Internal symmetry in protein structures: Prevalence, functional relevance and evolution

Current Opinion in Structural Biology

Volumn 32, Issue , 2015, Pages 156-166

  Balaji, Santhanam ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD79B ANTIGEN; GUANOSINE TRIPHOSPHATASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; INITIATION FACTOR 3; INITIATION FACTOR 3B; SODIUM CALCIUM EXCHANGE PROTEIN; SORTILIN; TOLL LIKE RECEPTOR 8; UNCLASSIFIED DRUG; PROTEIN;

AMINO ACID SEQUENCE; CATALYSIS; DNA REPLICATION; HUMAN; MOLECULAR EVOLUTION; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE; REVIEW; SEQUENCE ALIGNMENT; STRUCTURE ANALYSIS; ANIMAL; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR MODEL; PROTEIN CONFORMATION;

ANIMALS; EVOLUTION, MOLECULAR; HUMANS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEINS;

EID: 84935005249     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2015.05.004     Document Type: Review

References (60)

1. Perutz M.F., Rossmann M.G., Cullis A.F., Muirhead H., Will G., North A.C. Structure of haemoglobin: a three-dimensional Fourier synthesis at 5.5-A. resolution, obtained by X-ray analysis. Nature 1960, 185:416-422.
2. Perutz M.F. Structure of hemoglobin. Brookhaven Sym Biol 1960, 13:165-183.
3. Juo Z.S., Chiu T.K., Leiberman P.M., Baikalov I., Berk A.J., Dickerson R.E. How proteins recognize the TATA box. J Mol Biol 1996, 261:239-254.
4. Goodsell D.S., Olson A.J. Structural symmetry and protein function. Annu Rev Biophys Biomol Struct 2000, 29:105-153.
5. Kinoshita K., Kidera A., Go N. Diversity of functions of proteins with internal symmetry in spatial arrangement of secondary structural elements. Protein Sci 1999, 8:1210-1217.
6. Broom A., Doxey A.C., Lobsanov Y.D., Berthin L.G., Rose D.R., Howell P.L., McConkey B.J., Meiering E.M. Modular evolution and the origins of symmetry: reconstruction of a three-fold symmetric globular protein. Structure 2012, 20:161-171.
7. Lee J., Blaber M. Experimental support for the evolution of symmetric protein architecture from a simple peptide motif. Proc Natl Acad Sci U S A 2011, 108:126-130.
8. Longo L.M., Lee J., Tenorio C.A., Blaber M. Alternative folding nuclei definitions facilitate the evolution of a symmetric protein fold from a smaller peptide motif. Structure 2013, 21:2042-2050.
9. Gonczy P. Towards a molecular architecture of centriole assembly. Nat Rev Mol Cell Biol 2012, 13:425-435.
10. Rossmann M.G. Structure of viruses: a short history. Quart Rev Biophys 2013, 46:133-180.
11. Steitz T.A., Richmond T.J., Wise D., Engelman D. The lac repressor protein: molecular shape, subunit structure, and proposed model for operator interaction based on structural studies of microcrystals. Proc Natl Acad Sci U S A 1974, 71:593-597.
12. Milner-White E.J. Quaternary structure of oligomers with dihedral symmetry. Biochem J 1972, 128. 107P.
13. Ponstingl H., Kabir T., Gorse D., Thornton J.M. Morphological aspects of oligomeric protein structures. Progr Biophys Mol Biol 2005, 89:9-35.
14. Levy E.D., Pereira-Leal J.B., Chothia C., Teichmann S.A. 3D complex: a structural classification of protein complexes. PLoS Comput Biol 2006, 2:e155.
15. Marsh J.A., Teichmann S.A. Protein flexibility facilitates quaternary structure assembly and evolution. PLoS Biol 2014, 12:e1001870.
16. Marsh J.A., Hernandez H., Hall Z., Ahnert S.E., Perica T., Robinson C.V., Teichmann S.A. Protein complexes are under evolutionary selection to assemble via ordered pathways. Cell 2013, 153:461-470.
17. Erhan S., Greller L.D., Rasco B. Symmetry patterns in trypsinogen. Int J Pept Protein Res 1977, 9:5-10.
18. Edelman G.M., Cunningham B.A., Gall W.E., Gottlieb P.D., Rutishauser U., Waxdal M.J. The covalent structure of an entire gammaG immunoglobulin molecule. Proc Natl Acad Sci U S A 1969, 63:78-85.
19. Hendrickson W.A., Ward K.B. Pseudosymmetry in the structure of myohemerythrin. J Biol Chem 1977, 252:3012-3018.
20. Blundell T., Lindley P., Miller L., Moss D., Slingsby C., Tickle I., Turnell B., Wistow G. The molecular structure and stability of the eye lens: X-ray analysis of gamma-crystallin II. Nature 1981, 289:771-777.
21. Andreeva A., Howorth D., Chothia C., Kulesha E., Murzin A.G. SCOP2 prototype: a new approach to protein structure mining. Nucleic Acids Res 2014, 42:D310-D314.
22. Sillitoe I., Lewis T.E., Cuff A., Das S., Ashford P., Dawson N.L., Furnham N., Laskowski R.A., Lee D., Lees J.G., et al. CATH: comprehensive structural and functional annotations for genome sequences. Nucleic Acids Res 2015, 43:D376-D381.
23. Myers-Turnbull D., Bliven S.E., Rose P.W., Aziz Z.K., Youkharibache P., Bourne P.E., Prlic A. Systematic detection of internal symmetry in proteins using CE-Symm. J Mol Biol 2014, 426:2255-2268.
24. Yadid I., Kirshenbaum N., Sharon M., Dym O., Tawfik D.S. Metamorphic proteins mediate evolutionary transitions of structure. Proc Natl Acad Sci U S A 2010, 107:7287-7292.
25. Blaber M., Lee J. Designing proteins from simple motifs: opportunities in Top-Down Symmetric Deconstruction. Curr Opin Struct Biol 2012, 22:442-450.
26. Voet A.R., Noguchi H., Addy C., Simoncini D., Terada D., Unzai S., Park S.Y., Zhang K.Y., Tame J.R. Computational design of a self-assembling symmetrical beta-propeller protein. Proc Natl Acad Sci U S A 2014, 111:15102-15107.
27. Yadid I., Tawfik D.S. Functional beta-propeller lectins by tandem duplications of repetitive units. Protein Eng Design Selection: PEDS 2011, 24:185-195.
28. Kim C., Basner J., Lee B. Detecting internally symmetric protein structures. BMC Bioinformat 2010, 11:303.
29. Andre I., Strauss C.E., Kaplan D.B., Bradley P., Baker D. Emergence of symmetry in homooligomeric biological assemblies. Proc Natl Acad Sci U S A 2008, 105:16148-16152.
30. Lukatsky D.B., Shakhnovich B.E., Mintseris J., Shakhnovich E.I. Structural similarity enhances interaction propensity of proteins. J Mol Biol 2007, 365:1596-1606.
31. Tanji H., Ohto U., Shibata T., Taoka M., Yamauchi Y., Isobe T., Miyake K., Shimizu T. Toll-like receptor 8 senses degradation products of single-stranded RNA. Nat Struct Mol Biol 2015, 22:109-115.
32. Andreeva A., Howorth D., Chandonia J.M., Brenner S.E., Hubbard T.J., Chothia C., Murzin A.G. Data growth and its impact on the SCOP database: new developments. Nucleic Acids Res 2008, 36:D419-D425.
33. Chandonia J.M., Hon G., Walker N.S., Lo Conte L., Koehl P., Levitt M., Brenner S.E. The ASTRAL compendium in 2004. Nucleic Acids Res 2004, 32:D189-D192.
34. Murzin A.G., Brenner S.E., Hubbard T., Chothia C. SCOP: a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 1995, 247:536-540.
35. Balaji S., Aravind L. The RAGNYA fold: a novel fold with multiple topological variants found in functionally diverse nucleic acid, nucleotide and peptide-binding proteins. Nucleic Acids Res 2007, 35:5658-5671.
36. Liu Y., Neumann P., Kuhle B., Monecke T., Schell S., Chari A., Ficner R. Translation initiation factor eIF3b contains a nine-bladed beta-propeller and interacts with the 40S ribosomal subunit. Structure 2014, 22:923-930.
37. Quistgaard E.M., Madsen P., Groftehauge M.K., Nissen P., Petersen C.M., Thirup S.S. Ligands bind to Sortilin in the tunnel of a ten-bladed beta-propeller domain. Nat Struct Mol Biol 2009, 16:96-98.
38. Kern A.D., Oliveira M.A., Coffino P., Hackert M.L. Structure of mammalian ornithine decarboxylase at 1.6 A resolution: stereochemical implications of PLP-dependent amino acid decarboxylases. Structure 1999, 7:567-581.
39. Zhang X., Yan K., Zhang Y., Li N., Ma C., Li Z., Feng B., Liu J., Sun Y., Xu Y., et al. Structural insights into the function of a unique tandem GTPase EngA in bacterial ribosome assembly. Nucleic Acids Res 2014, 42:13430-13439.
40. Wu D., Hu Q., Yan Z., Chen W., Yan C., Huang X., Zhang J., Yang P., Deng H., Wang J., et al. Structural basis of ultraviolet-B perception by UVR8. Nature 2012, 484:214-219.
41. Christie J.M., Arvai A.S., Baxter K.J., Heilmann M., Pratt A.J., O'Hara A., Kelly S.M., Hothorn M., Smith B.O., Hitomi K., et al. Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges. Science 2012, 335:1492-1496.
42. Liao J., Li H., Zeng W., Sauer D.B., Belmares R., Jiang Y. Structural insight into the ion-exchange mechanism of the sodium/calcium exchanger. Science 2012, 335:686-690.
43. Abramson J., Paz A., Philipson K.D. Structural biology. It's all in the symmetry. Science 2012, 335:669-670.
44. McLachlan A.D. Repeating sequences and gene duplication in proteins. J Mol Biol 1972, 64:417-437.
45. Tang J., James M.N., Hsu I.N., Jenkins J.A., Blundell T.L. Structural evidence for gene duplication in the evolution of the acid proteases. Nature 1978, 271:618-621.
46. Lang D., Thoma R., Henn-Sax M., Sterner R., Wilmanns M. Structural evidence for evolution of the beta/alpha barrel scaffold by gene duplication and fusion. Science 2000, 289:1546-1550.
47. Rapp M., Seppala S., Granseth E., von Heijne G. Emulating membrane protein evolution by rational design. Science 2007, 315:1282-1284.
48. Liu L., Iwata K., Yohda M., Miki K. Structural insight into gene duplication, gene fusion and domain swapping in the evolution of PLP-independent amino acid racemases. FEBS Lett 2002, 528:114-118.
49. Yadid I., Tawfik D.S. Reconstruction of functional beta-propeller lectins via homo-oligomeric assembly of shorter fragments. J Mol Biol 2007, 365:10-17.
50. Choi S., Jeon J., Yang J.S., Kim S. Common occurrence of internal repeat symmetry in membrane proteins. Proteins 2008, 71:68-80.
51. Klingenberg M. Membrane protein oligomeric structure and transport function. Nature 1981, 290:449-454.
52. Pornillos O., Chang G. Inverted repeat domains in membrane proteins. FEBS Lett 2006, 580:358-362.
53. Rueda M., Orozco M., Totrov M., Abagyan R. BioSuper: a web tool for the superimposition of biomolecules and assemblies with rotational symmetry. BMC Struct Biol 2013, 13:32.
54. Shindyalov I.N., Bourne P.E. Protein structure alignment by incremental combinatorial extension (CE) of the optimal path. Protein Eng 1998, 11:739-747.
55. Konagurthu A.S., Whisstock J.C., Stuckey P.J., Lesk A.M. MUSTANG: a multiple structural alignment algorithm. Proteins 2006, 64:559-574.
56. Madej T., Lanczycki C.J., Zhang D., Thiessen P.A., Geer R.C., Marchler-Bauer A., Bryant S.H. MMDB and VAST+: tracking structural similarities between macromolecular complexes. Nucleic Acids Res 2014, 42:D297-D303.
57. Kawasaki H., Kretsinger R.H. HVM: a web-based tool for alignment of EF-hand lobes relative to their local pseudo two-fold axes. Protein Pept Lett 2015, 22:264-269.
58. Kawasaki H., Kretsinger R.H. Structural differences among subfamilies of EF-hand proteins-a view from the pseudo two-fold symmetry axis. Proteins 2014, 82:2915-2924.
59. Han H., Kursula P. The olfactomedin domain from gliomedin is a beta-propeller with unique structural properties. J Biol Chem 2015, 290:3612-3621.
60. Bai X.C., McMullan G., Scheres S.H. How cryo-EM is revolutionizing structural biology. Trends Biochem Sci 2015, 40:49-57.