Kurt Wüthrich, the ETH Zürich, and the development of NMR spectroscopy for the investigation of structure, dynamics, and folding of proteins

ChemBioChem

Volumn 4, Issue 2-3, 2003, Pages 135-142

  Schwalbe, Harald ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

History of science; NMR spectroscopy; Nobel prize; Protein folding; Protein structures

Indexed keywords

AMIDE; AMYLASE INHIBITOR; NITROGEN 15; POLYPEPTIDE; PROTEIN; TENDAMISTAT;

ELECTRON SPIN RESONANCE; FOURIER TRANSFORMATION; HISTORY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; SCIENCE; SHORT SURVEY; SPECTROSCOPY; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

EID: 0037416435     PISSN: 14394227     EISSN: None     Source Type: Journal    
DOI: 10.1002/cbic.200390023     Document Type: Short Survey

References (101)

1. General George Patton, quoted from Speeches, 2nd ed. (Ed.: B. MacArthur), Penguin Books, London, 1999.
2. 2+-katalysierten Reaktionen", Experientia 1964, 20, 599-601.
3. K. Wüthrich, R. G. Shulman, J. Peisach, "High resolution proton magnetic resonance spectra of sperm whale cyanometmyoglobin", Proc. Natl. Acad. Sci. USA 1968, 60, 373-380.
4. K. Wüthrich, "Studien der räumlichen Struktur von Proteinmolekülen mit magnetischer Kernresonanzspektroskopie", Chimia 1970, 24, 409-418; the title of this German publication is translated as follows by the Chemical Abstracts Service online: "Three-dimensional structure of protein molecules studied by nuclear magnetic resonance". The article is the written form of a lecture given at the Swiss chemists' association symposium about biopolymers in Bern, 26-28 August, 1970.
5. 13C NMR spectra of two different molecular conformations of a cyclic pentapeptide", FEBS Lett. 1972, 25, 104-108.
6. K. Wüthrich, G. Wagner, "NMR investigations of the dynamics of the aromatic amino acid residues in the basic pancreatic trypsin inhibitor", FEBS Lett. 1975, 50, 265-268.
7. 15N nuclear magnetic resonance of living cells", Nature 1975, 257, 817-818.
8. 1H NMR spectroscopy of biological macromolecules", Biochem. Biophys. Res. Commun. 1977, 78, 99-105;
9. b) K. Nagayama, K. Wüthrich, P. Bachmann, R. R. Ernst, "Two-dimensional NMR spectroscopy: a powerful tool for the investigation of biopolymers in solution", Naturwissenschaften 1977, 64, 581-582.
10. a) R. Richarz, K. Wüthrich, "NOE difference spectroscopy: a novel method for observing individual multiplets in proton NMR spectra of biological macromolecules", J. Magn. Reson. 1978, 30, 147-150;
11. b) S. L. Gordon, K. Wüthrich, "Transient proton-proton Overhauser effects in horse ferrocytochrome c", J. Am. Chem. Soc. 1978, 100, 7094- 7096;
12. 1H Overhauser effects in the presence of spin diffusion", J. Magn. Reson. 1979, 33, 675-680.
13. 1H NMR parameters of the common amino acid residues measured in aqueous solutions of the linear tetrapeptides H-Gly-Gly-X-L-Ala-OH", Biopolymers 1979, 18, 285-297.
14. G. Wagner, K. Wüthrich, "Correlation between the amide proton exchange rates and the denaturation temperatures in globular proteins related to the basic pancreatic trypsin inhibitor", J. Mol. Biol. 1979, 130. 31-37.
15. 1H NMR studies of biological macro-molecules", Biochem. Biophys. Res. Commun. 1979, 90, 305-311.
16. Anil-Kumar, R. R. Ernst, K. Wüthrich, "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. 1980, 95, 1-6.
17. a) K. Wüthrich, G. Wider, G. Wagner, W. Braun, "Sequential resonance assignments as a basis for determination of spatial protein structures by high resolution proton nuclear magnetic resonance", J. Mol. Biol. 1982, 155, 311-319;
18. 1H nuclear magnetic resonance spectra: computation of sterically allowed proton-proton distances and statistical analysis of proton-proton distances in single crystal protein conformations", J. Mol. Biol. 1982, 155, 321-346;
19. 1H nuclear magnetic resonance spectra: basic pancreatic trypsin inhibitor", J. Mol. Biol. 1982, 155, 347-366.
20. 1H spin-spin coupling constants in proteins", Biochem. Biophys. Res. Commun. 1983, 113, 967-974.
21. 1H proximities in solution", Bull. Math. Biol. 1984, 46, 673-698.
22. 3JHNα for identification of helical secondary structure", J. Mol. Biol. 1984, 180, 741-751.
23. a) M. P Williamson, T. F. Havel, K. Wüthrich, "Solution conformation of proteinase inhibitor IIA from bull seminal plasma by 1H nuclear magnetic resonance and distance geometry", J. Mol. Biol. 1985, 182, 295-315;
24. 1H nuclear magnetic resonance", J. Mol. Biol. 1985, 183, 503-507;
25. 1H nuclear magnetic resonance and distance geometry of the solution conformation of the α-amylase inhibitor Tendamistat", J. Mol. Biol. 1986, 189, 377-382.
26. 2H and temperature", Biochemistry 1985, 24, 7396-7407;
27. b) H. Roder, G. Wagner, K. Wüthrich, "Individual amide proton exchange rates in thermally unfolded basic pancreatic trypsin inhibitor", Biochemistry 1985, 24, 7407-7411.
28. H. Roder, K. Wüthrich, "Protein folding kinetics by combined use of rapid mixing techniques and NMR observation of individual amide protons", Proteins 1986, 1, 34-42.
29. a) A. D. Kline, W. Braun, K. Wüthrich, "Determination of the complete three-dimensional structure of the α-amylase inhibitor Tendamistat in aqueous solution by nuclear magnetic resonance and distance geometry", J. Mol. Biol. 1988, 204, 67S-724;
30. b) M. Billeter, A. D. Kline, W. Braun, R. Huber, K. Wüthrich, "Comparison of the high-resolution structures of the α-amylase inhibitor Tendamistat determined by nuclear magnetic resonance in solution and by X-ray diffraction in single crystals", J. Mol. Biol. 1989, 206, 677-687;
31. c) W. Braun, O. Epp, K. Wüthrich, R. Huber, "Solution of the phase problem in the X-ray diffraction method for proteins with the nuclear magnetic resonance solution structure as initial model", J. Mol. Biol. 1989, 206, 669-676.
32. G. Otting, K. Wüthrich, "Studies of protein hydration in aqueous solution by direct NMR observation of individual protein-bound water molecules", J. Am. Chem. Soc. 1989, III, 1871-1875.
33. 2)-double-half-filter", J. Magn. Reson. 1989, 85, 586-594.
34. 1H NMR assignments for the amino-terminal domain of the phage 434 repressor in the ureaunfolded form", Proc. Natl. Acad. Sci. USA 1992, 89, 4397-4401;
35. b) D. Ned, G. Wider, K. Wüthrich, "1H, 15N and 13C NMR assignments of the 434 repressor fragments 1-63 and 44-64 unfolded in 7M urea", FEBS Lett. 1992, 303, 129-135.
36. 2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution", Proc. Natl. Acad. Sci. USA 1997, 94, 12366-12371.
37. a) C. Fernandéz, K. Wüthrich, "Transverse relaxation-optimized NMR spectroscopy with the outer membrane protein OmpX in dihexanoyl phosphatidylcholine micelles", Proc. Natl. Acad. Sci. USA 2001, 98, 2358-2363;
38. b) C. Fernández, C. Hilty, S. Bonjour, K. Pervushin, K. Wüthrich, "Solution NMR studies of the integral membrane proteins OmpX and OmpA from Escherichia coli", FEBS Lett. 2001, 504, 173-178.
39. 2+ Komplexverbindungen in wässeriger Lösung", Helv. Chim. Acta 1965, 48, 779-790.
40. K. Wüthrich, R. E. Connick, "Nuclear magnetic resonance relaxation of oxygen-17 in aqueous solutions of vanadyl perchlorate and the rate of elimination of water molecules from the first coordination sphere", Inorg. Chem. 1967, 6, 583-590.
41. M. Saunders, A. Wishnia, K. G. Kirkwood, "The nuclear magnetic resonance spectrum of ribonuclease", J. Am. Chem. Soc. 1957, 79, 3289-3290.
42. J. C. Kendrew, "Myoglobin and the structure of proteins", Science 1963, 139, 1259-1266.
43. M. F. Perutz, "X-ray analysis of hemoglobin", Science 1963, 140, 863-869.
44. About 20% of the atomic coordinates deposited in the protein data bank have been determined by NMR spectroscopy.
45. J. Jeener, Ampère International Summer School (Basko Polje, Yugoslavia), 1971, unpublished results.
46. W. P. Aue, E. Bartholdi, R. R. Ernst, "Two-dimensional spectroscopy. Application to nuclear magnetic resonance", J. Chem. Phys. 1976, 64, 2229-2246.
47. S. Macura, R. R. Ernst, "Elucidation of cross relaxation in liquids by two-dimensional NMR spectroscopy", Mol. Phys. 1980, 41, 95-117.
48. a) J. Jeener, B. H. Meier, P. Bachmann, R. R. Ernst, "Investigation of exchange processes by two-dimensional NMR spectroscopy", J. Chem. Phys. 1979, 71, 4546-4553;
49. b) B. H. Meier, R. R. Ernst, "Elucidation of chemical exchange networks by two-dimensional NMR spectroscopy: The heptamethylbenzenonium Ion", J. Am. Chem. Soc. 1979, 101, 6441-6442.
50. R. R. Ernst, "Kemresonanz-Fourier-Transformations-Spektroskopie (Nobel-Vortrag)", Angew. Chem. 1992, 104, 817-836; "Nuclear Magnetic Resonance Fourier Transform Spectroscopy (Nobel Lecture)", Angew. Chem. Int. Ed. Engl. 1992, 31, 805-823.
51. R. R. Ernst, "Kemresonanz-Fourier-Transformations-Spektroskopie (Nobel-Vortrag)", Angew. Chem. 1992, 104, 817-836; "Nuclear Magnetic Resonance Fourier Transform Spectroscopy (Nobel Lecture)", Angew. Chem. Int. Ed. Engl. 1992, 31, 805-823.
52. T. F. Havel, I. Kuntz, G. M. Crippen, "Effects of distance constraints on macromolecular conformation. II. Simulation of experimental results and theoretical predictions", Biopolymers 1979, 18, 73-82.
53. R. Kaptein, E. R. P. Zuiderweg, R. M. Scheek, R. Boelens, W. F. A. van Gunsteren, "A protein structure from nuclear magnetic resonance data. Lac repressor headpiece", J. Mol. Biol. 1985, 182, 179-182.
54. 2", Biochemistry 1986, 2S, 5341-5350.
55. J. Pflugrath, E. Wiegand, R. Huber, L. Vertesy, "Crystal structure determination, refinement and molecular model of the α-amylase inhibitor Hoe-467A", J. Mol. Biol. 1986, 189, 377-382.
56. G. Wagner, A. DeMarco, K. Wüthrich, "Dynamics of the aromatic amino acid residues in the globular conformation of the basic pancreatic trypsin inhibitor (BPTI). I. Proton NMR studies", Biophys. Struct. Mech. 1976, 2, 139-158.
57. E. Liepinsh, G. Otting, K. Wüthrich, "NMR observation of individual molecules of hydration water bound to DNA duplexes: direct evidence for a spine of hydration water present in aqueous solution", Nucleic Acids Res. 1992, 20, 6549-6553.
58. a) A. Arseniev, R Schultze, E. Wörgötter, W. Braun, G. Wagner, M. Vasak, J. H. R. Kägi, K. Wüthrich, "Three-dimensional structure of rabbit liver [Cd7] metallothionein-2a in aqueous solution determined by nuclear magnetic resonance", J. Mol. Biol. 1988, 201, 637-657;
59. b) P. Schultze, E. Wörgötter, W. Braun, G. Wagner, M. Vasak, J. H. R. Kägi, K. Wüthrich, "Conformation of [Cd7]-metallothionein-2 from rat liver in aqueous solution determined by nuclear magnetic resonance spectroscopy", J. Mol. Biol. 1988, 203, 251-268.
60. 1H-nuclear-magnetic-resonance assignments", Eur. J. Biochem. 1988, 177, 295-305.
61. H. Widmer, M. Billeter, K. Wüthrich, "Three-dimensional structure of the neurotoxin ATX la from Anemonia sulcata in aqueous solution determined by nuclear magnetic resonance spectroscopy", Proteins 1989, 6, 357-371.
62. a) M. Billeter, Y. Q. Qian, G. Otting, M. Müller, W. J. Gehring, K. Wüthrich, "Determination of the three-dimensional structure of the Antennapedia homeodomain from Drosophila in solution by 1H nuclear magnetic resonance spectroscopy", J. Mol. Biol. 1990, 214, 183-197;
63. b) M. Billeter, Y. Q. Qian, G. Otting, M. Müller, W. J. Gehring, K. Wüthrich, "Determination of the nuclear magnetic resonance solution structure of an Antennapedia homeodomain - DNA complex", J. Mol. Biol. 1993, 234, 1084-1093.
64. a) P. Sodano, K. V. R. Chary, O. Björnberg, A. Holmgren, B. Kren, J. A. Fuchs, K. Wüthrich, "Nuclear magnetic resonance studies of recombinant Escherichia coli glutaredoxin: sequence-specific assignments and secondary structure determination of the oxidized form", Eur. J. Biochem. 1991, 200, 369-377;
65. b) T. Xia, J.H. Bushweller, P. Sodano, M. Billeter, O. Björnberg, A. Holmgren, K. Wüthrich, "NMR structure of oxidized Escherichia coli glutaredoxin: comparison with reduced E. coli glutaredoxin and functionally related proteins", Protein Sci. 1992, 1, 310-321.
66. J. Vendrell, M. Billeter, G. Wider, F. X. Avilés, K. Wüthrich, "The NMR structure of the activation domain isolated from porcine procarboxypeptidase B", EMBO J. 1991, 10, 11-15.
67. G. T. Montelione, K. Wüthrich, A. W. Burgess, E.C. Nice, G. Wagner, D. Gibson, H. A. Scheraga, "Solution structure of murine epidermal growth factor determined by NMR spectroscopy and refined by energy minimization with restraints", Biochemistry 1992, 31, 236-249.
68. T. Szyperski, P. Güntert, S. R. Stone, K. Wüthrich, "Nuclear magnetic resonance solution structure of hirudin(1-51) and comparison with corresponding three-dimensional structures determined using the complete 65-residue hirudin polypeptide chain", J. Mol. Biol. 1992, 228, 1193-1205.
69. K. D. Berndt, P. Güntert, L. P. M. Orbons, K. Wüthrich, "Determination of a high-quality nuclear magnetic resonance solution structure of the bovine pancreatic trypsin inhibitor and comparison with three crystal structures", J. Mol. Biol. 1992, 227, 757-775.
70. D. Neri, M. Billeter, K. Wüthrich, "Determination of the NMR solution structure of the DNA-binding domain 1-69 of the 434 repressor and comparison with the X-ray crystal structure", J. Mol. Biol. 1992, 223, 743-767.
71. K. D. Berndt, P. Güntert, K. Wüthrich, "Nuclear magnetic resonance solution structure of dendrotoxin K from the venom of Dendroaspis polylepis polylepis", J. Mol. Biol. 1993, 234, 735-750.
72. a) L. R. Brown, S. Mronga, R. A. Bradshaw, C. Ortenzi, P. Luporini, K. Wüthrich, "Nuclear magnetic resonance solution structure of the pheromone Er-10 from the ciliated protozoan Euplotes raikovi", J. Mol. Biol. 1993, 231, 800-816;
73. b) S. Mronga, R Luginbühl, L. R. Brown, C. Ortenzi, P. Luporini, R. A. Bradshaw, K. Wüthrich, "The NMR solution structure of the pheromone Er-1 from the ciliated protozoan Euplotes raikovi", Protein Sci. 1994, 3, 1527-1536;
74. c) M. Ottiger, T. Szyperski, L. Luginbühl, C. Ortenzi, P. Luporini, R. A. Bradshaw, K. Wüthrich, "The NMR solution structure of the pheromone Er-2 from the ciliated protozoan Euplotes raikovi", Protein Sci. 1994, 3, 1515-1526;
75. d) P. Luginbühl, J. Wu, O. Zerbe, C. Ortenzi, P. Luporini, K. Wüthrich, "The NMR solution structure of the pheromone Er-11 from the cilitated protozoan Euplotes raikovi" Protein Sci. 1996, 5, 1512-1522;
76. e) R. Zahn, F. Damberger, C. Ortenzi, P. Luporini, K. Wüthrich, "NMR structure of the Euplotes raikovi pheromone Er-23 and identification of its five disulfide bonds", J. Mol. Biol. 2001, 313, 923-931;
77. f) A. Liu, P. Luginbühl, O. Zerbe, C. Ortenzi, P. Luporini, K. Wüthrich, "NMR structure of the pheromone Er-22 from Euplotes raikovi", J. Biomol. NMR 2001, 19, 75-78.
78. W. Antuch, K. D. Berndt, M. A. Chavez, J. Delfin, K. Wüthrich, "The NMR solution structure of a Kunitz-type proteinase inhibitor from the sea anemone Stichodactyla helianthus", Eur. J. Biochem. 1993, 212, 675-684.
79. P. Sevilla-Sierra, G. Otting, K. Wüthrich, "Determination of the nuclear magnetic resonance structure of the DNA-binding domain of the P22 c2 repressor (1 to 76) in solution and comparison with the DNA-binding domain of the 434 repressor", J. Mol. Biol. 1994, 235, 1003-1020.
80. Y.Q. Qian, K. Furukubo-Tokunaga, D. Resendez-Perez, M. Müller, W.J. Gehring, K. Wüthrich, "Nuclear magnetic resonance solution structure of the fushi tarazu homeodomain from Drosophila and comparison with the Antennapedia homoedomain", J. Mol. Biol. 1994, 238, 333-345.
81. J. Johansson, T. Szyperski, T. Curstedt, K. Wüthrich, "The NMR structure of the pulmonary surfactant-associated polypeptide SP-C in an apolar solvent contains a valyl-rich α-helix", Biochemistry 1994, 33, 6015-6023.
82. W. Antuch, P. Güntert, M. Billeter, T. Hawthorne, H. Grossenbacher, K. Wüthrich, "NMR solution structure of the recombinant tick anticoagulant protein (rTAP), a factor XA inhibitor from the tick Ornithodoros moubata", FEBS Lett. 1994, 352, 251-257.
83. a) C. Spitzfaden, W. Braun, G. Wider, H. Widmer, K. Wüthrich, "Determination of the NMR solution structure of the cyclophilin A-cyclosporin A complex", J. Biomol. NMR 1994, 4, 463-482;
84. b) M. Ottiger, O. Zerbe, P. Güntert, K. Wüthrich, "The NMR solution conformation of unligated human cyclophilin A", J. Mol. Biol. 1997, 272, 64-81.
85. R. Riek, S. Hornemann, G. Wider, M. Billeter, R. Glockshuber, K. Wüthrich, "NMR structure of the mouse prion protein domain PrP(121-231)", Nature 1996, 382, 180-182.
86. W. Antuch, P. Güntert, K. Wüthrich, "Ancestral βγ-crystallin percursor structure in a yeast killer toxin", Nat. Struct. Biol. 1996, 3, 662-665.
87. T. Szyperski, M. Pellecchia, D. Wall, C. Georgopoulos, K. Wüthrich, "NMR structure determination of the Escherichia coli DnaJ molecular chaperone: secondary structure and backbone fold of the N-terminal region 2-108 comprising the highly conserved J-domain", Proc. Natl. Acad. Sci. USA 1994, 91, 11343-11347.
88. C. Fernández, T. Szyperski, T. Bruyère, P. Ramage, E. Mösinger, K. Wüthrich, "NMR solution structure of the pathogenesis-related protein P14a", J. Mol. Biol. 1997, 266, 576-593.
89. O. Schott, M. Billeter, B. Leiting, G. Wider, K. Wüthrich, "The NMR solution structure of the non-classical homeodomain from the rat liver LFB1/HNF1 transcription factor", J. Mol. Biol. 1997, 267, 673-683.
90. M. Pellecchia, P. Güntert, R, Glockshuber, K. Wüthrich, "NMR solution structure of the periplasmic chaperone FimC", Nat. Struct. Biol. 1998, 5, 885-890.
91. R. Riek, B. Prêcheur, Y. Wang, E. A. Mackay, G. Wider, R Güntert, A. Liu, J. H. R. Kägi, K. Wüthrich, "NMR structure of the sea urchin (Strongylocentrotus purpuratus) metallothionein MTA", J. Mol. Biol. 1999, 291, 417-428.
92. R. Fattorusso, M. Pellecchia, F. Viti, P. Neri, D. Neri, K. Wüthrich, "NMR structure of the human oncofoetal fibronectin ED-B domain, a specific marker for angiogenesis", Folding Des. 1999, 7, 381-390.
93. F. López Garcia, R. Zahn, R. Riek, K. Wüthrich, "NMR structure of the bovine prion protein", Proc. Natl. Acad. Sci. USA 2000, 97, 8334-8399.
94. L. Calzolai, D. Lysek, P. Güntert, C. von Schroetter, R. Riek, R. Zahn, K. Wüthrich, "NMR structures of three single-residue variants of the human prion protein", Proc. Natl. Acad. Sci. USA 2000, 97, 8340-8345.
95. R. Zahn, A. Liu, T. Lührs, R. Riek, C. von Schroetter, F. López Garcia, M. Billeter, L. Calzolai, G. Wider, K. Wüthrich, "NMR solution structure of the human prion protein", Proc. Natl. Acad. Sci. USA 2000, 97, 145-150.
96. F. Lòpez Garcia, T. Szyperski, J. H. Dyer, T. Choinowski, U. Seedorf, H. Hauser, K. Wüthrich, "NMR Structure of the sterol carrier protein-2: implications for the biological role", J. Mol. Biol. 2000, 295, 595-603.
97. L. Ellgaard, R. Riek, T. Herrmann, P. Güntert, D. Braun, A. Helenius, K. Wüthrich, "NMR structure of the calreticulin P-domain", Proc. Natl. Acad. Sci. USA 2001, 98, 3133-3138.
98. D. Lee, F. F. Damberger, R. Horst, P. Güntert, L. Nikonova, W. S. Leal, K. Wüthrich, "NMR Structure of the Unliganded Bombyx Mori PheromoneBinding Protein at Physiological pH", FEBS Lett. 2002, 531, 314-318.
99. R. H. Griffey, A. G. Redfield, "Proton-detected heteronuclear edited and correlated nuclear magnetic resonance and nuclear Overhauser effect in solution", Q. Rev. Biophys. 1987, 19, 51-82.
100. J. Fiaux, E. B. Bertelsen, A. L. Horwich, K. Wüthrich, "NMR analysis of a 900 K GroEL-GroES complex", Nature 2002, 418, 207-211.
101. Note added in proof: Kurt Wüthrich uses his belt to explain the process of NMR structure determination, as can be seen in the video recording of his lecture given on December 8, 2002, at the Magna Aula, Stockholm University, Sweden; www.nobel.se.