Nonnative intermediate state of acid-stable β-sheet protein

Cell Biochemistry and Biophysics

Volumn 33, Issue 3, 2000, Pages 253-273

  Yang, Jenny J ^a   Carroll, Amy R ^a   Yang, Wei ^b   Ye, Yiming ^a   Nguyen, Christina N ^a  

^a Center for Drug Design   (United States)

^b GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Flexibility of CD2; Nuclear magnetic resonance (NMR); Spectroscopy; Tryptophan

Indexed keywords

CD2 ANTIGEN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CELL ADHESION; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PH; PROTEIN FOLDING; RAT; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD2; CELL ADHESION; HYDROGEN-ION CONCENTRATION; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; PROTEIN FOLDING; RATS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 0034574238     PISSN: 10859195     EISSN: None     Source Type: Journal    
DOI: 10.1385/CBB:33:3:253     Document Type: Article

References (80)

1. Wang, J. H., Smolyar, A., Tan, K., Liu, J. H., Kim, M., Sun, Z. Y., Wagner, G., and Reinherz, E. L. (1999) Structure of a heterophilic adhesion complex between the human CD2 and CD58 (LFA-3) counterreceptors. Cell 97, 791-803.
2. Li, J., Smolyar, A., Sunder-Plassmann, R., and Reinherz, E. L. (1996) Ligand-induced conformational change within the CD2 ectodomain accompanies receptor clustering: implication for molecular lattice formation. J. Mol. Biol. 263, 209-226.
3. Wyss, D. F., Dayie, K. T., and Wagner, G. (1997) The Counterreceptor binding site of human CD2 exhibits an extended surface patch with multiple conformations fluctuating with millisecond to microsecond motions. Protein Sci. 6, 534-542.
4. Chothia, C., Lesk, A. M., Tramontano, A., Levitt, M., Smith-Gill, S. J., Air, G., Sheriff, S., Padlan, E. A., Davies, D., Tulip, W. R., et al. (1989) Conformations of immunoglobulin hypervariable regions. Nature 342, 877-883.
5. Al-Lazikani, B., Lesk, A. M., and Chothia, C. (1997) Standard conformations for the canonical structures of immunoglobulins. J. Mol. Biol. 273, 927-948.
6. Wu, T. T. and Kabat, E. A. (1970) An Analysis of the sequences of the variable regions of Bence Jones proteins and myeloma light chains and their implications for antibody complementarity. J. Exp. Med. 132, 211-250.
7. McAlister, M. S., Mott, H. R., van der Merwe, P. A., Campbell, I. D., Davis, S. J., and Driscoll, P. C. (1996) NMR analysis of interacting soluble forms of the cell-cell recognition molecules CD2 and CD48. Biochemistry 35, 5982-5991.
8. Shapiro, L., Fannon, A. M., Kwong, P. D., Thompson, A., Lehmann, M., Grubel, S. G., Legrand, J. F., Als-Nielsen, J., Colman, D. R., and Hendrickson, W. A. (1995) Structural basis of cell-cell adhesion by cadherins. Nature 374, 327-337.
9. Smith, D. K., and Xue, H. (1997) Sequence profiles of immunoglobulin and immunoglobulin-like domains. J. Mol. Biol. 274, 530-545.
10. Erickson, H. P. (1994) Reversible unfolding of fibronectin type III and immunoglobulin domains provides the structural basis for stretch and elasticity of titin and fibronectin. Proc. Natl. Acad. Sci. USA 91, 10414-10,118.
11. Koide, A., Bailey, C. W., Huang, X., and Koide, S. (1998) The Fibronectin type III domain as a scaffold for novel binding proteins. J. Mol. Biol. 284, 1141-1151.
12. Plaxco, K. W., Spitzfaden, C., Campbell, I. D., and Dobson, C. M. (1997) A Comparison of the folding kinetics and thermodynamics of two homologous fibronectin type III modules. J. Mol. Biol. 270, 763-770.
13. Bodian, D. L., Jones, E. Y., Harlos, K., Stuart, D. I., and Davis, S. J. (1994) Crystal structure of the extracellular region of the human cell adhesion molecule CD2 at 2.5 Å resolution. Structure 2, 755-766.
14. Wyss, D. F., Choi, J. S., Li, J., Knoppers, M. H., Willis, K. J., Arulanandam, A. R., Smolyar, A., Reinherz, E. L., and Wagner, G. (1995) Conformation and function of the N-linked glycan in the adhesion domain of human CD2. Science 269, 1273-1278.
15. Davis, S. J., Davies, E. A., and van der Merwe, P. A. (1995) Mutational analysis of the epitopes recognized by anti-(rat CD2) and anti-(rat CD48) monoclonal antibodies. Biochem. Soc. Trans. 23, 188-194.
16. Recny, M. A., Neidhardt, E. A., Sayre, P. H., Ciardelli, T. E., and Reinherz, E. L. (1990) Structural and functional characterization of the CD2 immunoadhesion domain. Evidence for inclusion of CD2 in an alpha-beta protein folding class. J. Biol. Chem. 265, 8542-8549.
17. Driscoll, P. C., Cyster, J. G., Campbell, I. D., and Williams, A. F. (1991) Structure of domain 1 of rat T lymphocyte CD2 antigen. Nature 353, 762-765.
18. Davis, S. J. and van der Merge, P. A. (1996) The Structure and ligand interactions of CD2: implications for T-cell function. Immunol. Today 17, 177-187.
19. Jones, E. Y., Davis, S. J., Williams, A. F., Harlos, K., and Stuart, D. I. (1992) Crystal structure at 2.8 A resolution of a soluble form of the cell adhesion molecule CD2. Nature 360, 232-239.
20. Meuer, S. C., Hussey, R. E., Fabbi, M., Fox, D., Acuto, O., Fitzgerald, K. A., Hodgdon, J. C., Protentis, J. P., Schlossman, S. F., and Reinherz, E. L. (1984) An alternative pathway of T-cell activation: a functional role for the 50 kd T11 sheep erythrocyte receptor protein. Cell 36, 897-906.
21. Rouleau, M., Bernard, A., Lantz, O., Vernant, J. P., Charpentier, B., and Senik, A. (1993) Apoptosis of activated CD8+/CD57+ T cells is induced by some combinations of anti-CD2 mAb. J. Immunol. 151, 3547-3556.
22. Murray, A. J., Lewis, S. J., Barclay, A. N., and Brady, R. L. (1995) One sequence, two folds: a metastable structure of CD2. Proc. Natl. Acad. Sci. USA 92, 7337-7341.
23. Murray, A. J., Head, J. G., Barker, J. J., and Brady, R. L. (1998) Engineering an intertwined form of CD2 for stability and assembly. Nat. Struct. Biol. 5, 778-782.
24. Hayes, M. V., Sessions, R. B., Brady, R. L., and Clarke, A. R. (1999) Engineered assembly of intertwined oligomers of an immunoglobulin chain. J. Mol. Biol. 285, 1857-1867.
25. Parker, M. J., Dempsey, C. E., Hosszu, L. L., Waltho, J. P., and Clarke, A. R. (1998) Topology, sequence evolution and folding dynamics of an immunoglobulin domain. Nat. Struct. Biol. 5, 194-198.
26. Yang, J. J., Yang, H., Ye, Y., Hopkins, H., and Hastings, G. Formation of a non-native intermediate of an all beta-sheet protein: domain 1 of CD2. Protein Science, submitted
27. Bychkova, V. E. and Ptitsyn, O. B. (1993) The molten globule in vitro and in vivo. Chemtracts Biochem. Mol. Biol. 4, 133-163.
28. Ptitsyn, O. B., Bychkova, V. E., and Uversky, V. N. (1995) Kinetic and equilibrium folding intermediates. Philos. Trans. R. Soc. Lond B Biol. Sci. 348, 35-41.
29. Landau, L. D. and Lifshits, E. M. (1982) Theoretical physics. Electrodynamics Continuous Media 8, 60.
30. Uversky, V. N., Narizhneva, N. V., Kirschstein, S. O., Winter, S., and Lober, G. (1997) Conformational transitions provoked by organic solvents in beta-lactoglobulin: Can a molten globule like intermediate be induced by the decrease in dielectric constant? Fold Des. 2, 163-172.
31. Buck, M. (1998) Trifluoroethanol and colleagues: cosolvents come of age. Recent studies with peptides and proteins. Q. Rev. Biophys. 3, 297-355.
32. Zhong, L. and Johnson, W. C., Jr. (1992) Environment affects amino acid preference for secondary structure. Proc. Natl. Acad. Sci. USA 89, 4462-4465.
33. Piotto, M., Saudek, V., and Sklenar, V. (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR 2, 661-665.
34. Kay, L. E. (1995) Field gradient techniques in NMR spectroscopy. Curr. Opin. Struct. Biol. 5, 674-681.
35. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids John Wiley, New York.
36. Woody, R. W. (1985) Circular dichroism of peptides. Peptides, 7, 15-114.
37. Yang, J. J., Buck, M., Pitkeathly, M., Kotik, M., Haynie, D. T., Dobson, C. M., and Radford, S. E. (1995) Conformational properties of four peptides spanning the sequence of hen. J. Mol. Biol. 252, 483-491.
38. 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.
39. Santoro, M. M. and Bolen, D. W. (1988) Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants. Biochemistry 27, 8063-8068.
40. Tanford, C. (1968) Protein denaturation. Adv. Prot. Chem. 23, 121-282.
41. Fink, A. L., Calciano, L. J., Goto, Y., Kurotsu, T., and Palleros, D. R. (1994) Classification of acid denaturation of proteins: intermediates and unfolded states. Biochemistry 33, 12,504-12,511.
42. Lilie, H., Jaenicke, R., and Buchner, J. (1995) Characterization of a quaternary-structured folding intermediate of an antibody Fab-fragment. Protein Sci. 4, 917-924.
43. Buchner, J., Renner, M., Lilie, H., Hinz, H. J., Jaenicke, R., Kiefhabel, T., and Rudolph, R. (1991) Alternatively folded states of an immunoglobulin. Biochemistry 30, 6922-6929.
44. Deutscher, S. L., Crider, M. E., Ringbauer, J. A., Komissarov, A. A., and Quinn, T. P. (1996) Stability studies of nucleic acid-binding Fab isolated from combinatorial bacteriophage display libraries. Arch. Biochem. Biophys. 333, 207-213.
45. Hendsch, Z. S. and Tidor, B. (1994) Do salt bridges stabilize proteins? A continuum electrostatic analysis. Protein Sci. 3, 211-226.
46. Sali, D., Bycroft, M., and Fersht, A. R. (1991) Surface electrostatic interactions contribute little to stability of barnase. J. Mol. Biol. 220, 779-788.
47. Bradley, E. K., Thomason, J. F., Cohen, F. F., Kosen, P. A., and Kuntz, I. D. (1990) Studies of synthetic helical peptides using circular dichroism and nuclear magnetic resonance. J. Mol. Biol. 215, 607-622.
48. Dill, K. A. (1990) Dominant forces in protein folding. Biochemistry 29, 7133-7155.
49. Ashikari, Y., Arata, Y., and Hamaguchi, K. (1985) pH-induced unfolding of the constant fragment of the immunoglobulin light chain: effect of reduction of the intrachain disulfide bond. J. Biochem. (Tokyo) 97, 517-528.
50. Davis, S. J., Davies, E. A., Tucknott, M. G., Jones, E. Y., and van der Merwe, P. A. (1998) The role of charged residues mediating low affinity protein-protein recognition at the cell surface by CD2. Proc. Natl. Acad. Sci. USA 95, 5490-5494.
51. Geourjon, C. and Deleage, G. (1995) SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments. Comput. Appl. Biosci. 11, 681-684.
52. Garnier, J., Gibrat, J. F., and Robson, B. (1996) GOR method for predicting protein secondary structure from amino acid sequence. Methods Enzymol. 266, 540-553.
53. Rost, B., Sander, C., and Schneider, R. (1994) PHD - an automatic mail server for protein secondary structure prediction. Comput. Appl. Biosci. 10, 53-60.
54. Yang, J. J., Pikeathly, M., and Radford, S. E. (1994) Far-UV circular dichroism reveals a conformational switch in a peptide fragment from the beta-sheet of hen lysozyme. Biochemistry 33, 7345-7353.
55. Narhi, L. O., Philo, J. S., Li, T., Zhang, M., Samal, B., and Arakawa, T. (1996) Induction of alpha-helix in the beta-sheet protein tumor necrosis factor-alpha: acid-induced denaturation. Biochemistry 35, 11,454-11,460.
56. Shiraki, K., Nishikawa, K., and Goto, Y (1995) Trifluoroethanol-induced stabilization of α-helical structure of β-lactoglobulin: implication for non-hierarchical protein folding. J. Mol. Biol. 245, 180-194.
57. Eisenberg, M., Gresalfi, T., Riccio, T., and McLaughlin, S. (1979) Adsorption of monovalent cations to bilayer membranes containing negative phospholipids. Biochemistry 18, 5213-5223.
58. Rajan, R., and Balaram, P. (1996) A model for the interaction of trifluoroethanol with peptides and proteins. Int. J. Pept. Protein. Res. 48, 328-336.
59. Yang, J. J., van den Berg, B., Pitkeathly, M., Smith, L. J., Bolin, K. A., Keiderling, T. A., Redfield, C., Dobson, C. M., and Radford, S. E. (1996) Native-like secondary structure in a peptide from the alpha-domain of hen lysozyme. Fold Des. 1, 473-484.
60. Gast, K., Zirwer, D., Muller-Frohne, M., and Damaschun, G. (1999) Trifluoroethanol-induced conformational transitions of proteins: insights gained from the differences between alpha-lactalbumin and ribonuclease A. Protein Sci. 8, 625-634.
61. 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.
62. Nelson, J. W. and Kallenbach, N. R. (1986) Stabilization of the ribonuclease S-peptide α-helix by trifluoroethanol. Proteins Struct. Funct. Genet 1, 211-217.
63. Segawa, S.-I., Fukuno, T., Fujiwara, K., and Noda, Y. (1991) Local structures in unfolded lysozyme and correlation with secondary structures in the native conformation: helix-forming or -breaking propensity of peptide segments. Biopolymers 31, 497-509.
64. Buck, M., Radford, S. E., and Dobson, C. M. (1993) A partially folded state of hen egg white lysozyme in trifluoroethanol: structural characterization and implications for protein folding. Biochemistry 32, 669-678.
65. Thomas, P. D. and Dill, K. A. (1993) Local and nonlocal interactions in globular proteins and mechanisms of alcohol denaturation. Protein Sci. 2, 2050-2065.
66. Luo, Y. and Baldwin, R. L. (1998) Trifluoroethanol stabilizes the pH 4 folding intermediate of sperm whale apomyoglobin. J. Mol. Biol. 279, 49-57.
67. Jasanoff, A. and Fersht, A. R. (1994) Quantitative determination of helical propensities from trifluoroethanol-titration curves. Biochemistry 33, 2129-2135.
68. Conio, G., Patrone, E., and Brighetti, S. (1970) The effect of aliphatic alcohols on the helix-coil transition of poly-L-ornithine and poly-L-glutamic acid. J. Biol. Chem. 245, 3335-3340.
69. Cammers-Goodwin, A., Allen, T. J., Oslick, S. L., McClure, K. F., Lee, J. H., and Kemp, D. S. (1996) Mechanism of stabilization of helical conformations of polypeptides by water containing trifluoroethanol. J. Am. Chem. Soc. 118, 3082-2090.
70. Walgers, R., Lee, T. C., and Cammers-Goodwin, A. (1998) An indirect chaotropic mechanism for the stabilization of helix conformation of peptides in aqueous trifluoroethanol and hexafluoro-2-propanol. J. Am. Chem. Soc. 120, 5073-5079.
71. Hirota, N., Mizuno, K., and Goto, Y. (1998) Group additive contributions to the alcohol-induced alpha-helix formation of melittin: implication for the mechanism of the alcohol effects on proteins. J. Mol. Biol 275, 365-378.
72. Main, E. R. and Jackson, S. E. (1999) Does trifluoroethanol affect folding pathways and can it be used as a probe of structure in transition states? Nat. Struct. Biol. 6, 831-835.
73. Bodkin, M. J. and Goodfellow, J. M. (1996) Hydrophobic solvation in aqueous trifluoroethanol solution. Biopolymers 39, 43-50.
74. Brandts, J. F. and Hunt, L. (1967) The thermodynamics of protein denaturation. 3. The denaturation of ribonuclease in water and in aqueous urea and aqueous ethanol mixtures. J. Am. Chem. Soc. 89, 4826-4838.
75. Schonbrunner, N., Wey, J., Engels, J., Georg, H., and Kiefhaber, T. (1996) Native-like beta-structure in a trifluoroethanol-induced partially folded state of the all-beta-sheet protein tendarnistat. J. Mol. Biol. 260, 432-445.
76. Privalov, P. L. and Gill, S. J. (1989) The hydrophobic effect: a reappraisal. Pure Appl. Chem. 61, 1097-1104.
77. Lorch, M., Mason, J. M., Clarke, A. R., and Parker, M. J. (1999) Effects of core mutations on the folding of a beta-sheet protein: implications for backbone organization in the I-state. Biochemistry 38, 1377-1385.
78. Kuwata, K., Hoshino, M., Era, S., Batt, C. A., and Goto, Y. (1998) alpha→beta transition of beta-lactoglobulin as evidenced by heteronuclear NMR. J. Mol. Biol. 283, 731-739.
79. Hamada, D., Kuroda, Y., Tanaka, T., and Goto, Y. (1995) High helical propensity of the peptide fragments derived from beta- lactoglobulin, a predominantly beta-sheet protein. J. Mol. Biol. 254, 737-746.
80. Fan, P., Bracken, C., and Baum, J. (1993) Structural characterization of monellin in the alcohol-denatured state by NMR: evidence for β-sheet to α-helix conversion. Biochemistry 32, 1573-1582.