E. coli chaperone network. Cell Reports 1, 251-264 (2012).
17. Castanié-Cornet, M.-P., Bruel, N., Genevaux, P. Chaperone networking facilitates protein targeting to the bacterial cytoplasmic membrane. Biochim. Biophys. Acta 1843, 1442-1456 (2014).
18. Baars, L. et al. Defining the role of the Escherichia coli chaperone SecB using comparative proteomics. J. Biol. Chem. 281, 10024-10034 (2006).
19. Tang, Y., Pan, X., Tai, P. C., Sui, S.-F. The structure of SecB/OmpA as visualized by electron microscopy: The mature region of the precursor protein binds asymmetrically to SecB. Biochem. Biophys. Res. Commun. 393, 698-702 (2010).
20. Saio, T., Guan, X., Rossi, P., Economou, A., Kalodimos, C. G. Structural basis for protein antiaggregation activity of the trigger factor chaperone. Science 344, 1250494 (2014).
21. Rosenzweig, R., Moradi, S., Zarrine-Afsar, A., Glover, J. R., Kay, L. E. Unraveling the mechanism of protein disaggregation through a ClpB-DnaK interaction. Science 339, 1080-1083 (2013).
22. Zhuravleva, A., Clérico, E. M., Gierasch, L. M. An interdomain energetic tug-of-war creates the allosterically active state in Hsp70 molecular chaperones. Cell 151, 1296-1307 (2012).
23. Kerfah, R., Plevin, M. J., Sounier, R., Gans, P., Boisbouvier, J. Methyl-specific isotopic labeling: a molecular tool box for solution NMR studies of large proteins. Curr. Opin. Struct. Biol. 32, 113-122 (2015).
24. Murén, E. M., Suciu, D., Topping, T. B., Kumamoto, C. A., Randall, L. L. Mutational alterations in the homotetrameric chaperone SecB that implicate the structure as dimer of dimers. J. Biol. Chem. 274, 19397-19402 (1999).
25. Xu, Z., Knafels, J. D., Yoshino, K. Crystal structure of the bacterial protein export chaperone secB. Nature Struct. Biol. 7, 1172-1177 (2000).
26. Dekker, C., de Kruijff, B., Gros, P. Crystal structure of SecB from Escherichia coli. J. Struct. Biol. 144, 313-319 (2003).
27. Burmann, B. M., Wang, C., Hiller, S. Conformation and dynamics of the periplasmic membrane-protein-chaperone complexes OmpX-Skp and tOmpA-Skp. Nature Struct. Mol. Biol. 20, 1265-1272 (2013).
28. Krishnamurthy, V. M., Semetey, V., Bracher, P. J., Shen, N., Whitesides, G. M. Dependence of effective molarity on linker length for an intramolecular protein-ligand system. J. Am. Chem. Soc. 129, 1312-1320 (2007).
29. Gelis, I. et al. Structural basis for signal-sequence recognition by the translocase motor SecA as determined by NMR. Cell 131, 756-769 (2007).
30. Clare, D. K., Bakkes, P. J., van Heerikhuizen, H., van der Vies, S. M., Saibil, H. R. Chaperonin complex with a newly folded protein encapsulated in the folding chamber. Nature 457, 107-110 (2009).
31. Popovych, N., Tzeng, S. R., Tonelli, M., Ebright, R. H., Kalodimos, C. G. Structural basis for cAMP-mediated allosteric control of the catabolite activator protein. Proc. Natl Acad. Sci. USA 106, 6927-6932 (2009).
32. Milbradt, A. G. et al. Increased resolution of aromatic cross peaks using alternate 13C labeling and TROSY. J. Biomol. NMR 62, 291-301 (2015).
33. Delaglio, F. et al. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293 (1995).
34. Güntert, P. Automated NMR structure calculation with CYANA. Methods Mol. Biol. 278, 353-378 (2004).
35. Shen, Y., Delaglio, F., Cornilescu, G., Bax, A. TALOS+ : a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J. Biomol. NMR 44, 213-223 (2009).
36. Brunger, A. T. Version 1.2 of the Crystallography and NMR system. Nature Protocols 2, 2728-2733 (2007).
37. Chun, S. Y., Strobel, S., Bassford, P., Jr & Randall, L. L. Folding of maltosebinding protein. Evidence for the identity of the rate-determining step in vivo and in vitro. J. Biol. Chem. 268, 20855-20862 (1993).
38. Betton, J. M., Sassoon, N., Hofnung, M., Laurent, M. Degradation versus aggregation of misfolded maltose-binding protein in the periplasm of Escherichia coli. J. Biol. Chem. 273, 8897-8902 (1998).
39. Marsh, J. A., Singh, V. K., Jia, Z., Forman-Kay, J. D. Sensitivity of secondary structure propensities to sequence differences between-and-synuclein: implications for fibrillation. Protein Sci. 15, 2795-2804 (2006).
40. Camilloni, C., De Simone, A., Vranken, W. F., Vendruscolo, M. Determination of secondary structure populations in disordered states of proteins using nuclear magnetic resonance chemical shifts. Biochemistry 51, 2224-2231 (2012).
41. Betton, J. M., Hofnung, M. Folding of a mutant maltose-binding protein of Escherichia coli which forms inclusion bodies. J. Biol. Chem. 271, 8046-8052 (1996).
42. Tejero, R., Snyder, D., Mao, B., Aramini, J. M., Montelione, G. T. PDBStat: a universal restraint converter and restraint analysis software package for protein NMR. J. Biomol. NMR 56, 337-351 (2013).