Aminotryptophan-containing barstar: Structure-function tradeoff in protein design and engineering with an expanded genetic code

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1764, Issue 7, 2006, Pages 1147-1158

  Rubini, Marina ^a   Lepthien, Sandra ^a   Golbik, Ralph ^a   Budisa, Nediljko ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

Aminotryptophan; Barstar; Genetic code; Protein folding; Stability

Indexed keywords

BARNASE; BARSTAR; RIBONUCLEASE; TRYPTOPHAN DERIVATIVE;

AMINO ACID SUBSTITUTION; ARTICLE; BACILLUS AMYLOLIQUEFACIENS; CRYSTAL STRUCTURE; DENATURATION; GENETIC CODE; KINETICS; PH; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN STABILITY; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; THERMODYNAMICS;

BACTERIAL PROTEINS; CIRCULAR DICHROISM; CRYSTALLOGRAPHY, X-RAY; GENETIC CODE; KINETICS; MODELS, MOLECULAR; PROTEIN BIOSYNTHESIS; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; TEMPERATURE; THERMODYNAMICS; TRYPTOPHAN; UREA;

BACILLUS AMYLOLIQUEFACIENS;

EID: 33746228616     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2006.04.012     Document Type: Article

References (63)

1. Budisa N. A Brief History of an Expanded Amino Acid Repretoire, in Engineering the Genetic Code (2005), Wiley, Weinheim 13-28
2. Hohsaka T., Sato K., Sisido M., Takai K., and Yokoyama S. Adaptability of nonnatural aromatic amino acids to the active center of the Escherichia coli ribosomal A-site. FEBS Lett. 335 (1993) 47-50
3. Budisa N. Prolegomena to future efforts on genetic code engineering by expanding its amino acid repertoire. Angew. Chem., Int. Ed. Engl. 43 (2004) 3387-3428
4. Hohsaka T., and Sisido M. Incorporation of non-natural amino acids into proteins. Curr. Opin. Chem. Biol. 6 (2002) 809-815
5. Link A.J., Mock M.L., and Tirrell D.A. Non-canonical amino acids in protein engineering. Curr. Opin. Biotechnol. 14 (2003) 603-609
6. Wang L., and Schultz P.G. Expanding the genetic code. Chem. Commun. (2002) 1-11
7. Budisa N. Some Practical Potentials of Reprogrammed Cellular Translation, in Engineering the Genetic Code (2005), Wiley, Weinheim 213-261
8. Budisa N., Minks C., Alefelder S., Wenger W., Dong F.M., Moroder L., and Huber R. Toward the experimental codon reassignment in vivo: protein building with an expanded amino acid repertoire. FASEB J. 13 (1999) 41-51
9. Minks C., Alefelder S., Moroder L., Huber R., and Budisa N. Towards new protein engineering: in vivo building and folding of protein shuttles for drug delivery and targeting by the selective pressure incorporation (SPI) method. Tetrahedron 56 (2000) 9431-9442
10. Link A.J., and Tirrell D.A. Reassignment of sense codons in vivo. Methods 36 (2005) 291-298
11. Twine S.M., and Szabo A.G. Fluorescent amino acid analogs. Methods Enzymol. 360 (2003) 104-127
12. Bae J.H., Pal P.P., Moroder L., Huber R., and Budisa N. Crystallographic evidence for isomeric chromophores in 3-fluorotyrosyl-green fluorescent protein. ChemBioChem 5 (2004) 720-722
13. Shafirovich V., and Geacintov N.E. Spectroscopic investigations of charge transfer in DNA. In: Wagenknecht H.A. (Ed). Charge Transfer in DNA (2005), Wiley-VCH, Weinheim 175-193
14. Budisa N., Rubini M., Bae J.H., Weyher E., Wenger W., Golbik R., Huber R., and Moroder L. Global replacement of tryptophan with aminotryptophans generates non-invasive protein-based optical pH sensors. Angew. Chem., Int. Ed. Engl. 41 (2002) 4066-4069
15. Bae J.H., Rubini M., Jung G., Wiegand G., Seifert M.H.J., Azim M.K., Kim J.S., Zumbusch A., Holak T.A., Moroder L., Huber R., and Budisa N. Expansion of the genetic code enables design of a novel "gold" class of green fluorescent proteins. J. Mol. Biol. 328 (2003) 1071-1081
16. Wong T.T.F. Evolution of the genetic code. Microbiol. Sci. 5 (1998) 174-181
17. Budisa N., Steipe B., Demange P., Eckerskorn C., Kellermann J., and Huber R. High-level biosynthetic substitution of methionine in proteins by its analogs 2-aminohexanoic acid, selenomethionine, telluromethionine and ethionine in Escherichia coli. Eur. J. Biochem. 230 (1995) 788-796
18. Nölting B., Golbik R., Neira J.L., Soler-Gonzalez A.S., Schreiber G., and Fersht A.R. The folding pathway of a protein at high resolution from microseconds to seconds. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 826-830
19. Golbik R., Fischer G., and Fersht A.R. Folding of barstar C40A/C82A/P27A and catalysis of the peptidyl-prolyl cis/trans isomerization by human cytosolic cyclophilin (Cyp18). Protein Sci. 8 (1999) 1505-1514
20. Minks C., Huber R., Moroder L., and Budisa N. Atomic mutations at the single tryptophan residue of human recombinant annexin V: Effects on structure, stability, and activity. Biochemistry 38 (1999) 10649-10659
21. Pace N.C., and Scholtz J.M. Measuring the conformational stability of a protein. In: Creighton T.E. (Ed). Protein Structure: A Practical Approach (1989), IRL Press, New York 299-321
22. Nolting B., Golbik R., Solergonzalez A.S., and Fersht A.R. Circular dichroism of denatured barstar suggests residual structure. Biochemistry 36 (1997) 9899-9905
23. Makhtadze G.I., and Privalov P.L. Contribution of hydration to protein folding. Thermodynamics I: The enthalpy of hydration. J. Mol. Biol. 232 (1993) 639-657
24. Martin C., Hartley R., and Mauguen Y. X-ray structural analysis of compensating mutations at the barnase-barstar interface. FEBS Lett. 452 (1999) 128-132
25. Bailey S. The CCP4 suite: programs for protein crystallography. Acta Crystallogr., D Biol. Crystallogr. 50 (1994) 760-763
26. Turk D., Guncar G., Podobnik M., and Turk B. Revised definition of substrate binding sites of papain-like cysteine proteases. Biol. Chem. 379 (1998) 137-147
27. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard M. Improved methods for building protein models in electron-density maps and the location of errors in these models. Acta Crystallogr., A 47 (1991) 110-119
28. Gasteiger J., and Marsili M. Iterative partial equalization of orbital electronegativity: a rapid access to atomic charges. Tetrahedron 36 (1980) 3219-3228
29. Wallace A.C., Laskowski R.A., and Thornton J.M. LIGPLOT-A program to generate schematic diagrams of protein ligand interactions. Protein Eng. 8 (1995) 127-134
30. Bae J.H., Alefelder S., Kaiser J.T., Friedrich R., Moroder L., Huber R., and Budisa N. Incorporation of beta-selenolo 3,2-b pyrrolyl-alanine into proteins for phase determination in protein X-ray crystallography. J. Mol. Biol. 309 (2001) 925-936
31. Janecek J., and Rickenberg H.V. Incorporation of beta-2-thienylalanine into beta-galactosidase of Escherichia coli. Biochim. Biophys. Acta 81 (1964) 108
32. Cowie D.B., Cohen G.N., Bolton E.T., and Derobichon-Szulmajster R.H. Amino acid analog incorporation into bacterial proteins. Biochim. Biophys. Acta 34 (1959) 39-46
33. Budisa N. Reprogramming the Cellular Translation Machinery, in Engineering the Genetic Code (2005), Wiley, Weinheim 90-184
34. Carter C.W. Tryptophanyl-tRNA synthetase. In: Bba M., Francklyn C., and Cusack S. (Eds). Aminoacyl-tRNA Synthetases (2004), Landes Bioscience, Austin
35. Lakowitz J.R. Protein Fluorescence. 2nd ed. (1999), Kluwer Academic/Plenum Publisher, New York
36. Woody R.W., and Dunker K. Aromatic and Cystine Side-Chain Circular Dichroism in Proteins (1996), Plenum Press, New York
37. Arnold G.E., Day L.A., and Dunker A.K. Tryptophan contributions to the unusual circular dichroism of fd bacteriophage. Biochemistry 31 (1992) 7948-7956
38. Kishi T., Tanaka M., and Tanaka J. Electronic absorption and fluorescence-spectra of 5-hydroxytryptamine (Serotonin)-Protonation in excited-state. Bull. Chem. Soc. Jpn. 50 (1977) 1267-1271
39. Wong K.B., Freund S.M.V., and Fersht A.R. Cold denaturation of barstar: H-1, N-15 and C-13 NMR assignment and characterisation of residual structure. J. Mol. Biol. 259 (1996) 805-818
40. Babu C.R., Hilser V.J., and Wand A.J. Direct access to the cooperative substructure of proteins and the protein ensemble via cold denaturation. Nat. Struct. Biol. 11 (2004) 352-357
41. Pradeep L., and Udgaonkar J.B. Osmolytes induce structure in an early intermediate on the folding pathway of Barstar. J. Biol. Chem. 279 (2004) 40303-40313
42. Burley S.K., and Petsko G.A. Weakly polar interactions in proteins. Adv. Protein Chem. 39 (1988) 125-189
43. Fauchere J.L., and Pliska V. Hydrophobic parameters π of amino acid side chains from the partitioning of N-acetyl amino acid amides. Eur. J. Med. Chem. 18 (1983) 369-375
44. Radzicka A., and Wolfenden R. Comparing the polarities of the amino acids-Side-chain distribution coefficients between the vapor-phase, cyclohexane, 1-octanol, and neutral aqueous solution. Biochemistry 27 (1988) 1664-1670
45. Shastry M.C., and Udgaonkar J.B. The folding mechanism of barstar: evidence for multiple pathways and multiple intermediates. J. Mol. Biol. 247 (1995) 1013-1027
46. Levitt M., Gerstein M., Huang E., Subbiah S., and Tsai J. Protein folding: the endgame. Ann. Rev. Biochem. 66 (1997) 549-579
47. Nölting B. Protein Folding Kinetics. 2nd ed. (2005), Springer, Berlin
48. Sridevi K., Juneja J., Bhuyan A.K., Krishnamoorthy G., and Udgaonkar J.B. The slow folding reaction of barstar: the core tryptophan region attains tight packing before substantial secondary and tertiary structure formation and final compaction of the polypeptide chain. J. Mol. Biol. 302 (2000) 479-495
49. Rami B.R., Krishnamoorthy G., and Udgaonkar J.B. Dynamics of the core tryptophan during the formation of a productive molten globule intermediate of barstar. Biochemistry 42 (2003) 7986-8000
50. Tidor B., and Lee L.P. Barstar is electrostatically optimized for tight binding to barnase. Nat. Struct. Biol. 8 (2001) 73-76
51. Rose G.D., and Wolfenden R. Hydrogen-bonding, hydrophobicity, packing, and protein-folding. Annu. Rev. Biophys. Biomol. Struct. 22 (1993) 381-415
52. Kauzmann W. Some factors in the interpretation of protein denaturation. Adv. Protein Chem. 14 (1959) 1-63
53. Budisa N. Basic Features of the Cellular Translation Apparatus, in Engineering the Genetic Code (2005), Viley, Weinheim 31-66
54. Wolfenden R., and Radzicka A. How hydrophilic is tryptophan. Trends Biochem. Sci. 11 (1986) 69-70
55. Trinquier G., and Sanejouand Y.H. Which effective property of amino acids is best preserved by the genetic code?. Protein Eng. 11 (1998) 153-169
56. Dayhoff M.O. Atlas of Protein Sequence and Structure vol. 5 (1972), National Biomedical Research Foundation, Washington, DC
57. Dougherty D.A. Cation-pi interactions in chemistry and biology: a new view of benzene, Phe, Tyr, and Trp. Science 271 (1996) 163-168
58. Baldwin R.L. Protein folding-Making a network of hydrophobic clusters. Science 295 (2002) 1657-1658
59. Nath U., and Udgaonkar J.B. Folding of tryptophan mutants of barstar: evidence for an initial hydrophobic collapse on the folding pathway. Biochemistry 36 (1997) 8602-8610
60. Bacher J.M., and Ellington A.D. In: Lapointe J., and Brakier-Gingras L. (Eds). The Directed Evolution of Organismal Chemistry: Unnatural Amino Acid Incorporation (2003), Translation Mechanisms, Georgetown
61. Ardell D.H., and Sella G. On the evolution of redundancy in genetic codes. J. Mol. Evol. 53 (2001) 269-281
62. Weber A.L., and Miller S.L. Reasons for the occurrence of the 20 coded protein amino acids. J. Mol. Evol. 17 (1981) 273-284
63. Budisa N., Pipitone O., Slivanowiz I., Rubini M., Pal P.P., Holak T.A., Huber R., and M.L. Efforts toward the design of 'Teflon' proteins: in vivo translation with trifluorinated leucine and methionine analogues. Chem. Biodiv. 1 (2004) 1465-1475