Proline scanning mutagenesis of a molten globule reveals non-cooperative formation of a protein's overall topology

Nature Structural Biology

Volumn 3, Issue 8, 1996, Pages 682-687

  Schulman, Brenda A ^a,b   Kim, Peter S ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA LACTALBUMIN; MUTANT PROTEIN; PROLINE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CIRCULAR DICHROISM; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE;

CIRCULAR DICHROISM; DISULFIDES; LACTALBUMIN; MODELS, CHEMICAL; MODELS, MOLECULAR; MUTAGENESIS; PROLINE; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY;

EID: 0029765444     PISSN: 10728368     EISSN: None     Source Type: Journal    
DOI: 10.1038/nsb0896-682     Document Type: Article

References (61)

1. Kuwajima, K. The molten globule state as a clue for understanding the folding and cooperativity of globular-protein structure. Proteins 6, 87-103 (1989).
2. Ptitsyn, O.B. The molten globule state. in Protein Folding (ed. Creighton, T.E.) 243-300 (W. H. Freeman and Co., New York, 1992).
3. Dobson, C.M. Solid evidence for molten globules. Curr. Biol. 4, 636-40 (1994).
4. Eliezer, D., Jennings, P.A., Wright, P.E., Doniach, S., Hodgson, K.O. & Tsuruta, H. The radius of gyration of an apomyoglobin folding intermediate. Science 270, 487-8 (1995).
5. Peng, Z.-y. & Kim, P.S. A protein dissection study of a molten globule. Biochemistry 33, 2136-41 (1994).
6. Wu, L.C., Peng, Z.-y. & Kim, P.S. Bipartite structure of the α-lactalbumin molten globule. Nature Struct. Biol. 2, 281-86 (1995).
7. Peng, Z.-y., Wu, L.C. & Kim, P.S. Local structural preferences in the α-lactalbumin molten globule. Biochemistry 34, 3248-52 (1995).
8. Polverino de Laureto, P., De Filippis, V., Di Bello, M., Zambonin, M. & Fontana, A. Probing the molten globule state of alpha-lactalbumin by limited proteolysis. Biochemistry 34, 12596-604 (1995).
9. Wilson, G. et al. Vibrational Raman optical activity of alpha-lactalbumin: comparison with lysozyme, and evidence for native tertiary folds in molten globule states. J. Mol. Biol. 254, 747-60 (1995).
10. Alexandrescu, A.T., Evans, P.A., Pitkeathly, M., Baum, J. & Dobson, C.M. Structure and dynamics of the acid-denatured molten globule state of alpha-lactalbumin: a two-dimensional NMR study. Biochemistry 32, 1707-1718 (1993).
11. Cunningham, B.C. & Wells, J.A. High-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis. Science 244, 1081-1085 (1989).
12. Richardson, J.S. & Richardson, D.C. Amino acid preferences for specific locations at the ends of alpha helices. Science 240, 1648-52 (1988).
13. Strehlow, K.G., Robertson, A.D. & Baldwin, R.L. Proline for alanine substitutions in the C-peptide helix of ribonuclease A. Biochemistry 30, 5810-4 (1991).
14. Minor, D., Jr. & Kim, P.S. Measurement of the beta-sheet-forming propensities of amino acids. Nature 367, 660-663 (1994).
15. Smith, C.K., Withka, J.M. & Regan, L. A thermodynamic scale for the beta-sheet forming tendencies of the amino acids. Biochemistry 33, 5510-5517 (1994).
16. Minor, D., Jr. & Kim, P.S. Context is a major determinant of beta-sheet propensity. Nature 371, 264-267 (1994).
17. Wood, S.J., Wetzel, R., Martin, J.D. & Hurle, M.R. Prolines and amyloidogenicity in fragments of the Alzheimer's peptide beta/A4. Biochemistry 34, 724-30 (1995).
18. O'Neil, K.T. & De Grado, W.F. A thermodynamic scale for the helix-forming tendencies of the commonly occurring amino acids. Science 250, 646-651 (1990).
19. Horovitz, A., Matthews, J.M. & Fersht, A.R. Alpha-helix stability in proteins. II. Factors that influence stability at an internal position. J. Mol. Biol. 227, 560-568 (1992).
20. Sauer, D.H., San, D.P. & Matthews, B.W. Tolerance of T4 lysozyme to proline substitutions within the long interdomain alpha-helix illustrates the adaptability of proteins to potentially destabilizing lesions. J. Biol. Chem. 267, 2393-2399 (1992).
21. Blaber, M., et al. Determination of alpha-helix propensity within the context of a folded protein. Sites 44 and 131 in bacteriophage T4 lysozyme. J. Mol. Biol. 235, 600-624 (1994).
22. Baum, J., Dobson, C.M., Evans, P.A. & Hanley, C. Characterization of a partly folded protein by NMR methods: studies on the molten globule state of guinea pig alpha-lactalbumin. Biochemistry 28, 7-13 (1989).
23. Chyan, C.L., Wormald, C., Dobson, C.M., Evans, P.A. & Baum, J. Structure and stability of the molten globule state of guinea-pig alpha-lactalbumin: a hydrogen exchange study. Biochemistry 32, 5681-5691 (1993).
24. Schulman, B.A., Peng, Z.-y., Redfield, C., Dobson, C.M. & Kim, P.S. Different subdomains are most protected from hydrogen exchange in the molten globule and native states of α-lactalbumin. J. Mol. Biol. 253, 651-657 (1995).
25. Nozaka, M., Kuwajima, K., Nitta, K. & Sugai, S. Detection and characterization of the intermediate on the folding pathway of human alpha-lactalbumin. Biochemistry 17, 3753-3758 (1978).
26. Acharya, K.R., Ren, J.S., Stuart, D.I., Phillips, D.C. & Fenna, R.E. Crystal structure of human alpha-lactalbumin at 1.7 A resolution. J. Mol. Biol. 221, 571-581 (1991).
27. Siddiqui, A.S. & Barton, G.J. Continuous and discontinuous domains: an algorithm for the automated generation of reliable protein domain definitions. Prot. Sci. 4, 872-884 (1995).
28. Xie, D., Bhakuni, V. & Freire, E. Calorimetric determination of the energetics of the molten globule intermediate in protein folding: apo-α-lactalbumin. Biochemistry 30, 10673-10678 (1991).
29. Yutani, K., Ogasahara, K. & Kuwajima, K. Absence of the thermal transition in apo-alpha-lactalbumin in the molten globule state. A study by differential scanning microcalorimetry. J. Mol. Biol. 228, 347-350 (1992).
30. Jennings, P.A. & Wright, P.E. Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin. Science 262, 892-8926 (1993).
31. Kreimer, D.I., Szosenfogel, R., Goldfarb, D., Silman, I. & Weiner, L. Two-state transition between molten globule and unfolded states of acetylcholinesterase as monitored by electron paramagnetic resonance spectroscopy. Proc. Natl. Acad. Sci. USA 91, 12145-12149 (1994).
32. Chan, H.S., Bromberg, S. & Dill, K.A. Models of cooperativity in protein folding. Philos. Trans. R. Soc. Lond. B Biol. Sci. 348, 61-70 (1995).
33. Ptitsyn, O.B., Bychkova, V.E. & Uversky, V.N. Kinetic and equilibrium folding intermediates. Philos. Trans. R. Soc. Lond. BB iol. Sci. 348, 35-41 (1995).
34. Kiefhaber, T. & Baldwin, R.L. Intrinsic stability of individual alpha helices modulates structure and stability of the apomyoglobin molten globule form. J. Mol. Biol. 252, 122-132 (1995).
35. Loh, S.N., Kay, M.S. & Baldwin, R.L. Structure and stability of a second molten globule intermediate in the apomyoglobin folding pathway. Proc. Natl. Acad. Sci. USA 92, 5446-5450 (1995).
36. Marmorino, J.L. & Pielak, G.J. A native tertiary interaction stabilizes the A state of cytochrome c. Biochemistry 34, 3140-3143 (1995).
37. Shimizu, A., Ikeguchi, M. & Sugai, S. Unfolding of the molten globule state of alpha-lactalbumin studied by 1H NMR. Biochemistry 32, 13198-203 (1993).
38. Dill, K.A. Dominant forces in protein folding. Biochemistry 29, 7133-55 (1990).
39. Kay, M.S. & Baldwin, R.L. Packing interactions in the apomyoglobin folding intermediate. Nature Struct. Biol. 3, 439-45 (1996).
40. Bai, Y., Sosnick, T.R., Mayne, L., & Englander, S.W. Protein folding intermediates: native-state hydrogen exchange. Science 269, 192-197 (1995).
41. Dill, K.A. & Shortle, D. Denatured states of proteins. Annu. Rev. Biochem. 60, 795-825 (1991).
42. Dobson, C.M. Unfolded proteins, compact states and molten globules. Curr. Opin. Struct. Biol. 2, 6-12 (1992).
43. Shortle, D. Denatured states of proteins and their roles in folding and stability. Curr. Opin. Struct. Biol. 3, 66-74 (1993).
44. Lumb, K.J. & Kim, P.S. Formation of a hydrophobic cluster in denatured bovine pancreatic trypsin inhibitor. J. Mol. Biol. 236, 412-420 (1994).
45. Agashe, V.R., Shastry, M.C.R., & Udgaonkar, J.B. Initial hydrophobic collapse in the folding of barstar. Nature 377, 754-757 (1995).
46. Oliveberg, M. & Fersht, A. Thermodynamics of transient conformations in the folding pathway of barnase: reorganization of the folding intermediate at low pH. Biochemistry 35, 2738-2749 (1996).
47. Hughson, P.M., Barrick, D. & Baldwin, R.L. Probing the stability of a partly folded apomyoglobin intermediate by site-directed mutagenesis. Biochemistry 30, 4113-4118 (1991).
48. Minor, D.L. Jr. & Kim, P.S. Context-dependent secondary structure formation of a designed protein sequence. Nature 380, 730-734 (1996).
49. Lau, K.F. & Dill, K.A. Theory for protein mutability and biogenesis. Proc. Natl. Acad. Sci. USA 87, 638-642 (1990).
50. Behe, M.J., Lattman, E.E. & Rose, G.D. The protein-folding problem: the native fold determines packing, but does packing determine the native fold? Proc. Natl. Acad. Sci. USA 88, 4195-4199 (1991).
51. Bowie, J.U., Luthy, R. & Eisenberg, D. A method to identify protein sequences that fold into a known three-dimensional structure. Science 253, 164-170 (1991).
52. Xiong, H., Buckwalter, B.L., Shieh, H.M. & Hecht, M.H. Periodicity of polar and nonpolar amino acids is the major determinant of secondary structure in self-assembling oligomeric peptides. Proc. Natl. Acad. Sci. USA 92, 6349-6353 (1995).
53. Ptitsyn, O.B. How does protein synthesis give rise to the 3D-structure? FEBS Letts 285, 176-181 (1991).
54. Edelhoch, H. Spectroscopic determination of tryptophan and tyrosine in proteins. Biochemistry 6, 1948-1954 (1967).
55. Laue, T.M., Shah, B.D., Ridgeway, T.M. & Pelletier, S.L. Computer-aided interpretation of analytical sedimentation data for proteins. in Analytical Ultracentrifugaton in Biochemistry and Polymer Science (eds S.E. Harding, A.J. Rowe & J.C. Horton) 90-125 (The Royal Society of Chemistry, Cambridge, 1992).
56. Chen, Y.H., Yang, J.T. & Chau, K.H. Determination of the helix and beta form of proteins in aqueous solution by circular dichroism. Biochemistry 13, 3350-3359 (1974).
57. Ellman, G.L. Tissue sulphydryl groups. Arch. Biochem. Biophys. 82, 70-77 (1959).
58. Priestle, J.P. RIBBON: A stereo cartoon drawing program for proteins. J. Appl. Crystallogr. 21, 572-576 (1988).
59. Woody, R.W. Circular Dichroism of Peptides. in The Peptides: Analysis, Synthesis, Structure (ed. V.J. Hruby) 15-114 (Academic Press, Orlando, 1985).
60. Manning, M.C. & Woody, R.W. Theoretical study of the contribution of aromatic side chains to the circular dichroism of basic bovine pancreatic trypsin inhibitor. Biochemistry 28, 8609-8613 (1989).
61. Chakrabartty, A., Kortemme, T., Padmanabhan, S. & Baldwin, R.L. Aromatic side-chain contribution to far-ultraviolet circular dichroism of helical peptides and its effect on measurement of helix propensities. Biochemistry 32, 5560-5565 (1993).