Role of local sequence in the folding of cellular retinoic acid binding protein I: Structural propensities of reverse turns

Biochemistry

Volumn 42, Issue 26, 2003, Pages 7976-7985

  Rotondi, Kenneth S ^a   Gierasch, Lila M ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTRACELLULAR LIPID BINDING PROTEINS;

CONFORMATIONS; LIPIDS; ORGANIC ACIDS; PROTEINS;

BIOCHEMISTRY;

CELLULAR RETINOIC ACID BINDING PROTEIN 1; LIPID BINDING PROTEIN; RETINOIC ACID BINDING PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CIRCULAR DICHROISM; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; CIRCULAR DICHROISM; CONSERVED SEQUENCE; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; RECEPTORS, RETINOIC ACID; SPECTROPHOTOMETRY, ULTRAVIOLET;

EID: 0038385501     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi034304k     Document Type: Article

References (61)

1. Baldwin, R. L. (1989) How does protein folding get started? Trends Biochem. Sci. 14, 291-294.
2. Dill, K. A., Fiebig, K. M., and Chan, H. S. (1993) Cooperativity in protein folding kinetics, Proc. Natl. Acad. Sci. U.S.A. 90, 1942-1946.
3. Brockwell, D. J., Smith, D. A., and Radford, S. E. (2000) Protein folding mechanisms: New methods and emerging ideas, Curr. Opin. Struct. Biol. 10, 16-25.
4. Daggett, V., and Fersht, A. R. (2003) Is there a unifying mechanism for protein folding? Trends Biochem. Sci. 28, 18-25.
5. Dyson, H. J., and Wright, P. E. (1993) Peptide conformation and protein folding, Curr. Opin. Struct. Biol. 3, 60-65.
6. Serrano, L. (2000) The relationship between sequence and structure in elementary folding units, Adv. Protein Chem. 53, 49-85.
7. Brown, J. E., and Klee, W. A. (1971) Helix-coil transition of the isolated amino terminus of ribonuclease, Biochemistry 10, 470-476.
8. Kim, P. S., and Baldwin, R. L. (1984) A helix stop signal in the isolated S-peptide of ribonuclease A, Nature 307, 329-334.
9. Dyson, H. J., and Wright, P. E. (2002) Insights into the structure and dynamics of unfolded proteins from nuclear magnetic resonance, Adv. Protein Chem. 62, 311-340.
10. Chakrabartty, A., and Baldwin, R. L. (1995) Stability of α-helices, Adv. Protein Chem. 46, 141-176.
11. Karplus, M., and Weaver, D. L. (1994) Protein folding dynamics: The diffusion-collision model and experimental data, Protein Sci. 3, 650-669.
12. Taddei, N., Chiti, F., Fiaschi, T., Bucciantini, M., Capanni, C., Stefani, M., Serrano, L., Dobson, C. M., and Ramponi, G. (2000) Stabilisation of α-helices by site-directed mutagenesis reveals the importance of secondary structure in the transition state for acylphosphatase folding, J. Mol. Biol. 300, 633-647.
13. Myers, J. K., and Oas, T. G. (2001) Preorganized secondary structure as an important determinant of fast protein folding, Nat. Struct. Biol. 8, 552-558.
14. Schwalbe, H., Fiebig, K. M., Buck, M., Jones, J. A., Grimshaw, S. B., Spencer, A., Glaser, S. J., Smith, L. J., and Dobson, C. M. (1997) Structural and dynamical properties of a denatured protein. Heteronuclear 3D NMR experiments and theoretical simulations of lysozyme in 8 M urea, Biochemistry 36, 8977-8991.
15. Shortle, D., and Ackerman, M. S. (2001) Persistence of native-like topology in a denatured protein in 8M urea, Science 293, 487-489.
16. Capaldi, A., and Radford, S. E. (1998) Kinetic studies of β-sheet protein folding, Curr. Opin. Struct. Biol. 8, 86-92.
17. Haque, T. S., and Gellman, S. H. (1997) Insights on β-hairpin stability in aqueous solution from peptides with enforced type I′ and type II′ β-turns, J. Am. Chem. Soc. 119, 2303-2304.
18. Blanco, F., Ramírez-Alvarado, M., and Serrano, L. (1998) Formation and stability of β-hairpin structures in polypeptides, Curr. Opin. Struct. Biol. 8, 107-111.
19. McCallister, E. L., Alm, E., and Baker, D. (2000) Critical role of β-hairpin formation in protein G folding, Nat. Struct. Biol. 7, 669-673.
20. Kortemme, T., Kelly, M. J., Kay, L. E., Forman-Kay, J., and Serrano, L. (2000) Similarities between the spectrin SH3 domain denatured state and its folding transition state, J. Mol. Biol. 297, 1217-1229.
21. Nauli, S., Kuhlman, B., and Baker, D. (2001) Computer-based redesign of a protein folding pathway, Nat. Struct. Biol. 8, 602-605.
22. Banaszak, L., Winter, N., Xu, Z., Bernlohr, D. A., Cowan, S., and Jones, T. A. (1994) Lipid-binding proteins: a family of fatty acid and retinoid transport proteins, Adv. Protein Chem. 45, 89-151.
23. Kleywegt, G. J., Bergfors, T., Senn, H., Le Motte, P., Gsell, B., Shudo, K., and Jones, T. A. (1994) Crystal structures of cellular retinoic acid binding proteins I and II in complex with all-trans-retinoic acid and a synthetic retinoid, Structure 2, 1241-1258.
24. Clark, P. L., Liu, Z.-P., Zhang, J., and Gierasch, L. M. (1996) Intrinsic tryptophans of CRABPI as probes of structure and folding, Protein Sci. 5, 1108-1117.
25. Clark, P. L., Liu, Z.-P., Rizo, J., and Gierasch, L. M. (1997) Cavity formation before stable hydrogen bonding in the folding of a β-clam protein, Nat. Struct. Biol. 4, 883-886.
26. Gierasch, L. M., Rotondi, K. S., Gunasekaran, K., Habink, J. A., and Hagler, A. T. (2001) Local and long-range sequence contributions to the folding of a predominantly β-sheet protein, in Proceedings of the Seventeenth American Peptide Symposium (Lebl, M., and Houghten, R. A., Eds.) pp 391-393, The American Peptide Society, San Diego.
27. Rose, G. D., Gierasch, L. M., and Smith, J. A. (1985) Turns in peptides and proteins, Adv. Protein Chem. 37, 1-109.
28. Sibanda, B. L., Blundell, T. L., and Thornton, J. M. (1989) Conformation of β-hairpins in protein structures: A systematic classification with applications to modeling by homology, electron density fitting and protein engineering, J. Mol. Biol. 206, 759-777.
29. Rotondi, K. S., Rotondi, L. F., and Gierasch, L. M. (2003) Native structural propensity in cellular retinoic acid binding protein I 64-88: The role of locally encoded structure in the folding of a β-barrel protein, Biophys. Chem. 100, 421-436.
30. Merrifield, R. B. (1963) Solid phase synthesis of linear peptides, J. Am. Chem. Soc. 85, 2149-2154.
31. Bothner-By, A. A., Stephens, R. L., Lee, J.-M., Warren, C. D., and Jeanloz, R. W. (1984) The CAMELSPIN-experiment (cross-relaxation appropriate of minimolecules emulated by locked spins), J. Am. Chem. Soc. 106, 811-813.
32. Bax, A., and Davis, D. G. (1985) MLEV-17 based two-dimensional homonuclear magnetization transfer spectroscopy, J. Magn. Reson. 65, 355-360.
33. Bax, A., and Davis, D. G. (1985) Practical aspects of two-dimensional transverse NOE spectroscopy, J. Magn. Reson. 63, 207-213.
34. Williamson, M. P. (1990) Secondary-structure dependent chemical shifts in proteins, Biopolymers 29, 1423-1431.
35. 15N resonance assignments and secondary structure of cellular retinoic acid binding protein with and without bound ligand, J. Biomol. NMR 4, 741-760.
36. Smith, L. J., Feibig, K. M., Schwalbe, H., and Dobson, C. M. (1996) The concept of a random coil. Residual structures in peptides and denatured proteins, Folding Des. 1, R95-R106.
37. Smith, L. J., Bolin, K. A., Schwalbe, H., MacArthur, M. W., Thomton, J. M., and Dobson, C. M. (1996) Analysis of main chain torsion angles in proteins: Prediction of NMR coupling constants for native and random coil conformations, J. Mol. Biol. 255, 494-506.
38. Wishart, D. S., Sykes, B. D., and Richards, F. M. (1991) Relationship between nuclear magnetic resonance chemical shift and protein secondary structure, J. Mol. Biol. 222, 311-333.
39. Wishart, D. S., Sykes, B. D., and Richards, F. M. (1992) The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy, Biochemistry 31, 1647-1651.
40. Cierpicki, T., and Otlewski, J. (2001) Amide proton temperature coefficients as hydrogen bond indicators in proteins, J. Biomol. NMR 21, 249-261.
41. Cierpicki, T., Zhukov, I., Byrd, R. A., and Otlewski, J. (2002) Hydrogen bonds in human ubiquitin reflected in temperature coefficients of amide protons, J. Magn. Reson. 157, 178-180.
42. Andersen, N. H., Neidigh, J. W., Harris, S. M., Lee, G. M., Liu, Z., and Tong, H. (1997) Extracting information from the temperature gradients of polypeptide NH chemical shifts. 1. The importance of conformational averaging, J. Am. Chem. Soc. 119, 8547-8561.
43. Dyson, H. J., Rance, M., Houghten, R. A., Wright, P. E., and Lerner, R. A. (1988) Folding of immunogenic peptide fragments of proteins in water solution: II. The nascent helix, J. Mol. Biol. 201, 201-217.
44. Woody, R. W. (1985) Circular dichroism of peptides, in The Peptides: Analysis, Synthesis, Biology (Udenfriend, S., and Meienhofer, J., Eds.) pp 15-114, Harcourt Brace Jovanovich, New York.
45. Wüthrich, K. (1986) NMR of proteins and nucleic acids, John Wiley and Sons, New York.
46. Ramírez-Alvarado, M., Blanco, F. J., and Serrano, L. (1996) De novo design and structural analysis of a model β-hairpin peptide system, Nat. Struct. Biol. 3, 604-612.
47. 1H NMR chemical shifts, J. Am. Chem. Soc. 124, 14903-14909.
48. Shortle, D. (2002) The expanded denatured state: An ensemble of conformations trapped in a locally encoded topological space, Adv. Protein Chem. 62, 1-23.
49. Sukumar, M., and Gierasch, L. M. (1997) Local interactions in a Schellman motif dictate interhelical arrangement in a protein fragment, Folding Des. 2, 211-222.
50. Gunasekaran, K., Hagler, A. T., and Gierasch, L. M. (2003) Sequence and structural analysis of cellular retinoic acid binding proteins reveals a network of conserved hydrophobic interactions, Proteins: Struct., Funct., Genet. (in press).
51. Kim, K., Ramanathan, R., and Frieden, C. (1997) Intestinal fatty acid binding protein: A specific residue in one turn appears to stabilize the native structure and be responsible for slow refolding, Protein Sci. 6, 364-372.
52. Kim, K., and Frieden, C. (1998) Turn scanning by site-directed mutagenesis: Application to the protein folding problem using the intestinal fatty acid binding protein, Protein Sci. 7, 1821-1828.
53. 19F NMR, Proc. Natl. Acad. Sci. U.S.A. 89, 7222-7226.
54. Blanco, F., and Serrano, L. (1995) Folding of protein G B1 domain studied by the conformational characterization of fragments comprising its secondary structure elements, Eur. J. Biochem. 230, 634-649.
55. Ramírez-Alvarado, M., Serrano, L., and Blanco, F. (1997) Conformational analysis of peptides corresponding to all the secondary structure elements of protein L B1 domain: Secondary structure propensities are not conserved in proteins with the same fold, Protein Sci. 6, 162-174.
56. Blanco, F. J., Jimenez, M. A., Herranz, J., Rico, M., Santoro, J., and Nieto, J. L. (1993) NMR evidence of a short linear peptide that folds into a β-hairpin in aqueous solution, J. Am. Chem. Soc. 115, 5887-5888.
57. Ilyina, E., Milius, R., and Mayo, K. H. (1994) Synthetic peptides probe folding initiation sites in platelet factor-4: Stable chain reversal found within the hydrophobic sequence LIATLKNGRKISL, Biochemistry 33, 13436-13444.
58. Searle, M. S., Dudley, H. W., and Packman, L. C. (1995) A short linear peptide derived from the N-terminal sequence of ubiquitin folds into a water-stable non-native β-hairpin, Nat. Struct. Biol. 2, 999-1006.
59. de Alba, E., Jiménez, M. A., and Rico, M. (1997) Turn residue sequence determines β-hairpin conformation in designed peptides, J. Am. Chem. Soc. 119, 175-183.
60. Chen, P. Y., Gopalacushina, B. G., Yang, C. C., Chan, S. I., and Evans, P. A. (2001) The role of a β-bulge in the folding of the β-hairpin structure in ubiquitin, Protein Sci. 10, 2063-2074.
61. Richardson, J. S., and Richardson, D. C. (2002) Natural β-sheet proteins use negative design to avoid edge-to-edge aggregation, Proc. Natl. Acad. Sci. U.S.A. 99, 2754-2759.