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Biological Chemistry

Editor-in-Chief: Brüne, Bernhard

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Volume 394, Issue 8

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Molecular function of the prolyl cis/trans isomerase and metallochaperone SlyD

Michael Kovermann
  • Institut für Physik, Biophysik, und Mitteldeutsches Zentrum für Struktur und Dynamik der Proteine (MZP), Martin-Luther Universität Halle-Wittenberg, D-06120 Halle, Germany
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Franz X. Schmid
  • Laboratorium für Biochemie und Bayreuther Zentrum für Molekulare Biowissenschaften, Universität Bayreuth, D-95440 Bayreuth, Germany
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Jochen Balbach
  • Corresponding author
  • Institut für Physik, Biophysik, und Mitteldeutsches Zentrum für Struktur und Dynamik der Proteine (MZP), Martin-Luther Universität Halle-Wittenberg, D-06120 Halle, Germany
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  • Other articles by this author:
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Published Online: 2013-03-28 | DOI: https://doi.org/10.1515/hsz-2013-0137

Abstract

SlyD is a bacterial two-domain protein that functions as a molecular chaperone, a prolyl cis/trans isomerase, and a nickel-binding protein. This review summarizes recent findings about the molecular enzyme mechanism of SlyD. The chaperone function located in one domain of SlyD is involved in twin-arginine translocation and increases the catalytic efficiency of the prolyl cis/trans isomerase domain in protein folding by two orders of magnitude. The C-terminal tail of SlyD binds Ni2+ ions and supplies them for the maturation of [NiFe] hydrogenases. A combined biochemical and biophysical analysis revealed the molecular basis of the delicate interplay of the different domains of SlyD for optimal function.

Keywords: chaperone; enzyme mechanism; nickel metalloprotein; protein folding; prolyl isomerase

References

  • Balbach, J., Steegborn, C., Schindler, T., and Schmid, F.X. (1999). A protein folding intermediate of ribonuclease T1 characterized at high resolution by 1D and 2D real-time NMR spectroscopy. J. Mol. Biol. 285, 829–842.Google Scholar

  • Balbach, J. and Schmid, F.X. (2000). Prolyl isomerization and its catalysis in protein folding. In: Mechanisms of Protein Folding, R.H. Pain, ed. (Oxford: Oxford University Press), pp. 212–237.Google Scholar

  • Bolanos-Garcia, V.M. and Davies, O.R. (2006). Structural analysis and classification of native proteins from E. coli commonly co-purified by immobilised metal affinity chromatography. Biochim. Biophys. Acta 1760, 1304–1313.Google Scholar

  • Brüser, T. (2007). The twin-arginine translocation system and its capability for protein secretion in biotechnological protein production. Appl. Microbiol. Biotechnol. 76, 35–45.Web of ScienceGoogle Scholar

  • Cheng, T., Li, H., Xia, W., and Sun, H. (2011). Multifaceted SlyD from Helicobacter pylori: implication in [NiFe] hydrogenase maturation. J. Biol. Inorg. Chem. 17, 331–343.Google Scholar

  • Dubini, A. and Sargent, F. (2003). Assembly of Tat-dependent [NiFe] hydrogenases: identification of precursor-binding accessory proteins. FEBS Lett. 549, 141–146.Google Scholar

  • Erdmann, F. and Fischer, G. (2007). The nickel-regulated peptidyl prolyl cis/trans isomerase SlyD. Metal Ions Life Sci 2, 501–528.Google Scholar

  • Fanghänel, J. and Fischer, G. (2004). Insights into the catalytic mechanism of peptidyl prolyl cis/trans isomerases. Front. Biosci. 9, 3453–3478.Google Scholar

  • Geitner, A.J. and Schmid, F.X. (2012). Combination of the human prolyl isomerase FKBP12 with unrelated chaperone domains leads to chimeric folding enzymes with high activity. J. Mol. Biol. 420, 335–349.Web of ScienceGoogle Scholar

  • Graubner, W., Schierhorn, A., and Brüser, T. (2007). DnaK plays a pivotal role in Tat targeting of CueO and functions beside SlyD as a general Tat signal binding chaperone. J. Biol. Chem. 282, 7116–7124.Web of ScienceGoogle Scholar

  • Haupt, C., Patzschke, R., Weininger, U., Groger, S., Kovermann, M., and Balbach, J. (2011a). Transient enzyme-substrate recognition monitored by real-time NMR. J. Am. Chem. Soc. 133, 11154–11162.Web of ScienceGoogle Scholar

  • Haupt, C., Weininger, U., Kovermann, M., and Balbach, J. (2011b). Local and coupled thermodynamic stability of the two domain and bifunctional enzyme SlyD from Escherichia coli. Biochemistry 50, 7321–7329.Web of ScienceGoogle Scholar

  • Hottenrott, S., Schumann, T., Plückthun, A., Fischer, G., and Rahfeld, J.U. (1997). The Escherichia coli SlyD is a metal ion-regulated peptidyl-prolyl cis/trans-isomerase. J. Biol. Chem. 272, 15697–15701.Google Scholar

  • Jakob, R.P., Zoldak, G., Aumüller, T., and Schmid, F.X. (2009). Chaperone domains convert prolyl isomerases into generic catalysts of protein folding. Proc. Natl. Acad. Sci. USA 106, 20282–20287.Google Scholar

  • Kahra, D., Kovermann, M., Löw, C., Hirschfeld, V., Haupt, C., Balbach, J., and Hübner, C.G. (2011). Conformational plasticity and dynamics in the generic protein folding catalyst SlyD unraveled by single-molecule FRET. J. Mol. Biol. 411, 781–790.Web of ScienceGoogle Scholar

  • Kaluarachchi, H., Sutherland, D.E.K., Young, A., Pickering, I.J., Stillman, M.J., and Zamble, D.B. (2009). The Ni(II)-binding properties of the metallochaperone SlyD. J. Am. Chem. Soc. 131, 18489–18500.Google Scholar

  • Kaluarachchi, H., Zhang, J.W., and Zamble, D.B. (2011). Escherichia coli SlyD, more than a Ni(II) reservoir. Biochemistry 50, 10761–10763.Web of ScienceGoogle Scholar

  • Kaluarachchi, H., Altenstein, M., Sugumar, S.R., Balbach, J., Zamble, D.B., and Haupt, C. (2012). Nickel binding and [NiFe]-hydrogenase maturation by the metallochaperone SlyD with a single metal-binding site in Escherichia coli. J. Mol. Biol. 417, 28–35.Web of ScienceGoogle Scholar

  • Knappe, T.A., Eckert, B., Schaarschmidt, P., Scholz, C., and Schmid, F.X. (2007). Insertion of a chaperone domain converts FKBP12 into a powerful catalyst of protein folding. J. Mol. Biol. 368, 1458–1468.Web of ScienceGoogle Scholar

  • Kovermann, M., Zierold, R., Haupt, C., Löw, C., and Balbach, J. (2011). NMR relaxation unravels interdomain crosstalk of the two domain prolyl isomerase and chaperone SlyD. Biochim. Biophys. Acta 1814, 873–881.Google Scholar

  • Kovermann, M. and Balbach, J. (2013). Dynamic control of the prolyl isomerase function of the dual-domain SlyD protein. Biophys. Chem. 171, 16–23.Web of ScienceGoogle Scholar

  • Leach, M.R. and Zamble, D.B. (2007). Metallocenter assembly of the hydrogenase enzymes. Curr. Opin. Chem. Biol. 11, 159–165.Web of ScienceGoogle Scholar

  • Li, Y. and Zamble, D.B. (2009). Nickel homeostasis and nickel regulation: an overview. Chem. Rev. 109, 4617–4643.Web of ScienceGoogle Scholar

  • Löw, C., Neumann, P., Tidow, H., Weininger, U., Haupt, C., Friedrich-Epler, B., Scholz, C., Stubbs, M.T., and Balbach, J. (2010). Crystal structure determination and functional characterization of the metallochaperone SlyD from Thermus thermophilus. J. Mol. Biol. 398, 375–390.Web of ScienceGoogle Scholar

  • Löw, C., Stubbs, M., Haupt, C., and Balbach, J. (2012). Metallochaperone SlyD. In: Encyclopedia of inorganic and Bioinorganic Chemistry, A., Scott, ed. (Sussex: John Wiley & Sons, Ltd.), DOI: 10.1002/9781119951438.eibc2061.CrossrefGoogle Scholar

  • Martinez-Hackert, E. and Hendrickson, W.A. (2011). Structural analysis of protein folding by the long-chain archaeal chaperone FKBP26. J. Mol. Biol. 407, 450–464.Web of ScienceGoogle Scholar

  • Martino, L., He, Y., Hands-Taylor, K.L.D., Valentine, E.R., Kelly, G., Giancola, C., and Conte, M.R. (2009). The interaction of the Escherichia coli protein SlyD with nickel ions illuminates the mechanism of regulation of its peptidyl-prolyl isomerase activity. FEBS J. 276, 4529–4544.Google Scholar

  • Mücke, M. and Schmid, F.X. (1994a). Folding mechanism of ribonuclease T1 in the absence of the disulfide bonds. Biochemistry 33, 14608–14619.Google Scholar

  • Mücke, M. and Schmid, F.X. (1994b). Intact disulfide bonds decelerate the folding of ribonuclease T1. J. Mol. Biol. 239, 713–725.Google Scholar

  • Quistgaard, E.M., Nordlund, P., and Löw, C. (2012). High-resolution insights into binding of unfolded polypeptides by the PPIase chaperone SlpA. FASEB J. 26, 4003–4013.Web of ScienceGoogle Scholar

  • Roof, W.D., Horne, S.M., Young, K.D., and Young, R. (1994). SlyD, a host gene required for phi X174 lysis, is related to the FK506-binding protein family of peptidyl-prolyl cis-trans-isomerases. J. Biol. Chem. 269, 2902–2910.Google Scholar

  • Roof, W.D., Fang, H.Q., Young, K.D., Sun, J., and Young, R. (1997). Mutational analysis of slyD, an Escherichia coli gene encoding a protein of the FKBP immunophilin family. Mol. Microbiol. 25, 1031–1046.Google Scholar

  • Scholz, C., Schaarschmidt, P., Engel, A.M., Andres, H., Schmitt, U., Faatz, E., Balbach, J., and Schmid, F.X. (2005). Functional solubilization of aggregation-prone HIV envelope proteins by covalent fusion with chaperone modules. J. Mol. Biol. 345, 1229–1241.Google Scholar

  • Scholz, C., Eckert, B., Hagn, F., Schaarschmidt, P., Balbach, J., and Schmid, F.X. (2006). SlyD proteins from different species exhibit high prolyl isomerase and chaperone activities. Biochemistry 45, 20–33.Google Scholar

  • Scholz, C., Thirault, L., Schaarschmidt, P., Zarnt, T., Faatz, E., Engel, A.M., Upmeier, B., Bollhagen, R., Ecket, B., and Schmid, F.X. (2008). Chaperone-aided in vitro renaturation of an engineered E1 envelope protein for detection of anti-Rubella virus IgG antibodies. Biochemistry 47, 4276–4287.Web of ScienceGoogle Scholar

  • Steegborn, C., Schneider-Hassloff, H., Zeeb, M., and Balbach, J. (2000). Cooperativity of a protein folding reaction probed at multiple chain positions by real-time 2D NMR spectroscopy. Biochemistry 39, 7910–7919.Google Scholar

  • Suzuki, R., Nagata, K., Yumoto, F., Kawakami, M., Nemoto, N., Furutani, M., Adachi, K., Maruyama, T., and Tanokura, M. (2003). Three-dimensional solution structure of an archaeal FKBP with a dual function of peptidyl prolyl cis-trans isomerase and chaperone-like activities. J. Mol. Biol. 328, 1149–1160.Google Scholar

  • Theuerkorn, M., Fischer, G., and Schiene-Fischer, C. (2011). Prolyl cis/trans isomerase signalling pathways in cancer. Curr. Opin. Pharmacol. 11, 281–287.Google Scholar

  • Van Duyne, G.D., Standaert, R.F., Karplus, P.A., Schreiber, S.L., and Clardy, J. (1991). Atomic structure of FKBP-FK506, an immunophilin-immunosuppressant complex. Science 252, 839–842.Google Scholar

  • Weininger, U., Haupt, C., Schweimer, K., Graubner, W., Kovermann, M., Brüser, T., Scholz, C., Schaarschmidt, P., Zoldak, G., Schmid, F.X., and Balbach, J. (2009). NMR solution structure of SlyD from Escherichia coli: spatial separation of prolyl isomerase and chaperone function. J. Mol. Biol. 387, 295–305.Web of ScienceGoogle Scholar

  • Yan, S.Z., Beeler, J.A., Chen, Y., Shelton, R.K., and Tang, W.J. (2001). The regulation of type 7 adenylyl cyclase by its C1b region and Escherichia coli peptidylprolyl isomerase, SlyD. J. Biol. Chem. 276, 8500–8506.Google Scholar

  • Zhang, J.W., Butland, G., Greenblatt, J.F., Emili, A., and Zamble, D.B. (2005). A role for SlyD in the Escherichia coli hydrogenase biosynthetic pathway. J. Biol. Chem. 280, 4360–4366.Google Scholar

  • Zoldák, G., Carstensen, L., Scholz, C., and Schmid, F.X. (2009). Consequences of domain insertion on the stability and folding mechanism of a protein. J. Mol. Biol. 386, 1138–1152.Web of ScienceGoogle Scholar

  • Zoldák, G. and Schmid, F.X. (2011). Cooperation of the prolyl isomerase and chaperone activities of the protein folding catalyst SlyD. J. Mol. Biol. 406, 176–194.Web of ScienceGoogle Scholar

About the article

Michael Kovermann

Michael Kovermann received his diploma degree in medical physics at the Martin-Luther-Universität Halle-Wittenberg, Germany, 2006. During his PhD in the biophysics lab of Jochen Balbach in the Physics Department of the same university, he focused on the NMR characterization of functional protein states. He solved several protein structures by this method and could relate protein function with protein dynamics. Currently, he is a postdoctoral fellow at the Umeå University in the group of Magnus Wolf-Watz.

Franz X. Schmid

Franz-Xaver Schmid studied chemistry at the Technische Universität Berlin and the Universität Regensburg (Germany), where he received his PhD for an analysis of substrate binding to dehydrogenases in 1977. After a postdoctoral stay at Stanford with Robert L. Baldwin, he received the venia legendi for biochemistry at the Universität Regensburg in the department of Rainer Jaenicke. Since 1988, he has been professor of biochemistry at the Universität Bayreuth, where he focuses on protein folding and its catalysis by folding enzymes. He is a member of the Deutsche Nationale Akademie der Wissenschaften, Leopoldina.

Jochen Balbach

Jochen Balbach studied chemistry at the Technische Universität München, where he also received his PhD for protein NMR studies in 1994. After a postdoctoral stay at the University of Oxford with Chris M. Dobson, he received the venia legendi for biochemistry at the University of Bayreuth under the supervision of Franz X. Schmid. Since 2004, he is professor of biophysics and medical physics at the Martin-Luther-Universität Halle-Wittenberg. He is interested in the structural biology and biophysics of proteins, their dynamics and folding reactions.


Corresponding author: Jochen Balbach, Institut für Physik, Biophysik, und Mitteldeutsches Zentrum für Struktur und Dynamik der Proteine (MZP), Martin-Luther Universität Halle-Wittenberg, D-06120 Halle, Germany


Received: 2013-01-31

Accepted: 2013-03-26

Published Online: 2013-03-28

Published in Print: 2013-08-01


Citation Information: Biological Chemistry, Volume 394, Issue 8, Pages 965–975, ISSN (Online) 1437-4315, ISSN (Print) 1431-6730, DOI: https://doi.org/10.1515/hsz-2013-0137.

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