The NMR solution conformation of unligated human cyclophilin A

Journal of Molecular Biology

Volumn 272, Issue 1, 1997, Pages 64-81

  Ottiger, Marcel ^a,b   Zerbe, Oliver ^a   Güntert, Peter ^a   Wüthrich, Kurt ^a  

^a ETH ZURICH   (Switzerland)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Cyclophilin A; Cyclosporin A; Immunophilins; NMR structure; Protein dynamics

Indexed keywords

AMIDE; CALCINEURIN; CELL PROTEIN; CYCLOPHILIN A; CYCLOSPORIN A; NITROGEN 15;

AMINO ACID SEQUENCE; ARTICLE; CHEMICAL STRUCTURE; COMPUTER ANALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG PROTEIN BINDING; ESCHERICHIA COLI; HUMAN; HYDROGEN BOND; LIGAND BINDING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; RELAXATION TIME; STEREOCHEMISTRY; T LYMPHOCYTE; X RAY CRYSTALLOGRAPHY;

ESCHERICHIA COLI;

EID: 0031565727     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.1220     Document Type: Article

References (91)

1. Altschuh D., Braun W., Kallen J., Mikol V., Spitzfaden C., Thierry J. C., Vix O., Walkinshaw M. D., Wüthrich K. Conformational polymorphism of cyclosporin A. Structure. 2:1994;963-972.
2. Anil-Kumar, Ernst R. R., Wüthrich K. A two-dimensional nuclear Overhauser enhancement (2D NOE) experiment for the elucidation of complete proton-proton cross relaxation networks in biological macromolecules. Biochem. Biophys. Res. Commun. 95:1980;1-6.
3. 15β. J. Magn. Reson. 95:1991;636-641.
4. Bartels C., Güntert P., Wüthrich K. IFLAT - a new automatic baseline-correction method for multidimensional NMR spectra with strong solvent signals. J. Magn. Reson. Ser. A. 117:1995a;330-333.
5. Bartels C., Xia T., Billeter M., Güntert P., Wüntert K. The program XEASY for computer-supported NMR spectral analysis of biological macromolecules. J. Biomol. NMR. 6:1995b;1-10.
6. Bax A., Pochapsky S. S. Optimized recording of heteronuclear multidimensional NMR spectra using pulsed field gradients. J. Magn. Reson. 99:1992;638-643.
7. 111311313. J. Magn. Reson. 88:1990;425-431.
8. 3. J. Biomol. NMR. 4:1994;787-797.
9. Billeter M., Schaumann T., Braun W., Wüthrich K. Restrained energy refinement with two different algorithms and force fields of the structure of the α-amylase inhibitor tendamistat determined by NMR in solution. Biopolymers. 29:1990;695-706.
10. Bodenhausen G., Ruben D. J. Natural abundance nitrogen-15 NMR by enhanced heteronuclear spectroscopy. Chem. Phys. Letters. 69:1980;185-189.
11. Borel J. F. Editor ofCiclosporin. 1986;Karger.
12. Borel J. F. Pharmacology of cyclosporin (Sandimmune) IV. Pharmacological propertiesin vivo. Pharmacol. Rev. 41:1989;259-371.
13. Braun W., Kallen J., Mikol V., Walkinshaw M. D., Wüthrich K. Three-dimensional structure and actions of immunosuppressants and their immunophilins. FASEB J. 9:1995;63-72.
14. Braunschweiler L., Ernst R. R. Coherence transfer by isotropic mixing: application to proton correlation spectroscopy. J. Magn. Reson. 53:1983;521-528.
15. NAB. J. Magn. Reson. 93:1991;218-224.
16. 15. Biochemistry. 32:1993;9000-9010.
17. 15. Biochemistry. 33:1994;4093-4100.
18. Clubb R. T., Ferguson S. B., Walsh C. T., Wagner G. Three-dimensional solution structure ofEscherichia coli. Biochemistry. 33:1994;2761-2772.
19. Edison A. S., Westler W. M., Markley J. L. Elucidation of amino acid spin systems in proteins and determination of heteronucler coupling constants by carbon-proton-proton three-dimensional NMR. J. Magn. Reson. 92:1991;434-438.
20. Fesik S. W., Zuiderweg E. R. P. Heteronuclear three-dimensional NMR spectroscopy. A strategy for the simplification of homonuclear two-dimensional NMR spectra. J. Magn. Reson. 78:1988;588-593.
21. 13. Biochemistry. 30:1991;6574-6583.
22. Fischer G., Wittmann-Liebold B., Lang K., Kiefhaber T., Schmid F. X. Cyclophilin and peptidyl-prolylcis-trans. Nature. 337:1989;476-478.
23. 11315Bacillus alcalophilus. J. Biomol. NMR. 5:1995;259-270.
24. Franke E. K., Yuan H. E., Luban J. Specific incorporation of cyclophilin A into HIV-1 virions. Nature. 372:1994;359-362.
25. Gamble T. R., Vajdos F. F., Yoo S., Worthylake D. K., Houseweart M., Sundquist W. I., Hill C. P. Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1capsiol. Cell. 87:1996;1285-1294.
26. 1. J. Am. Chem. Soc. 110:1988;7870-7872.
27. Griffith J. P., Kim J. L., Kim E. E., Sintchak M. D., Thomson J. A., Fitzgibbon M. J., Fleming M. A., Caron P. R., Hsiao K., Navia M. A. X-ray structure of calcineurin inhibited by the immunophilin-immunosuppressant FKBP12-FK506 complex. Cell. 82:1995;507-522.
28. Grzesiek S., Bax A. Correlating backbone amide and side chain resonances in larger proteins by multiple relayed triple resonance NMR. J. Am. Chem. Soc. 114:1992;6291-6293.
29. 1315. J. Biomol. NMR. 3:1993;185-204.
30. Güntert P., Wüthrich K. Improved efficiency of protein structure calculations from NMR data using the program DIANA with redundant dihedral angle constraints. J. Biomol. NMR. 1:1991;447-456.
31. 1. J. Am. Chem. Soc. 111:1989;3997-4004.
32. Güntert P., Braun W., Wüthrich K. Efficient computation of three-dimensional protein structures in solution from nuclear magnetic resonance data using the program DIANA and the supporting programs CALIBA, HABAS and GLOMSA. J. Mol. Biol. 217:1991;517-530.
33. Güntert P., Dötsch V., Wider G., Wüthrich K. Processing of multi-dimensional NMR data with the new software PROSA. J. Biomol. NMR. 2:1992;619-629.
34. Güntert P., Berndt K. D., Wüthrich K. The program ASNO for computer-supported collection of NOE upper distance constraints as input for protein structure determination. J. Biomol. NMR. 3:1993;601-606.
35. Handschumacher R. E., Harding M. W., Rice J., Drugge R. J., Speicher D. W. Cyclophilin: a specific cytosolic binding protein for cyclosporin A. Science. 226:1984;544-547.
36. Holm L., Sander C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233:1993;123-138.
37. 13. J. Magn. Reson. 86:1990;204-209.
38. 113113. J. Biomol. NMR. 1:1991;299-304.
39. Kallen J., Walkinshaw M. D. The X-ray structure of a tetrapeptide bound to the active site of human cyclophilin A. FEBS Letters. 300:1992;286-290.
40. Kallen J., Spitzfaden C., Zurini M. G. M., Wider G., Widmer H., Wüthrich K., Walkinshaw M. D. Structure of human cyclophilin and its binding site for cyclosporin A determined by X-ray crystallography and NMR spectroscopy. Nature. 353:1991;276-279.
41. Kay L. E., Ikura M., Bax A. Proton-proton correlation via carbon-carbon couplings: a three-dimensional NMR approach for the assignment of aliphatic resonances in proteins labeled with carbon-13. J. Am. Chem. Soc. 112:1990;888-889.
42. Ke H. Similarities and differences between human cyclophilin A and other β-barrel structures. J. Mol. Biol. 228:1992;539-550.
43. Ke H., Zydowsky L. D., Liu J., Walsh C. T. Crystal structure of recombinant human T-cell cyclophilin A. at 2.5 Å resolution. Proc. Natl Acad. Sci. USA. 88:1991;9483-9487.
44. Ke H., Mayrose D., Cao W. Crystal structure of cyclophilin A complexed with substrate Ala-Pro suggests a solvent-assisted mechanism ofcis-trans. Proc. Natl Acad. Sci. USA. 90:1993a;3324-3328.
45. Ke H., Zhao Y., Luo F., Weissman I., Friedman J. Crystal structure of murine cyclophilin C complexed with immunosuppressive drug cyclosporin A. Proc. Natl Acad. Sci. USA. 90:1993b;11850-11854.
46. Ke H., Mayrose D., Belshaw P. J., Alberg D. G., Schreiber S. L., Chang Z. Y., Etzkorn F. A., Ho S., Walsh C. T. Crystal structures of cyclophilin A complexed with cyclosporin A and N-methyl-4-[(E)-2-butenyl]-4,4-dimethylthreonine cyclosporin A. Structure. 2:1994;33-44.
47. Kissinger C. R., Parge H. E., Knighton D. R., Lewis C. T., Pelletier L. A., Tempzyk A., Kalish V. J., Tucker K. D., Showalter R. E., Moomaw E. W., Gastinel L. N., Habuka N., Chen X., Maldonado F., Baker J. E., Bacquet R., Villafranca J. E. Crystal structures of human calcineurin and the human FKBP12-FK506-calcineurin complex. Nature. 378:1995;641-644.
48. Konno M., Ito M., Hayano T., Takahashi N. The substrate-binding site inEscherichia colicistrans. J. Mol. Biol. 256:1996;897-908.
49. Koradi R., Billeter M., Wüthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14:1996;52-55.
50. Levitt M. Protein folding by restrained energy minimization and molecular dynamics. J. Mol. Biol. 170:1983;723-764.
51. Lima C. D., Wang J. C., Mondragón A. Three-dimensional structure of the 67K N-terminal fragment ofE. coli. Nature. 367:1994;138-146.
52. Loosli H. R., Kessler H., Oschkinat H., Weber H. P., Petcher T. J., Widmer A. The conformation of cyclosporin A in the crystal and in solution. Helv. Chim. Acta. 68:1985;682-704.
53. Luban J., Bossolt K. L., Franke E. K., Kalpana G. V., Goff S. P. Human immunodeficiency virus type 1 Gag protein binds to cyclophilins A and B. Cell. 73:1993;1067-1078.
54. Luginbühl P., Güntert P., Billeter M., Wüthrich K. The new program OPAL for molecular dynamics simulations and energy refinements of biological macromolecules. J. Biomol. NMR. 8:1996;136-146.
55. Madsen J. C., Sørensen O. W. Multidimensional NMR experiments with improved resolution. J. Magn. Reson. 100:1992;431-436.
56. Marion D., Ikura M., Tschudin R., Bax A. Rapid recording of 2D NMR spectra without phase cycling: application to the study of hydrogen exchange in proteins. J. Magn. Reson. 85:1989;393-399.
57. 2. J. Magn. Reson. 85:1989;608-613.
58. Mikol V., Kallen J., Pflügl G., Walkinshaw M. D. X-ray structure of a monomeric cyclophilin A-cyclosporin A crystal complex at 2.1 Å resolution. J. Mol. Biol. 234:1993;1119-1130.
59. 1. Protein Eng. 7:1994a;597-603.
60. Mikol V., Kallen J., Walkinshaw M. D. X-ray structure of a cyclophilin B/cyclosporin complex: comparison with cyclophilin A and delineation of its calcineurin-binding domain. Proc. Natl Acad. Sci. USA. 91:1994b;5183-5186.
61. Mikol V., Papageorgiou C., Borer X. The role of water molecules in the structure-based design of (5-hydroxynorvaline)-2-cyclosporin: synthesis, biological activity, and crystallographic analysis with cyclophilin A. J. Med. Chem. 38:1995;3361-3367.
62. 13. Biochemistry. 28:1989;7510-7516.
63. 11. Quart. Rev. Biophys. 23:1990;39-96.
64. Papageorgiou C., Florineth A., Mikol V. Improved binding affinity for cyclophilin A by a cyclosporin derivative singly modified at its effector domain. J. Med. Chem. 37:1994;3674-3676.
65. Peng J. W., Wagner G. Investigation of protein motionsvia. Methods Enzymol. 239:1994;563-596.
66. Perkins S. J., Wüthrich K. Ring current effects in the conformation-dependent NMR chemical shifts of aliphatic proteins in the basic pancreatic trypsin inhibitor. Biochim. Biophys. Acta. 576:1979;409-423.
67. Pflügl G., Kallen J., Schirmer T., Jansonius J. N., Zurini M. G. M., Walkinshaw M. D. X-ray structure of a decameric cyclophilin-cyclosporin crystal complex. Nature. 361:1993;91-94.
68. Pflügl G., Kallen J., Jansonius J. N., Walkinshaw M. D. The molecular replacement solution and X-ray refinement to 2.8 Å of a decameric complex of human cyclophilin A with the immunosuppressive drug cyclosporin A. J. Mol. Biol. 244:1994;385-409.
69. Sambrook J., Fritsch E. F., Maniatis T. Molecular Cloning: A Laboratory Manual. 1989;Cold Spring Harbor Laboratory Press, Plainview.
70. Schreiber S. L. Chemistry and biology of the immunophilins and their immunosuppressant ligands. Science. 251:1991;283-287.
71. 113. FEBS Letters. 249:1989;113-118.
72. Spitzfaden C., Weber H. P., Braun W., Kallen J., Wider G., Widmer H., Walkinshaw M. D., Wüthrich K. Cyclosporin A-cyclophilin complex formation. A model based on X-ray and NMR data. FEBS Letters. 300:1992;291-300.
73. Spitzfaden C., Braun W., Wider G., Widmer H., Wüthrich K. Determination of the NMR solution structure of the cyclophilin-cyclosporin A complex. J. Biomol. NMR. 4:1994;463-482.
74. Szyperski T., Güntert P., Otting G., Wüthrich K. Determination of scalar coupling constants by inverse Fourier transformation of in-phase multiples. J. Magn. Reson. 99:1992;552-560.
75. 15. J. Biomol. NMR. 3:1993;151-164.
76. Thali M., Bukovsky A., Kondo E., Rosenwirth B., Walsh C. T., Sodroski J., Göttlinger H. G. Functional association of cyclopholin A with HIV-1 virions. Nature. 372:1994;363-365.
77. Thériault Y., Logan T. M., Meadows R., Yu L., Olejniczak E. T., Holzman T. F., Simmer R. L., Fesik S. W. Solution structure of the cyclosporin A/cyclophilin complex by NMR. Nature. 361:1993;88-91.
78. 1313. J. Magn. Reson. 98:1992;428-435.
79. Weber C., Wider G., von Freyberg B., Traber R., Braun W., Widmer H., Wüthrich K. The NMR structure of cyclosporin A bound to cyclophilin in aqueous solution. Biochemistry. 30:1991;6563-6574.
80. Weiner S. J., Kollman P. A., Nguyen D. T., Case D. A. An all atom force field for simulations of proteins and nucleic acids. J. Comput. Chem. 7:1986;230-252.
81. Wider G., Wüthrich K. A simple experimental scheme using pulsed field gradients for coherence-pathway rejection and solvent suppression in phase-sensitive heteronuclear correlation spectra. J. Magn. Reson. Ser. B. 102:1993;239-241.
82. Wüthrich K. NMR of Proteins and Nucleic Acids. 1986;Wiley, New York.
83. Wüthrich K., Billeter M., Braun W. Pseudo-structures for the 20 common amino acids for use in studies of protein conformations by measurements of intramolecular proton-proton distance constraints with nuclear magnetic resonance. J. Mol. Biol. 169:1983;949-961.
84. Wüthrich K., Billeter M., Braun W. Polypeptide secondary structure determination by nuclear magnetic resonance observation of short proton-proton distances. J. Mol. Biol. 180:1984;715-740.
85. Wüthrich K., Spitzfaden C., Memmert K., Widmer H., Wider G. Protein secondary structure determination by NMR: application with recombinant human cyclophilin. FEBS Letters. 285:1991a;237-247.
86. Wüthrich K., von Freyberg B., Weber C., Wider G., Traber R., Widmer H., Braun W. Receptor-induced conformation change of the immunosuppressant cyclosporin A. Science. 254:1991b;953-954.
87. 13β1δ/ε13via. J. Am. Chem. Soc. 115:1993;11054-11055.
88. 113113. J. Biomol. NMR. 7:1996;99-106.
89. Zhao Y., Ke H. Crystal structure implies that cyclophilin predominantly catalyzes thetranscis. Biochemistry. 35:1996a;7356-7361.
90. Zhao Y., Ke H. Mechanistic implication of crystal structures of the cyclophilin-dipeptide complexes. Biochemistry. 35:1996b;7362-7368.
91. Zhao Y., Chen Y., Schutkowski M., Fischer G., Ke H. Cyclophilin A complexed with a fragment of HIV-1 gag protein: insights into HIV-1 infectious activity. Structure. 5:1997;139-146.