Folding mechanism of three structurally similar β-sheet proteins

Proteins: Structure, Function and Genetics

Volumn 33, Issue 1, 1998, Pages 107-118

  Burns, Lora L ^a   Dalessio, Paula M ^a   Ropson, Ira J ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

sheet proteins; Folding intermediates; Protein folding; Stopped flow kinetics; Structural homology

Indexed keywords

AMINO ACID SEQUENCE; ARTICLE; CONFORMATIONAL TRANSITION; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; CARRIER PROTEINS; CIRCULAR DICHROISM; FATTY ACID-BINDING PROTEINS; KINETICS; MICE; MOLECULAR SEQUENCE DATA; MYELIN P2 PROTEIN; NEOPLASM PROTEINS; NERVE TISSUE PROTEINS; PROTEIN CONFORMATION; PROTEIN FOLDING; RATS; RECEPTORS, RETINOIC ACID; RECOMBINANT FUSION PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 0032190351     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0134(19981001)33:1<107::AID-PROT10>3.0.CO;2-P     Document Type: Article

References (58)

1. Dill, K.A., Chan, H.S. From Levinthal to pathways to funnels. Nature Struct. Biol. 4:10-19, 1997.
2. Fersht, A.R. Nucleation mechanisms in protein folding. Curr. Opin. Struct. Biol. 7:3-9, 1997.
3. Matthews, C.R. Pathways of protein of folding. Ann. Rev. Biochem. 62:653-683, 1993.
4. Miranker, A.D., Dobson, C.M. Collapse and cooperativity in protein folding. Curr. Opin. Struct. Biol. 6:31-42, 1996.
5. Levinthal, C. Are there pathways for protein folding? J. Chim. Phys. 65:44-45, 1968.
6. Banaszak, L., Winter, N., Xu, Z., Bernlohr, D.A., Cowan, S., Jones, T.A. Lipid-binding proteins: A family of fatty acid and retinoid transport proteins. Adv. Protein Chem. 45:89-151, 1994.
7. Gordon, J.I., Sacchettini, J.C., Ropson, I.J., Frieden, C., Li, E., Rubin, D.C., Roth, K.A., Cistola, D.P. Intracellular fatty-acid-binding proteins and their genes: Useful models for diverse biological questions. Curr. Opin. Lipidol. 2:125-137, 1991.
8. Ropson, I.J., Gordon, J.I., Frieden, C. Folding of a predominantly β-structure protein: Rat intestinal fatty acid binding protein. Biochemistry 29:9591-9599, 1990.
9. 19F NMR. Proc. Natl. Acad. Sci. U.S.A. 89:7222-7226, 1992.
10. Frieden, C., Hoeltzli, S.D., Ropson, I.J. NMR and protein folding: Equilibrium and stopped-flow studies. Prot. Sci. 2:2007-2014, 1993.
11. Jiang, N., Frieden, C. Characterization of mutant proteins containing inserted cysteine residues. Biochemistry 32: 11015-11021, 1993.
12. Frieden, C., Jiang, N., Cistola, D.P. Intestinal fatty acid binding protein: Folding of fluorescein-modified proteins. Biochemistry 34:2724-2730, 1995.
13. Cistola, D.P., Kim, K., Rogl, H., Frieden, C. Fatty acid interactions with a helix-less variant of intestinal fatty acid-binding protein. Biochemistry 35:7559-7565, 1996.
14. Kim, K., Cistola, D.P., Frieden, C. Intestinal fatty acid binding protein: The structure and stability of a helix-less variant. Biochemistry 35:7553-7558, 1996.
15. Ropson, I.J., Dalessio, P.M. Fluorescence spectral changes during the folding of intestinal fatty-acid binding protein. Biochemistry 36:8594-8601. 1997.
16. Kim, K., Ramanathan, R., Frieden, C. Intestinal fatty acid binding protein: A specific residue in one turn appears to stabilize the native structure and be responsible for slow folding. Prot. Sci. 6:364-372, 1997.
17. Zhang, J., Liu, Z.P., Jones, A., Gierasch, L.M., Sambrook, J.F. Mutating the charged residues in the binding pocket of cellular retinoic acid-binding protein simultaneously reduces its binding affinity to retinoic acid and increases its thermostability. Proteins 13:87-99, 1992.
18. Liu, Z.P., Riao, J., Gierasch, L.M. Equilibrium folding studies of cellular retinoic acid binding protein, a predominantly β-sheet protein. Biochemistry 33:134-142, 1994.
19. Clark, P.L., Liu, Z.P., Zhang, J., Gierasch, L.M. Intrinsic tryptophans of CRABP I as probes of structure and folding. Prot. Sci. 5:1108-1117, 1996.
20. Sacchettini, J.C., Banaszak, L.J., Gordon, J.I. Expression of rat intestinal fatty acid binding protein in E. coli and its subsequent structural analysis: A model for studying the molecular details of fatty acid-protein interaction. Mol. Cell. Biochem. 98:81-93, 1990.
21. Norris, A.W., Cheng, L., Giguére, V., Rosenberger, M., Li, E. Measurement of subnanomolar retinoic acid binding affinities for cellular retinoic acid binding proteins by fluorometric titration. Biochim. Biophys. Acta 1209:10-18, 1994.
22. Li, E., Locke, B., Yang, N.C., Ong, D.E., Gordon, J.I. Characterization of rat cellular retinol-binding protein II expressed in Escherichia coli. J. Biol. Chem. 262:13773-13779, 1987.
23. Glatz, J.F.C., Veerkamp, J.H. A radiochemical procedure for the assay of fatty acid binding by proteins. Anal. Biochem. 132:89-95, 1983.
24. Pace, C.N., Vajdos, F., Fee, L., Grimsley, G., Gray, T. How to measure and predict the molar absorption coefficient of a protein. Prot. Sci. 4:2411-2423, 1995.
25. Pace, C.N. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 131:266-280, 1986.
26. Eisenhaber, F., Argos, P. Improved strategy in analytic surface calculation for molecular systems: Handling of singularities and computational efficiency. J. Comp. Chem. 14:1272-1280, 1993.
27. Santoro, M.M., Bolen, D.W. Unfolding free energy changes determined by the linear extrapolation method: Unfolding of phenylmethanesulfonyl α-chymotrypsin using different denaturants. Biochemistry 27:8063-8068, 1988.
28. Mannervik, B. Regression analysis, experimental error, and statistical criteria in the design and analysis of experiments for discrimination between rival kinetic models. Methods Enzymol 87:370-390, 1982.
29. Motulsky, H.J., Ransnas, L.A. Fitting curves to data using nonlinear regression: A practical and nonmathematical review. FASEB J. 1:365-374, 1987.
30. 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 32:5282-5290, 1993.
31. Hodsdon, M.E., Cistola, D.P. Discrete backbone disorder in the NMR solution structure of apo intestinal fatty acid-binding protein: Implications for the mechanism of ligand entry. Biochemistry 36:1450-1460, 1997.
32. Johnson, W.C. Secondary structure of proteins through circular dichroism spectroscopy. Ann. Rev. Biophys. Biophys. Chem. 17:145-166, 1988.
33. Silow, M., Oliveberg, M. Transient aggregates in protein folding are easily mistaken for folding intermediates. Proc. Natl. Acad. Sci. U.S.A. 94:6084-6086, 1997.
34. Stackhouse, T.M., Onuffer, J.J., Matthews, C.R., Ahmed, S.A., Miles, E.W. Folding of homologous proteins: Conservation of the folding mechanism of the α subunit of tryptophan synthase from Escherichia coli, Salmonella typhimurium, and five interspecies hybrids. Biochemistry 27:824-832, 1988.
35. Hooke, S.D., Radford, S.E., Dobson, C.M. The refolding of human lysozyme: A comparison with the structurally homologous hen lysozyme. Biochemistry 33:5867-5876, 1994.
36. Kragelund, B.B., Hojrup, P., Jensen, M.S., Schjerling, C.K., Juul, E., Knudsen, J., Poulsen, F.M. Fast and one-step folding of closely and distantly related homologous pro-teins of a four-helix bundle family. J. Mol. Biol. 256:187-200, 1996.
37. Lang, K., Wrba, A., Krebs, H., Schmid, F.X., Beintema, J.J. Folding kinetics of mammalian ribonucleases. FEBS Lett. 204:135-139, 1986.
38. Hollecker, M., Creighton, T.E. Evolutionary conservation and variation of protein folding pathways: Two protease inhibitor homologues from black mamba venom. J. Mol. Biol. 168:409-437, 1983.
39. Woody, R.W. Circular dichroism. Methods Enzymol. 246:34-71, 1996.
40. Borén, K., Freskgård. P.O., Carlsson, U. A comparative CD study of carbonic anhydrase isozymes with different number of tryptophans: Impact on calculation of secondary structure content. Prot. Sci. 5:2479-2484, 1996.
41. Vuilleumier, S., Sancho, J., Loewenthal, R., Fersht, A.R. Circular dichroism studies of barnase and its mutants: Characterization of the contribution of aromatic side chains. Biochemistry 32:10303-10313, 1993.
42. Permyakov, E.A. "Luminescent Spectroscopy of Proteins." Boca Raton, Florida: CRC Press, 1993.
43. Locke, B.C., MacInnis, J.M., Qian, S., Gordon, J.I., Li, E., Fleming, G.R., Yang, N.C. Fluorescence studies of rat cellular retinol binding protein II produced in Escherichia coli: An analysis of four tryptophan substitution mutants. Biochemistry 31:2376-2383, 1992.
44. Lumry, R., Biltonen, R., Brandts, J.F. Validity of the two-state hypothesis for conformational transitions of proteins. Biopolymers 4:917-944, 1966.
45. Privalov, P.L. Stability of proteins: Small globular proteins. Adv. Protein Chem. 33:167-241, 1979.
46. Myers, J.K., Pace, C.N., Scholtz, J.M. Denaturant m values and heat capacity changes: Relation to changes in accessible surface areas of protein unfolding. Prot. Sci. 4:2138-2148, 1995.
47. Shortle, D. Staphylococcal nuclease: A showcase of m-value effects. Adv. Protein Chem. 46:217-247, 1995.
48. Goldenberg, D.P. Genetic studies of protein stability and mechanisms of folding. Ann. Rev. Biophys. Biophys. Chem. 17:481-507, 1988.
49. Zaidi, F.N., Nath, U., Udgaonaker, J.B. Multiple intermediates and transition states during protein unfolding. Nat. Struct. Biol. 4:1016-1024, 1997.
50. Kuwajima, K. The molten globule state as a clue for understanding the folding and cooperativity of globular-protein structure. Proteins 6:87-103, 1989.
51. Dalessio, P.M., Ropson, I.J. pH dependence of the folding of intestinal fatty-acid binding protein. Arch. Biochem. Biophys., in press.
52. Sosnick, T.R., Shtilerman, M.D., Mayne, L., Englander, S.W. Ultrafast signals in protein folding and the polypeptide contracted state. Proc. Natl. Acad. Sci. U.S.A. 94:8545-8550, 1997.
53. Clark, P.L., Liu, Z.P., Rizo, J., Gierasch, L.M. Cavity formation before stable hydrogen bonding in the folding of a β-clam protein. Nat. Struct. Biol. 4:883-886, 1997.
54. Nall, B.T. Proline isomerization as a rate-limiting step. In Pain, R.H. (ed): Mechanisms of Protein Folding." New York: Oxford University Press, 1994:80-99.
55. Khorasanizadeh, S., Peters, I.D., Butt, T.R., Roder, H. Stability and folding of a tryptophan-containing mutant of ubiquitin. Biochemistry 32:7054-7063, 1993.
56. Winter, N.S., Bratt, J.M., Banaszak, L.J. Crystal structures of holo and apo-cellular retinol-binding protein II. J. Mol. Biol. 230:1247-1259, 1993.
57. Thompson, J.R., Bratt, J.M., Banaszak, L.J. Crystal structure of cellular retinoic acid binding protein 1 shows increased access to the binding cavity due to formation of an intermolecular β-sheet. J. Mol. Biol. 252:433-446, 1995.
58. Scapin, G., Gordon, J.I., Sacchettini, J.C. Refinement of the structure of recombinant rat intestinal fatty-acid binding apoprotein at 1.2 Å resolution. J. Biol. Chem. 267:4253-4269, 1992.