Modular evolution and the origins of symmetry: Reconstruction of a three-fold symmetric globular protein

Structure

Volumn 20, Issue 1, 2012, Pages 161-171

  Broom, Aron ^a   Doxey, Andrew C ^a,d   Lobsanov, Yuri D ^b   Berthin, Lisa G ^a   Rose, David R ^a   Howell, P Lynne ^b,c   McConkey, Brendan J ^a   Meiering, Elizabeth M ^a  

^a UNIVERSITY OF WATERLOO   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA TREFOIL PROTEIN; GLOBULAR PROTEIN; TREFOIL PEPTIDE; UNCLASSIFIED DRUG;

ARTICLE; HALOARCULA MARISMORTUI; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; SOLUBILITY; THERMOSTABILITY;

AMINO ACID SEQUENCE; COMPUTATIONAL BIOLOGY; EVOLUTION, MOLECULAR; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEINS; SEQUENCE ANALYSIS, DNA;

LOTUS;

EID: 84855771724     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2011.10.021     Document Type: Article

References (62)

1. S. Akanuma, T. Matsuba, E. Ueno, N. Umeda, and A. Yamagishi Mimicking the evolution of a thermally stable monomeric four-helix bundle by fusion of four identical single-helix peptides J. Biochem. 147 2010 371 379
2. S.F. Altschul, T.L. Madden, A.A. Schäffer, J. Zhang, Z. Zhang, W. Miller, and D.J. Lipman Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res. 25 1997 3389 3402 (Pubitemid 27359211)
3. I. André, C.E.M. Strauss, D.B. Kaplan, P. Bradley, and D. Baker Emergence of symmetry in homooligomeric biological assemblies Proc. Natl. Acad. Sci. USA 105 2008 16148 16152
4. J.W. Arndt, J. Gu, L. Jaroszewski, R. Schwarzenbacher, M.A. Hanson, F.J. Lebeda, and R.C. Stevens The structure of the neurotoxin-associated protein HA33/A from Clostridium botulinum suggests a reoccurring β-trefoil fold in the progenitor toxin complex J. Mol. Biol. 346 2005 1083 1093 (Pubitemid 40215532)
5. D. Barrick, D.U. Ferreiro, and E.A. Komives Folding landscapes of ankyrin repeat proteins: experiments meet theory Curr. Opin. Struct. Biol. 18 2008 27 34
6. H.G. Beisel, S. Kawabata, S. Iwanaga, R. Huber, and W. Bode Tachylectin-2: crystal structure of a specific GlcNAc/GalNAc-binding lectin involved in the innate immunity host defense of the Japanese horseshoe crab Tachypleus tridentatus EMBO J. 18 1999 2313 2322 (Pubitemid 29213265)
7. H.M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T.N. Bhat, H. Weissig, I.N. Shindyalov, and P.E. Bourne The Protein Data Bank Nucleic Acids Res. 28 2000 235 242 (Pubitemid 30047768)
8. O. Blixt, S. Head, T. Mondala, C. Scanlan, M.E. Huflejt, R. Alvarez, M.C. Bryan, F. Fazio, D. Calarese, and J. Stevens Printed covalent glycan array for ligand profiling of diverse glycan binding proteins Proc. Natl. Acad. Sci. USA 101 2004 17033 17038 (Pubitemid 39627769)
9. D.T. Capraro, M. Roy, J.N. Onuchic, and P.A. Jennings Backtracking on the folding landscape of the β-trefoil protein interleukin-1β? Proc. Natl. Acad. Sci. USA 105 2008 14844 14848
10. I. Chaudhuri, J. Söding, and A.N. Lupas Evolution of the β-propeller fold Proteins 71 2008 795 803
11. B.E. Collins, and J.C. Paulson Cell surface biology mediated by low affinity multivalent protein-glycan interactions Curr. Opin. Chem. Biol. 8 2004 617 625 (Pubitemid 39535723)
12. G. Dantas, B. Kuhlman, D. Callender, M. Wong, and D. Baker A large scale test of computational protein design: folding and stability of nine completely redesigned globular proteins J. Mol. Biol. 332 2003 449 460 (Pubitemid 37013512)
13. A.C. Doxey, M.D.J. Lynch, K.M. Müller, E.M. Meiering, and B.J. McConkey Insights into the evolutionary origins of clostridial neurotoxins from analysis of the Clostridium botulinum strain A neurotoxin gene cluster BMC Evol. Biol. 8 2008 316
14. V.K. Dubey, J. Lee, T. Somasundaram, S. Blaber, and M. Blaber Spackling the crack: stabilizing human fibroblast growth factor-1 by targeting the N and C terminus β-strand interactions J. Mol. Biol. 371 2007 256 268 (Pubitemid 47030467)
15. R.C. Edgar MUSCLE: multiple sequence alignment with high accuracy and high throughput Nucleic Acids Res. 32 2004 1792 1797 (Pubitemid 38832724)
16. S. Eisenbeis, and B. Höcker Evolutionary mechanism as a template for protein engineering J. Pept. Sci. 16 2010 538 544
17. N. Fernandez-Fuentes, J.M. Dybas, and A. Fiser Structural characteristics of novel protein folds PLoS Comput. Biol. 6 2010 e1000750
18. R.D. Finn, J. Mistry, J. Tate, P. Coggill, A. Heger, J.E. Pollington, O.L. Gavin, P. Gunasekaran, G. Ceric, and K. Forslund The Pfam protein families database Nucleic Acids Res. 38 Database issue 2010 D211 D222
19. D.S. Goodsell, and A.J. Olson Structural symmetry and protein function Annu. Rev. Biophys. Biomol. Struct. 29 2000 105 153 (Pubitemid 30599590)
20. E. Grahn, G. Askarieh,. Holmner, H. Tateno, H.C. Winter, I.J. Goldstein, and U. Krengel Crystal structure of the Marasmius oreades mushroom lectin in complex with a xenotransplantation epitope J. Mol. Biol. 369 2007 710 721 (Pubitemid 46709914)
21. B. Hazes The (QxW)3 domain: a flexible lectin scaffold Protein Sci. 5 1996 1490 1501 (Pubitemid 26257214)
22. R.B. Hill, D.P. Raleigh, A. Lombardi, and W.F. DeGrado De novo design of helical bundles as models for understanding protein folding and function Acc. Chem. Res. 33 2000 745 754
23. 4- half-barrels Proc. Natl. Acad. Sci. USA 101 2004 16448 16453 (Pubitemid 39557733)
24. 8- barrel protein designed from identical half-barrels Biochemistry 48 2009 1145 1147
25. A. Houbrechts, B. Moreau, R. Abagyan, V. Mainfroid, G. Préaux, A. Lamproye, A. Poncin, E. Goormaghtigh, J.-M. Ruysschaert, and J.A. Martial Second-generation octarellins: two new de novo (β/α)8 polypeptides designed for investigating the influence of β-residue packing on the α/β-barrel structure stability Protein Eng. 8 1995 249 259
26. R.S. Houliston, C. Liu, L.M.R. Singh, and E.M. Meiering pH and urea dependence of amide hydrogen-deuterium exchange rates in the β-trefoil protein hisactophilin Biochemistry 41 2002 1182 1194 (Pubitemid 34083771)
27. X. Hu, H. Wang, H. Ke, and B. Kuhlman Computer-based redesign of a β sandwich protein suggests that extensive negative design is not required for de novo β sheet design Structure 16 2008 1799 1805
28. T. Hwang, and A. Olson Water suppression that works: excitation sculpting using arbitrary wave-forms and pulsed-field gradients J. Magn. Reson. A 112 1995 275 279
29. E. Krissinel, and K. Henrick Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Acta Crystallogr. D Biol. Crystallogr. 60 2004 2256 2268 (Pubitemid 41742778)
30. D. Lang, R. Thoma, M. Henn-Sax, R. Sterner, and M. Wilmanns Structural evidence for evolution of the β/α barrel scaffold by gene duplication and fusion Science 289 2000 1546 1550
31. J. Lee, and M. Blaber Experimental support for the evolution of symmetric protein architecture from a simple peptide motif Proc. Natl. Acad. Sci. USA 108 2011 126 130
32. J. Lee, S.I. Blaber, V.K. Dubey, and M. Blaber A polypeptide "building block" for the β-trefoil fold identified by "top-down symmetric deconstruction" J. Mol. Biol. 407 2011 744 763
33. H. Li, R. Helling, C. Tang, and N. Wingreen Emergence of preferred structures in a simple model of protein folding Science 273 1996 666 669 (Pubitemid 26262124)
34. A.N. Lupas, C.P. Ponting, and R.B. Russell 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? J. Struct. Biol. 134 2001 191 203
35. E.R. Main, A.R. Lowe, S.G. Mochrie, S.E. Jackson, and L. Regan A recurring theme in protein engineering: the design, stability and folding of repeat proteins Curr. Opin. Struct. Biol. 15 2005 464 471 (Pubitemid 41073839)
36. A. Marchler-Bauer, J.B. Anderson, F. Chitsaz, M.K. Derbyshire, C. DeWeese-Scott, J.H. Fong, L.Y. Geer, R.C. Geer, N.R. Gonzales, and M. Gwadz CDD: specific functional annotation with the Conserved Domain Database Nucleic Acids Res. 37 Database issue 2009 D205 D210
37. A.D. McLachlan Three-fold structural pattern in the soybean trypsin inhibitor (Kunitz) J. Mol. Biol. 133 1979 557 563
38. E.M. Meiering, L. Serrano, and A.R. Fersht Effect of active site residues in barnase on activity and stability J. Mol. Biol. 225 1992 585 589
39. A. Miyanaga, T. Koseki, H. Matsuzawa, T. Wakagi, H. Shoun, and S. Fushinobu Crystal structure of a family 54 α-L-arabinofuranosidase reveals a novel carbohydrate-binding module that can bind arabinose J. Biol. Chem. 279 2004 44907 44914 (Pubitemid 39430903)
40. D. Mukhopadhyay The molecular evolutionary history of a winged bean alpha-chymotrypsin inhibitor and modeling of its mutations through structural analyses J. Mol. Evol. 50 2000 214 223 (Pubitemid 30429974)
41. A.G. Murzin, A.M. Lesk, and C. Chothia β-Trefoil fold. Patterns of structure and sequence in the Kunitz inhibitors interleukins-1 β and 1 α and fibroblast growth factors J. Mol. Biol. 223 1992 531 543
42. A.G. Murzin, S.E. Brenner, T. Hubbard, and C. Chothia SCOP: a structural classification of proteins database for the investigation of sequences and structures J. Mol. Biol. 247 1995 536 540
43. V. Notenboom, A.B. Boraston, S.J. Williams, D.G. Kilburn, and D.R. Rose High-resolution crystal structures of the lectin-like xylan binding domain from Streptomyces lividans xylanase 10A with bound substrates reveal a novel mode of xylan binding Biochemistry 41 2002 4246 4254 (Pubitemid 34259867)
44. C.A. Orengo, and J.M. Thornton Protein families and their evolution-a structural perspective Annu. Rev. Biochem. 74 2005 867 900 (Pubitemid 40995526)
45. C.A. Orengo, D.T. Jones, and J.M. Thornton Protein superfamilies and domain superfolds Nature 372 1994 631 634
46. J. Osterhout, T. Handel, G. Na, A. Toumadje, R. Long, P. Connolly, J. Hoch, W. Johnson, D. Live, and W. Degrado Characterization of the structural-properties of alpha-1B, a peptide designed to form a 4-helix bundle J. Am. Chem. Soc. 114 1992 331 337
47. C.N. Pace, F. Vajdos, L. Fee, G. Grimsley, and T. Gray How to measure and predict the molar absorption coefficient of a protein Protein Sci. 4 1995 2411 2423
48. J.W. Pflugrath The finer things in X-ray diffraction data collection Acta Crystallogr. D Biol. Crystallogr. 55 1999 1718 1725 (Pubitemid 29504426)
49. C.P. Ponting, and R.B. Russell Identification of distant homologues of fibroblast growth factors suggests a common ancestor for all β-trefoil proteins J. Mol. Biol. 302 2000 1041 1047
50. 8-barrel protein from an ancestral quarter-barrel stabilised by disulfide bonds J. Mol. Biol. 398 2010 763 773
51. B. Rost Twilight zone of protein sequence alignments Protein Eng. 12 1999 85 94 (Pubitemid 29103686)
52. A. Sali, and T.L. Blundell Comparative protein modelling by satisfaction of spatial restraints J. Mol. Biol. 234 1993 779 815 (Pubitemid 24007801)
53. R.S. Sedeh, A.A. Fedorov, E.V. Fedorov, S. Ono, F. Matsumura, S.C. Almo, and M. Bathe Structure, evolutionary conservation, and conformational dynamics of Homo sapiens fascin-1, an F-actin crosslinking protein J. Mol. Biol. 400 2010 589 604
54. J. Söding, and A.N. Lupas More than the sum of their parts: on the evolution of proteins from peptides Bioessays 25 2003 837 846 (Pubitemid 37081749)
55. P. Stenmark, D. Gurmu, and P. Nordlund Crystal structure of CaiB, a type-III CoA transferase in carnitine metabolism Biochemistry 43 2004 13996 14003 (Pubitemid 39482749)
56. N. Tokuriki, and D.S. Tawfik Stability effects of mutations and protein evolvability Curr. Opin. Struct. Biol. 19 2009 596 604
57. J.T. Vivian, and P.R. Callis Mechanisms of tryptophan fluorescence shifts in proteins Biophys. J. 80 2001 2093 2109 (Pubitemid 32401976)
58. S.K. Wetzel, G. Settanni, M. Kenig, H.K. Binz, and A. Plückthun Folding and unfolding mechanism of highly stable full-consensus ankyrin repeat proteins J. Mol. Biol. 376 2008 241 257
59. H.C. Winter, K. Mostafapour, and I.J. Goldstein The mushroom Marasmius oreades lectin is a blood group type B agglutinin that recognizes the Galα 1,3Gal and Galα 1,3Galβ 1,4GlcNAc porcine xenotransplantation epitopes with high affinity J. Biol. Chem. 277 2002 14996 15001 (Pubitemid 34952574)
60. I. Yadid, and D.S. Tawfik Functional β-propeller lectins by tandem duplications of repetitive units Protein Eng. Des. Sel. 24 2011 185 195
61. I. Yadid, N. Kirshenbaum, M. Sharon, O. Dym, and D.S. Tawfik Metamorphic proteins mediate evolutionary transitions of structure Proc. Natl. Acad. Sci. USA 107 2010 7287 7292
62. B.H. Zimm The scattering of light and the radial distribution function of high polymer solutions J. Chem. Phys. 16 1948 1093 1099