Most proteins adopt an approximate structural symmetry. However, they have no symmetry detectable in their sequences and it is unclear for most of these proteins whether their structural symmetry originates from duplication. As one of the six popular folds (super-folds) possessing an approximate structural symmetry, the triosephosphate isomerase barrel (TIM-barrel) domain has been widely studied. Using modified recurrent quantification analysis of primary sequences, we identified the same 2-, 3-, and 4-fold symmetry pattern as their tertiary structures. This result indicates that the symmetry in tertiary structure is coded by symmetry in the primary sequence and that the TIM-barrel adopts a 2-, 3-, or 4-fold repeat pattern during evolution. This discovery will be useful for understanding the evolutionary mechanisms of this protein family and the symmetry pattern that may be a clue into the ancient origin of duplication of half-barrels or the β a unit.
References
[1]
Anfinsen, C.B. (1973) Principles That Govern the Folding of Protein Chains. Science, 181, 223-230. http://dx.doi.org/10.1126/science.181.4096.223
[2]
Soding, J. and Lupas, A.N. (2003) More than the Sum of Their Parts: On the Evolution of Proteins from Peptides. Bioessays, 25, 837-846. http://dx.doi.org/10.1002/bies.10321
[3]
Lupas, A.N., Ponting, C.P. and Russell, R.B. (2001) On the Evolution of Protein Folds: Are Similar Motifs in Different Protein Folds the Result of Convergence, Insertion, or Relics of an Ancient Peptide World? Journal of Structural Biology, 134, 191-203. http://dx.doi.org/10.1006/jsbi.2001.4393
[4]
Nagano, N., Orengo, C.A. and Thornton, J.M. (2002) One Fold with Many Functions: The Evolutionary Relationships between TIM Barrel Families Based on Their Sequences, Structures and Functions. Journal of Molecular Biology, 321, 741-765. http://dx.doi.org/10.1016/S0022-2836(02)00649-6
[5]
Branden, C. and Tooze, J. (1991) Introduction to Protein Structure. Garland, New York.
[6]
Lang, D., Thoma, R., Henn-Sax, M., Sterner, R. and Wilmanns, M. (2000) Structural Evidence for Evolution of the Beta/Alpha Barrel Scaffold by Gene Duplication and Fusion. Science, 289, 1546-1550. http://dx.doi.org/10.1126/science.289.5484.1546
[7]
Fani, R., Lio, P., Chiarelli, I. and Bazzicalupo, M. (1994) The Evolution of the Histidine Biosynthetic Genes in Prokaryotes: A Common Ancestor for the hisA and hisF Genes. Journal of Molecular Evolution, 38, 489-495. http://dx.doi.org/10.1007/BF00178849
[8]
Lee, J. and Blaber, M. (2011) Experimental Support for the Evolution of Symmetric Protein Architecture from a Simple Peptide Motif. Proceedings of the National Academy of Sciences of the United States of America, 108, 126-130. http://dx.doi.org/10.1073/pnas.1015032108
[9]
List, F., Sterner, R. and Wilmanns, M. (2011) Related (Betaal-pha)8-barrel Proteins in Histidine and Tryptophan Biosynthesis: A Paradigm to Study Enzyme Evolution. ChemBioChem, 12, 1487-1494. http://dx.doi.org/10.1002/cbic.201100082
[10]
Richter, M., Bosnali, M., Carstensen, L., Seitz, T., Durchschlag, H., Blanquart, S., Merkl, R. and Sterner, R. (2010) Computational and Experimental Evidence for the Evolution of a (βα)< sub> 8-Barrel Protein from an Ancestral Quarter- Barrel Stabilised by Disulfide Bonds. Journal of Molecular Biology, 398, 763-773. http://dx.doi.org/10.1016/j.jmb.2010.03.057
[11]
Pellegrini, M., Renda, M.E. and Vecchio, A. (2012) Ab Initio Detection of Fuzzy Amino Acid Tandem Repeats in Protein Sequences. BMC Bioinformatics, 13, S8. http://dx.doi.org/10.1186/1471-2105-13-S3-S8
[12]
Luo, H., Lin, K., David, A., Nijveen, H. and Leunissen, J.A. (2012) ProRepeat: An Integrated Repository for Studying Amino Acid Tandem Repeats in Proteins. Nucleic Acids Research, 40, D394-D399. http://dx.doi.org/10.1093/nar/gkr1019
[13]
Senthilkumar, R., Sabarinathan, R., Hameed, B.S., Banerjee, N., Chidambarathanu, N., Karthik, R. and Sekar, K. (2010) FAIR: A Server for Internal Sequence Repeats. Bioinformation, 4, 271-275. http://dx.doi.org/10.6026/97320630004271
[14]
Marsella, L., Sirocco, F., Trovato, A., Seno, F. and Tosatto, S.C. (2009) REPETITA: Detection and Discrimination of the Periodicity of Protein Solenoid Repeats by Discrete Fourier Transform. Bioinformatics, 25, i289-i295. http://dx.doi.org/10.1093/bioinformatics/btp232
[15]
Nirjhar Banerjee, N.C.D.M. (2008) An Algorithm to Find All Identical Internal Sequence Repeats. Current Science India, 95, 188-195.
[16]
Soding, J., Remmert, M. and Biegert, A. (2006) HHrep: De Novo Protein Repeat Detection and the Origin of TIM Barrels. Nucleic Acids Research, 34, W137-W142. http://dx.doi.org/10.1093/nar/gkl130
[17]
Szklarczyk, R. and Heringa, J. (2004) Tracking Repeats Using Significance and Transitivity. Bioinformatics, 20, i311-i317. http://dx.doi.org/10.1093/bioinformatics/bth911
[18]
Heger, A. and Holm, L. (2000) Rapid Automatic Detection and Alignment of Repeats in Protein Sequences. Proteins: Structure, Function, and Bioinformatics, 41, 224-237. http://dx.doi.org/10.1002/1097-0134(20001101)41:2<224::AID-PROT70>3.0.CO;2-Z
[19]
Rackovsky, S. (1998) “Hidden” Sequence Periodicities and Protein Architecture. Proceedings of the National Academy of Sciences of the United States of America, 95, 8580-8584. http://dx.doi.org/10.1073/pnas.95.15.8580
[20]
Xu, R. and Xiao, Y. (2005) A Common Sequence-Associated Physicochemical Feature for Proteins of Beta-Trefoil Family. Computational Biology and Chemistry, 29, 79-82. http://dx.doi.org/10.1016/j.compbiolchem.2004.12.003
[21]
Ji, X., Chen, H. and Xiao, Y. (2007) Hidden Symmetries in the Primary Sequences of Beta-Barrel Family. Computational Biology and Chemistry, 31, 61-63. http://dx.doi.org/10.1016/j.compbiolchem.2007.01.002
[22]
Yadid, I. and Tawfik, D.S. (2011) Functional Beta-Propeller Lectins by Tandem Duplications of Repetitive Units. Protein Engineering, Design and Selection, 24, 185-195. http://dx.doi.org/10.1093/protein/gzq053
[23]
Wang, X., Huang, Y. and Xiao, Y. (2008) Structural-Symmetry-Related Sequence Patterns of the Proteins of Beta- Propeller Family. Journal of Molecular Graphics and Modelling, 26, 829-833. http://dx.doi.org/10.1016/j.jmgm.2007.04.014
[24]
Ji, X., Wang, H., Hao, J., Zheng, Y., Wang, W. and Sun, M. (2010) Identification of Sequence Repetitions in Immunoglobulin Folds. Journal of Molecular Graphics and Modelling, 28, 788-791. http://dx.doi.org/10.1016/j.jmgm.2010.02.003
[25]
Huang, Y. and Xiao, Y. (2007) Detection of Gene Duplication Signals of Ig Folds from Their Amino Acid Sequences. Proteins: Structure, Function, and Bioinformatics, 68, 267-272. http://dx.doi.org/10.1002/prot.21330
[26]
Shen, X. (2011) Conformation and Sequence Evidence for Two-Fold Symmetry in Left-Handed Beta-Helix Fold. Journal of Theoretical Biology, 285, 77-83. http://dx.doi.org/10.1016/j.jtbi.2011.06.011
[27]
Ji, X., Sheng, J., Wang, F., Zhang, S., Hao, J., Wang, H. and Sun, M. (2011) Identification of Latent Periodicity in Domains of Alkaline Proteases. Biochemistry (Moscow), 76, 1037-1042. http://dx.doi.org/10.1134/S0006297911090082
[28]
Yamazaki, T. and Maruyama, T. (1972) Evidence for the Neutral Hypothesis of Protein Polymorphism. Science, 178, 56-58. http://dx.doi.org/10.1126/science.178.4056.56
[29]
Sillitoe, I., Cuff, A.L., Dessailly, B.H., Dawson, N.L., Furnham, N., Lee, D., Lees, J.G., Lewis, T.E., Studer, R.A., Rentzsch, R., Yeats, C., Thornton, J.M. and Orengo, C.A. (2013) New Functional Families (FunFams) in CATH to Improve the Mapping of Conserved Functional Sites to 3D Structures. Nucleic Acids Research, 41, D490-D498. http://dx.doi.org/10.1093/nar/gks1211
[30]
Konopka, A.K. (2005) Sequence Complexity and Composition. eLS.
[31]
Panek, J., Eidhammer, I. and Aasland, R. (2005) A New Method for Identification of Protein (Sub) Families in a Set of Proteins Based on Hydropathy Distribution in Proteins. Proteins: Structure, Function, and Bioinformatics, 58, 923-934. http://dx.doi.org/10.1002/prot.20356
