Structural and Functional Studies of FkpA from Escherichia coli, a cis/trans Peptidyl-prolyl Isomerase with Chaperone Activity

Journal of Molecular Biology

Volumn 335, Issue 2, 2004, Pages 595-608

  Saul, F A ^a   Arie J P ^a   Vulliez le Normand, B ^a   Kahn, R ^b   Betton, J M ^a   Bentley, G A ^a  

^a INSTITUT PASTEUR   (France)

^b INSTITUT DE BIOLOGIE STRUCTURALE   (France)

Author keywords

Chaperone; Crystal structure; FK506 complex; FKBP family; Peptidyl prolyl isomerase

Indexed keywords

BACTERIAL PROTEIN; CHAPERONE; CYCLOPHILIN; LIGAND; PROTEIN FKPA; TACROLIMUS; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CIS TRANS ISOMERISM; CONTROLLED STUDY; CRYSTAL STRUCTURE; DELETION MUTANT; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE;

ESCHERICHIA COLI;

EID: 0346366809     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2003.10.056     Document Type: Article

References (51)

1. Anfinsen C.B. Principles that govern the folding of protein chains. Science. 181:1973;223-230.
2. Dobson C.M., Karplus M. The fundamentals of protein folding: bringing together theory and experiment. Curr. Opin. Struct. Biol. 9:1999;92-101.
3. Schienne C., Fischer G. Enzymes that catalyse the restructuring of proteins. Curr. Opin. Struct. Biol. 10:2000;40-45.
4. Feldman D.E., Frydman J. Protein folding in vivo: the importance of molecular chaperones. Curr. Opin. Struct. Biol. 10:2000;26-33.
5. Hartl F.U. Hayer-Hartl molecular chaperones in the cytosol: from nascent chain to folded protein. Science. 295:2002;1852-1858.
6. Missiakas D., Raina S. Protein folding in the bacterial periplasm. J. Bacteriol. 179:1997;2465-2471.
7. Danese P.N., Silhavy T.J. Targeting and assembly of periplasmic and outer-membrane proteins in Escherichia coli. Annu. Rev. Genet. 32:1998;59-94.
8. E and Cpx regulatory pathways: overlapping but distinct envelope stress responses. Curr. Opin. Microbiol. 2:1999;159-165.
9. Horne S.M., Young K.D. Escherichia coli and other species of the Enterobacteriacae encode a protein similar to the family of Mip-like FK506-binding proteins. Arch. Microbiol. 163:1995;357-365.
10. Missiakas D., Betton J.-M., Raina S. New components of protein folding in extracytoplasmic compartments of Escherichia coli SurA, FkpA Skp/OmpH. Mol. Microbiol. 21:1996;871-884.
11. Arié J.-P., Sassoon N., Betton J.-M. Chaperone function of FkpA, a heat shock prolyl isomerase in the periplasm of Escherichia coli. Mol. Microbiol. 39:2001;199-210.
12. Ramm K., Plückthun A. The periplasmic Escherichia coli peptidylprolyl cis,trans-isomerase FkpA. J. Biol. Chem. 275:2000;17106-17113.
13. Rosen M.K., Standaert R.F., Galat A., Nakatsuka M., Schreiber S.L. Inhibition of FKBP rotamase activity by immunosuppressant FK506: twisted amide surrogate. Science. 248:1990;863-866.
14. Saul F.A., Mourez M., Vulliez-Le Normand B., Sassoon N., Bentley G.A., Betton J.-M. Crystal structure of a defective folding protein. Protein Sci. 12:2003;577-585.
15. Ramm K., Plückthun A. High enzymatic activity and chaperone function are mechanistically related features of dimeric E. coli peptidyl-prolyl-isomerase FkpA. J. Mol. Biol. 310:2001;485-498.
16. Van Duyne G.D., Standaert R.F., Karplus P.A., Schreiber S.L., Clardy J. Atomic structure of FKBP-FK506, an immunophilin-immunosuppressant complex. Science. 252:1991;839-842.
17. Van Duyne G.D., Standaert R.F., Karplus P.A., Scheiber S.L., Clardy J. Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J. Mol. Biol. 229:1993;105-124.
18. Wooton J.C., Federhen S. Analysis of compositionally biased regions in sequence databases. Doolittle R.F. Computer Methods for Macromolecular Sequence Analysis, Methods in Enzymology. Computer Methods for Macromolecular Sequence Analysis, Methods in Enzymology. vol. 266:1996;554-571 Academic Press Ltd. London.
19. Wilson K.P., Yamashita M.M., Sintchak M.D., Rotstein S.H., Murcko M.A., Boger J., et al. Comparative X-ray structures of the major binding protein for the Immunosuppressant FK506 (tacrolimus) in unliganded form and in complex with FK506 and rapamycin. Acta Crystallog. sect. D. 51:1995;511-521.
20. Kay J.E. Structure-function relationships in the FK506-binding protein (FKBP) family of peptidylprolyl cis-trans isomerases. Biochem. J. 314:1996;361-385.
21. Taga T., Tanaka H., Goto T., Tada S. Structure of a macrolide antibiotic. Acta Crystallog. sect. C. 43:1987;751-753.
22. Petros A.M., Luly J.R., Liang H., Fesik S.W. Conformation of an FK506 analog in aqueous solution is similar to the FKBP-bound conformation of FK506. J. Am. Chem. Soc. 115:1993;9920-9924.
23. Connelly P.R., Aldape R.A., Bruzzese F.J., Chambers P., Fitzgibbon M.J., Fleming M.A., et al. Enthalpy of hydrogen bond formation in a protein-ligand binding reaction. Proc. Natl Acad. Sci. USA. 91:1994;1964-1968.
24. 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. 273:1998;8897-8902.
25. Buchner J., Grallert H., Jakob U. Analysis of chaperone function using citrate synthase as non-native substrate protein. Lorimer G.H., Baldwin T.O. Molecular Chaperones, Methods in Enzymology. Molecular Chaperones, Methods in Enzymology. vol. 290:1998;323-338 Academic Press Ltd. London.
26. Fischer G., Bang H., Ludwig B., Mann K., Hacker J. Mip protein of Legionella pneumophila exhibits peptidyl-prolyl-cis/trans isomerase (PPIase) activity. Mol. Microbiol. 6:1992;175-1383.
27. Riboldi-Tunnicliffe A., Konig B., Jessen S., Weiss M.S., Rahfeld J., Hacker J., et al. Crystal structure of Mip, a prolylisomerase from Legionella pneumophila. Nature Struct. Biol. 8:2001;779-783.
28. BarbosaPereira P.J., Vega M.C., Gonzalez-Rey E., Fernandez-Carazo R., Macedo-Ribeiro S., Gomis-Rüth F.X., et al. Trypanosoma cruzi macrophage infectivity potentiator has a rotamase core and a highly exposed α-helix. EMBO Rep. 3:2002;88-94.
29. Moro A., Ruiz-Cabello F., Fernandez-Cano A., Stock R.P., Gonzalez A. Secretion by Trypanosoma cruzi of a peptidyl-prolyl cis-trans isomerase involved in cell infection. EMBO J. 14:1995;2483-2490.
30. Zarnt T., Tradler T., Stoller G., Scholz C., Schmid F.X., Fischer G. Modular structure of the trigger factor required for high activity in protein folding. J. Mol. Biol. 271:1997;827-837.
31. Scholz C., Stoller G., Zarnt T., Fischer G., Schmid F.X. Cooperation of enzymatic and chaperone functions of trigger factor in the catalysis of protein folding. EMBO J. 16:1997;54-58.
32. Pirkl F., Fischer E., Modrow S., Buchner J. Localization of the chaperone domain of FKBP52. J. Biol. Chem. 276:2001;37034-37041.
33. Furutani M., Ideno A., Iida T., Maruyama T. FK506 binding protein from a thermophilic archaeon, Methanococcus thermolithotropicus, has a chaperone-like activity in vitro. Biochemistry. 39:2000;453-462.
34. Suzuki R., Nagata K., Yumoto F., Kawakami M., Nemoto N., Furutani M., et al. Three-dimensional structure of an archaeal FKBP with a dual function of peptidyl prolyl cis-trans isomerase and chaperone-like activities. J. Mol. Biol. 328:2003;1149-1160.
35. Chen J., Song J., Zhang S., Wang Y., Cui D., Wang C. Chaperone activity of DsbC. J. Biol. Chem. 274:1999;19601-19605.
36. McCarthy A.A., Haebel P.W., Törrönen A., Rybin V., Baker E.N., Metcalf P. Crystal structure of the protein disulfide bond isomerase, DsbC, from Escherichia coli. Nature Struct. Biol. 7:2000;196-199.
37. Miller J.H. A Short Course in Bacterial Genetics. 1992;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
38. Betton J.-M., Boscus D., Missiakas D., Raina S., Hofnung M. Probing the structural role of an αβ loop of maltose-binding protein by mutagenesis: heat-shock induction by loop variants of the maltose-binding protein that form periplasmic inclusion bodies. J. Mol. Biol. 262:1996;140-150.
39. Otwinowski Z., Minor M. Processing X-ray diffraction data collected in oscillation mode. Carter C.W., Sweet R.M. Macromolecular Crystallography: Part A Methods in Enzymology. Macromolecular Crystallography: Part A Methods in Enzymology. vol. 276:1997;307-326 Academic Press Ltd. London.
40. The CCP4 Suite: programs for protein crystallography. Acta Crystallog. sect. D. 50:1994;760-763.
41. Navaza J. AMoRe: an automated package for molecular replacement. Acta Crystallog. sect. A. 50:1994;157-163.
42. Jones T.A., Zou J.-Y., Cowan S.W. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119.
43. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of molecular structures by the maximum likelihood method. Acta Crystallog. sect. D. D53:1997;240-255.
44. Winn M.D., Isupov M.N., Murshudov G.N. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallog. sect. D. 57:2001;122-133.
45. Thompson J.D., Higgins D.G., Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22:1994;4673-4680.
46. Kraulis P. MOLSCRIPT - a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
47. Merrit E., Bacon D. Raster3D: photorealistic molecular graphics. Carter C.W., Sweet R.M. Macromolecular Crystallography Methods in Enzymology. Macromolecular Crystallography Methods in Enzymology. vol. 277:1997;505-524 Academic Press Ltd. London.
48. Esnout R.M. Further additions to MolScript version 1.4, including reading and contouring of electron density maps. Acta Crystallog. sect. D. 55:1999;938-940.
49. Nicholls A., Sharp K.A., Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins: Struct. Funct. Genet. 11:1991;281-296.
50. Diederichs K., Karplus P.A. Improved R-factors for diffraction data analysis in macromolecular crystallography. Nature Struct. Biol. 4:1997;269-275.
51. Kabsch W., Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers. 22:1983;2577-2637.