Collective dynamics differentiates functional divergence in protein evolution

PLoS Computational Biology

Volumn 8, Issue 3, 2012, Pages

  Glembo, Tyler J ^a   Farrell, Daniel W ^b   Gerek, Z Nevin ^a   Thorpe, M F ^a   Ozkan, S Banu ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYSTAL ATOMIC STRUCTURE; DYNAMICS; MAXIMUM LIKELIHOOD; MOLECULAR BIOLOGY;

BAYESIAN; BINDING STUDIES; COLLECTIVE DYNAMICS; LIGAND BINDING; MAXIMUM LIKELIHOOD METHODS; PROTEIN EVOLUTION; PROTEIN SEQUENCES; RECEPTORS PROTEINS; STEROID RECEPTORS; STRUCTURAL EVOLUTION;

PROTEINS;

GLUCOCORTICOID RECEPTOR;

AMINO ACID SEQUENCE; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; HUMAN; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; MUTATIONAL ANALYSIS; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN SECONDARY STRUCTURE; SEQUENCE ANALYSIS; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

EID: 84861139691     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002428     Document Type: Article

References (75)

1. James LC, Tawfik DS, (2003) Conformational diversity and protein evolution- a 60-year-old hypothesis revisited. Trends Biochem Sci 28: 361-368.
2. Ma B, Shatsky M, Woflson HJ, Nussinov R, (2009) Multiple diverse ligands binding at a single protein site: A matter of preexisting populations. Protein Sci 11: 184-197.
3. O'Brien PJ, Herschlag D, (1999) Catalytic promiscuity and the evolution of new enzymatic activities. Chem Biol 6: R97-R105.
4. Jimenez R, Salazar G, Yin J, Joo T, Romesberg FE, et al. (2003) Protein dynamics and the immunological evolution of molecular recognition. Proc Nat Acad Sci U S A 101: 3803-3808.
5. Zimmerman J, Oakman EL, Thorpe IF, Shi X, Abbyad P, et al. (2006) Antibody Evolution Constains Conformational Heterogeneity by Tailoring Protein Dynamics. Proc Nat Acad Sci U S A 103: 13722-13727.
6. Radkiewicz JL, CLB III, (2000) Protein Dynamics in Enzymatic Catalysis: Exploration of Dihydrofolate Reductase. J Am Chem Soc 122: 225-231.
7. Hespenheide BM, Rader AJ, Thorpe MF, Kuhn LA, (2002) Identifying protein folding cores from the evolution of flexible regions during unfolding. J Mol Graphics Modell 21: 195-207.
8. Kuhlman B, Dantas G, Ireton GC, Varani G, Stoddard BL, et al. (2003) Design of a Novel Globular Protein Fold with Atomic-Level Accuracy. Science 21: 1364-1368.
9. Jiang L, Althoff EA, Clemente FR, Doyle L, Rothlisberger D, et al. (2008) De novo computational design of retro-aldol enzymes. Science 319: 1387-1391.
10. Bolon DN, Mayo SL, (2001) Enzyme-like proteins by computational design. Proc Nat Aca Sci U S A 98: 14274-14279.
11. Looger LL, Dwyer MA, Smith JJ, Hellinga HW, (2003) Computational design of receptor and sensor proteins with novel functions. Nature 423: 185-190.
12. Joachimiak LA, Kortemme K, Stoddard BL, Baker D, (2006) Computational design of a new hydrogen bond network and at least a 300-fold specificity switch at a protein-protein interface. J Mol Biol 361: 195-208.
13. Lazar GA, Dang W, Karki S, Vafa O, Peng JS, et al. (2006) Engineered antibody Fc variants with enhanced effector function. Proc Nat Aca Sci U S A 103: 4005-4010.
14. Cochran FV, Wu SP, Wang W, Nanda V, Saven JG, et al. (2005) Computational de novo design and characterization of a four-helix bundle protein that selectively binds a nonbiological cofactor. J Am Chem Soc 127: 1346-1347.
15. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, et al. (2010) A method and server for predicting damaging missense mutations. Nat Methods 7: 248-249.
16. Chen R, Davydov EV, Sirota M, Butte AJ, (2010) Non-synonymous and synonymous coding SNPs show similar likelihood and effect size of human disease association. PLoS One 5: e13574.
17. Bromberg Y, Yachdav G, Rost B, (2008) SNAP predicts effect of mutations on protein function. Bioinformatics 24: 2397-2398.
18. Harms MJ, Thornton JW, (2010) Analyzing protein structure and function using ancestral gene reconstruction. Curr Opin Struct Biol 20: 360-366.
19. Donald JE, Shakhnovich, (2009) SDR: a database of predicted specificity-determining residues in proteins. Nucleic Acids Res 37 (suppl 1): D191-194.
20. Chakrabarti S, Lanczycki CJ, (2007) Analysis and prediction of functionally important sites in proteins. Protein Sci 16: 4-13.
21. Buske FA, Their R, Gillam EM, Boden M, (2009) In silico characterization of protein chimeras: relating sequence and function within the same fold. Proteins 77: 111-120.
22. Yang Z, Kumar S, (1996) Approximate methods for estimating the pattern of nucleotide substitution and the variation of substition rates among sites. Mol Biol Evol 13: 650-659.
23. Liberies, (2007) Ancestral Sequence reconstruction USA Oxford University Press.
24. Yokoyama S, Tada T, Zhang H, Britt L, (2008) Elucidation of phenotypic adaptations: Molecular analyses of dim-light vision proteins in vertebrates. Proc Nat Aca Sci U S A 105: 13480-13485.
25. Yokoyama S, Yang H, Starmer WT, (2008) Molecular basis of spectral tuning in the red- and green-sensitive (M/L WS) pigments in vertebrates. Genetics 179: 2037-2043.
26. Field SF, Matz MV, (2010) Retracing evolution of red flourescence in GFP-like proteins from Faviina corals. Mol Biol Evol 27: 225-233.
27. Ugalde JA, Chang BS, Matz MV, (2004) Evolution of coral pigments recreated. Science 305: 1433.
28. Gaucher EA, Govindarajan S, Ganesh OK, (2008) Paleotemperature trend for Precambrian life inferred from resurrected proteins. Nature 451: 704-707.
29. Gaucher EA, Thomson JM, Burgan MF, Benner SA, (2003) Inferring the palaeoenvironment of ancient bacteria on the basis of resurrected proteins. Nature 425: 285-288.
30. Kaiser SM, Malik HS, Emerman M, (2007) Restriction of an extinct retrovirus by the human TRIM5alpha antiviral protein. Science 316: 1756-1758.
31. Kuang D, Yao Y, Maclean D, Wang M, Hampson DR, et al. (2006) Ancestral reconstruction of the ligand-binding pocket of Family C G protein-coupled receptors. Proc Nat Aca Sci U S A 103: 14050-14055.
32. Thomson JM, Gaucher EA, Burgan MF, Kee DWD, Li T, et al. (2005) Resurrecting ancestral alcohol dehydrogenases from yeast. Nat Genet 37: 630-635.
33. Bridgham JT, Ortlund EA, Thornton JW, (2009) An epistatic ratchet constrains the direction of glucocorticoid receptor evolution. Nature 461: 515-519.
34. Ortlund EA, Bridgham JT, Redinbo MR, Thornton JW, (2007) Crystal Structure fo an Ancient Protein: Evolution by Conformational Epistasis. Science 317: 1544-1548.
35. Xia Y, Levitt M, (2004) Simulating protein evolution in sequence and structure space. Curr Opin Struct Biol 14: 202-207.
36. Kar G, Keskin O, Gursoy A, Nussinov R, (2010) Allostery and population shift in drug discovery. Curr Opin Pharmacol 10: 715-722.
37. Bakan A, Meireles LM, Bahar I, (2011) ProDy: Protein Dynamics Inferred from Theory and Experiments. Bioinformatics 27: 1575-1577.
38. Liu Y, Gierasch LM, Bahar I, (2010) Role of Hsp70 ATPase domain intrinsic dynamics and sequence evolution in enabling its functional interactions with NEFs. PLoS Comp Biol 6: PMID: 20862304.
39. Todd AE, Orengo CA, Thornton JM, (2001) Evolution of function in protein superfamilies, from a structural perspective. J Mol Biol 307: 1113-1143.
40. Tokuriki N, Oldfield CJ, Uversky VN, Berezovsky IN, Tawfick DS, (2009) Do viral proteins possess unique biophysical features. Trends Biochem Sci 34: 53-59.
41. Tokuriki N, Tawfik DS, (2009) Stability effects of mutations and protein evolvability. Curr Opin Struct Biol 19: 596-604.
42. Jackson CJ, Foo J-L, Tokuriki N, Agriat L, Carr PD, et al. (2009) Conformational sampling, catalysis, and evolution of bacterial phosphotriesterase. Proc Nat Aca Sci U S A 106: 21631-21636.
43. Bhattacharyya M, Vishveshwara S, (2011) Probing the Allosteric Mechanism in Pyrrolysyl-tRNA Synthetase Using Energy-Weighted Network Formalism. Biochemistry 50: 6225-6236.
44. Ghosh A, Vishveshwara S, (2008) Variations in Clique and Community Patterns in Protein Structures during Allosteric Communication: Investigation of Dynamically Equilibrated Structures of Methionyl tRNA Synthetase Complexes. Biochemistry 47: 11398-11407.
45. Glembo TJ, Ozkan SB, (2010) Union of Geometric Constraint-Based Simulations with Molecular Dynamics for Protein Structure Prediction. Biophys J 98: 1046-1054.
46. Ozkan SB, Wu GA, Chodera JD, Dill KA, (2007) Protein folding by zipping and assembly. Proc Nat Aca Sci U S A 104: 11987-11992.
47. Wells S, Menor S, Hespenheide B, Thorpe MF, (2005) Constrained geometric simulation of diffusive motion in proteins. Phys Biol 2: S127-S136.
48. Farrell DW, Speranskiy K, Thorpe MF, (2010) Generating Stereochemically Acceptable Protein Pathways. Proteins 78: 2908-2921.
49. Li Y, Suino K, Daugherty J, Xu HE, (2005) Structural and Biochemical Mechanisms for the Specificity of Hormone Binding and Coactivator Assembly by Mineralocorticoid Receptor. Mol Cell 19: 367-380.
50. Cozzetto D, Kryshtafovych A, Tramontano A, (2009) Evaluation of CASP8 model quality predictions. Proteins 77: 157-166.
51. Jones TA, Kleywegt GJ, (1999) Comparative Modeling: Assessment. Proteins 3: 30-46.
52. Tress M, Ezkurdia I, Grana O, Lopez G, Valencia A, (2005) Assessment of Predictions Submitted for the CASP6 Comparative Modeling Category. Proteins 7: 27-45.
53. Peterson EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comp Chem 13: 1605-1612.
54. Wintrode PL, Zhang D, Vaidehi N, Arnold FH, Goddard WAI, (2003) Protein dynamics in a family of laboratory evolved thermophilic Enzymes. J Mol Biol 327: 745-757.
55. Soskine M, Tawfik DS, (2010) Mutational effects and the evolution of new protein functions. Nature 11: 572-583.
56. McIntosh BE, Hogenesch JB, Bradfield CA, (2010) Mammalian Per-Arnt-Sim proteins in environmental adaptation. Annu Rev Physiol 72: 625-645.
57. Zheng W, Brooks BR, Thirumalai D, (2006) Low-frequency normal modes that describe allosteric transitions in biological nanomachines are robust to sequence variations. Proc Nat Aca Sci U S A 103: 7664-7669.
58. Tawfik DS, (2010) Messy biology and the origins of evolutionary innovations. Nat Chem Biol 6: 692-696.
59. Campagnoli MF, Pimazzoni R, Bosio S, Zecchina G, DeGobbi M, et al. (2002) Onset of cataract in early infancy associated with the 32G→C transtion in the iron responsive element of L-ferritin. Eur J Pediatr 161: 499-502.
60. Curtis ARJ, Fey C, Morris CM, Bindoff LA, Ince PG, et al. (2001) Mutation in the gene encoding ferritin light polypeptide causes dominant adult-onset basal ganglia disease. Nat Genet 28: 350-354.
61. Foglieni B, Ferrari F, Goldwurm S, Santambrogio P, Castiglioni E, et al. (2007) Analysis of ferritin genes in Parkinson's disease. Clin Chem Lab Med 45: 1450-1456.
62. Wang Z, Li C, ellenburg M, Soistman E, Ruble J, et al. (2006) Structure of human ferritin L chain. Acta Crystallogr D D62: 800-806.
63. Shell M, Ozkan S, Voelz V, G Wu KD, (2009) Blind Test of Physics-Based Prediction of Protein Structures. Biophys J 96: 917-924.
64. Cygler M, Schrag JD, Sussman JL, Harel M, Silman I, et al. (1993) Relationship between sequence conservation and three-dimensional structure in a large family of esterases, lipases, and related proteins. Protein Sci 2: 366-382.
65. Redfern OC, Dessailly B, Orengo CA, (2008) Exploring the structure and function paradigm. Curr Opin Struct Biol 18: 394-402.
66. Sadowski MI, Jones DT, (2009) The sequence-structure relationship and protein funciton prediction. Curr Opin Struct Biol 19: 357-362.
67. Mehta PK, Heringa J, Argos P, (1995) A simple and fast approach to prediction of protein secondary structure from multiply aligned sequences with accuracy above 70%. Protein Sci 4: 2517-2525.
68. Biggadike K, Bledsoe RK, Coe DM, Cooper TW, House D, et al. (2009) Design and x-ray crystal structures of high-potency nonsteroidal glucocorticoid agonists exploiting a novel binding site on the receptor. Proc Nat Acad Sci U S A 106: 18114-18119.
69. Seitz T, Thoma R, Schoch GA, Stihle M, Benz J, et al. (2010) Enhancing stability and solubility of the glucocorticoid receptor ligand-binding domain by high-throughput library screening. J Mol Biol 403: 562-77.
70. Stehlin-Gaon C, Willmann D, Zeyer D, Sanglier S, Dorsselaer AV, et al. (2003) All-trans retinoic acid is a ligand for the orphan nuclear receptor ROR beta. Nat Struct Biol 10: 820-825.
71. Suino-Powell K, Xu Y, Zhang C, Tao YG, Tolbert WD, et al. (2008) Doubling the size of the glucocorticoid receptor ligand binding pocket by deacylcortivazol. Mol Cell Biol 28: 1915-1923.
72. Farrell DW, Speranskiy K, Thorpe MF, (2010) Generating stereochemically acceptable protein pathways. Proteins 78: 2908-2921.
73. Roitberg A, Okur A, Simmerling C, (2007) Coupling of Replica Exchange Simulations to a Non-Boltzmann Structure Reservoir. J Phys Chem B 111: 2415-2418.
74. Pearlman D, Case D, Caldwell J, Ross W, Cheatham T III, et al. (1995) AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules. Comput Phys Commun 91: 1-41.
75. Amadei A, Linssen ABM, Berendson HJC, (1993) Essential Dynamics of Proteins. Proteins 17: 412-425.