Cooperation of the prolyl isomerase and chaperone activities of the protein folding catalyst SlyD

Journal of Molecular Biology

Volumn 406, Issue 1, 2011, Pages 176-194

  Zoldák, Gabriel ^a,b   Schmid, Franz X ^a  

^a UNIVERSITY OF BAYREUTH   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

AEDANS; cis trans isomerization; resonance energy transfer; trigger factor

Indexed keywords

BACTERIAL PROTEIN; CHAPERONE; PEPTIDYLPROLYL ISOMERASE; SENSITIVE TO LYSIS D PROTEIN; TETRAPEPTIDE; UNCLASSIFIED DRUG;

ARTICLE; ENZYME ACTIVITY; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION;

ESCHERICHIA COLI;

EID: 79151480151     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.12.010     Document Type: Article

References (61)

1. Kim P.S., and Baldwin R.L. Intermediates in the folding reactions of small proteins Annu. Rev. Biochem. 59 1990 631 660
2. Jaenicke R. Folding and association of proteins Prog. Biophys. Mol. Biol. 49 1987 117 237
3. Matthews C.R. Pathways of protein folding Annu. Rev. Biochem. 62 1993 653 683
4. Englander S.W., Mayne L., and Krishna M.M. Protein folding and misfolding: mechanism and principles Q. Rev. Biophys. 40 2008 287 326
5. Dobson C.M. Principles of protein folding, misfolding and aggregation Semin. Cell Dev. Biol. 15 2004 3 16
6. Hartl F.U., and Hayer-Hartl M. Converging concepts of protein folding in vitro and in vivo Nat. Struct. Mol. Biol. 16 2009 574 581
7. Buchner J. Supervising the fold: functional principles of molecular chaperones FASEB J. 10 1996 10 19
8. Walter S., and Buchner J. Molecular chaperones-cellular machines for protein folding Angew. Chem. Int. Ed. 41 2002 1098 1113
9. Bukau B., Deuerling E., Pfund C., and Craig E.A. Getting newly synthesized proteins into shape Cell 101 2000 119 122
10. Fanghänel J., and Fischer G. Insights into the catalytic mechanism of peptidyl prolyl cis/trans isomerases Front. Biosci. 9 2004 3453 3478
11. Fischer G., and Schmid F.X. Peptidyl-prolyl cis/trans isomerases B. Bukau, Molecular Biology of Chaperones and Folding Catalysts 1999 Harwood Academic Publishers New York, NY 461 489
12. Balbach J., and Schmid F.X. Prolyl isomerization and its catalysis in protein folding R.H. Pain, Mechanisms of Protein Folding 2000 Oxford University Press Oxford, UK 212 237
13. Schmid F.X. Catalysis of protein folding by prolyl isomerases A.L. Fink, Y. Goto, Molecular Chaperones in the Life Cycle of Proteins 1998 Marcel Dekker, Inc. New York, NY 361 389
14. Gruber C.W., Cemazar M., Heras B., Martin J.L., and Craik D.J. Protein disulfide isomerase: the structure of oxidative folding Trends Biochem. Sci. 31 2006 455 464
15. Stoller G., Rücknagel K.P., Nierhaus K., Schmid F.X., Fischer G., and Rahfeld J.U. Identification of the peptidyl-prolyl cis/trans isomerase bound to the Escherichia coli ribosome as the trigger factor EMBO J. 14 1995 4939 4948
16. Schiene-Fischer C., Habazettl J., Schmid F.X., and Fischer G. The hsp70 chaperone DnaK is a secondary amide peptide bond cis-trans isomerase Nat. Struct. Biol. 9 2002 419 424
17. Ramm K., and Plückthun A. High enzymatic activity and chaperone function are mechanistically related features of the dimeric E. coli peptidyl-prolyl-isomerase FkpA J. Mol. Biol. 310 2001 485 498
18. Hottenrott S., Schumann T., Plückthun A., Fischer G., and Rahfeld J.U. The Escherichia coli SlyD is a metal ion-regulated peptidyl-prolyl cis/trans isomerase J. Biol. Chem. 272 1997 15697 15701
19. Scholz C., Eckert B., Hagn F., Schaarschmidt P., Balbach J., and Schmid F.X. SlyD proteins from different species exhibit high prolyl isomerase and chaperone activities Biochemistry 45 2006 20 33
20. McCarthy A.A., Haebel P.W., Torronen A., Rybin V., Baker E.N., and Metcalf P. Crystal structure of the protein disulfide bond isomerase, DsbC, from Escherichia coli Nat. Struct. Biol. 7 2000 196 199
21. Heras B., Edeling M.A., Schirra H.J., Raina S., and Martin J.L. Crystal structures of the DsbG disulfide isomerase reveal an unstable disulfide Proc. Natl Acad. Sci. USA 101 2004 8876 8881
22. Tian G., Xiang S., Noiva R., Lennarz W.J., and Schindelin H. The crystal structure of yeast protein disulfide isomerase suggests cooperativity between its active sites Cell 124 2006 61 73
23. Roof W.D., and Young R. Phi X174 lysis requires slyD, a host gene which is related to the FKBP family of peptidyl-prolyl cis-trans isomerases FEMS Microbiol. Rev. 17 1995 213 218
24. Roof W.D., Fang H.Q., Young K.D., Sun J., and Young R. Mutational analysis of slyD, an Escherichia coli gene encoding a protein of the FKBP immunophilin family Mol. Microbiol. 25 1997 1031 1046
25. Bernhardt T.G., Roof W.D., and Young R. The Escherichia coli FKBP-type PPIase SlyD is required for the stabilization of the E lysis protein of bacteriophage phi X174 Mol. Microbiol. 45 2002 99 108
26. Mendel S., Holbourn J.M., Schouten J.A., and Bugg T.D. Interaction of the transmembrane domain of lysis protein E from bacteriophage {phi}X174 with bacterial translocase MraY and peptidyl-prolyl isomerase SlyD Microbiology 152 2006 2959 2967
27. Roof W.D., Horne S.M., Young K.D., and Young R. 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 1994 2902 2910
28. Zhang J.W., Butland G., Greenblatt J.F., Emili A., and Zamble D.B. A role for SlyD in the Escherichia coli hydrogenase biosynthetic pathway J. Biol. Chem. 280 2005 4360 4366
29. Young R. Bacteriophage lysis: mechanism and regulation Microbiol. Rev. 56 1992 430 481
30. Graubner W., Schierhorn A., and Brüser T. 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 2007 7116 7124
31. Weininger U., Haupt C., Schweimer K., Graubner W., Kovermann M., and Brüser T. NMR solution structure of SlyD from Escherichia coli: spatial separation of prolyl isomerase and chaperone function J. Mol. Biol. 387 2009 295 305
32. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
33. Wülfing C., Lombardero J., and Plückthun A. An Escherichia coli protein consisting of a domain homologous to FK506-binding proteins (FKBP) and a new metal binding motif J. Biol. Chem. 269 1994 2895 2901
34. Löw C., Neumann P., Tidow H., Weininger U., Haupt C., and Friedrich-Epler B. Crystal structure determination and functional characterization of the metallochaperone SlyD from Thermus thermophilus J. Mol. Biol. 398 2010 375 390
35. Zoldák G., Carstensen L., Scholz C., and Schmid F.X. Consequences of domain insertion on the stability and folding mechanism of a protein J. Mol. Biol. 386 2009 1138 1152
36. Knappe T.A., Eckert B., Schaarschmidt P., Scholz C., and Schmid F.X. Insertion of a chaperone domain converts FKBP12 into a powerful catalyst of protein folding J. Mol. Biol. 368 2007 1458 1468
37. Harrison R.K., and Stein R.L. Substrate specificities of the peptidyl prolyl cis-trans isomerase activities of cyclophilin and FK-506 binding protein: evidence for the existence of a family of distinct enzymes Biochemistry 29 1990 3813 3816
38. Jakob R.P., Zoldák G., Aumüller T., and Schmid F.X. Chaperone domains convert prolyl isomerases into generic catalysts of protein folding Proc. Natl Acad. Sci. USA 106 2009 20282 20287
39. Mayr L.M., Landt O., Hahn U., and Schmid F.X. Stability and folding kinetics of ribonuclease T1 are strongly altered by the replacement of cis-proline 39 with alanine J. Mol. Biol. 231 1993 897 912
40. Mücke M., and Schmid F.X. Folding mechanism of ribonuclease T1 in the absence of the disulfide bonds Biochemistry 33 1994 14608 14619
41. Wang Z.X. An exact mathematical expression for describing competitive binding of two different ligands to a protein molecule FEBS Lett. 360 1995 111 114
42. Schlee S., and Reinstein J. Characterization of ATPase cycles of molecular chaperones by fluorescence and transient kinetic methods J. Buchner, T. Kiefhaber, Protein Folding Handbook vol. 2 2005 Wiley-VCH Weinheim, Germany 105 167 2 volumes
43. Kuzmic P., Moss M.L., Kofron J.L., and Rich D.H. Fluorescence displacement method for the determination of receptor-ligand binding constants Anal. Biochem. 205 1992 65 69
44. Zoldák G., Aumüller T., Lücke C., Hritz J., Oostenbrink C., Fischer G., and Schmid F.X. A library of fluorescent peptides for exploring the substrate specificities of prolyl isomerases Biochemistry 48 2009 10423 10436
45. Garcia-Echeverria C., Kofron J.L., Kuzmic P., Kishore V., and Rich D.H. Continuous fluorimetric direct (uncoupled) assay for peptidyl prolyl cis-trans isomerases J. Am. Chem. Soc. 114 1992 2758 2759
46. Van Duyne G.D., Standaert R.F., Karplus P.A., Schreiber S.L., and Clardy J. Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin J. Mol. Biol. 229 1993 105 124
47. Schmid F.X. Mechanism of folding of ribonuclease A. Slow refolding is a sequential reaction via structural intermediates Biochemistry 22 1983 4690 4696
48. Scholz C., Stoller G., Zarnt T., Fischer G., and Schmid F.X. Cooperation of enzymatic and chaperone functions of trigger factor in the catalysis of protein folding EMBO J. 16 1997 54 58
49. Scholz C., Mücke M., Rape M., Pecht A., Pahl A., Bang H., and Schmid F.X. Recognition of protein substrates by the prolyl isomerase trigger factor is independent of proline residues J. Mol. Biol. 277 1998 723 732
50. Schreiber G., Haran G., and Zhou H.X. Fundamental aspects of protein-protein association kinetics Chem. Rev. 109 2009 839 860
51. Sugase K., Dyson H.J., and Wright P.E. Mechanism of coupled folding and binding of an intrinsically disordered protein Nature 447 2007 1021 1025
52. Nishiyama, M. & Glockshuber, R., The outer membrane usher guarantees the formation of functional pili by selectively catalyzing donor-strand exchange between subunits that are adjacent in the mature pilus. J. Mol. Biol. 396, 1-8.
53. Wright P.E., and Dyson H.J. Linking folding and binding Curr. Opin. Struct. Biol. 19 2009 31 38
54. Maier R., Scholz C., and Schmid F.X. Dynamic association of trigger factor with protein substrates J. Mol. Biol. 314 2001 1181 1190
55. Kiefhaber T., Grunert H.P., Hahn U., and Schmid F.X. Replacement of a cis proline simplifies the mechanism of ribonuclease T1 folding Biochemistry 29 1990 6475 6480
56. Mayr L.M., Odefey C., Schutkowski M., and Schmid F.X. Kinetic analysis of the unfolding and refolding of ribonuclease T1 by a stopped-flow double-mixing technique Biochemistry 35 1996 5550 5561
57. Pace C.N. Determination and analysis of urea and guanidine hydrochloride denaturation curves Methods Enzymol. 131 1986 266 280
58. Santoro M.M., and Bolen D.W. Unfolding free energy changes determined by the linear extrapolation method: 1. Unfolding of phenylmethanesulfonyl a-chymotrypsin using different denaturants Biochemistry 27 1988 8063 8068
59. Mücke M., and Schmid F.X. Enzymatic catalysis of prolyl isomerization in an unfolding protein Biochemistry 31 1992 7848 7854
60. Peterman B.F. Measurement of the dead time of a fluorescence stopped-flow instrument Anal. Biochem. 93 1979 442 444
61. Eftink M.R., Jia Y., Hu D., and Ghiron C.A. Fluorescence studies with tryptophan analogues: excited state interactions involving the side chain amino group J. Phys. Chem. 99 1995 5713 5723