Tandem repeats in proteins: From sequence to structure

Journal of Structural Biology

Volumn 179, Issue 3, 2012, Pages 279-288

  Kajava, Andrey V ^a  

^a CNRS   (France)

Author keywords

3D structure; Amino acid; Bioinformatics; Proteomes; Tandem repeat

Indexed keywords

ALPHA CRYSTALLIN; PROTEIN; PROTEOME;

AMINO ACID SEQUENCE; ARTICLE; BIOINFORMATICS; BIOPHYSICS; CRYOELECTRON MICROSCOPY; DATA BASE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN STRUCTURE; TANDEM REPEAT;

ALGORITHMS; AMINO ACID SEQUENCE; ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; COMPUTATIONAL BIOLOGY; COMPUTER SIMULATION; DATABASES, PROTEIN; FIBRILLAR COLLAGENS; FOURIER ANALYSIS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POLYGLUTAMIC ACID; PROTEIN CONFORMATION; PROTEINS; REPETITIVE SEQUENCES, AMINO ACID; VIRULENCE FACTORS, BORDETELLA;

EID: 84865174088     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2011.08.009     Document Type: Article

References (107)

1. Abraham A.L., Rocha E.P., Pothier J. Swelfe: a detector of internal repeats in sequences and structures. Bioinformatics 2008, 24:1536-1537.
2. Aksel T., Majumdar A., Barrick D. The contribution of entropy, enthalpy, and hydrophobic desolvation to cooperativity in repeat-protein folding. Structure 2011, 19:349-360.
3. Alvarez M., Zeelen J.P., Mainfroid V., Rentier-Delrue F., Martial J.A., et al. Triose-phosphate isomerase (TIM) of the psychrophilic bacterium Vibrio marinus. Kinetic and structural properties. J. Biol. Chem. 1998, 273:2199-2206.
4. Andrade M.A., Ponting C.P., Gibson T.J., Bork P. Homology-based method for identification of protein repeats using statistical significance estimates. J. Mol. Biol. 2000, 298:521-537.
5. Auer H.E., Doty P. The conformational stability of alpha-helical nonpolar polypeptides in solution. Biochemistry 1966, 5:1716-1725.
6. Bartual S.G., Otero J.M., Garcia-Doval C., Llamas-Saiz A.L., Kahn R., et al. Structure of the bacteriophage T4 long tail fiber receptor-binding tip. Proc. Natl. Acad. Sci. U S A 2010, 107:20287-20292.
7. Bateman A., Murzin A.G., Teichmann S.A. Structure and distribution of pentapeptide repeats in bacteria. Protein Sci. 1998, 7:1477-1480.
8. Baumann U., Wu S., Flaherty K.M., McKay D.B. Three-dimensional structure of the alkaline protease of Pseudomonas aeruginosa: a two-domain protein with a calcium binding parallel beta roll motif. Embo J. 1993, 12:3357-3364.
9. Baxa U., Cassese T., Kajava A.V., Steven A.C. Structure, function, and amyloidogenesis of fungal prions: filament polymorphism and prion variants. Adv. Prot. Chem. 2006, 73:125-180.
10. Bella J., Eaton M., Brodsky B., Berman H.M. Crystal and molecular structure of a collagen-like peptide at 1.9A resolution. Science 1994, 266:75-81.
11. Biegert A., Soding J. De novo identification of highly diverged protein repeats by probabilistic consistency. Bioinformatics 2008, 24:807-814.
12. Binz H.K., Amstutz P., Kohl A., Stumpp M.T., Briand C., et al. High-affinity binders selected from designed ankyrin repeat protein libraries. Nat. Biotechnol. 2004, 22:575-582.
13. Bohn S., Beck F., Sakata E., Walzthoeni T., Beck M., et al. Structure of the 26S proteasome from Schizosaccharomyces pombe at subnanometer resolution. Proc. Natl. Acad. Sci. U S A 2010, 107:20992-20997.
14. Bork P., Doolittle R.F. Drosophila kelch motif is derived from a common enzyme fold. J. Mol. Biol. 1994, 236:1277-1282.
15. Bourne Y., Zamboni V., Barre A., Peumans W.J., Van Damme E.J., et al. Helianthus tuberosus lectin reveals a widespread scaffold for mannose-binding lectins. Structure 1999, 7:1473-1482.
16. Buard J., Vergnaud G. Complex recombination events at the hypermutable minisatellite CEB1 (D2S90). Embo J. 1994, 13:3203-3210.
17. Bucher P., Karplus K., Moeri N., Hofmann K. A flexible motif search technique based on generalized profiles. Comput. Chem. 1996, 20:3-23.
18. Choi H.J., Weis W.I. Crystal structure of a rigid four-spectrin-repeat fragment of the human desmoplakin plakin domain. J Mol Biol 2011, 409:800-812.
19. Chothia C., Murzin A.G. New folds for all-beta proteins. Structure 1993, 1:217-222.
20. Cohen C., Parry D.A. Alpha-helical coiled coils: more facts and better predictions. Science 1994, 263:488-489.
21. Coward E., Drablos F. Detecting periodic patterns in biological sequences. Bioinformatics 1998, 14:498-507.
22. Ellegren H. Microsatellite mutations in the germline: implications for evolutionary inference. Trends Genet. 2000, 16:551-558.
23. Ellgaard L., Riek R., Herrmann T., Guntert P., Braun D., et al. NMR structure of the calreticulin P-domain. Proc. Natl. Acad. Sci. U S A 2001, 98:3133-3138.
24. Fan X., Dion P., Laganiere J., Brais B., Rouleau G.A. Oligomerization of polyalanine expanded PABPN1 facilitates nuclear protein aggregation that is associated with cell death. Hum. Mol. Genet. 2001, 10:2341-2351.
25. Faux N.G., Bottomley S.P., Lesk A.M., Irving J.A., Morrison J.R., et al. Functional insights from the distribution and role of homopeptide repeat-containing proteins. Genome Res. 2005, 15:537-551.
26. Fernandez-Tornero C., Lopez R., Garcia E., Gimenez-Gallego G., Romero A. A novel solenoid fold in the cell wall anchoring domain of the pneumococcal virulence factor LytA. Nat. Struct. Biol. 2001, 8:1020-1024.
27. Fraser R.D.B., MacRae T.P. Conformation in fibrous proteins and related synthetic polypeptides 1973, London and New York, Academic Press.
28. Garnham C.P., Campbell R.L., Davies P.L. From the cover: anchored clathrate waters bind antifreeze proteins to ice. Proc. Natl. Acad. Sci. U S A 2011, 108:7363-7367.
29. 2+-dependent bacterial antifreeze protein domain has a novel beta-helical ice-binding fold. Biochem. J. 2008, 411:171-180.
30. Graether S.P., Kuiper M.J., Gagne S.M., Walker V.K., Jia Z., et al. Beta-helix structure and ice-binding properties of a hyperactive antifreeze protein from an insect. Nature 2000, 406:325-328.
31. Gribskov M., McLachlan A.D., Eisenberg D. Profile analysis: detection of distantly related proteins. Proc. Natl. Acad. Sci. U S A 1987, 84:4355-4358.
32. Groves M.R., Barford D. Topological characteristics of helical repeat proteins. Curr. Opin. Struct. Biol. 1999, 9:383-389.
33. Gruber M., Soding J., Lupas A.N. REPPER-repeats and their periodicities in fibrous proteins. Nucleic Acids Res. 2005, 33:W239-243.
34. Harrison O.J., Jin X., Hong S., Bahna F., Ahlsen G., et al. The extracellular architecture of adherens junctions revealed by crystal structures of type I cadherins. Structure 2011, 19:244-256.
35. Heger A., Holm L. Rapid automatic detection and alignment of repeats in protein sequences. Proteins 2000, 41:224-237.
36. Heringa J. Detection of internal repeats: how common are they?. Curr. Opin. Struct. Biol. 1998, 8:338-345.
37. Hermoso J.A., Monterroso B., Albert A., Galan B., Ahrazem O., et al. Structural basis for selective recognition of pneumococcal cell wall by modular endolysin from phage Cp-1. Structure 2003, 11:1239-1249.
38. Ho J.G., Greco A., Rupnik M., Ng K.K. Crystal structure of receptor-binding C-terminal repeats from Clostridium difficile toxin A. Proc. Natl. Acad. Sci. U S A 2005, 102:18373-18378.
39. Hofmann K., Bucher P., Falquet L., Bairoch A. The PROSITE database, its status in 1999. Nucleic Acids Res. 1999, 27:215-219.
40. Hunter S., Apweiler R., Attwood T.K., Bairoch A., Bateman A., et al. InterPro: the integrative protein signature database. Nucleic Acids Res. 2009, 37:D211-215.
41. Huntley M., Golding G.B. Evolution of simple sequence in proteins. J. Mol. Evol. 2000, 51:131-140.
42. Jorda J., Kajava A.V. T-REKS: identification of Tandem REpeats in sequences with a K-meanS based algorithm. Bioinformatics 2009, 25:2632-2638.
43. Jorda J., Kajava A.V. Protein homorepeats sequences, structures, evolution, and functions. Adv. Prot. Chem. Struct. Biol. 2010, 79:59-88.
44. Jorda J., Xue B., Uversky V.N., Kajava A.V. Protein tandem repeats - the more perfect, the less structured. Febs J. 2010, 277:2673-2682.
45. Kajava A.V. Structural diversity of leucine-rich repeat proteins. J. Mol. Biol. 1998, 277:519-527.
46. Kajava A.V. Dimorphism of polyglycine I: structural models for crystal modifications. Acta Crystallogr. D Biol. Crystallogr. 1999, 55:436-442.
47. Kajava A.V. Review: proteins with repeated sequence-structural prediction and modeling. J. Struct. Biol. 2001, 134:132-144.
48. Kajava A.V., Cheng N., Cleaver R., Kessel M., Simon M.N., et al. Beta-helix model for the filamentous hemagglutinin adhesin of Bordetella pertussis and related bacterial secretory proteins. Mol. Microbiol. 2001, 42:279-292.
49. Kajava A.V., Gorbea C., Ortega J., Rechsteiner M., Steven A.C. New HEAT-like repeat motifs in proteins regulating proteasome structure and function. J. Struct. Biol. 2004, 146:425-430.
50. Kajava A.V., Kobe B. Assessment of the ability to model proteins with leucine-rich repeats in light of the latest structural information. Prot. Sci. 2002, 11:1082-1090.
51. Kajava A.V., Squire J.M., Parry D.A. Beta-structures in fibrous proteins. Adv. Prot. Chem. 2006, 73:1-15.
52. Kajava A.V., Steven A.C. Beta-rolls, beta-helices, and other beta-solenoid proteins. Adv. Prot. Chem. 2006, 73:55-96.
53. Kajava A.V., Steven A.C. The turn of the screw: variations of the abundant beta-solenoid motif in passenger domains of type V secretory proteins. J. Struct. Biol. 2006, 000:000.
54. Kalita M.K., Ramasamy G., Duraisamy S., Chauhan V.S., Gupta D. ProtRepeatsDB: a database of amino acid repeats in genomes. BMC Bioinf. 2006, 7:336.
55. Karpenahalli M.R., Lupas A.N., Soding J. TPRpred: a tool for prediction of TPR-, PPR- and SEL1-like repeats from protein sequences. BMC Bioinf. 2007, 8:2.
56. Katti M.V., Sami-Subbu R., Ranjekar P.K., Gupta V.S. Amino acid repeat patterns in protein sequences: their diversity and structural-functional implications. Prot. Sci. 2000, 9:1203-1209.
57. Kippert F., Gerloff D.L. Highly sensitive detection of individual HEAT and ARM repeats with HHpred and COACH. PLoS One 2009, 4:e7148.
58. Kobe B., Deisenhofer J. The leucine-rich repeat: a versatile binding motif. Trends Biochem. Sci. 1994, 19:415-421.
59. Kobe B., Kajava A.V. When protein folding is simplified to protein coiling: the continuum of solenoid protein structures. Trends Biochem. Sci. 2000, 25:509-515.
60. Kobe B., Kajava A.V. The leucine-rich repeat as a protein recognition motif. Curr. Opin. Struct. Biol. 2001, 11:725-732.
61. Koebnik R., Locher K.P., Van Gelder P. Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol. Microbiol. 2000, 37:239-253.
62. Kruglyak S., Durrett R.T., Schug M.D., Aquadro C.F. Equilibrium distributions of microsatellite repeat length resulting from a balance between slippage events and point mutations. Proc. Natl. Acad. Sci. U S A 1998, 95:10774-10778.
63. Kusunoki H., Minasov G., Macdonald R.I., Mondragon A. Independent movement, dimerization and stability of tandem repeats of chicken brain alpha-spectrin. J. Mol. Biol. 2004, 344:495-511.
64. Lee M.S., Gippert G.P., Soman K.V., Case D.A., Wright P.E. Three-dimensional solution structure of a single zinc finger DNA-binding domain. Science 1989, 245:635-637.
65. Lukacik P., Roversi P., White J., Esser D., Smith G.P., et al. Complement regulation at the molecular level: the structure of decay-accelerating factor. Proc. Natl. Acad. Sci. U S A 2004, 101:1279-1284.
66. Lupas A.N., Gruber M. The structure of alpha-helical coiled coils. Adv. Prot. Chem. 2005, 70:37-78.
67. 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.
68. Makabe K., Biancalana M., Yan S., Tereshko V., Gawlak G., et al. High-resolution structure of a self-assembly-competent form of a hydrophobic peptide captured in a soluble beta-sheet scaffold. J. Mol. Biol. 2008, 378:459-467.
69. Marcotte E.M., Pellegrini M., Yeates T.O., Eisenberg D. A census of protein repeats. J. Mol. Biol. 1999, 293:151-160.
70. Marsella L., Sirocco F., Trovato A., Seno F., Tosatto S.C. REPETITA: detection and discrimination of the periodicity of protein solenoid repeats by discrete Fourier transform. Bioinformatics 2009, 25:i289-295.
71. McDonnell A.V., Menke M., Palmer N., King J., Cowen L., et al. Fold recognition and accurate sequence-structure alignment of sequences directing beta-sheet proteins. Proteins 2006, 63:976-985.
72. McLachlan A.D., Stewart M. The 14-fold periodicity in alpha-tropomyosin and the interaction with actin. J. Mol. Biol. 1976, 103:271-298.
73. Mitraki A., Papanikolopoulou K., Van Raaij M.J. Natural triple beta-stranded fibrous folds. Adv. Prot. Chem. 2006, 73:97-124.
74. Moult J. A decade of CASP: progress, bottlenecks and prognosis in protein structure prediction. Curr. Opin. Struct. Biol. 2005, 15:285-289.
75. Murzin A.G. Structural principles for the propeller assembly of beta-sheets: the preference for seven-fold symmetry. Proteins 1992, 14:191-201.
76. Murzin A.G., Lesk A.M., Chothia C. Beta-Trefoil fold. Patterns of structure and sequence in the Kunitz inhibitors interleukins-1 beta and 1 alpha and fibroblast growth factors. J. Mol. Biol. 1992, 223:531-543.
77. Neer E.J., Schmidt C.J., Nambudripad R., Smith T.F. The ancient regulatory-protein family of WD-repeat proteins. Nature 1994, 371:297-300.
78. Nelson R., Eisenberg D. Structural models of amyloid-like fibrils. Adv. Prot. Chem. 2006, 73:235-282.
79. Newman A.M., Cooper J.B. XSTREAM: a practical algorithm for identification and architecture modeling of tandem repeats in protein sequences. BMC Bioinf. 2007, 8:382.
80. Orr H.T., Zoghbi H.Y. Trinucleotide repeat disorders. Annu. Rev. Neurosci. 2007, 30:575-621.
81. Passmore L.A., Booth C.R., Venien-Bryan C., Ludtke S.J., Fioretto C., et al. Structural analysis of the anaphase-promoting complex reveals multiple active sites and insights into polyubiquitylation. Mol. Cell. 2005, 20:855-866.
82. Pauling L., Corey R.B. The structure of fibrous proteins of the collagen-gelatin group. Proc. Natl. Acad. Sci. U S A 1951, 37:272-281.
83. Pellegrini M., Marcotte E.M., Yeates T.O. A fast algorithm for genome-wide analysis of proteins with repeated sequences. Proteins 1999, 35:440-446.
84. Perutz M.F. Glutamine repeats and neurodegenerative diseases: molecular aspects. Trends Biochem. Sci. 1999, 24:58-63.
85. Ponting C.P., Russell R.B. Identification of distant homologues of fibroblast growth factors suggests a common ancestor for all beta-trefoil proteins. J. Mol. Biol. 2000, 302:1041-1047.
86. Rich A., Crick F.H. The structure of collagen. Nature 1955, 176:915-916.
87. Sabarinathan R., Basu R., Sekar K. ProSTRIP: a method to find similar structural repeats in three-dimensional protein structures. Comput. Biol. Chem. 2010, 34:126-130.
88. Sadre-Bazzaz K., Whitby F.G., Robinson H., Formosa T., Hill C.P. Structure of a Blm10 complex reveals common mechanisms for proteasome binding and gate opening. Mol. Cell. 2010, 37:728-735.
89. Schrag J.D., Bergeron J.J., Li Y., Borisova S., Hahn M., Thomas D.Y., et al. The Structure of calnexin, an ER chaperone involved in quality control of protein folding. Mol. Cell. 2001, 8:633-644.
90. Schuler B., Furst F., Osterroth F., Steinbacher S., Huber R., et al. Plasticity and steric strain in a parallel beta-helix: rational mutations in the P22 tailspike protein. Proteins 2000, 39:89-101.
91. Schultz J., Milpetz F., Bork P., Ponting C.P. SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. U S A 1998, 95:5857-5864.
92. Shi, S., Pei, J., Sadreyev, R.I., Kinch, L.N., Majumdar, I., et al., 2009. Analysis of CASP8 targets, predictions and assessment methods. Database (Oxford) 2009, bap003.
93. Shih E.S., Hwang M.J. Alternative alignments from comparison of protein structures. Proteins 2004, 56:519-527.
94. Sikorski P., Atkins E. New model for crystalline polyglutamine assemblies and their connection with amyloid fibrils. Biomacromolecules 2005, 6:425-432.
95. Sonnhammer E.L., Eddy S.R., Birney E., Bateman A., Durbin R. Pfam: multiple sequence alignments and HMM-profiles of protein domains. Nucleic Acids Res. 1998, 26:320-322.
96. Stromme P., Mangelsdorf M.E., Shaw M.A., Lower K.M., Lewis S.M., et al. Mutations in the human ortholog of Aristaless cause X-linked mental retardation and epilepsy. Nat. Genet. 2002, 30:441-445.
97. Suits M.D., Sperandeo P., Deho G., Polissi A., Jia Z. Novel structure of the conserved gram-negative lipopolysaccharide transport protein A and mutagenesis analysis. J. Mol. Biol. 2008, 380:476-488.
98. Szklarczyk R., Heringa J. Tracking repeats using significance and transitivity. Bioinformatics 2004, 20(Suppl. 1):i311-317.
99. Tanaka Y., Sakamoto S., Kuroda M., Goda S., Gao Y.G., et al. A helical string of alternately connected three-helix bundles for the cell wall-associated adhesion protein Ebh from Staphylococcus aureus. Structure 2008, 16:488-496.
100. Testa O.D., Moutevelis E., Woolfson D.N. CC+: a relational database of coiled-coil structures. Nucleic Acids Res. 2009, 37:D315-322.
101. Tompa P. Intrinsically unstructured proteins evolve by repeat expansion. Bioessays 2003, 25:847-855.
102. Urvoas A., Guellouz A., Valerio-Lepiniec M., Graille M., Durand D., et al. Design, production and molecular structure of a new family of artificial alpha-helicoidal repeat proteins (alphaRep) based on thermostable HEAT-like repeats. J. Mol. Biol. 2010, 404:307-327.
103. van Raaij M.J., Schoehn G., Burda M.R., Miller S. Crystal structure of a heat and protease-stable part of the bacteriophage T4 short tail fibre. J. Mol. Biol. 2001, 314:1137-1146.
104. Vo A., Nguyen N., Huang H. Solenoid and non-solenoid protein recognition using stationary wavelet packet transform. Bioinformatics 2010, 26:i467-473.
105. Yeo H.J., Cotter S.E., Laarmann S., Juehne T., St Geme J.W., et al. Structural basis for host recognition by the Haemophilus influenzae Hia autotransporter. Embo J. 2004, 23:1245-1256.
106. Yoder M.D., Keen N.T., Jurnak F. New domain motif: the structure of pectate lyase C, a secreted plant virulence factor. Science 1993, 260:1503-1507.
107. Zheng N., Schulman B.A., Song L., Miller J.J., Jeffrey P.D., et al. Structure of the Cul1-Rbx1-Skp1-F boxSkp2 SCF ubiquitin ligase complex. Nature 2002, 416:703-709.