A polypeptide "building block" for the β-trefoil fold identified by "top-down symmetric deconstruction"

Journal of Molecular Biology

Volumn 407, Issue 5, 2011, Pages 744-763

  Lee, Jihun ^a,c   Blaber, Sachiko I ^a   Dubey, Vikash K ^b   Blaber, Michael ^a  

^a FLORIDA STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b INDIAN INSTITUTE OF TECHNOLOGY GUWAHATI   (India)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

protein design; protein evolution; protein symmetry; top down symmetric deconstruction; trefoil

Indexed keywords

FIBROBLAST GROWTH FACTOR 1; POLYPEPTIDE; TREFOIL PEPTIDE;

AMINO ACID SEQUENCE; ARTICLE; FRAGMENTATION REACTION; MUTATION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN STABILITY; PROTEIN STRUCTURE; THERMOSTABILITY;

LOTUS;

EID: 79952735272     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.02.002     Document Type: Article

References (83)

1. DeGrado, W. F., Regan, L. & Ho, S. P (1987). The design of a four-helix bundle protein. Cold Spring Harbor Symp. Quant. Biol. 52, 521-526.
2. Regan, L. & DeGrado, W. F. (1988). Characterization of a helical protein designed from first principles. Science, 241, 976-978.
3. Richardson, J. & Richardson, D. C. (1989). The de novo design of protein structures. Trends Biochem. Sci. 14, 304-309.
4. Hecht, M. H., Richardson, J. S., Richardson, D. C. & Ogden, R. C. (1990). De novo design, expression, and characterization of Felix: a four-helix bundle protein of native-like sequence. Science, 249, 884-891.
5. Quinn, T. P., Tweedy, N. B., Williams, R. W., Richardson, J. S. & Richardson, D. C. (1994). Betadoublet: de novo design, synthesis, and characterization of a β-sandwich protein. Proc. Natl Acad. Sci. USA, 91, 8747-8751.
6. Bryson, J. W., Betz, S. F., Lu, H. S., Suich, D. J., Zhou, H. X., O'Neil, K. T. & DeGrado, W. F. (1995). Protein design: a hierarchic approach. Science, 270, 935-941.
7. Fu, X., Kono, H. & Saven, J. G. (2003). Probabilistic approach to the design of symmetric protein quaternary structures. Protein Eng. 16, 971-977. (Pubitemid 38281747)
8. Offredi, F., Dubail, F., Kischel, P., Sarinski, K., Stern, A. S., Van de Weerdt, C. et al. (2003). De novo backbone and sequence design of an idealized α/β-barrel protein: evidence of stable tertiary structure. J. Mol. Biol. 325, 163-174.
9. Tsai, H. H., Tsai, C. J., Ma, B. & Nussinov, R. (2004). In silico protein design by combinatorial assembly of protein building blocks. Protein Sci. 13, 2753-2765.
10. Heinemann, M. & Panke, S. (2006). Synthetic biology - putting engineering into biology. Bioinformatics, 22, 2790-2799.
11. Haspel, N., Wainreb, G., Inbar, Y., Tsai, H. H., Tsai, C. J., Wolfson, H. J. & Nussinov, R. (2007). A hierarchical protein folding scheme based on the building block folding model. Methods Mol. Biol. 350, 189-204.
12. He, Y., Zhou, R., Huang, Y. & Xiao, Y (2009). Foldable subunits of helix protein. Comput. Biol. Chem. 33, 325-328.
13. Armstrong, C. T., Boyle, A. L., Bromley, E. H., Mahmoud, Z. N., Smith, L., Thomson, A. R. & Woolfson, D. N. (2009). Rational design of peptide-based building blocks for nanoscience and synthetic biology. Faraday Discuss. 143, 305-317.
14. Andre, I., Bradley, P., Wang, C. & Baker, D. (2007). Prediction of the structure of symmetrical protein assemblies. Proc. Natl. Acad. Sci. USA, 104, 17656-17661.
15. Wolynes, P. G. (1996). Symmetry and the energy landscapes of biomolecules. Proc. Natl Acad. Sci. USA, 93, 14249-14255.
16. Lowe, A. R. & Itzhaki, L. S. (2007). Rational redesign of the folding pathway of a modular protein. Proc. Natl Acad. Sci. USA, 104, 2679-2684.
17. Wootton, J. C. & Federhen, S. (1993). Statistics of local complexity in amino acid sequences and sequence databases. Computers Chem. 17, 149-163.
18. Romero, P., Obradovic, Z., Li, X., Garner, E. C., Brown, C. J. & Dunker, A. K. (2001). Sequence complexity of disordered proteins. Proteins, 42, 38-48.
19. Wright, C. F., Teichmann, S. A., Clarke, J. & Dobson, C. M. (2005). The importance of sequence diversity in the aggregation and evolution of proteins. Nature, 438, 878-881. (Pubitemid 41753072)
20. Hoang, T. X., Marsella, L., Trovato, A., Seno, F., Banavar, J. R. & Maritan, A. (2006). Common attributes of native-state structures of proteins, disordered proteins, and amyloid. Proc. Natl Acad. Sci. USA, 103, 6883-6888.
21. Lee, J. & Blaber, M. (2011). Experimental support for the evolution of symmetric protein architecture from a simple peptide motif. Proc. Natl Acad. Sci. USA, 108, 126-130.
22. Blaber, S. I., Culajay, J. F., Khurana, A. & Blaber, M. (1999). Reversible thermal denaturation of human FGF-1 induced by low concentrations of guanidine hydrochloride. Biophys. J. 77, 470-477. (Pubitemid 29305243)
23. Brych, S. R., Blaber, S. I., Logan, T. M. & Blaber, M. (2001). Structure and stability effects of mutations designed to increase the primary sequence symmetry within the core region of a β-trefoil. Protein Sci. 10, 2587-2599. (Pubitemid 33091582)
24. Brych, S. R., Kim, J., Logan, T. M. & Blaber, M. (2003). Accommodation of a highly symmetric core within a symmetric protein superfold. Protein Sci. 12, 2704-2718. (Pubitemid 37445096)
25. Brych, S. R., Dubey, V. K., Bienkiewicz, E., Lee, J., Logan, T. M. & Blaber, M. (2004). Symmetric primary and tertiary structure mutations within a symmetric superfold: a solution, not a constraint, to achieve a foldable polypeptide. J. Mol. Biol. 344, 769-780.
26. Dubey, V. K., Lee, J. & Blaber, M. (2005). Redesigning symmetry-related "mini-core" regions of FGF-1 to increase primary structure symmetry: thermodynamic and functional consequences of structural symmetry. Protein Sci. 14, 2315-2323.
27. Dubey, V. K., Lee, J., Somasundaram, T., Blaber, S. & Blaber, M. (2007). Spackling the crack: stabilizing human fibroblast growth factor-1 by targeting the N and C terminus β-strand interactions. J. Mol. Biol. 371, 256-268.
28. Blaber, M., DiSalvo, J. & Thomas, K. A. (1996). X-ray crystal structure of human acidic fibroblast growth factor. Biochemistry, 35, 2086-2094. (Pubitemid 26071642)
29. Orengo, C. A., Jones, D. T. & Thornton, J. M. (1994). Protein superfamilies and domain superfolds. Nature, 372, 631-634.
30. Thornton, J. M., Orengo, C. A., Todd, A. E. & Pearl, F. M. (1999). Protein folds, functions and evolution. J. Mol. Biol. 293, 333-342.
31. Kim, C., Basner, J. & Lee, B. (2010). Detecting internally symmetric protein structures. BMC Bioinf. 11, 303-318.
32. Ghirlanda, G., Lear, J. D., Ogihara, N. L., Eisenberg, D. & DeGrado, W. F. (2002). A hierarchic approach to the design of hexameric helical barrels. J. Mol. Biol. 319, 243-253.
33. Pantoliano, M. W., Horlick, R. A., Springer, B. A., Van Dyk, D. E., Tobery, T., Wetmore, D. R. et al. (1994). Multivalent ligand-receptor binding interactions in the fibroblast growth factor system produce a cooperative growth factor and heparin mechanism for receptor dimerization. Biochemistry, 33, 10229-10248. (Pubitemid 24281788)
34. Pellegrini, L., Burke, D. F., von Delft, F., Mulloy, B. & Blundell, T. L. (2000). Crystal structure of fibroblast growth factor receptor ectodomain bound to ligand and heparin. Nature, 407, 1029-1034.
35. Schlessinger, J., Plotnikov, A. N., Ibrahimi, O. A., Eliseenkova, A. V., Yeh, B. K., Yayon, A. et al. (2000). Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol. Cell. Biol. 6, 743-750.
36. Bashkin, P., Doctrow, S., Klagsbrun, M., Svahn, C. M., Folkman, J. & Vlodavsky, I. (1989). Basic fibroblast growth factor binds to subendothelial extracellular matrix and is released by heparitinase and heparin-like molecules. Biochemistry, 28, 1737-1743. (Pubitemid 19072047)
37. Weiner, H. L. & Swain, J. L. (1989). Acidic fibroblast growth factor mRNA is expressed by cardiac myocytes in culture and the protein is localized to the extracellular matrix. Proc. Natl Acad. Sci. USA, 86, 2683-2687.
38. Chintala, S. K., Miller, R. R. & McDevitt, C. A. (1994). Basic fibroblast growth factor binds to heparan sulfate in the extracellular matrix of rat growth plate chondrocytes. Arch. Biochem. Biophys. 310, 180-186.
39. Schreiber, G., Buckle, A. M. & Fersht, A. R. (1994). Stability and function: two constraints in the evolution of barstar and other proteins. Structure, 2, 945-951.
40. Shoichet, B. K., Baase, W. A., Kuroki, R. & Matthews, B. W. (1995). A relationship between protein stability and protein function. Proc. Natl Acad. Sci. USA, 92, 452-456.
41. Beadle, B. M. & Shoichet, B. K. (2002). Structural basis of stability-function tradeoffs in enzymes. J. Mol. Biol. 321, 285-296.
42. Bloom, J. D., Wilke, C. O., Arnold, F. H. & Adami, C. (2004). Stability and the evolvability of function in a model protein. Biophys. J. 86, 2758-2764. (Pubitemid 38552682)
43. Bloom, J. D., Labthavikul, S. T., Otey, C. R. & Arnold, F. H. (2006). Protein stability promotes evolvability. Proc. Natl Acad. Sci. USA, 103, 5869-5874.
44. Tokuriki, N., Stricher, F., Serrano, L. & Tawfik, D. S. (2008). How protein stability and new functions trade off. PLoS Comput. Biol. 4, e1000002.
45. Auton, M. & Bolen, D. W. (2005). Predicting the energetics of osmolyte-induced protein folding/unfolding. Proc. Natl Acad. Sci. USA, 102, 15065-15068.
46. Argos, P. & Palau, J. (1982). Amino acid distribution in protein secondary structures. Int. J. Pept. Protein Res. 19, 380-393.
47. Padmanabhan, S., Marqusee, S., Ridgeway, T., Laue, T. M. & Baldwin, R. L. (1990). Relative helix-forming tendencies of nonpolar amino acids. Nature, 344, 268-270.
48. Blaber, M., Zhang, X. J. & Matthews, B. W. (1993). Structural basis of amino acid α helix propensity. Science, 260, 1637-1640. (Pubitemid 23247144)
49. Kim, C. A. & Berg, J. M. (1993). Thermodynamic β-sheet propensities measured using a zinc-finger host peptide. Nature, 362, 267-270.
50. Minor, D. L., Jr & Kim, P. S. (1994). Measurement of the β-sheet-forming propensities of amino acids. Nature, 367, 660-663.
51. Smith, C. K., Withka, J. M. & Regan, L. (1994). A thermodynamic scale for the β-sheet forming tendencies of the amino acids. Biochemistry, 33, 5510-5517.
52. Chaudhuri, I., Soding, J. & Lupas, A. N. (2008). Evolution of the β-propeller fold. Proteins, 71, 795-803.
53. Corey, E. J. & Cheng, X. M. (1989). The Logic of Chemical Synthesis. John Wiley & Sons, Inc., New York.
54. McLachlan, A. D. (1979). Three-fold structural pattern in the soybean trypsin inhibitor (Kunitz). J. Mol. Biol. 133, 557-563.
55. Murzin, A. G., Lesk, A. M. & Chothia, C. (1992). β-Trefoil fold patterns of structure and sequence in the Kunitz inhibitors interleukins-1β and 1α and fibroblast growth factors. J. Mol. Biol. 223, 531-543.
56. Soskine, M. & Tawfik, D. S. (2010). Mutational effects and the evolution of new protein functions. Nat. Rev. 11, 572-582.
57. Bernett, M. J., Somasundaram, T. & Blaber, M. (2004). An atomic resolution structure for human fibroblast growth factor 1. Proteins, 57, 626-634. (Pubitemid 39390817)
58. Arakawa, T., Horan, T. P., Narhi, L. O., Rees, D. C., Schiffer, S. G., Holst, P. L. et al. (1993). Production and characterization of an analog of acidic fibroblast growth factor with enhanced stability and biological activity. Protein Eng. 6, 541-546. (Pubitemid 23239701)
59. Kim, J., Brych, S. R., Lee, J., Logan, T. M. & Blaber, M. (2003). Identification of a key structural element for protein folding within β-hairpin turns. J. Mol. Biol. 328, 951-961.
60. Lee, J., Dubey, V. K., Longo, L. M. & Blaber, M. (2008). A logical OR redundancy with the Asx-Pro-Asx-Gly type I β-turn motif. J. Mol. Biol. 377, 1251-1264.
61. Culajay, J. F., Blaber, S. I., Khurana, A. & Blaber, M. (2000). Thermodynamic characterization of mutants of human fibroblast growth factor 1 with an increased physiological half-life. Biochemistry, 39, 7153-7158. (Pubitemid 30413104)
62. Lee, J. & Blaber, M. (2009). The interaction between thermostability and buried free cysteines in regulating the functional half-life of fibroblast growth factor-1. J. Mol. Biol. 393, 113-127.
63. Lee, J. & Blaber, M. (2009). Structural basis for conserved cysteine in the fibroblast growth factor family: evidence for a vestigial half-cystine. J. Mol. Biol. 393, 128-139.
64. Zakrzewska, M., Krowarsch, D., Wiedlocha, A., Olsnes, S. & Otlewski, J. (2005). Highly stable mutants of human fibroblast growth factor-1 exhibit prolonged biological action. J. Mol. Biol. 352, 860-875.
65. Gimenez-Gallego, G., Conn, G., Hatcher, V. B. & Thomas, K. A. (1986). The complete amino acid sequence of human brain-derived acidic fibroblast growth factor. Biochem. Biophys. Res. Commun. 128, 611-617.
66. Linemeyer, D. L., Menke, J. G., Kelly, L. J., Disalvo, J., Soderman, D., Schaeffer, M. T. et al. (1990). Disulfide bonds are neither required, present, nor compatible with full activity of human recombinant acidic fibroblast growth factor. Growth Factors, 3, 287-298.
67. Ortega, S., Schaeffer, M. T., Soderman, D., DiSalvo, J., Linemeyer, D. L., Gimenez-Gallego, G. & Thomas, K. A. (1991). Conversion of cysteine to serine residues alters the activity, stability, and heparin dependence of acidic fibroblast growth factor. J. Biol. Chem. 266, 5842-5846.
68. Zazo, M., Lozano, R. M., Ortega, S., Varela, J., Diaz-Orejas, R., Ramirez, J. M. & Gimenez-Gallego, G. (1992). High-level synthesis in Escherichia coli of a shortened and full-length human acidic fibroblast growth factor and purification in a form stable in aqueous solutions. Gene, 113, 231-238.
69. Tsai, P. K., Volkin, D. B., Dabora, J. M., Thompson, K. C., Bruner, M. W., Gress, J. O. et al. (1993). Formulation design of acidic fibroblast growth factor. Pharm. Res. 10, 649-659.
70. Gill, S. C. & von Hippel, P. H. (1989). Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182, 319-326.
71. Eftink, M. R. (1994). The use of fluorescence methods to monitor unfolding transitions in proteins. Biophys. J. 66, 482-501.
72. Pace, C. N. & Scholtz, J. M. (1997). Measuring the conformational stability of a protein. In Protein Structure: a Practical Approach (Creighton, T. E., ed.), pp. 299-321, Oxford University Press, Oxford.
73. Backmann, J., Schafer, G., Wyns, L. & Bonisch, H. (1998). Thermodynamics and kinetics of unfolding of the thermostable trimeric adenylate kinase from the archaeon Sulfolobus acidocaldarius. J. Mol. Biol. 284, 817-833.
74. Jelesarov, I. & Lu, M. (2001). Thermodynamics of trimer-of-hairpins formation by the SIV gp41 envelope protein. J. Mol. Biol. 307, 637-656.
75. Grek, S. B., Davis, J. K. & Blaber, M. (2001). An efficient, flexible-model program for the analysis of differential scanning calorimetry protein denaturation data. Protein Pept. Lett. 8, 429-436.
76. Fersht, A. R. (1999). Kinetics of Protein Folding. Structure and Mechanism in Protein Science. W. H. Freeman and Co., New York.
77. Otwinowski, Z. (1993). Proceedings of the CCP4 Study Weekend: Data Collection and Processing. SERC Daresbury Laboratory, England.
78. Otwinowski, Z. & Minor, W. (1997). Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326. (Pubitemid 27085611)
79. Zwart, P. H., Afonine, P. V., Grosse-Kunstleve, R. W., Hung, L. W., Loerger, T. R., McCoy, A. J. et al. (2008). Automated structure solution with the PHENIX suite. Methods Mol. Biol. 426, 419-435.
80. Brunger, A. T. (1992). Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature, 355, 472-475.
81. Emsley, P. & Cowtan, K. (2004). Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2126-2132. (Pubitemid 41742764)
82. Lee, J., Blaber, S. I., Irsigler, A., Aspinwall, E. & Blaber, M. (2009). X-ray structure and biophysical properties of rabbit fibroblast growth factor 1. Acta Crystallogr., Sect. F. 65, 1097-1104.
83. Plotnikov, A. N., Hubbard, S. R., Schlessinger, J. & Mohammadi, M. (2000). Crystal structures of two FGF-FGFR complexes reveal the determinants of ligand-receptor specificity. Cell, 101, 413-424.