A circularly permuted myoglobin possesses a folded structure and ligand binding similar to those of the wild-type protein but with a reduced thermodynamic stability

Biochemistry

Volumn 41, Issue 44, 2002, Pages 13318-13327

  Fishburn, Anna L ^a,b   Keeffe, Jennifer R ^a,c   Lissounov, Alexei V ^a   Peyton, David H ^d   Anthony Cahill, Spencer J ^a  

^a WESTERN WASHINGTON UNIVERSITY   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d PORTLAND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL DENATURATION; LIGAND BINDING;

AMINO ACIDS; ASSAYS; ESCHERICHIA COLI; NUCLEAR MAGNETIC RESONANCE; PROTEINS; STRUCTURE (COMPOSITION); THERMODYNAMIC STABILITY;

BIOCHEMISTRY;

MYOGLOBIN;

ARTICLE; ESCHERICHIA COLI; LIGAND BINDING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN STRUCTURE; THERMODYNAMICS; WHALE;

AMINO ACID SEQUENCE; ANIMALS; CIRCULAR DICHROISM; ESCHERICHIA COLI; LIGANDS; MOLECULAR SEQUENCE DATA; MYOGLOBIN; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; THERMODYNAMICS; UREA; WHALES;

CETACEA; ESCHERICHIA COLI; PHYSETER CATODON;

EID: 0037027311     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi026404g     Document Type: Article

References (73)

1. Matthews, B. W., Nicholson, H., and Becktel, W. J. (1987) Enhanced Protein Thermostability From Site-Directed Mutations that Decrease the Entropy of Unfolding, Proc. Natl. Acad. Sci. U.S.A. 84, 6663-6667.
2. Shortle, D. (1989) Probing determinants of protein folding and stability with amino acid substitutions, J. Biol. Chem. 264, 5315-5318.
3. Perry, L. J., and Wetzel, R. (1984) Disulfide bond engineered into T4 lysozyme: Stabilization of the protein toward thermal inactivation, Science 226, 555-557.
4. Sauer, R. T., Hehir, K., Stearman, R. S., Weiss, M. A., Jeitler-Nilsson, A., Suchanek, E. G., and Pabo, C. O. (1986) An engineered intersubunit disulfide enhances the stability and DNA binding of the N-terminal domain of λrepressor, Biochemistry 25, 5992-5998.
5. Matsumura, M., Signor, G., and Matthews, B. W. (1989) Substantial increase of protein stability by multiple disulphide bonds, Nature 342, 291-293.
6. Mitchinson, C., and Wells, J. A. (1989) Protein engineering of disulfide bonds in subtilisin BPN′. Biochemistry 28, 4807-4815.
7. Zhao, H., Giver, L., Shao, Z., Affholter, J. A., and Arnold, F. H. (1998) Molecular evolution by staggered extension process (STEP) in vitro recombination, Nat. Biotechnol. 16, 258-261.
8. Shoichet, B. K., Baase, W. A., Kuroki, R., and Matthews, B. W. (1995) A relationship between protein stability and protein function, Proc. Natl. Acad. Sci. U.S.A. 92, 452-456.
9. Puri, R. K., Hoon, D. S., Leland, P., Snoy, P., Rand, R. W., Pastan, I., and Kreitman, R. J. (1996) Preclinical development of a recombinant toxin containing circularly permuted interleukin 4 and truncated Pseudomonas exotoxin for therapy of malignant astrocytoma, Cancer Res. 56, 5631-5637.
10. v fragment by base-loop interconnection and VHVL permutation. J. Mol. Biol. 268, 107-117.
11. McWherter, C. A., Feng, Y., Zurfluh, L. L., Klein, B. K., Baganoff, M. P., Polazzi, J. O., Hood, W. F., Paik, K., Abegg, A. L., Grabbe, E. S., Shieh, J.-J., Donnelly, A. M., and McKearn, J. P. (1999) Circular permutation of the granulocyte colony-stimulating factor receptor agonist domain of myelopoietin, Biochemistry 38, 4564-4571.
12. Englander, S. W., and Mayne, L. (1992) Protein folding studied using hydrogen-exchange labelling and proton NMR, Annu. Rev. Biophys. Biomol. Struct. 21, 243-265.
13. Jennings, P. A., and Wright, P. E. (1993) Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin, Science 262, 892-896.
14. Fersht, A. (1994) Characterizing transition states in protein folding: An essential step in the puzzle, Curr. Opin. Struct. Biol. 5, 79-84.
15. Viguera, A. R., Serrano, L., and Wilmanns, M. (1996) Different folding transition states may result in the same native structure, Nat. Struct. Biol. 3, 874-880.
16. Otzen, D. E., and Fersht, A. R. (1998) Folding of circular permuted chymotrypsin inhibitor 2: Retention of the folding nucleus, Biochemistry 37, 8139-8146.
17. Hennecke, J., Sebbel, P., and Glockshuber, R. (1999) Random circular permutation of DsbA reveals segments that are essential for protein folding and stability, J. Mol. Biol. 286, 1197-1215.
18. Iwakura, M., Nakamura, T., Yamane, C., and Maki, K. (2000) Systematic circular permutation of an entire protein reveals essential folding elements, Nat. Struct. Biol. 7, 580-585.
19. Graf, R., and Schachman, H. K. (1996) Random circular permutation of genes and expressed polypeptide chains: Application of the method to the catalytic chains of aspartate transcarbamoylase, Proc. Natl. Acad. Sci. U.S.A. 93, 11591-11596.
20. Baird, G. S., Zacharias, D. A., and Tsien, R. Y. (1999) Circular permutation and receptor insertion within green fluorescent proteins, Proc. Natl. Acad. Sci. U.S.A. 96, 11241-11246.
21. Springer, B. A., and Sligar, S. G. (1987) High level expression of sperm whale myoglobin in Escherichia coli, Proc. Natl. Acad. Sci. U.S.A. 84, 8961-8965.
22. Hughson, F. M., and Baldwin, R. L. (1989) Use of site-directed mutagenesis to destabilize native apomyoglobin relative to folding intermediates, Biochemistry 28, 4415-4422.
23. Hughson, F. M., Wright, P. E., and Baldwin, R. L. (1990) Structural characterization of a partly folded apomyoglobin intermediate, Science 249, 1544-1548.
24. Lin, L., Pinker, R. J., Forde, K., Rose, G. D., and Kallenbach, N. R. (1994) Molten globular characteristics of the native state of apomyoglobinin, Nat. Struct. Biol. 1, 447-452.
25. Hargrove, M. S., Kryzwda, S., Wilkinson, A. J., Dou, Y., Ikeda-Saito, M., and Olson, J. S. (1994) Stability of myoglobin: A model for the folding of heme proteins, Biochemistry 33, 11767-11775.
26. Griko, Y. V., and Privalov, P. L. (1994) Thermodynamic puzzle of apomyoglobin unfolding. J. Mol. Biol. 235, 1318-1325.
27. Kiefhaber, T., and Baldwin, R. L. (1995) Intrinsic stability of individual alpha helices modulates structure and stability of the apomyoglobin molten globule form, J. Mol. Biol. 252, 122-132.
28. Loh, S., Kay, M., and Baldwin, R. (1995) Structure and stability of a second molten globule intermediate in the apomyoglobin folding pathway, Proc. Natl. Acad. Sci. U.S.A. 92, 5446-5450.
29. Kay, M. S., and Baldwin, R. L. (1996) Packing interactions in the apomyoglobin folding intermediate, Nat. Struct. Biol. 3, 439-445.
30. Hargrove, M. S., and Olson, J. S. (1996) The stability of holomyoglobin is determined by heme affinity, Biochemistry 35, 11310-11318.
31. Ballew, R. M., Sabelko, J., and Gruebele, M. (1996) Direct observation of fast protein folding: The initial collapse of apomyoglobin, Proc. Natl. Acad. Sci. U.S.A. 93, 5759-5764.
32. Jamin, M., and Baldwin, R. L. (1996) Refolding and unfolding kinetics of the equilibrium folding intermediate of apomyoglobin, Nat. Struct. Biol. 3, 613-618.
33. Cavagnero, S., Dyson, H. J., and Wright, P. E. (1999) Effect of H helix destabilizing mutations on the kinetic and equilibrium unfolding of apomyoglobin, J. Mol. Biol. 285, 269-282.
34. Mathews, A. J., Rohlfs, R. J., Olson, J. S., Tame, J., Renaud, J.-P., and Nagai, K. (1989) The effects of E7 and E11 mutations on the kinetics of ligand binding to R state human hemoglobin, J. Biol. Chem. 264, 16573-16583.
35. Rohlfs, R. J., Mathews, A. J., Carver, T. E., Olson, J. S., Springer, B. A., Egeberg, K. D., and Sligar, S. G. (1990) The effects of amino acid substitution at position E7 (residue 64) on the kinetics of ligand binding to sperm whale myoglobin, J. Biol. Chem. 265, 3168-3176.
36. Doherty, D. H., Doyle, M. P., Curry, S. R., Vali, R. J., Fattor, T. J., Olson, J. S., and Lemon, D. D. (1998) Rate of reaction with nitric oxide determines the hypertensive effect of cell-free hemoglobin, Nat. Biotechnol. 16, 672-676.
37. Sanders, K. E., Lo, J., and Sligar, S. G. (2002) Intersubunit permutation of human hemoglobin, Blood 100, 299-305.
38. Barrick, D., and Baldwin, R. L. (1993) Three-state analysis of sperm whale apomyoglobin folding, Biochemistry 32, 3790-3796.
39. Eliezer, D., Yao, J., Dyson, H. J., and Wright, P. E. (1998) Structural and dynamic characterization of partially folded states of apomyoglobin and implications for protein folding, Nat. Struct. Biol. 5, 148-155.
40. Feng, Z., Ha, J.-H., and Loh, S. N. (1999) Identifying the site of initial tertiary structure disruption during apomyoglobin unfolding, Biochemistry 38, 14433-14439.
41. Viguera, A. R., Blanco, F. J., and Serrano, L. (1995) The order of secondary structure elements does not determine the structure of a protein but does affect its folding kinetics, J. Mol. Biol. 247, 670-681.
42. Johnson, J. L., and Rauschel, F. M. (1996) Influence of primary sequence transpositions on the folding pathways of ribonuclease TI, Biochemistry 35, 10223-10233.
43. Pappu, R. V., and Weaver, D. L. (1998) The early folding kinetics of apomyoglobin, Protein Sci. 7, 480-490.
44. Antonini, E., and Brunori, M. (1971) Hemoglobin and Myoglobin in Their Reactions with Ligands, Elsevier, North-Holland, New York.
45. Pace, C. N. (1986) Determination and analysis of urea and guanidine hydrochloride denaturation curves, Methods Enzymol. 131, 266-280.
46. Santoro, M. M., and Bolen, D. W. (1988) Unfolding free energy changes determined by the linear extrapolation method. I. Unfolding of phenylmethylsulfonyl α-chymotrypsin using different denaturants, Biochemistry 27, 8063-8068.
47. Jue, T., Krishnamoorthi, R., and La Mar, G. N. (1983) Proton NMR study of the mechanism of the heme-apoprotein reaction for myoglobin, J. Am. Chem. Soc. 105, 5701-5703.
48. Inubishi, T., and Becker, E. D. J. (1983) Efficient detection of paramagnetically shifted NMR resonances by optimizing the WEFT sequence, J. Magn. Reson. 51, 128-133.
49. Kumar, A., Ernst, R. R., and Wüthrich. K. (1980) 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, 1-6.
50. 1H spin-spin coupling constants in proteins, Biochem. Biophys. Res. Commun. 113, 967-974.
51. La Mar, G. N., and de Ropp, J. S. (1993) NMR Methodology for Paramagnetic Proteins, in Biological Magnetic Resonance (Berliner, L. J., and Rebuen, J., Eds.) pp 1-78, Plenum Press, New York.
52. Emerson, S. D., and La Mar, G. N. (1990) Solution structural characteristics of cyanometmyoglobin: resonance assignment of heme cavity residues by two-dimensional NMR, Biochemistry 29, 1545-1556.
53. Balacco, G. (1994) SwaN-MR: A complete and expansible NMR software for the Macintosh, J. Chem. Inf. Comput. Sci. 34, 1235- 1241.
54. Balacco, G. (2000) SwaN-MR: From infancy to maturity. Mol. Biol. Today 1, 23-28.
55. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes, J. Biomol. NMR 6, 277- 293.
56. Johnson, B. A., and Blevins, R. A. (1994) NMRView: A computer program for the visualization of NMR data, J. Biomol. NMR 4. 603-614.
57. Hirel, P. H., Schmitter, J. M., Dessen, P., Fayat, G., and Blanquet, S. (1989) Extent of N-terminal methionine excision from Escherichia coli proteins is governed by the side-chain length of the penultimate amino acid, Proc. Natl. Acad. Sci. U.S.A. 86, 8247-8251.
58. Apostol, I., Aitken, J., Levine, J., Lippincott, J., Davidson, J. S., and Abbott-Brown, D. (1995) Recombinant protein sequences can trigger methylation of N-terminal amino acids in Escherichia coli, Protein Sci. 4, 2616-2618.
59. La Mar, G. N., Satterlee, J. D., and de Ropp, J. S. (1999) Nuclear magnetic resonance of hemoproteins, in The Porphyrin Handbook (Kadish, K. M., Smith, K. M., and Guilard, R., Eds.) pp 185-298, Academic Press, San Diego.
60. Horlick, R. A., George, H. J., Cooke, G. M., Tritch, R. J., Newton, R. C., Dwivedi, A., Lischwe, M., Salemme, F. R., Weber, P. C., and Horuk, R. (1992) Permuteins of interleukin 1 beta: A simplified approach for the construction of permutated proteins having new termini, Protein Eng. 5, 427-431.
61. Zhang, T., Bertelsen, E., Benvegnu, D., and Alber, T. (1993) Circular permutation of T4 lysozyme, Biochemistry 32, 12311- 12318.
62. Yang, Y. R., and Schachman, H. K. (1993) Aspartate transcarbamoylase containing circularly permuted catalytic polypeptide chains, Proc. Natl. Acad. Sci. U.S.A. 90, 11980-11984.
63. Smith, V. F., and Matthews, C. R. (2001) Testing the role of chain connectivity on the stability and structure of dihydrofolate reductase from E. coli: Fragment complementation and circular permutation reveal stable, alternatively folded forms, Protein Sci. 10, 116-128.
64. Brantley, R. E., Smerdon, S. J., Wilkinson, A. J., Singleton, E. W., and Olson, J. S. (1993) The mechanism of autooxidation of myoglobin, J. Biol. Chem. 268, 6995-7010.
65. Emerson, S. D., and La Mar, G. N. (1990) NMR determination of the orientation of the magnetic susceptibility tensor in cyanometmyoglobin: a new probe of steric tilt of bound ligand. Biochemistry 29, 1556-1566.
66. Watson, H. C. (1969) The Stereochemistry of the Protein Myoglobin. Prog. Stereochem. 4. 299.
67. Iwakura, M., and Nakamura. T. (1998) Effects of the length of a glycine linker connecting the N- and C-termini of a circularly permuted dihydrofolate reductase, Protein Eng. 11, 707-713.
68. Viguera, A.-R., and Serrano, L. (1997) Loop length, intramolecular diffusion and protein folding, Nat. Struct. Biol. 4, 939-946.
69. Winslow, R. M. (1992) Hemoglobin-based Red Cell Substitutes, Johns Hopkins University Press, Baltimore.
70. Looker, D., Abbott-Brown, D., Cozart, P., Durfee, S., Hoffman, S., Mathews, A. J., Miller-Roehrich, J., Shoemaker, S., Trimble, S., Fermi, G., Komiyama, N. H., Nagai, K., and Stetler, G. L. (1992) A human recombinant haemoglobin designed for use as a blood substitute, Nature 356, 258-260.
71. Gould, S. A., Sehgal, L. R., Sehgal, H. L., and Moss, G. S. (1995)-The development of hemoglobin solutions as red cell substitutes: Hemoglobin solutions, Transfus. Sci. 16, 5-17.
72. D'Agnillo, F., and Chang, T. M. S. (1998) Polyhemoglobin-superoxide dismutase-catalase as a blood substitute with antioxidant properties, Nat. Biotechnol. 16, 667-671.
73. Zhang, T., Bertelsen, E., and Alber, T. (1994) Entropic effects of disulphide bonds on protein stability, Nat. Struct. Biol. 1, 434-438.