Abstract
The diffusion-collision model of protein folding is assessed. A description is given of the qualitative aspects and quantitative results of the diffusion-collision model and their relation to available experimental data. We consider alternative mechanisms for folding and point out their relationship to the diffusion-collision model. We show that the diffusion-collision model is supported by a growing body of experimental and theoretical evidence, and we outline future directions for developing the model and its applications.
Full Text
The Full Text of this article is available as a PDF (2.2 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Barnes K. P., Warren J. R., Gordon J. A. Effect of urea on the circular dichroism of lysozyme. J Biol Chem. 1972 Mar 25;247(6):1708–1712. [PubMed] [Google Scholar]
- Bashford D., Cohen F. E., Karplus M., Kuntz I. D., Weaver D. L. Diffusion-collision model for the folding kinetics of myoglobin. Proteins. 1988;4(3):211–227. doi: 10.1002/prot.340040308. [DOI] [PubMed] [Google Scholar]
- Bashford D., Weaver D. L., Karplus M. Diffusion-collision model for the folding kinetics of the lambda-repressor operator-binding domain. J Biomol Struct Dyn. 1984 Mar;1(5):1243–1255. doi: 10.1080/07391102.1984.10507515. [DOI] [PubMed] [Google Scholar]
- 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. 1989 Jan 10;28(1):7–13. doi: 10.1021/bi00427a002. [DOI] [PubMed] [Google Scholar]
- Berthou J., Jollès P. The influence of urea on crystallization and polymorphism of hen lysozyme. FEBS Lett. 1973 Apr 15;31(2):189–192. doi: 10.1016/0014-5793(73)80100-0. [DOI] [PubMed] [Google Scholar]
- Blake C. C., Pulford W. C., Artymiuk P. J. X-ray studies of water in crystals of lysozyme. J Mol Biol. 1983 Jul 5;167(3):693–723. doi: 10.1016/s0022-2836(83)80105-3. [DOI] [PubMed] [Google Scholar]
- Blond S., Goldberg M. Partly native epitopes are already present on early intermediates in the folding of tryptophan synthase. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1147–1151. doi: 10.1073/pnas.84.5.1147. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brandts J. F., Halvorson H. R., Brennan M. Consideration of the Possibility that the slow step in protein denaturation reactions is due to cis-trans isomerism of proline residues. Biochemistry. 1975 Nov 4;14(22):4953–4963. doi: 10.1021/bi00693a026. [DOI] [PubMed] [Google Scholar]
- Briggs M. S., Roder H. Early hydrogen-bonding events in the folding reaction of ubiquitin. Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2017–2021. doi: 10.1073/pnas.89.6.2017. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown J. E., Klee W. A. Helix-coil transition of the isolated amino terminus of ribonuclease. Biochemistry. 1971 Feb 2;10(3):470–476. doi: 10.1021/bi00779a019. [DOI] [PubMed] [Google Scholar]
- Bryngelson J. D., Wolynes P. G. Spin glasses and the statistical mechanics of protein folding. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7524–7528. doi: 10.1073/pnas.84.21.7524. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bycroft M., Matouschek A., Kellis J. T., Jr, Serrano L., Fersht A. R. Detection and characterization of a folding intermediate in barnase by NMR. Nature. 1990 Aug 2;346(6283):488–490. doi: 10.1038/346488a0. [DOI] [PubMed] [Google Scholar]
- Chakrabartty A., Schellman J. A., Baldwin R. L. Large differences in the helix propensities of alanine and glycine. Nature. 1991 Jun 13;351(6327):586–588. doi: 10.1038/351586a0. [DOI] [PubMed] [Google Scholar]
- Chan H. S., Dill K. A. Origins of structure in globular proteins. Proc Natl Acad Sci U S A. 1990 Aug;87(16):6388–6392. doi: 10.1073/pnas.87.16.6388. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chothia C. Proteins. One thousand families for the molecular biologist. Nature. 1992 Jun 18;357(6379):543–544. doi: 10.1038/357543a0. [DOI] [PubMed] [Google Scholar]
- Chrunyk B. A., Matthews C. R. Role of diffusion in the folding of the alpha subunit of tryptophan synthase from Escherichia coli. Biochemistry. 1990 Feb 27;29(8):2149–2154. doi: 10.1021/bi00460a027. [DOI] [PubMed] [Google Scholar]
- Creighton T. E. Experimental studies of protein folding and unfolding. Prog Biophys Mol Biol. 1978;33(3):231–297. doi: 10.1016/0079-6107(79)90030-0. [DOI] [PubMed] [Google Scholar]
- Creighton T. E. Toward a better understanding of protein folding pathways. Proc Natl Acad Sci U S A. 1988 Jul;85(14):5082–5086. doi: 10.1073/pnas.85.14.5082. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Daggett V., Kollman P. A., Kuntz I. D. A molecular dynamics simulation of polyalanine: an analysis of equilibrium motions and helix-coil transitions. Biopolymers. 1991 Aug;31(9):1115–1134. doi: 10.1002/bip.360310911. [DOI] [PubMed] [Google Scholar]
- Dill K. A. Theory for the folding and stability of globular proteins. Biochemistry. 1985 Mar 12;24(6):1501–1509. doi: 10.1021/bi00327a032. [DOI] [PubMed] [Google Scholar]
- Dolgikh D. A., Kolomiets A. P., Bolotina I. A., Ptitsyn O. B. 'Molten-globule' state accumulates in carbonic anhydrase folding. FEBS Lett. 1984 Jan 2;165(1):88–92. doi: 10.1016/0014-5793(84)80020-4. [DOI] [PubMed] [Google Scholar]
- Dorit R. L., Schoenbach L., Gilbert W. How big is the universe of exons? Science. 1990 Dec 7;250(4986):1377–1382. doi: 10.1126/science.2255907. [DOI] [PubMed] [Google Scholar]
- Dyson H. J., Merutka G., Waltho J. P., Lerner R. A., Wright P. E. Folding of peptide fragments comprising the complete sequence of proteins. Models for initiation of protein folding. I. Myohemerythrin. J Mol Biol. 1992 Aug 5;226(3):795–817. doi: 10.1016/0022-2836(92)90633-u. [DOI] [PubMed] [Google Scholar]
- Dyson H. J., Rance M., Houghten R. A., Wright P. E., Lerner R. A. Folding of immunogenic peptide fragments of proteins in water solution. II. The nascent helix. J Mol Biol. 1988 May 5;201(1):201–217. doi: 10.1016/0022-2836(88)90447-0. [DOI] [PubMed] [Google Scholar]
- Epand R. M. Conformational properties of cyanogen bromide-cleaved glucagon. J Biol Chem. 1972 Apr 10;247(7):2132–2138. [PubMed] [Google Scholar]
- Faber H. R., Matthews B. W. A mutant T4 lysozyme displays five different crystal conformations. Nature. 1990 Nov 15;348(6298):263–266. doi: 10.1038/348263a0. [DOI] [PubMed] [Google Scholar]
- Gilmanshin R. I., Ptitsyn O. B. An early intermediate of refolding alpha-lactalbumin forms within 20 ms. FEBS Lett. 1987 Nov 2;223(2):327–329. doi: 10.1016/0014-5793(87)80313-7. [DOI] [PubMed] [Google Scholar]
- Go N., Abe H. Noninteracting local-structure model of folding and unfolding transition in globular proteins. I. Formulation. Biopolymers. 1981 May;20(5):991–1011. doi: 10.1002/bip.1981.360200511. [DOI] [PubMed] [Google Scholar]
- Godzik A., Skolnick J., Kolinski A. Simulations of the folding pathway of triose phosphate isomerase-type alpha/beta barrel proteins. Proc Natl Acad Sci U S A. 1992 Apr 1;89(7):2629–2633. doi: 10.1073/pnas.89.7.2629. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goldenberg D. P., Creighton T. E. Energetics of protein structure and folding. Biopolymers. 1985 Jan;24(1):167–182. doi: 10.1002/bip.360240114. [DOI] [PubMed] [Google Scholar]
- Gratzer W. B., Beaven G. H. Relation between conformation and association state. A study of the association equilibrium of glucagon. J Biol Chem. 1969 Dec 25;244(24):6675–6679. [PubMed] [Google Scholar]
- Haas E., Wilchek M., Katchalski-Katzir E., Steinberg I. Z. Distribution of end-to-end distances of oligopeptides in solution as estimated by energy transfer. Proc Natl Acad Sci U S A. 1975 May;72(5):1807–1811. doi: 10.1073/pnas.72.5.1807. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hammes G. G., Schullery S. E. Structure of macromolecular aggregates. I. Aggregation-induced conformational changes in polypeptides. Biochemistry. 1968 Nov;7(11):3882–3887. doi: 10.1021/bi00851a014. [DOI] [PubMed] [Google Scholar]
- Harding M. M., Williams D. H., Woolfson D. N. Characterization of a partially denatured state of a protein by two-dimensional NMR: reduction of the hydrophobic interactions in ubiquitin. Biochemistry. 1991 Mar 26;30(12):3120–3128. doi: 10.1021/bi00226a020. [DOI] [PubMed] [Google Scholar]
- Harrison S. C., Durbin R. Is there a single pathway for the folding of a polypeptide chain? Proc Natl Acad Sci U S A. 1985 Jun;82(12):4028–4030. doi: 10.1073/pnas.82.12.4028. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hibbard L. S., Tulinsky A. Expression of functionality of alpha-chymotrypsin. Effects of guanidine hydrochloride and urea in the onset of denaturation. Biochemistry. 1978 Dec 12;17(25):5460–5468. doi: 10.1021/bi00618a021. [DOI] [PubMed] [Google Scholar]
- Hollecker M., Larcher D. Conformational forces affecting the folding pathways of dendrotoxins I and K from black mamba venom. Eur J Biochem. 1989 Jan 15;179(1):87–94. doi: 10.1111/j.1432-1033.1989.tb14524.x. [DOI] [PubMed] [Google Scholar]
- Holley L. H., Karplus M. Protein secondary structure prediction with a neural network. Proc Natl Acad Sci U S A. 1989 Jan;86(1):152–156. doi: 10.1073/pnas.86.1.152. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Howarth O. W., Lian L. Y. Hen egg white lysozyme: carbon-13 nuclear magnetic resonance assignments and dependence of conformational flexibility on inhibitor binding and temperature. Biochemistry. 1984 Jul 17;23(15):3522–3526. doi: 10.1021/bi00310a021. [DOI] [PubMed] [Google Scholar]
- Hughson F. M., Barrick D., Baldwin R. L. Probing the stability of a partly folded apomyoglobin intermediate by site-directed mutagenesis. Biochemistry. 1991 Apr 30;30(17):4113–4118. doi: 10.1021/bi00231a001. [DOI] [PubMed] [Google Scholar]
- Jeng M. F., Englander S. W. Stable submolecular folding units in a non-compact form of cytochrome c. J Mol Biol. 1991 Oct 5;221(3):1045–1061. doi: 10.1016/0022-2836(91)80191-v. [DOI] [PubMed] [Google Scholar]
- Jennings P. A., Wright P. E. Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin. Science. 1993 Nov 5;262(5135):892–896. doi: 10.1126/science.8235610. [DOI] [PubMed] [Google Scholar]
- Kabsch W., Sander C. How good are predictions of protein secondary structure? FEBS Lett. 1983 May 8;155(2):179–182. doi: 10.1016/0014-5793(82)80597-8. [DOI] [PubMed] [Google Scholar]
- Kanehisa M. I., Tsong T. Y. Mechanism of the multiphasic kinetics in the folding and unfolding of globular proteins. J Mol Biol. 1978 Sep 5;124(1):177–194. doi: 10.1016/0022-2836(78)90155-9. [DOI] [PubMed] [Google Scholar]
- Karplus M., Weaver D. L. Protein-folding dynamics. Nature. 1976 Apr 1;260(5550):404–406. doi: 10.1038/260404a0. [DOI] [PubMed] [Google Scholar]
- Kuroda Y., Kidokoro S., Wada A. Thermodynamic characterization of cytochrome c at low pH. Observation of the molten globule state and of the cold denaturation process. J Mol Biol. 1992 Feb 20;223(4):1139–1153. doi: 10.1016/0022-2836(92)90265-l. [DOI] [PubMed] [Google Scholar]
- Kuroda Y. Residual helical structure in the C-terminal fragment of cytochrome c. Biochemistry. 1993 Feb 9;32(5):1219–1224. doi: 10.1021/bi00056a004. [DOI] [PubMed] [Google Scholar]
- Kuwajima K., Hiraoka Y., Ikeguchi M., Sugai S. Comparison of the transient folding intermediates in lysozyme and alpha-lactalbumin. Biochemistry. 1985 Feb 12;24(4):874–881. doi: 10.1021/bi00325a010. [DOI] [PubMed] [Google Scholar]
- Kuwajima K. The molten globule state as a clue for understanding the folding and cooperativity of globular-protein structure. Proteins. 1989;6(2):87–103. doi: 10.1002/prot.340060202. [DOI] [PubMed] [Google Scholar]
- Kuwajima K., Yamaya H., Miwa S., Sugai S., Nagamura T. Rapid formation of secondary structure framework in protein folding studied by stopped-flow circular dichroism. FEBS Lett. 1987 Aug 31;221(1):115–118. doi: 10.1016/0014-5793(87)80363-0. [DOI] [PubMed] [Google Scholar]
- Labhardt A. M. Kinetic circular dichroism shows that the S-peptide alpha-helix of ribonuclease S unfolds fast and refolds slowly. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7674–7678. doi: 10.1073/pnas.81.24.7674. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lee B., Richards F. M. The interpretation of protein structures: estimation of static accessibility. J Mol Biol. 1971 Feb 14;55(3):379–400. doi: 10.1016/0022-2836(71)90324-x. [DOI] [PubMed] [Google Scholar]
- Lee S. Y., Karplus M., Bashford D., Weaver D. Brownian dynamics simulation of protein folding: a study of the diffusion-collision model. Biopolymers. 1987 Apr;26(4):481–506. doi: 10.1002/bip.360260404. [DOI] [PubMed] [Google Scholar]
- Levinthal C. Molecular model-building by computer. Sci Am. 1966 Jun;214(6):42–52. doi: 10.1038/scientificamerican0666-42. [DOI] [PubMed] [Google Scholar]
- Levitt M. A simplified representation of protein conformations for rapid simulation of protein folding. J Mol Biol. 1976 Jun 14;104(1):59–107. doi: 10.1016/0022-2836(76)90004-8. [DOI] [PubMed] [Google Scholar]
- Levitt M., Chothia C. Structural patterns in globular proteins. Nature. 1976 Jun 17;261(5561):552–558. doi: 10.1038/261552a0. [DOI] [PubMed] [Google Scholar]
- Levitt M., Warshel A. Computer simulation of protein folding. Nature. 1975 Feb 27;253(5494):694–698. doi: 10.1038/253694a0. [DOI] [PubMed] [Google Scholar]
- Makhatadze G. I., Privalov P. L. Protein interactions with urea and guanidinium chloride. A calorimetric study. J Mol Biol. 1992 Jul 20;226(2):491–505. doi: 10.1016/0022-2836(92)90963-k. [DOI] [PubMed] [Google Scholar]
- Mann C. J., Matthews C. R. Structure and stability of an early folding intermediate of Escherichia coli trp aporepressor measured by far-UV stopped-flow circular dichroism and 8-anilino-1-naphthalene sulfonate binding. Biochemistry. 1993 May 25;32(20):5282–5290. doi: 10.1021/bi00071a002. [DOI] [PubMed] [Google Scholar]
- Marqusee S., Robbins V. H., Baldwin R. L. Unusually stable helix formation in short alanine-based peptides. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5286–5290. doi: 10.1073/pnas.86.14.5286. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Matouschek A., Kellis J. T., Jr, Serrano L., Bycroft M., Fersht A. R. Transient folding intermediates characterized by protein engineering. Nature. 1990 Aug 2;346(6283):440–445. doi: 10.1038/346440a0. [DOI] [PubMed] [Google Scholar]
- Mitchinson C., Baldwin R. L. The design and production of semisynthetic ribonucleases with increased thermostability by incorporation of S-peptide analogues with enhanced helical stability. Proteins. 1986 Sep;1(1):23–33. doi: 10.1002/prot.340010106. [DOI] [PubMed] [Google Scholar]
- Moult J., Unger R. An analysis of protein folding pathways. Biochemistry. 1991 Apr 23;30(16):3816–3824. doi: 10.1021/bi00230a003. [DOI] [PubMed] [Google Scholar]
- Oas T. G., Kim P. S. A peptide model of a protein folding intermediate. Nature. 1988 Nov 3;336(6194):42–48. doi: 10.1038/336042a0. [DOI] [PubMed] [Google Scholar]
- Ohgushi M., Wada A. 'Molten-globule state': a compact form of globular proteins with mobile side-chains. FEBS Lett. 1983 Nov 28;164(1):21–24. doi: 10.1016/0014-5793(83)80010-6. [DOI] [PubMed] [Google Scholar]
- Osterhout J. J., Jr, Baldwin R. L., York E. J., Stewart J. M., Dyson H. J., Wright P. E. 1H NMR studies of the solution conformations of an analogue of the C-peptide of ribonuclease A. Biochemistry. 1989 Aug 22;28(17):7059–7064. doi: 10.1021/bi00443a042. [DOI] [PubMed] [Google Scholar]
- Panijpan B., Gratzer W. B. Conformational nature of monomeric glucagon. Eur J Biochem. 1974 Jun 15;45(2):547–553. doi: 10.1111/j.1432-1033.1974.tb03580.x. [DOI] [PubMed] [Google Scholar]
- Post C. B., Brooks B. R., Karplus M., Dobson C. M., Artymiuk P. J., Cheetham J. C., Phillips D. C. Molecular dynamics simulations of native and substrate-bound lysozyme. A study of the average structures and atomic fluctuations. J Mol Biol. 1986 Aug 5;190(3):455–479. doi: 10.1016/0022-2836(86)90015-x. [DOI] [PubMed] [Google Scholar]
- Privalov P. L. Thermodynamic problems of protein structure. Annu Rev Biophys Biophys Chem. 1989;18:47–69. doi: 10.1146/annurev.bb.18.060189.000403. [DOI] [PubMed] [Google Scholar]
- Ptitsyn O. B., Pain R. H., Semisotnov G. V., Zerovnik E., Razgulyaev O. I. Evidence for a molten globule state as a general intermediate in protein folding. FEBS Lett. 1990 Mar 12;262(1):20–24. doi: 10.1016/0014-5793(90)80143-7. [DOI] [PubMed] [Google Scholar]
- Ptitsyn O. B., Rashin A. A. Samoorganizatsiia molekuly mioglobina. Dokl Akad Nauk SSSR. 1973 Nov 11;213(2):473–475. [PubMed] [Google Scholar]
- Radford S. E., Dobson C. M., Evans P. A. The folding of hen lysozyme involves partially structured intermediates and multiple pathways. Nature. 1992 Jul 23;358(6384):302–307. doi: 10.1038/358302a0. [DOI] [PubMed] [Google Scholar]
- Roder H., Elöve G. A., Englander S. W. Structural characterization of folding intermediates in cytochrome c by H-exchange labelling and proton NMR. Nature. 1988 Oct 20;335(6192):700–704. doi: 10.1038/335700a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roder H., Wüthrich K. Protein folding kinetics by combined use of rapid mixing techniques and NMR observation of individual amide protons. Proteins. 1986 Sep;1(1):34–42. doi: 10.1002/prot.340010107. [DOI] [PubMed] [Google Scholar]
- Rooman M. J., Wodak S. J. Identification of predictive sequence motifs limited by protein structure data base size. Nature. 1988 Sep 1;335(6185):45–49. doi: 10.1038/335045a0. [DOI] [PubMed] [Google Scholar]
- Rost B., Sander C. Prediction of protein secondary structure at better than 70% accuracy. J Mol Biol. 1993 Jul 20;232(2):584–599. doi: 10.1006/jmbi.1993.1413. [DOI] [PubMed] [Google Scholar]
- Sachs D. H., Schechter A. N., Eastlake A., Anfinsen C. B. An immunologic approach to the conformational equilibria of polypeptides. Proc Natl Acad Sci U S A. 1972 Dec;69(12):3790–3794. doi: 10.1073/pnas.69.12.3790. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sasaki K., Dockerill S., Adamiak D. A., Tickle I. J., Blundell T. X-ray analysis of glucagon and its relationship to receptor binding. Nature. 1975 Oct 30;257(5529):751–757. doi: 10.1038/257751a0. [DOI] [PubMed] [Google Scholar]
- Schneller W., Weaver D. L. Simulation of alpha-helix-coil transitions in simplified polyvaline: equilibrium properties and Brownian dynamics. Biopolymers. 1993 Oct;33(10):1519–1535. doi: 10.1002/bip.360331004. [DOI] [PubMed] [Google Scholar]
- Scholtz J. M., Marqusee S., Baldwin R. L., York E. J., Stewart J. M., Santoro M., Bolen D. W. Calorimetric determination of the enthalpy change for the alpha-helix to coil transition of an alanine peptide in water. Proc Natl Acad Sci U S A. 1991 Apr 1;88(7):2854–2858. doi: 10.1073/pnas.88.7.2854. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Semisotnov G. V., Rodionova N. A., Kutyshenko V. P., Ebert B., Blanck J., Ptitsyn O. B. Sequential mechanism of refolding of carbonic anhydrase B. FEBS Lett. 1987 Nov 16;224(1):9–13. doi: 10.1016/0014-5793(87)80412-x. [DOI] [PubMed] [Google Scholar]
- Serrano L., Matouschek A., Fersht A. R. The folding of an enzyme. VI. The folding pathway of barnase: comparison with theoretical models. J Mol Biol. 1992 Apr 5;224(3):847–859. doi: 10.1016/0022-2836(92)90566-3. [DOI] [PubMed] [Google Scholar]
- Shakhnovich E. I., Finkelstein A. V. Theory of cooperative transitions in protein molecules. I. Why denaturation of globular protein is a first-order phase transition. Biopolymers. 1989 Oct;28(10):1667–1680. doi: 10.1002/bip.360281003. [DOI] [PubMed] [Google Scholar]
- Shoemaker K. R., Kim P. S., Brems D. N., Marqusee S., York E. J., Chaiken I. M., Stewart J. M., Baldwin R. L. Nature of the charged-group effect on the stability of the C-peptide helix. Proc Natl Acad Sci U S A. 1985 Apr;82(8):2349–2353. doi: 10.1073/pnas.82.8.2349. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Snape K. W., Tjian R., Blake C. C., Koshland D. E. Crystallographic study of the interaction of urea with lysozyme. Nature. 1974 Jul 26;250(464):295–298. doi: 10.1038/250295a0. [DOI] [PubMed] [Google Scholar]
- States D. J., Dobson C. M., Karplus M. A new two-disulphide intermediate in the refolding of reduced bovine pancreatic trypsin inhibitor. J Mol Biol. 1984 Apr 5;174(2):411–418. doi: 10.1016/0022-2836(84)90345-0. [DOI] [PubMed] [Google Scholar]
- States D. J., Dobson C. M., Karplus M., Creighton T. E. A conformational isomer of bovine pancreatic trypsin inhibitor protein produced by refolding. Nature. 1980 Aug 7;286(5773):630–632. doi: 10.1038/286630a0. [DOI] [PubMed] [Google Scholar]
- Strynadka N. C., James M. N. Lysozyme revisited: crystallographic evidence for distortion of an N-acetylmuramic acid residue bound in site D. J Mol Biol. 1991 Jul 20;220(2):401–424. doi: 10.1016/0022-2836(91)90021-w. [DOI] [PubMed] [Google Scholar]
- Tanford C. Protein denaturation. Adv Protein Chem. 1968;23:121–282. doi: 10.1016/s0065-3233(08)60401-5. [DOI] [PubMed] [Google Scholar]
- Tsong T. Y., Baldwin R. L., Elson E. L. Properties of the refolding and unfolding reactions of ribonuclease A. Proc Natl Acad Sci U S A. 1972 Jul;69(7):1809–1812. doi: 10.1073/pnas.69.7.1809. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Udgaonkar J. B., Baldwin R. L. NMR evidence for an early framework intermediate on the folding pathway of ribonuclease A. Nature. 1988 Oct 20;335(6192):694–699. doi: 10.1038/335694a0. [DOI] [PubMed] [Google Scholar]
- Wright P. E., Dyson H. J., Lerner R. A. Conformation of peptide fragments of proteins in aqueous solution: implications for initiation of protein folding. Biochemistry. 1988 Sep 20;27(19):7167–7175. doi: 10.1021/bi00419a001. [DOI] [PubMed] [Google Scholar]
- Yapa K., Weaver D. L., Karplus M. Beta-sheet coil transitions in a simple polypeptide model. Proteins. 1992 Mar;12(3):237–265. doi: 10.1002/prot.340120304. [DOI] [PubMed] [Google Scholar]
- Zhang X., Mesirov J. P., Waltz D. L. Hybrid system for protein secondary structure prediction. J Mol Biol. 1992 Jun 20;225(4):1049–1063. doi: 10.1016/0022-2836(92)90104-r. [DOI] [PubMed] [Google Scholar]