Thermodynamic and structural compensation in "size-switch" core repacking variants of bacteriophage T4 lysozyme

Journal of Molecular Biology

Volumn 259, Issue 3, 1996, Pages 542-559

  Baldwin, Enoch ^a   Xu, Jian ^a   Hajiseyedjavadi, Omid ^a,b   Baase, Walter A ^a   Matthews, Brian W ^a  

^a UNIVERSITY OF OREGON   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Coordinated substitutions; Correlated mutations; Hydrophobic core; Intragenic suppressor; Packing mutants

Indexed keywords

ALANINE; LYSOZYME; METHIONINE; MUTANT PROTEIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BACTERIOPHAGE T4; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME CONFORMATION; ENZYME STABILITY; ENZYME STRUCTURE; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN STABILITY;

EID: 0029892667     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0338     Document Type: Article

References (50)

1. Anderson, D. E., Hurley, J. H., Nicholson, H., Baase, W. A. & Matthews, B. W. (1993). Hydrophobic core repacking and aromatic-aromatic interaction in the thermostable mutant of T4 lysozyme Ser117 → Phe. Protan Sci. 2, 1285-1290.
2. Baldwin, E. P., Hajiseyedjavadi, O., Baase, W. A. & Matthews, B. W. (1993a). The role of backbone flexibility in the accommodation of variants that repack the core of T4 lysozyme. Science, 262, 1715-1718.
3. Baldwin, E. P., Xu, J. & Hajiseyedjavadi, O. (1993b). Construction and functional selection of T4lysozyme gene library randomized at five adjacent interior sites. In Techniquesin Protein Chemistry (R. Angeletti, ed.), vol. 4, pp. 495-507, Academic Press, New York.
4. Baldwin, E. P. & Matthews, B. W. (1994). Core packing constraints, hydrophobicity and protein design. Curr. Opin. Struct. Biol. 5, 396-402.
5. Blaber, M., Zhang, X-J., Lindstrom, J. D., Pepiot, S. D., Baase, W. A. & Matthews, B. W. (1994). Determination of α-helix propensity within the context of a folded protein: Sites 44 and 131 in bacteriophage T4 lysozyme. J. Mol. Biol. 235, 600-624.
6. Bordo, D., Djinovic, K. & Bolognesi, M. (1994). Conserved patterns in the Cu,Zn superoxide dismutase family. J. Mol. Biol. 238, 366-386.
7. Connolly, M. L. (1983). Solvent-accessible surfaces of proteins and nucleic acids. Science, 221, 709-713.
8. Dao-pin, S., Alber, T., Baase, W. A., Wozniak, J. A. & Matthews, B. W. (1991). Structural and thermodynamic analysis of the packing of two α-helices in bacteriophage T4lysozyme. J. Mol. Biol. 221, 647-667.
9. di Rago, J. P., Herman-le Denmat, S., Paques, F., Risler, F. P., Netter, P. & Sonimski, P. P. (1995). Genetic analysis of the folded structure of yeast cytochrome b by selection of intragenic second-site revertants. J. Mol. Biol. 248, 804-811.
10. Eijsink, V. G. H., Dijkstra, B. W., Vriend, G., van der Zee, J. R., Veltman, O. R., van der Vinne, B., van den Burg, B., Kempe, S. & Venema, G. (1992). The effect of cavity-filling mutations on the thermostability of Bacillus stearothermophilus neutral protease. Protein Eng. 5, 421-426.
11. Eriksson, A. E., Baase, W. A., Zhang, X-J., Heinz, D. W., Blaber, M., Baldwin, E. P. & Matthews, B. W. (1992). The response of a protein structure to cavity-creating mutations and its relationship to the hydrophobic effect. Science, 255, 178-183.
12. Eriksson, A. E., Baase, W. A. & Matthews, B. W. (1993). Similar hydrophobic replacements of Leu99 and Phe153 within the core of T4lysozyme have different structural and thermodynamic consequences. J. Mol. Biol. 229, 747-769.
13. Fauchére, J.-L. & Pliška, V. (1983). Hydrophobic parameters π of amino add side-chains form the partioning of N-acetyl-amino-acid amides. Eur. J. Med. Chem. 18, 369-375.
14. Gerstein, M., Sonnhammer, E. L. & Chothia, C. (1994). Volume changes in protein evolution. J. Mol. Bid. 36, 1067-1078.
15. Hamlin, R. (1985). Multiwire area X-ray diffractometers. Methods Enzymol. 114, 416-452.
16. Hurley, J. H., Baase, W. A. & Matthews, B. W. (1992). Design and structural analysis of alternative hydrophobic core packing arrangements in bacteriophage T4 lysozyme. J. Mol. Biol. 224, 1143-1159.
17. International Union of Pure and Applied Chemistry-International Union of Biochemistry Commission on Biochemical Nomendature (1970). Abbreviations and symbols for the description of the conformation of polypeptide chains. J Mol. Biol. 52, 4-17.
18. Ishikawa, K., Nakamura, H., Morikawa, K. & Kanaya, S. (1993). Stabilization of Escherichiacoli ribonuclease HI by cavity-filling mutations within a hydrophobic core. Biochemistry, 32, 6171-6178.
19. Karpusas, M., Baase, W. A., Matsumura, M. & Matthews, B. W. (1989). Hydrophobic packing in T4 lysozyme probed by cavity-filling mutants. Proc. Natl Acad. Sci. USA, 86, 8237-8241.
20. Kellis, J. T., Nyberg, K., Sali, D. & Fersht, A. R. (1988). Contribution of hydrophobic interactions to protein stability. Nature, 333, 784-786.
21. Khorasanizadeh, S., Peters, I. D., Butt, T. R. & Roder, H. (1993). Folding and stability of a tryptophan-containing mutant of ubiquitin. Biochemistry, 32, 7054-7063.
22. Kimura, M. (1985). The role of compensatory neutral mutations in molecular evolution. J. Genet. 64, 7-19.
23. Kunkel, T. A., Roberts, J. D. & Zakour, R. A. (1987). Rapid and effident site-specific mutagenesis without phenotypic selection. Methods Enzymd. 154, 367-382.
24. Lee, B. & Richards, F. M. (1971). The interpretation of protein structures: estimation of static accessibility. J Mol. Biol. 55, 379-400.
25. Lesk, A. M. & Chothia, C. (1980). How different amino acid sequences determine similar protein structures: the structure and evolutionary dynamics of the globins. J Mol. Biol. 136, 225-270.
26. Lesk, A. M. & Chothia, C. (1982). Evolution of proteins formed by β-sheets. II. The core of the immunoglobulin domains. J Mol. Biol. 160, 325-342.
27. Lim, W. A. & Sauer, R. T. (1991). The role of internal packing inter actions in determining the structure and stability of a protein. J. Mol. Biol. 219, 359-376.
28. Lim, W. A., Farruggio, D. C. & Sauer, R. T. (1992). Structural and energetic consequences of disruptive mutations in a protein core. Biochemistry, 31, 4324-4333.
29. Lim, W. A., Hodel, A., Sauer, R. T. & Richards, F. M. (1994). Crystal structure of a mutant protein with altered but improved hydrophobic core packing. Proc. Natl Acad. Sci. USA, 91, 423-427.
30. Malcolm, B. A., Wilson, K. P., Matthews, B. W., Kirsch, J. F. & Wilson, A. C. (1990). Ancestral lysozymes reconstructed, neutrality tested and thermostability linked to hydrocarbon packing. Nature, 344, 86-89.
31. Mande, S., Mainfroid, M., Kalk, K. H., Goraj, K., Martial, J A. & Hol, W. M. G. (1994). Crystal structure of triosephosphate isomerase at 2.8 Å resolution. Triosephosphate isomerase-related human genetic disorders and comparison with the trypanosomal enzyme. Protein Sci. 3, 810-821.
32. Matsumura, M. & Matthews, B. W. (1989). Control of enzyme activity by an engineered disulfide bond. Science, 243, 792-794.
33. Matsumura, M., Becktel, W. J. & Matthews, B. W. (1988). Hydrophobic stabilization in T4 lysozyme determined directly by multiple substitutions of lle3. Nature, 334, 406-410.
34. Mitraki, A., Fane, B., Haase-Pettingell, C., Sturtevant, J. & King, J (1991). Global suppression of protein folding defects and inclusion body formation. Science, 253, 54-58.
35. 15N labelling of proteins for proton and nitrogen-15 NMR. Methods Enzymd. 177, 44-73.
36. Ponder, J. W. & Richards, F. M. (1987). Tertiary templates for proteins. Use of packing criteria in the enumeration of allowed sequences for different structural classes. J. Mol. Biol. 193, 775-791.
37. Poteete, A. R., Dao-pin, S., Nicholson, H. & Matthews, B. W. (1991). Second-site revertants of an inactive T4 lysozyme mutant restore activity structuring the active site deft. Biochemistry, 30, 1425-1432.
38. Richards, F M. (1974). The interpretation of protein structures: total volume, group volume distributions and packing density. J. Mol. Biol. 82, 1-14.
39. Richards, F. M. (1977). Areas, volumes, packing and protein structure. Annu. Rev. Biophys. Bioeng. 6, 151-176.
40. Sandberg, W. S. & Terwilliger, T. C. (1989). Influence of interior packing and hydrophobicity on the stability of a protein. Science, 245, 54-57.
41. Sandberg, W. S. & Terwilliger, T. C. (1991). Energetics of repacking a protein interior. Proc. Natl Acad. Sci. USA, 88, 1706-1710.
42. Serrano, L., Day, A. G. & Fersht, A. R. (1993). Step-wise mutation of barnase to binase. A procedure for engineering increased stability of proteins and an experimental analysis of the evolution of protein stability. J. Mol. Biol. 233, 305-312.
43. Shortle, D., Stites, W. E. & Meeker, A. K. (1990). Contributions of the large hydrophobic amino acids to the stability of staphylococcal nuclease. Biochemisty, 29, 8033-8041.
44. Tronrud, D. E. (1996). Knowledge-based temperature factor restraints for the refinement of proteins. J. Appl. Crystallog. In the press.
45. Tronrud, D. E., Ten Eyck, L. F & Matthews, B. W. (1987). An efficient general-purpose least-squares refinement program for macromolecular structures. Acta Crystallog. sect. A, 43, 489-503.
46. Tsuji, T., Chrunyk, B. A., Chen, X. & Matthews, C. R. (1993). Mutagenic analysis of the interior packing of an α/α barrel protein. Effects on the stabilities and rates of the α subunit of tryptophan synthase. Biochemistry, 32, 5566-5575.
47. Vernet, T., Tessier, D. C., Khourin, H. E. & Altschuh, D. (1992). Correlation of coordinated amino acid changes at the two-domain interface of cysteine proteases with protein stability. J. Mol. Biol. 224, 501-509.
48. Weaver, L. H. & Matthews, B. W. (1987). Structure of bacteriophage T4 lysozyme refined at 1.7 Å resolution. J. Mol. Biol. 193, 189-199.
49. Wilson, K. P., Malcolm, B. A. & Matthews, B. W. (1992). Structural and thermodynamic analysis of compensating mutationswithin thecoreof chicken egg white lysozyme. J. Biol. Chem. 267, 10842-10849.
50. Zhang, X-J. & Matthews, B. W. (1995). EDPDB: a multi-functional tool for protein structure analysis. J. Appl. Crystallog. 28, 624-630.