Solution structure of the superactive monomeric des-[Phe(B25)] human insulin mutant: Elucidation of the structural basis for the monomerization of des-[Phe(B25)] insulin and the dimerization of native insulin

Journal of Molecular Biology

Volumn 257, Issue 3, 1996, Pages 684-699

  Jørgensen, Anne Marie M ^a   Olsen, Helle B ^a,b   Balschmidt, Per ^b   Led, Jens J ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b NOVO NORDISK A S   (Denmark)

Author keywords

Insulin; Monomer; Self association; Solution structure; Structure function

Indexed keywords

DISULFIDE; HUMAN INSULIN; MONOMER; MUTANT PROTEIN;

ARTICLE; CONFORMATIONAL TRANSITION; DIMERIZATION; GEOMETRY; HUMAN; HYDROGEN BOND; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

EID: 0029986510     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0194     Document Type: Article

References (77)

1. Adams, M. J., Blundell, T. L., Dodson, E. J., Dodson, G. G., Vijayan, M., Baker, E. N., Harding, M. M., Hodgkin, D. M. C., Rimmer, B. & Sheat, S. (1969). Structure of rhombohedral 2 zinc insulin crystal. Nature, 224, 491-495.
2. Baker, E. N., Blundell, T. L., Cutfield, J. F., Cutfield, S. M., Dodson, E. J., Dodson, G. G., Hodgkin, D. M. C., Hubbard, R. E., Isaacs, N. W., Reynolds, C. D., Sakabe, K., Sakabe, N. & Vijayan, N. M. (1988). The structure of 2Zn pig insulin crystals at 1.5 Å resolution. Phil. Trans. Roy. Soc. ser. B, 319, 369-456.
3. Balschmidt, P. & Brange, J. J. V. (1992). Fast acting human insulin analogues with a single amino acid deletion in the B-chain. Diabetologia, 35 I-VI, A4 (supplement 1).
4. Bax, A. & Davis, D. G. (1985). MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy. J. Magn. Reson. 65, 355-360.
5. Bax, A. & Drobny G. P. (1985). Optimization of two-dimensional homonuclear relayed coherence transfer NMR spectrocscopy. J. Magn. Reson. 61, 306-322.
6. Bi, R. C., Dauter, A., Dodson, E. J., Dodson, G. G., Giordano, F. & Reynolds, C. D. (1984). Insulin's structure as a modified and monomeric molecule. Biopolymers, 23, 391-395.
7. Blundell, T. L., Cutfield, J. F., Cutfield, S. M., Dodson, E. J., Dodson, G. G., Hodgkin, D. M. C., Mercola, D. A. & Vijayan, M. (1971). Atomic positions in rhombohedral 2-zinc insulin crystals. Nature, 231, 506-511.
8. Blundell, T. L., Dodson, G. G., Hodgkin, D. M. C. & Mercola, D. A. (1972). Insulin: the structure in the crystal and its reflection in chemistry and biology Advan. Protein Chem. 26, 279-402.
9. Bodenhausen, G. & Ruben, D. J. (1980). Natural abundance nitrogen-15 NMR by enhanced heteronuclear spectroscopy Chem. Phys. Letters, 69, 185-189.
10. Bodenhausen, G., Void, R. L. & Void, R. R. (1980). Multiple quantum spin-echo spectroscopy. J. Magn. Reson. 37, 93-106.
11. Brange, J., Ribel, U., Hansen, J. F., Dodson, G. G., Hansen, M. T., Havelund, S., Melberg, S. G., Norris, F., Norris, K., Snel, L., Sørensen, A. R. & Voigt, H. O. (1988). Monomeric insulins obtained by protein engineering and their medical implications. Nature, 333, 679-682.
12. Brange, J., Dodson, G. G. & Xiao, B. (1991). Designing insulin for diabetes therapy by protein engineering. Curr. Opin. Struct. Biol. 1, 934-940.
13. Braunschweiler, L. & Ernst, R. R. (1983). Coherence transfer by isotropic mixing: application to proton correlation spectroscopy. J. Magn. Reson. 53, 521-528.
14. Brems, D. N., Alter, L. A., Beckage, M. J., Chance, R. E., DiMarchi, R. D., Green, L. K., Harlan, B. L., Pekar, A. H., Shields, J. E. & Frank, B. H. (1992). Altering the association properties of insulin by amino acid replacement. Protein Eng. 5, 527-533.
15. Brooks, B., Bruccoleri, R., Olafson, B., States, D., Swaminathan, S. & Karplus, M. (1983). CHARMM: a program for macromolecular energy minimization, and molecular dynamics calculations. J. Comp. Chem. 4, 187-217.
16. Brünger, A. T. (1992). X-PLOR version 3.1. A system for crystallography and NMR. X-PLOR Manual, Yale University New Haven, CT.
17. Chothia, C. & Janin, J. (1975). Principles of protein-protein recognition. Nature, 256, 705-708.
18. Cutfield, J., Cutfield, S., Dodson, E., Dodson, G., Hodgkin, D. & Reynolds, C. (1981). Evidence concerning insulin activity from the structure of a crosslinked derivative. Hoppe-Seyler's Z. Physiol. Chem. 362, 755-761.
19. de Dios, A. C., Pearson, J. G. & Oldfield, E. (1993). Secondary and tertiary structural effects on protein NMR chemical shifts: an ab initio approach. Science, 260, 1491-1496.
20. Derewenda, U. & Dodson, G. G. (1993). The structure and sequence of insulin. In Molecular Structures in Biology (Diamond, R., Koetzle, T. F., Prout, K. & Richardson, J. S., eds), pp. 260-277, Oxford University Press, Oxford.
21. Derewenda, U., Derewenda, Z., Dodson, E. J., Dodson, G. G., Reynolds, C. D., Smith, G. D., Sparks, C. & Swenson, D. (1989). Phenol stabilizes more helix in a new symmetrical zinc insulin hexamer. Nature, 338, 594-596.
22. Derewenda, U., Derewenda, Z., Dodson, E. J., Dodson, G. G., Bing, X. G. & Markussen, J. (1991). X-ray analysis of the single chain B29-A1 peptide-linked insulin molecule. J. Mol. Biol. 220, 425-433.
23. Dodson, E. J., Dodson, G. G., Hubbard, R. E. Reynolds, C. D. (1983). Insulin's structural behavior and its relation to activity Biopolymers, 22, 281-291.
24. Driscoll, P. C., Clore, M. G., Beress, L. & Gronenborn, A. M. (1989). A proton nuclear magnetic resonance study of the antihypertensive and antiviral protein BDS-I from the sea anemone Anemonia sulcata: sequential and stereospecific resonance assignment and secondary structure. Biochemistry, 28, 2178-2187.
25. Drobny G., Pines, A., Sinton, S., Weitekamp, D. P. & Wemmer, D. (1979). Fourier transform multiple quantum nuclear magnetic resonance. Faraday Div. Chem. Soc. Symp. 13, 49-55.
26. Eich, G., Bodenhausen, G. & Ernst, R. R. (1982). Exploring nuclear spin systems by relayed magnetization transfer. J. Am. Chem. Soc. 104, 3731-3732.
27. Fischer, W. H., Saunders, D., Brandenburg, D., Wollmer, A. & Zahn, H. (1985). A shortened insulin with full in vitro potency Biol. Chem. Hoppe-Seyler, 366, 521-525.
28. Goldman, J. & Carpenter, F. H. (1974). Zinc binding, circular dichroism, and equilibrium sedimentation studies on insulin (bovine) and several of its derivatives. Biochemistry, 13, 4566-4574.
29. Havel, T. F. (1986). DISGEO, Quantum Chemistry Program Exchange no. 507, Indiana University, Bloomington, IN.
30. 1H proximities in solution. Bull. Math. Biol. 46, 673-698.
31. Howarth, O. W. & Lilley D. M. J. (1978). Carbon-13-NMR of peptides and proteins. Prog. NMR Spectrosc. 12, 1-40.
32. 1H NMR assignment of a des-pentapeptide analogue and comparison with crystal structure. Biochemistry, 29, 10545-10555.
33. Hua, Q. & Weiss, M. A. (1991). Comparative 2D NMR studies of human insulin and des-pentapeptide insulin: sequential resonance assignment and implications for protein dynamics and receptor recognition. Biochemistry, 30, 5505-5515.
34. Hua, Q. X., Shoelson, S. E., Kochoyan, M. & Weiss, M. A. (1991). Receptor binding redefined by a structural switch in a mutant human insulin. Nature, 354, 238-241.
35. Hua, Q., Jia, W., Frank, B. H. & Weiss, M. A. (1993). Comparison of the dynamics of an engineered insulin monomer and dimer by acid-quenched amide proton exchange. Non-local stabilization of interchain hydrogen bonds by dimerization. J. Mol. Biol. 230, 387-394
36. Jeffrey, P. D., Milthorpe, B. K. & Nichol, L. W. (1976). Polymerization pattern of insulin at pH 7.0. Biochemistry, 15, 4660-4665.
37. Jeener, J., Meier, B. H., Bachmann, P & Ernst, R. R. (1979). Investigation of exchange processes by two-dimensional NMR spectroscopy. J. Chem. Phys. 71, 4546-4553.
38. Jørgensen, A. M. M., Kristensen, S. M., Led, J. J. & Balschmidt, P (1992). Three-dimensional solution structure of an insulin dimer. A study of the B9(Asp) mutant of human insulin using nuclear magnetic resonance, distance geometry and restrained molecular dynamics. J. Mol. Biol. 227, 1146-1163.
39. Kessler, H., Schmieder, P. & Bermel, W. (1990). Complete assignment of noncarbonylic carbon-13 resonances of tendamistat. Biopolymers, 30, 465-475.
40. 1H NMR assignments for human insulin. Biochemistry, 29, 2906-2913.
41. 1H-NMR study of des-(B26-B30)-insulin in combination with distance geometry and restrained molecular dynamics. Eur. J. Biochem. 202, 447-458.
42. Kristensen, S. M. & Led, J. J. (1995). A carbon-13 NMR study of the Asp(B9) mutant of human insulin: sequence-specific carbon-13 assignments and structural information. Magn. Reson. Chem. 33, 461-470.
43. Kristensen, S. M., Jørgensen, A. M. M., Led, J. J., Balschmidt, P. & Hansen, F. B. (1991). Proton nuclear magnetic resonance study of the B9(Asp) mutant of human insulin. Sequential assignment and secondary structure. J. Mol. Biol. 218, 221-231.
44. Led, J. J. & Gesmar H. (1991). Linear prediction enhancement of 2D heteronuclear correlated spectra of proteins. J. Biomol. NMR, 1, 237-246.
45. Ludvigsen, S., Roy M., Tøgersen, H. & Kaarsholm, N. C. (1994). High-resolution structure of an engineered biologically potent insulin monomer, B16Tyr → His, as determined by nuclear magnetic resonance spectroscopy Biochemistry, 33, 7998-8006.
46. Macura, S., Huang, Y., Suter, D. & Ernst, R. R. (1981). Two-dimensional chemical exchange and cross-relaxation spectroscopy of coupled nuclear spins. J. Magn. Reson. 43, 259-281.
47. Marion, D. & Bax, A. (1988). Baseline distortion in real-Fourier-transform NMR spectra. J. Magn. Reson. 79, 352-356.
48. Marion, D. & Bax, A. (1989). Baseline correction of 2D FT NMR spectra using a simple linear prediction extrapolation of the time-domain data. J. Magn. Reson. 83, 205-211.
49. 1H spin-spin coupling constants in proteins. Biochem. Biophys. Res. Commun. 113, 967-974.
50. Mark, A. E. & Jeffrey, P. D. (1990). The self-association of zinc-free bovine insulin. Four model patterns and their significance. Biol. Chem. Hoppe-Seyler, 371, 1165-1174.
51. Mark, A. E., Nichol, L. W. & Jeffrey P. D. (1987). The self-association of zinc-free bovine insulin. A single model based on interactions in the crystal that describes the association pattern in solution at pH 2, 7 and 10. Biophys. Chem. 27, 103-117.
52. Milthorpe, B. K., Nichol, L. W. & Jeffrey, P. D. (1977). The polymerization pattern of zinc (ii) insulin at pH 7.0. Biochim. Biophys. Acta, 495, 195-202.
53. Mirmira, R. G. & Tager, H. S. (1989). Role of the henylalanine B24 side-chain in directing insulin interaction with its receptor. J. Biol. Chem. 264, 6349-6354.
54. Mirmira, R. G. & Tager, H. S. (1991). Disposition of the phenylalanine B25 side-chain during insulin-receptor and insulin-insulin interactions. Biochemistry, 30, 8222-8229.
55. 1H NMR spectra. J. Am. Chem. Soc. 116, 747-749.
56. Nakagawa, S. H. & Tager, S. (1986). Role of the phenylalanine B25 side-chain in directing insulin interaction with its receptor. J. Biol. Chem. 261, 7332-7341.
57. Nakagawa, S. H. & Tager, H. S. (1987). Role of the COOH-terminal B-chain domain in insulin-receptor interactions. J. Biol. Chem. 262, 12054-12058.
58. Nanjo, K., Sanke, T., Miyano, M., Okai, K., Sowa, R., Kondo, M., Nishimura, S., Iwo, K., Miyamura, K., Given, B. D., Chan, S. J., Tager, H. S., Steiner, D. F. & Rubinstein, A. H. (1986). Diabetes due to secretion of a structurally abnormal insulin (insulin Wakajama). J. Clin. Invest. 77, 514-519.
59. Nilges, M., Clore, G. M. & Gronenborn, A. M. (1988). Determination of three-dimensional structures of proteins from interproton distance data by hybrid distance geometry-dynamical simulated annealing calculations. FEBS Letters, 229, 317-324.
60. 15N spectroscopy. J. Magn. Reson. 87, 488-501.
61. 1H NMR spectrum. J. Am. Chem. Soc. 115, 1456-1460.
62. Plateau, P., Dumas, C. & Guéron, M. (1983). Solvent-peak-suppressed NMR: correction of baseline distortions and use of strong-pulse exitation. J. Magn. Reson. 54, 46-53.
63. Pocker, Y. & Biswas, S. B. (1981). Self-association of insulin and the role of hydrophobic bonding: a thermodynamic model of insulin dimerization. Biochemistry, 20, 4354-4361.
64. Rance, M. (1987). Improved techniques for homonuclear rotating-frame and isotropic mixing experiments. J. Magn. Reson. 74, 557-564.
65. Rance, M., Sørensen, O. W., Bodenhausen, G., Wagner, G., Ernst, R. R. & Wüthrich, K. (1983). Improved spectral resolution in COSY proton NMR spectra of proteins via double quantum filtering. Biochem. Biophys. Res. Commun. 117, 479-485.
66. Redfield, A. G. & Kunz, S. D. (1975). Quadrature Fourier NMR detection: simple multiplex for dual detection and discussion. J. Magn. Reson. 19, 250-254.
67. Shaka, A. J., Lee, C. J. & Pines, A. (1988). Iterative schemes for bilinear operators. Application to spin decoupling. J. Magn. Reson. 77, 274-293.
68. Sørensen, O. W., Rance, M. & Ernst, R. R. (1984). z filters for purging phase-or multiplet-distorted spectra. J. Magn. Reson. 56, 527-539.
69. Tirendi, C. F. & Martin, J. F. (1989). Fast linear prediction processing in two-dimensional NMR spectroscopy J. Magn. Reson. 81, 577-585.
70. Titman, J. J. & Keeler, J. (1990). Measurement of homonuclear coupling constants from NMR correlation spectra. J. Magn. Reson. 89, 640-646.
71. Weiss, M. A., Nguyen, D. T., Khait, I., Inouye, K., Frank, B. H., Beckage, M., O'Shea, E., Shoelson, S. E., Karplus, M. & Neuringer, L. J. (1989). Two-dimensional NMR and photo-CIDNP studies of the insulin monomer: assignment of aromatic resonances with application to protein folding, structure, and dynamics. Biochemistry, 28, 9855-9873.
72. Weiss, M. A., Frank, B. H., Khait, I., Pekar, A., Heiney, R., Shoelson, S. E. & Neuringer, L. J. (1990). NMR and photo-CIDNP studies of human proinsulin and prohormone processing intermediates with application to endopeptidase recognition. Biochemistry, 30, 8389-8401.
73. 13C labeling with application to protein design. Biochemistry, 30, 7373-7389.
74. Williamson, M. P., Asakura, T., Nakamura, E. & Demura, M. (1992). A method for calculation of protein α-CH chemical shifts. J. Biomol. NMR, 2, 83-98.
75. Wishart, D. S. & Sykes, B. D. (1994). Chemical shifts as a tool for structure determination. Methods Enzymol. 239, 363-392.
76. Wollmer, A., Gilge, G., Brandenburg, D. & Gattner, H.-G. (1994). An insulin with the native sequence but virtually no activity Biol. Chem. Hoppe-Seyler, 375, 219-222.
77. Wüthrich, K. (1986). N.M.R. of Proteins and Nucleic Acids. John Wiley and Sons, Inc. New York.