Protein repeats: Structures, functions, and evolution

Journal of Structural Biology

Volumn 134, Issue 2-3, 2001, Pages 117-131

  Andrade, Miguel A ^a,b   Perez Iratxeta, Carolina ^a,b   Ponting, Chris P ^c  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; LEUCINE; PEPTIDE; PROTEIN;

AMINO ACID SEQUENCE; MOLECULAR EVOLUTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; STRUCTURE ANALYSIS; SURFACE PROPERTY;

ARMADILLO;

EID: 0035783061     PISSN: 10478477     EISSN: None     Source Type: Journal    
DOI: 10.1006/jsbi.2001.4392     Document Type: Article

References (108)

1. Abergel, C., Bouveret, E., Claverie, J. M., Brown, K., Rigal, A., Lazdunski, C., and Benedetti, H. (1999) Structure of the Escherichia coli TolB protein determined by MAD methods at 1.95 A resolution, Struct. Fold Des. 7, 1291.
2. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs, Nucleic Acids Res. 25, 3389-3402.
3. Andrade, M. A., and Bork, P. (1995) HEAT repeats in the Huntington's disease protein, Nature Genet. 11, 115-116.
4. Andrade, M. A., Petosa, C., O'Donoghue, S. I., Müller, C. W., and Bork, P. (2001) Comparison of ARM and HEAT protein-repeats, J. Mol. Biol. 309, 1-18.
5. Andrade, M. A., Ponting, C., Gibson, T., and Bork, P. (2000) Identification of protein repeats and statistical significance of sequence comparisons, J. Mol. Biol. 298, 521-537.
6. Argos, P., Pedersen, K., Marks, M. D., and Larkins, B. A. (1982) A structural model for maize zein proteins, J. Biol. Chem. 257, 9984-9990.
7. Bairoch, A., and Apweiler, R. (2000) The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000, Nucleic Acids Res. 28, 45-48.
8. Barton, G. J., Newman, R. H., Freemont, P. S., and Crumpton, M. J. (1991) Amino acid sequence analysis of the annexin super-gene family of proteins, Eur. J. Biochem. 198, 749-760.
9. Batchelor, A. H., Piper, D. E., de la Brousse, F. C., McKnight, S. L., and Wolberger, C. (1998) The structure of GABPα/β: An ETS domain-ankyrin repeat heterodimer bound to DNA, Science 279, 1037-1041.
10. Bateman, A., Birney, E., Durbin, R., Eddy, S. R., Howe, K. L., and Sonnhammer, E. L. (2000) The Pfam protein families database, Nucleic Acids Res. 28, 263-266.
11. Bayliss, R., Littlewood, T., and Stewart, M. (2000) Structural basis for the interaction between FxFG nucleoporin repeats and importin-beta in nuclear trafficking, Cell 102, 99-108.
12. Boguski, M. S., Murray, A. W., and Powers, S. (1992) Novel repetitive sequence motifs in the alpha and beta subunits of prenyl-protein transferases and homology of the subunit to the MAD2 gene product of yeast, New Biol. 4, 408-411.
13. Bork, P., and Gibson, T. J. (1996) Applying motif and profile searches, Methods Enzymol. 266, 162-184.
14. Burkhard, P., Stetefeld, J., and Strelkov, S. V. (2001) Coiled coils: A highly versatile protein folding motif, Trends Cell Biol. 11, 82-88.
15. Cingolani, G., Petosa C., Weis K., and Müller, C. W. (1999) Structure of importin-β bound to the IBB domain of importin-α, Nature 399, 221-229.
16. Chook, Y. M., and Blobel, G. (1999) Structure of the nuclear transport complex karyopherin-beta2-Ran x GppNHp, Nature 399, 230-237.
17. Conti, E., Uy, M., Leighton, L., Blobel, G., and Kuriyan, J. (1998) Crystallographic analysis of the recognition of a nuclear localization signal by the nuclear import factor karyopherin alpha, Cell 94, 193-204.
18. Das, A. K., Cohen, P. W., and Barford, D. (1998) The structure of the tetratricopeptide repeats of protein phosphatase 5: Implications for TPR-mediated protein-protein interactions, EMBO J. 17, 1192-1199.
19. Diederich, R. J., Matsuno, K., Hing, H., and Artavanis-Tsakonas, S. (1994) Cytosolic interaction between deltex and Notch ankyrin repeats implicates deltex in the Notch signaling pathway, Development 120, 473-481.
20. Eddy, S. (1998) Profile hidden Markov models, Bioinformatics 14, 755-763.
21. Eriksson, A. E., Cousens, L. S., and Matthews, B. W. (1993) Refinement of the structure of human basic fibroblast growth factor at 1.6 A resolution and analysis of presumed heparin binding sites by selenate substitution, Protein Sci. 2, 1274-1284.
22. Fülöp, V., Böcskei, Z., and Polgár, L. (1998) Prolyl oligopeptidase: An unusual β-propeller domain regulates proteolysis, Cell 94, 161-170.
23. Gindhart, J. G., Jr., and Goldstein, L. S. (1996) Tetratrico peptide repeats are present in the kinesin light chain, Trends Biochem Sci. 21, 52-53.
24. Gorina, S., and Pavletich, N. P. (1996) Structure of the p53 tumor suppressor bound to the ankyrin and SH3 domains of 53BP2, Science 274, 1001-1005.
25. Graham, L. A., Liou, Y. C., Walker, V. K., and Davies, P. L. (1997) Hyperactive antifreeze protein from beetles, Nature 388, 727-728.
26. Green, N. M., Wrigley, N. G., Russell, W. C., Martin, S. R., and McLachlan, A. D. (1983) Evidence for a repeating cross-beta sheet structure in the adenovirus fibre, EMBO J. 2, 1357-1365.
27. Groves, M. R., Hanlon, N., Turowski, P., Hemmings, B. A., and Bartford, D. (1999) The structure of the protein phosphatase 2A PR65/A subunit reveals the conformation of its 15 tandemly repeated HEAT motifs, Cell 96, 99-110.
28. Gurian-Sherman, D., and Lindow, S. E. (1993) Bacterial ice nucleation: Significance and molecular basis, FASEB J. 7, 1338-1343.
29. Hayashi, C. Y., and Lewis, R. V. (2000) Molecular architecture and evolution of a modular spider silk protein gene, Science 287, 1477-1479.
30. Heger, A., and Holm, L. (2000) Rapid automatic detection and alignment of repeats in protein sequences, Proteins 41, 224-237.
31. Hildebrand, A., Romaris, M., Rasmussen, L. M., Heinegard, D., Twardzik, D. R., Border, W. A., and Ruoslahti, E. (1994) Interaction of the small interstitial proteoglycans biglycan, decorin and fibromodulin with transforming growth factor beta, Biochem. J. 302, 527-534.
32. Hill, R. E., and Hastie, N. D. (1987) Accelerated evolution in the reactive centre regions of serine protease inhibitors, Nature 326, 96-99.
33. Hirano, K., Phan, B. C., and Hartshorne, D. J. (1994) Interactions of the subunits of smooth muscle myosin phosphatase, J. Biol. Chem. 272, 3683-3688.
34. Iozzo, R. V. (1998) Matrix proteoglycans: From molecular design to cellular function, Annu. Rev. Biochem. 67, 609-652.
35. Ito, N., Phillips, S. E., Stevens, C., Ogel, Z. B., McPherson, M. J., Keen, J. N., Yadav, K. D., Ju, B. G., Jeong, S., Bae, E., Hyun, S., Carroll, S. B., Yim, J., and Kim, J. (2000) Fringe forms a complex with Notch, Nature 405, 191-195.
36. Kickhoefer, V. A., Rajavel, K. S., Scheffer, G. L., Dalton, W. S., Scheper, R. J., and Rome, L. H. (1998) Vaults are up-regulated in multidrug-resistant cancer cell lines, J. Biol. Chem. 273, 8971-8974.
37. Kobe, B., and Deisenhofer, J. (1994) The leucine-rich repeat: A versatile binding motif, Trends Biochem. Sci. 19, 415-421.
38. Kobe, B., and Deisenhofer, J. (1995) A structural basis of the interactions between leucine-rich repeats and protein ligands, Nature 374, 183-186.
39. Kong, L. B., Siva, A. C., Rome, L. H., and Stewart, P. L. (1999) Structure of the vault, a ubiquitous cellular component, Structure 7, 371-379.
40. Lamb, J. R., Tugendreich, S., and Hieter, P. (1995) Tetratrico peptide repeat interactions: To TPR or not to TPR? Trends Biochem. Sci. 20, 257-259.
41. phox in complex with Rac-GTP, Mol. Cell 6, 899-907.
42. Liou, Y. C., Tocilj, A., Davies, P. L., and Jia, Z. (2000) Mimicry of ice structure by surface hydroxyls and water of a beta-helix antifreeze protein, Nature 406, 322-324.
43. Lo Conte, L., Ailey, B., Hubbard, T. J., Brenner, S. E., Murzin, A. G., and Chothia, C. (2000) SCOP: A structural classification of proteins database, Nucleic Acids Res. 28, 257-259.
44. Lohi, O., and Lehto, V. P. (1998) VHS domain marks a group of proteins involved in endocytosis and vesicular trafficking, FEBS Lett. 440, 255-257.
45. Lux, S. E., John, K. M., and Bennett, V. (1990) Analysis of cDNA for human erythrocyte ankyrin indicates a repeated structure with homology to tissue-differentiation and cell-cycle control proteins, Nature 344, 36-42.
46. Malik, H. S., Eickbush, T. H., and Goldfarb, D. S. (1997) Evolutionary specialization of the nuclear targeting apparatus, Proc. Natl. Acad. Sci. USA 94, 13738-13742.
47. Mao, Y., Nickitenko, A., Duan, X., Lloyd, T. E., Wu, M. N., Bellen, H., and Quiocho, F. A. (2000) Crystal structure of the VHS and FYVE tandem domains of Hrs, a protein involved in membrane trafficking and signal transduction, Cell 100, 447-456.
48. Marcotrigiano, J., Lomakin, I. B., Sonenberg, N., Pestova, T. V., Hellen, C. U. T., and Burley, S. K. (2001) A conserved HEAT domain within eIF4G directs assembly of the translation initiation machinery, Mol. Cell 7, 193-203.
49. Marcotte, E. M., Pellegrini, M., Yeates, T. O., and Eisenberg, D. (1999) A census of protein repeats, J. Mol. Biol. 293, 151-160.
50. Marino, M., Braun, L., Cossart, P., and Ghosh, P. (1999) Structure of the lnlB leucine-rich repeats, a domain that triggers host cell invasion by the bacterial pathogen L. monocytogenes, Mol. Cell 4, 1063-1072.
51. Matsushima, N., Danno, G., Takezawa, H., and Izumi, Y. (1997) Three-dimensional structure of maize alpha-zein proteins studied by small-angle X-ray scattering, Biochem. Biophys. Acta 1339, 14-22.
52. McLachlan, A. D. (1983) Analysis of gene duplication repeats in the myosin rod, J. Mol. Biol. 169, 15-30.
53. Mott, R., and Tribe, R. (1999) Approximate statistics of gapped alignments, J. Comput. Biol. 6, 91-112.
54. Mott, R. (2000) Accurate formula for P-values of gapped local sequence and profile alignments, J. Mol Biol. 300, 649-659.
55. Murzin, A. G. (1999) Structural principles for the propeller assembly of beta-sheets: The preference for seven-fold symmetry, Proteins 14, 191-201.
56. Murzin, A. G., Lesk, A. M., and Chothia, C. (1992) β-trefoil fold. Patterns of structure and sequence in the Kunitz inhibitors interleukins-1 beta and 1 alpha and fibroblast growth factors, J. Mol. Biol. 223, 531-543.
57. Neer, E. J., Schmidt, C. J., Nambudripad, R., and Smith, T. F. (1994) The ancient regulatory-protein family of WD-repeat proteins, Nature 371, 297-300.
58. Neer, E. J., and Smith, T. F. (1996) G protein heterodimers: New structures propel new questions, Cell 84, 175-178.
59. Neuwald, A. F., and Hirano, T. (2000) HEAT repeats associated with condensins, cohesins, and other complexes involved in chromosome-related functions, Genome Res. 10, 1445-1452.
60. Oh, B., Hwang, S. Y., Solter, D., and Knowles, B. B. (1997) Spindlin, a major maternal transcript expressed in the mouse during the transition from oocyte to embryo, Development 124, 493-503.
61. Ohno, S. (1970) Evolution by Gene Duplication, Springer-Verlag, Berlin.
62. Ordway, R. W., Pallanck, L., and Ganetzky, B. (1994) A TPR domain in the SNAP secretory proteins, Trends Biochem Sci. 19, 530-531.
63. Pascual, J., Pfuhl, M., Walther, D., Saraste, M., and Nilges, M. (1997) Solution structure of the spectrin repeat: A left-handed antiparallel triple-helical coiled-coil, J. Mol. Biol. 273, 740-751.
64. Peifer, M., Berg, S., and Reynolds, B. (1994) A repeating amino acid motif shared by proteins with diverse cellular roles, Cell 76, 789-791.
65. Pellegrini, M., Marcotte, E. M., and Yeates, T. O. (1999) A fast algorithm for genome-wide analysis of proteins with repeated structures, Proteins 35, 440-446.
66. Penkett, C. J., Dobson, C. M., Smith, L. J., Bright, J. R., Pickford, A. R., Campbell, I. D., and Potts, J. R. (2000) Identification of residues involved in the interaction of Staphylococcus aureus fibronectin-binding protein with the (4)F1(5)F1 module pair of human fibronectin using heteronuclear NMR spectroscopy, Biochemistry 39, 2887-2893.
67. Peters, J. W., Stowell, M. H., and Rees, D. C. (1996) A leucine-rich repeat variant with a novel repetitive protein structural motif, Nat. Struct. Biol. 3, 991-994.
68. Pfuhl, M., Winder, S. J., Castiglione Morelli, M. A., Labeit, S., and Pastore, A. (1996) Correlation between conformational and binding properties of nebulin repeats, J. Mol. Biol. 257, 367-384.
69. Ponting, C. P. (2000) Proteins of the endoplasmic-reticulum-associated degradation pathway: Domain detection and function prediction, Biochem. J. 351, 527-535.
70. Ponting, C. P., and Pallen, M. J. (1999a) A beta-propeller domain within TolB, Mol. Microbiol. 31, 739-740.
71. Ponting, C. P., and Pallen, M. J. (1999b) β-propeller repeats and a PDZ domain in the tricorn protease: Predicted self-compartmentalisation and C-terminal polypeptide-binding strategies of substrate selection, FEMS Microbiol. Lett. 179, 447-451.
72. Ponting, C. P., Aravind, L., Schultz, J., Bork, P., and Koonin, E. V. (1999) Eukaryotic signalling domain homologues in archaea and bacteria: Ancient ancestry and horizontal gene transfer, J. Mol. Biol. 289, 729-745.
73. Ponting, C. P., and Birney, E. (2000) Identification of domains from protein sequences, in Webster, D. (Ed.), Protein Structure Prediction, Humana Press, Clifton, NJ.
74. Ponting, C. P., and Russell, R. B. (2000) Identification of distant homologues of fibroblast growth factors suggests a common ancestor for all β-trefoil proteins, J. Mol. Biol. 302, 1041-1047.
75. Preker, P. J., and Keller, W. (1998) The HAT helix, a repetitive motif implicated in RNA processing, Trends Biochem. Sci. 23, 15-16.
76. Price, S. R., Evans, P. R., and Nagai, K. (1998) Crystal structure of the spliceosomal U2B"-U2A′ protein complex bound to a fragment of U2 small nuclear RNA, Nature 394, 645-650.
77. Ray, M.-C., Germon, P., Vianney, A., Portalier, R., and Lazzaroni, J. C. (2000) Identification by genetic suppression of Escherichia coli TolB residues important for TolB-Pal interaction, J. Bacteriol. 182, 821-824.
78. Renault, L., Nassar, N., Vetter, I., Becker, J., Klebe, C., Roth, M., and Wittinghofer, A. (1998) The 1.7 A crystal structure of the regulator of the chromosome condensation (RCC1) reveals a seven-bladed propeller, Nature 392, 97-101.
79. Riggleman, B., Wieschaus, E., and Schedl, P. (1989) Molecular analysis of the armadillo locus: Uniformly distributed transcripts and a protein with novel internal repeats are associated with a Drosophila segment polarity gene, Genes Dev. 3, 96-113.
80. Russell, R. B., Sasieni, P. D., and Sternberg, M. J. E. (1998) Supersites within superfolds. Binding site similarity in the absence of homology, J. Mol. Biol. 282, 903-918.
81. Saupe, S., Turcq, B., and Begueret, J. (1995) A gene responsible for vegetative incompatibility in the fungus Podospora anserina encodes a protein with a GTP-binding motif and G beta homologous domain, Gene 162, 135-139.
82. Scheufler, C., Brinker, A., Bourenkov, G., Pegoraro, S., Moroder, L., Bartunik, H., Hartl, F. U., and Moarefi, I. (2000) Structure of TPR domain-peptide complexes: Critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine, Cell 101, 199-210.
83. Sedgwick, S. G., and Smerdon, S. J. (1999) The ankyrin repeat: A diversity of interactions on a common structural framework, Trends Biochem. Sci. 24, 311-316.
84. Schuler, G. D., Altschul, S. F., and Lipman, D. J. (1991) A workbench for multiple alignment construction and analysis, Proteins 9, 180-190.
85. Schultz, J., Doerks, T., Ponting, C. P., Copley, R. R., and Bork, P. (2000) More than 1000 putative novel human signalling proteins revealed by EST data mining, Nature Genet. 25, 201-204.
86. Schultz, J., Milpetz, F., Bork, P., and Ponting, C. P. (1998) SMART, a simple modular architecture research tool: Identification of signaling domains, Proc. Natl. Acad. Sci. USA 95, 5857-5864.
87. Shen, Y., Romo, G. M., Dong, J., Schade A., McIntire, L. V., Kenny, D., Whisstock, J. C., Berndt, M. C., López, J. A., and Andrews, R. K. (2000) Requirement of leucine-rich repeats of glycoprotein (GP) Ib for shear-dependent and static binding of von Willebrand factor to the platelet membrane GP Ib-IX-V complex, Blood 95, 903-910.
88. Sikorski, R. S., Boguski, M. S., Goebl, M., and Hieter, P. (1990) A repeating amino acid motif in CDC23 defines a family of proteins and a new relationship among genes required for mitosis and RNA synthesis, Cell 60, 307-317.
89. A protein βγ dimer at 2.1Å resolution, Nature 379, 369-374.
90. Sonnhammer, E. L., and Durbin, R. (1995) A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis, Gene 167, GC1-10.
91. Speicher, D. W., and Marchesi, V. T. (1984) Erythrocyte spectrin is comprised of many homologous triple helical segments, Nature 311, 177-180.
92. Springer, T. A. (1997) Folding of the N-terminal, ligand-binding region of integrin alpha-subunits into a beta-propeller domain, Proc. Natl. Acad. Sci. USA 94, 65-72.
93. Springer, T. A. (1998) An extracellular beta-propeller module predicted in lipoprotein and scavenger receptors, tyrosine kinases, epidermal growth factor precursor, and extracellular matrix components, J. Mol. Biol. 283, 837-862.
94. Svensson, L., Narlid, I., and Oldberg, A. (2000) Fibromodulin and lumican bind to the same region on collagen type I fibrils, FEBS Lett. 470, 178-182.
95. Tsai, C. J., Lin, S. L, Wolfson, H. J., and Nussinov, R. (1997) Studies of protein-protein interfaces: A statistical analysis of the hydrophobic effect, Protein Sci. 6, 53-64.
96. Tsuda, S., Ito, A., and Matsushima, N. (1997) A hairpin-loop conformation in tandem repeat sequence of the ice nucleation protein revealed by NMR spectroscopy, FEBS Lett. 409, 227-231.
97. Van Der Biezen, E. A., and Jones, J. D. G. (1998) Plant disease-resistance proteins and the gene-for-gene concept, Trends Biochem. Sci. 23, 454-456.
98. van Raaij, M. J., Mitraki, A., Lavigne, G., and Cusack, S. (1999) A triple beta-spiral in the adenovirus fibre shaft reveals a new structural motif for a fibrous protein, Nature 401, 935-938.
99. Vasu, S. K., Kedersha, N. L., and Rome, L. H. (1993) cDNA cloning and disruption of the major vault protein alpha gene (mvpA) in Dictyostelium discoideum, J. Biol. Chem. 268, 15356-153560.
100. Walker, E. H., Perisic, O., Ried, C., Stephens, L., and Williams, R. L. (1999) Structural insights into phosphoinositide 3-kinase catalysis and signalling, Nature 402, 313-320.
101. Watari, J., Takata, Y., Ogawa, M., Sahara, H., Koshino, S., Onnela, M. L., Airaksinen, U., Jaatinen, R., Penttila, M., and Keranen, S. (1994) Molecular cloning and analysis of the yeast flocculation gene FLO1, Yeast 10, 211-225.
102. Weng, X., Luecke, H., Song, I. S., Kang, D. S., Kim, S. H., and Huber, R. (1993) Crystal structure of human annexin I at 2.5 A resolution, Protein Sci. 2, 448-458.
103. Wharton, K. A., Johansen, K. M., Xu, T., and Artavanis-Tsakonas, S. (1985) Nucleotide sequence from the neurogenic locus notch implies a gene product that shares homology with proteins containing EGF-like repeats, Cell 43, 567-581.
104. Wheelan, S., Marchler-Bauer, A., and Bryant, S. H. (2000) Domain size distribution can predict domain boundaries, Bioinformatics 16, 613-619.
105. Wiche, G., Becker, B., Luber, K., Weitzer, G., Castanon, M. J., Hauptmann, R, Stratowa, C., and Stewart, M. (1991) Cloning and sequencing of rat plectin indicates a 466-kD polypeptide chain with a three-domain structure based on a central alpha-helical coiled coil, J. Cell. Biol. 114, 83-99.
106. Worrall, D., Elias, L., Ashford, D., Smallwood, M., Sidebottom, C., Lillford, P., Telford, J., Holt, C., and Bowles, D. (1998) A carrot leucine-rich-repeat protein that inhibits ice recrystallization, Science 282, 115-117.
107. Wren, B. W. (1991) A family of clostridial and streptococcal ligand-binding proteins with conserved C-terminal repeat sequences, Mol. Microbiol. 5, 797-803.
108. Zhang, K., Smouse, D., and Perrimon, N. (1991) The crooked neck gene of Drosophila contains a motif found in a family of yeast cycle genes, Genes Dev. 5, 1080-1091.