Computational and experimental evidence for the evolution of a (βα)8-barrel protein from an ancestral quarter-barrel stabilised by disulfide bonds

Journal of Molecular Biology

Volumn 398, Issue 5, 2010, Pages 763-773

  Richter, Markus ^a   Bosnali, Manal ^b   Carstensen, Linn ^a   Seitz, Tobias ^a   Durchschlag, Helmut ^a   Blanquart, Samuel ^c   Merkl, Rainer ^a   Sterner, Reinhard ^a,b  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

^c INSTITUT DES SCIENCES DE L EVOLUTION   (France)

Author keywords

Disulfide bond; Protein evolution; Sequence reconstruction

Indexed keywords

DISULFIDE; GLOBULAR PROTEIN; HISTIDINE; PROTEIN BETA ALPHA 8 BARREL; PROTEIN HISF; TETRAMER; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; HYDROLASE; IMIDAZOLE GLYCEROL PHOSPHATE SYNTHASE; RECOMBINANT PROTEIN;

ARTICLE; CONTROLLED STUDY; EXPERIMENTAL DESIGN; GENE CONSTRUCT; HETEROLOGOUS EXPRESSION; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STABILITY; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; BIOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; THERMOTOGA MARITIMA;

AMINOHYDROLASES; BACTERIAL PROTEINS; COMPUTATIONAL BIOLOGY; DISULFIDES; EVOLUTION, MOLECULAR; MODELS, MOLECULAR; PROTEIN FOLDING; RECOMBINANT PROTEINS; THERMOTOGA MARITIMA;

EID: 77952303485     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.03.057     Document Type: Article

References (52)

1. Lupas A.N., Koretke K.K. Evolution of protein folds. Computational Structural Biology-Methods and Applications 2008, World Scientific, Hackensack, NJ. T. Schwede, M.C. Peitsch (Eds.).
2. Söding J., Lupas A.N. More than the sum of their parts: on the evolution of proteins from peptides. Bioessays 2003, 25:837-846.
3. Main E.R., Lowe A.R., Mochrie S.G., Jackson S.E., Regan L. A recurring theme in protein engineering: the design, stability and folding of repeat proteins. Curr. Opin. Struct. Biol. 2005, 15:464-471.
4. Caetano-Anolles G., Kim H.S., Mittenthal J.E. The origin of modern metabolic networks inferred from phylogenomic analysis of protein architecture. Proc. Natl Acad. Sci. USA 2007, 104:9358-9363.
5. 8-barrel enzyme fold. Chem. Rev. 2005, 105:4038-4055.
6. Wierenga R.K. The TIM-barrel fold: a versatile framework for efficient enzymes. FEBS Lett. 2001, 492:193-198.
7. Lang D., Thoma R., Henn-Sax M., Sterner R., Wilmanns M. Structural evidence for evolution of the β/α barrel scaffold by gene duplication and fusion. Science 2000, 289:1546-1550.
8. Thoma R., Schwander M., Liebl W., Kirschner K., Sterner R. A histidine gene cluster of the hyperthermophile Thermotoga maritima: sequence analysis and evolutionary significance. Extremophiles 1998, 2:379-389.
9. 8-barrel enzyme into two folded halves. Nat. Struct. Biol. 2001, 8:32-36.
10. 4-half-barrels. Proc. Natl Acad. Sci. USA 2004, 101:16448-16453.
11. 8-barrel protein designed from identical half-barrels. Biochemistry 2009, 48:1145-1147.
12. 8-barrel protein designed from identical half barrels. J. Mol. Biol. 2007, 372:114-129.
13. 8-barrel protein scaffolds. Proc. Natl Acad. Sci. USA 2009, 106:3704-3709.
14. Gerlt J.A., Babbitt P.C. Barrels in pieces?. Nat. Struct. Biol. 2001, 8:5-7.
15. Nagano N., Orengo C.A., Thornton J.M. One fold with many functions: the evolutionary relationships between TIM barrel families based on their sequences, structures and functions. J. Mol. Biol. 2002, 321:741-765.
16. Richter, M. (2008). Studies on the evolution of the (βα)8-barrel fold from (βα)2 modules. PhD thesis, University of Regensburg.
17. Sander C., Schneider R. Database of homology-derived protein structures and the structural meaning of sequence alignment. Proteins 1991, 9:56-68.
18. Söding J., Remmert M., Biegert A. HHrep: de novo protein repeat detection and the origin of TIM barrels. Nucleic Acids Res. 2006, 34:W137-W142.
19. Boussau B., Blanquart S., Necsulea A., Lartillot N., Gouy M. Parallel adaptations to high temperatures in the Archaean eon. Nature 2008, 456:942-945.
20. Fondi M., Emiliani G., Lio P., Gribaldo S., Fani R. The evolution of histidine biosynthesis in archaea: insights into the his genes structure and organization in LUCA. J. Mol. Evol. 2009, 69:512-526.
21. Kabsch W., Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 1983, 22:2577-2637.
22. Puigbo P., Wolf Y.I., Koonin E.V. Search for a 'Tree of Life' in the thicket of the phylogenetic forest. J. Biol. 2009, 8:59.
23. Beismann-Driemeyer S., Sterner R. Imidazole glycerol phosphate synthase from Thermotoga maritima. Quaternary structure, steady-state kinetics, and reaction mechanism of the bienzyme complex. J. Biol. Chem. 2001, 276:20387-20396.
24. Klem T.J., Davisson V.J. Imidazole glycerol phosphate synthase: the glutamine amidotransferase in histidine biosynthesis. Biochemistry 1993, 32:5177-5186.
25. Mann H.B., Whitney D.R. On a test of whether one of two random variables is stochastically larger than the other. Ann. Math. Stat. 1947, 18:50-60.
26. Buck M. Trifluoroethanol and colleagues: cosolvents come of age. Recent studies with peptides and proteins. Q. Rev. Biophys. 1998, 31:297-355.
27. Zitzewitz J.A., Gualfetti P.J., Perkons I.A., Wasta S.A., Matthews C.R. Identifying the structural boundaries of independent folding domains in the ? subunit of tryptophan synthase, a β/α barrel protein. Protein Sci. 1999, 8:1200-1209.
28. Yadid I., Tawfik D.S. Reconstruction of functional β-propeller lectins via homo-oligomeric assembly of shorter fragments. J. Mol. Biol. 2007, 365:10-17.
29. Zhang B., Peng Z. A minimum folding unit in the ankyrin repeat protein p16(INK4). J. Mol. Biol. 2000, 299:1121-1132.
30. Betz S.F. Disulfide bonds and the stability of globular proteins. Protein Sci. 1993, 2:1551-1558.
31. Linke K., Jakob U. Not every disulfide lasts forever: disulfide bond formation as a redox switch. Antioxid. Redox Signal. 2003, 5:425-434.
32. Raines R.T. Nature's transitory covalent bond. Nat. Struct. Biol. 1997, 4:424-427.
33. Beeby M., O'Connor B.D., Ryttersgaard C., Boutz D.R., Perry L.J., Yeates T.O. The genomics of disulfide bonding and protein stabilization in thermophiles. PLoS Biol. 2005, 3:e309.
34. Mallick P., Boutz D.R., Eisenberg D., Yeates T.O. Genomic evidence that the intracellular proteins of archaeal microbes contain disulfide bonds. Proc. Natl Acad. Sci. USA 2002, 99:9679-9684.
35. Schwab T., Skegro D., Mayans O., Sterner R. A rationally designed monomeric variant of anthranilate phosphoribosyltransferase from Sulfolobus solfataricus is as active as the dimeric wild-type enzyme but less thermostable. J. Mol. Biol. 2008, 376:506-516.
36. Thoma R., Hennig M., Sterner R., Kirschner K. Structure and function of mutationally generated monomers of dimeric phosphoribosylanthranilate isomerase from Thermotoga maritima. Struct. Fold. Des. 2000, 8:265-276.
37. Walden H., Bell G.S., Russell R.J., Siebers B., Hensel R., Taylor G.L. Tiny TIM: a small, tetrameric, hyperthermostable triosephosphate isomerase. J. Mol. Biol. 2001, 306:745-757.
38. Sterner R., Liebl W. Thermophilic adaptation of proteins. Crit. Rev. Biochem. Mol. Biol. 2001, 36:39-106.
39. Vieille C., Zeikus G.J. Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability. Microbiol. Mol. Biol. Rev. 2001, 65:1-43.
40. Fani R., Lio P., Lazcano A. Molecular evolution of the histidine biosynthetic pathway. J. Mol. Evol. 1995, 41:760-774.
41. Ho S.N., Hunt H.D., Horton R.M., Pullen J.K., Pease L.R. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 1989, 77:51-59.
42. Pace C.N., Vajdos F., Fee L., Grimsley G., Gray T. How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 1995, 4:2411-2423.
43. Yphantis D.A. Equilibrium ultracentrifugation of dilute solutions. Biochemistry 1964, 3:297-317.
44. Cohn E., Edsall J. Proteins, Amino Acids and Peptides as Ions and Dipolar Ions 1943, Reinhold, New York.
45. van Stokkum I.H., Spoelder H.J., Bloemendal M., van Grondelle R., Groen F.C. Estimation of protein secondary structure and error analysis from circular dichroism spectra. Anal. Biochem. 1990, 191:110-118.
46. Whitmore L., Wallace B.A. DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res. 2004, 32:W668-W673.
47. Whitmore L., Wallace B.A. Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases. Biopolymers 2008, 89:392-400.
48. Smith T.F., Waterman M.S. Identification of common molecular subsequences. J. Mol. Biol. 1981, 147:195-197.
49. Student The probable error of a mean. Biometrika 1908, 6:1-25.
50. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
51. Maglott D., Ostell J., Pruitt K.D., Tatusova T. Entrez Gene: gene-centered information at NCBI. Nucleic Acids Res. 2005, 33:D54-D58.
52. Katoh K., Kuma K., Toh H., Miyata T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 2005, 33:511-518.