Exploring subdomain cooperativity in T4 lysozyme I: Structural and energetic studies of a circular permutant and protein fragment

Protein Science

Volumn 16, Issue 5, 2007, Pages 842-851

  Cellitti, Jason ^a   Llinas, Manuel ^a,d   Echols, Nathaniel ^a   Shank, Elizabeth A ^a,e   Gillespie, Blake ^c   Kwon, Ester ^a   Crowder, Scott M ^a,f   Dahlquist, Frederick W ^b   Alber, Tom ^a   Marqusee, Susan ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CALIFORNIA STATE UNIVERSITY CHANNEL ISLANDS   (United States)

^d PRINCETON UNIVERSITY   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

^f RIGEL PHARMACEUTICALS INC   (United States)

Author keywords

Intermediates; Native state hydrogen exchange; Protein folding; T4 lysozyme; X ray crystallography

Indexed keywords

LYSOZYME; PROTEIN; PROTEIN CP13; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; X RAY CRYSTALLOGRAPHY;

BACTERIOPHAGE T4; CIRCULAR DICHROISM; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; MURAMIDASE; MUTATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; THERMODYNAMICS;

EID: 34247593368     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.062628607     Document Type: Article

References (42)

1. Anderson, D.E., Lu, J., McIntosh, L.P., and Dahlquist, F.W. 1993. The folding, stability and dynamics of T4 lysozyme: A perspective using nuclear magnetic resonance. NMR of Proteins. (eds. G.M. Clore and A.M. Gronenborn), pp. 258-304. McMillan Press, London.
2. Baldwin, R.L. and Rose, G.D. 1999. Is protein folding hierarchic? II. Folding intermediates and transition states. Trends Biochem. Sci. 24: 77-83.
3. Bilsel, O. and Matthews, C.R. 2006. Molecular dimensions and their distributions in early folding intermediates. Curr. Opin. Struct. Biol. 16: 86-93.
4. Cellitti, J., Bernstein, R., and Marqusee, S. 2007. Exploring subdomain cooperativity in T4 lysozyme II: Uncovering the C-terminal subdomain as a hidden intermediate in the kinetic folding pathway. Protein Sci. (this issue).
5. Chamberlain, A.K. and Marqusee, S. 2000. Comparison of equilibrium and kinetic approaches for determining protein folding mechanisms. Adv. Protein Chem. 53: 283-328.
6. Chamberlain, A.K., Handel, T.M., and Marqusee, S. 1996. Detection of rare partially folded molecules in equilibrium with the native conformation of RNaseH. Nat. Struct. Biol. 3: 782-787.
7. Creighton, T.E. 1992. Protein folding. W.H. Freeman, New York.
8. Doolittle, R.F. 1995. The multiplicity of domains in proteins. Annu. Rev. Biochem. 64: 287-314.
9. Elwell, M. and Schellman, J. 1975. Phage T4 lysozyme. Physical properties and reversible unfolding. Biochim. Biophys. Acta 386: 309-323.
10. Fersht, A.R. 1998. Structure and mechanism in protein science: A guide to enzyme catalysis and protein folding. W.H. Freeman, New York.
11. Fischer, K.F. and Marqusee, S. 2000. A rapid test for identification of autonomous folding units in proteins. J. Mol. Biol. 302: 701-712.
12. Fontana, A., de Laureto, P.P., Spolaore, B., Frare, E., Picotti, P., and Zambonin, M. 2004. Probing protein structure by limited proteolysis. Acta Biochim. Pol. 51: 299-321.
13. Holton, J. and Alber, T. 2004. Automated protein crystal structure determination using ELVES. Proc. Natl. Acad. Sci. 101: 1537-1542.
14. Hondoh, T., Kato, A., Yokoyama, S., and Kuroda, Y. 2006. Computer-aided NMR assay for detecting natively folded structural domains. Protein Sci. 15: 871-883.
15. Jackson, S.E. 1998. How do small single-domain proteins fold? Fold. Des. 3: R81-R91.
16. Jaenicke, R. 1999. Stability and folding of domain proteins. Prog. Biophys. Mol. Biol. 71: 155-241.
17. Jones, T.A., Zou, J.Y., Cowan, S.W., and Kjeldgaard, M. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47: 110-119.
18. Kato, H., Feng, H., and Bai, Y. 2007. The folding pathway of T4 lysozyme: The high-resolution structure and folding of a hidden intermediate. J. Mol. Biol. 365: 870-880.
19. Krishna, M.M., Hoang, L., Lin, Y., and Englander, S.W. 2004. Hydrogen exchange methods to study protein folding. Methods 34: 51-64.
20. Llinas, M. and Marqusee, S. 1998. Subdomain interactions as a determinant in the folding and stability of T4 lysozyme. Protein Sci. 7: 96-104.
21. Llinas, M., Gillespie, B., Dahlquist, F.W., and Marqusee, S. 1999. The energetics of T4 lysozyme reveal a hierarchy of conformations. Nat. Struct. Biol. 6: 1072-1078.
22. Lu, J. and Dahlquist, F.W. 1992. Detection and characterization of an early folding intermediate of T4 lysozyme using pulsed hydrogen exchange and two-dimensional NMR. Biochemistry 31: 4749-4756.
23. Matsumura, M. and Matthews, B.W. 1989. Control of enzyme activity by an engineered disulfide bond. Science 243: 792-794.
24. Matthews, B.W. 1995. Studies on protein stability with T4 lysozyme. Adv. Protein Chem. 46: 249-278.
25. Matthews, B.W. 1996. Structural and genetic analysis of the folding and function of T4 lysozyme. FASEB J. 10: 35-41.
26. McHaourab, H.S., Oh, K.J., Fang, C.J., and Hubbell, W.L. 1997. Conformation of T4 lysozyme in solution. Hinge-bending motion and the substrate-induced conformational transition studied by site-directed spin labeling. Biochemistry 36: 307-316.
27. Murshudov, G.N., Vagin, A.A., and Dodson, E.J. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53: 240-255.
28. Orengo, C.A., Michie, A.D., Jones, S., Jones, D.T., Swindells, M.B., and Thornton, J.M. 1997. CATH - A hierarchic classification of protein domain structures. Structure 5: 1093-1108.
29. Otwinowski, Z. and Minor, W. 1997. Processing X-ray diffraction data collected in oscillation mode. In Methods in enzymology: Macromolecular crystallography, Part A (ed. R. Carter Jr.), pp. 307-326. Academic Press, New York.
30. Parker, M.J. and Marqusee, S. 1999. The cooperativity of burst phase reactions explored. J. Mol. Biol. 293: 1195-1210.
31. Peng, Z.Y. and Kim, P.S. 1994. A protein dissection study of a molten globule. Biochemistry 33: 2136-2141.
32. Perrakis, A., Morris, R.M., and Lamzin, V.S. 1999. Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 6: 458-463.
33. Privalov, P.L. 1996. Intermediate states in protein folding. J. Mol. Biol. 258: 707-725.
34. Sagermann, M., Baase, W.A., Mooers, B.H., Gay, L., and Matthews, B.W. 2004. Relocation or duplication of the helix A sequence of T4 lysozyme causes only modest changes in structure but can increase or decrease the rate of folding. Biochemistry 43: 1296-1301.
35. Sheldrick, G.M. and Schneider, T.R. 1997. SHELXL: High-resolution refinement. Methods Enzymol. 277: 319-343.
36. Thornton, J.M. and Sibanda, B.L. 1983. Amino and carboxy-terminal regions in globular proteins. J. Mol. Biol. 167: 443-460.
37. Vagin, A. and Teplyakov, A. 2000. An approach to multi-copy search in molecular replacement. Acta Crystallogr. D Biol. Crystallogr. 56: 1622-1624.
38. Weaver, L.H. and Matthews, B.W. 1987. Structure of bacteriophage T4 lysozyme refined at 1.7 Å resolution. J. Mol. Biol. 193: 189-199.
39. Wu, L.C., Grandori, R., and Carey, J. 1994. Autonomous subdomains in protein folding. Protein Sci. 3: 369-371.
40. Zhang, T., Berkelsen, E., Benvegnu, D., and Alter, T. 1993. Circular permutation of T4 lysozyme. Biochemistry 32: 12311-12318.
41. Zhang, X.J., Wozniak, J.A., and Matthews, B.W. 1995. Protein flexibility and adaptability seen in 25 crystal forms of T4 lysozyme. J. Mol. Biol. 250: 527-552.
42. Zhou, Z., Huang, Y., and Bai, Y. 2005. An on-pathway hidden intermediate and the early rate-limiting transition state of Rd-apocytochrome b562 characterized by protein engineering. J. Mol. Biol. 352: 757-764.