Structural dynamics flexibility informs function and evolution at a proteome scale

Evolutionary Applications

Volumn 6, Issue 3, 2013, Pages 423-433

  Nevin Gerek, Zeynep ^a   Kumar, Sudhir ^a,b   Banu Ozkan, Sefika ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Elastic network models; Functional genomics; Single nucleotide variants; Structural dynamics

Indexed keywords

EID: 84875686450     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12052     Document Type: Article

References (76)

1. Adzhubei, I. A., S. Schmidt, L. Peshkin, V. E. Ramensky, A. Gerasimova, P. Bork, A. S. Kondrashov et al. 2010. A method and server for predicting damaging missense mutations. Nature Methods 7:248-249.
2. Atilgan, C., and A. R. Atilgan . 2009. Perturbation-response scanning reveals ligand entry-exit mechanisms of ferric binding protein. PLoS Computational Biology 5:e1000544.
3. Atilgan, A. R., S. R. Durell, R. L. Jernigan, M. C. Demirel, O. Keskin, and I. Bahar . 2001. Anisotropy of fluctuation dynamics of proteins with an elastic network model. Biophysical Journal 80:505-515.
4. Atilgan, C., Z. N. Gerek, S. B. Ozkan, and A. R. Atilgan . 2010. Manipulation of conformational change in proteins by single-residue perturbations. Biophysical Journal 99:933-943.
5. Bahar, I., A. R. Atilgan, and B. Erman . 1997. Direct evaluation of thermal fluctuations in proteins using a single-parameter harmonic potential. Folding and Design 2:173-181.
6. Bahar, I., T. R. Lezon, A. Bakan, and I. H. Shrivastava . 2010a. Normal mode analysis of biomolecular structures: functional mechanisms of membrane proteins. Chemical Reviews 110:1463-1497.
7. Bahar, I., T. R. Lezon, L. W. Yang, and E. Eyal . 2010b. Global dynamics of proteins: bridging between structure and function. Annual Review of Biophysics 39:23-42.
8. Bartlett, G. J., C. T. Porter, N. Borkakoti, and J. M. Thornton . 2002. Analysis of catalytic residues in enzyme active sites. Journal of Molecular Biology 324:105-121.
9. Bernstein, F. C., T. F. Koetzle, G. J. Williams, E. F. Meyer Jr, M. D. Brice, J. R. Rodgers, O. Kennard et al. 1977. The Protein Data Bank: a computer-based archival file for macromolecular structures. Journal of Molecular Biology 112:535-542.
10. Bhabha, G., J. Lee, D. C. Ekiert, J. Gam, I. A. Wilson, H. J. Dyson, S. J. Benkovic et al. 2011. A dynamic knockout reveals that conformational fluctuations influence the chemical step of enzyme catalysis. Science 332:234-238.
11. Chasman, D., and R. M. Adams . 2001. Predicting the functional consequences of non-synonymous single nucleotide polymorphisms: structure-based assessment of amino acid variation. Journal of Molecular Biology 307:683-706.
12. Cheng, T. M., Y. E. Lu, M. Vendruscolo, P. Lio, and T. L. Blundell . 2008. Prediction by graph theoretic measures of structural effects in proteins arising from non-synonymous single nucleotide polymorphisms. PLoS Computational Biology 4:e1000135.
13. Cline, M. S., and R. Karchin . 2010. Using bioinformatics to predict the functional impact of SNVs. Bioinformatics 27:441-448.
14. David, A., R. Razali, M. N. Wass, and M. J. Sternberg . 2012. Protein-protein interaction sites are hot spots for disease-associated nonsynonymous SNPs. Human Mutation 33:359-363.
15. Dill, K. A., and H. S. Chan . 1997. From Levinthal to pathways to funnels. Nature Structural Biology 4:10-19.
16. Dill, K. A., and J. L. MacCallum . 2012. The protein-folding problem, 50 years on. Science 338:1042-1046.
17. Dima, R. I., and D. Thirumalai . 2006. Determination of network of residues that regulate allostery in protein families using sequence analysis. Protein Science 15:258-268.
18. Echave, J. 2008. Evolutionary divergence of protein structure: the linearly forced elastic network model. Chemical Physics Letters 457:4-6.
19. Echave, J., and F. M. Fernandez . 2009. A perturbative view of protein structural variation. Proteins: Structure, Function and Bioinformatics 78:173-180.
20. Eisenmesser, E. Z., D. A. Bosco, M. Akke, and D. Kern . 2002. Enzyme dynamics during catalysis. Science 295:1520-1523.
21. Eisenmesser, E. Z., O. Millet, W. Labeikovsky, D. M. Korzhnev, M. Wolf-Watz, D. A. Bosco, J. J. Skalicky et al. 2005. Intrinsic dynamics of an enzyme underlies catalysis. Nature 438:117-121.
22. Fitch, W. M.. 1971. Toward defining the course of evolution: minimum change for a specific tree topology. Systematic Zoology 20:406-416.
23. Franzosa, E. A., and Y. Xia . 2009. Structural determinants of protein evolution are context-sensitive at the residue level. Molecular Biology and Evolution 26:2387-2395.
24. Frauenfelder, H., G. A. Petsko, and D. Tsernoglou . 1979. Temperature-dependent X-ray diffraction as a probe of protein structural dynamics. Nature 280:558-563.
25. Frauenfelder, H., S. G. Sligar, and P. G. Wolynes . 1991. The energy landscapes and motions of proteins. Science 254:1598-1603.
26. Gerek, Z. N., and S. B. Ozkan . 2011. Change in allosteric network affects binding affinities of PDZ domains: analysis through perturbation response scanning. PLoS Computational Biology 7:e1002154.
27. Glembo, T. J., M. F. Thorpe, D. W. Farrell, Z. N. Gerek, and S. B. Ozkan . 2012. Collective dynamics differentiates functional divergence in protein evolution. PLoS Computational Biology 8:e1002428.
28. Guerois, R., J. E. Nielsen, and L. Serrano . 2002. Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations. Journal of Molecular Biology 320:369-387.
29. Gunasekaran K, Ma B, Nussinov R . 2004. Is allostery an intrinsic property of all dynamic proteins? Proteins: Structure Function and Bioinformatics: 57:433-443.
30. Henzler-Wildman, K., and D. Kern . 2007. Dynamic personalities of proteins. Nature 450:964-972.
31. Hinsen, K. 1998. Analysis of domain motions by approximate normal mode calculations. Proteins: Structure, Function and Bioinformatics 33:417-429.
32. Ikeguchi, M., J. Ueno, M. Sato, and A. Kidera . 2005. Protein structural change upon ligand binding: linear response theory. Physical Review Letters 94:078102.
33. Jackson, C. J., J. L. Foo, N. Tokuriki, L. Afriat, P. D. Carr, H. K. Kim, G. Schenk et al. 2009. Conformational sampling, catalysis, and evolution of the bacterial phosphotriesterase. Proceedings of the National Academy of Sciences of the United States of America 106:21631-21636.
34. James, L. C., and D. S. Tawfik . 2003. Conformational diversity and protein evolution-a 60-year-old hypothesis revisited. Trends in Biochemical Sciences 28:361-368.
35. Jordan, D. M., V. E. Ramensky, and S. R. Sunyaev . 2010. Human allelic variation: perspective from protein function, structure, and evolution. Current Opinion in Structural Biology 20:342-350.
36. Juritz, E., M. S. Fornasari, P. L. Martelli, P. Fariselli, R. Casadio, and G. Parisi . 2012. On the effect of protein conformation diversity in discriminating among neutral and disease related single amino acid substitutions. BMC Genomics 13(Suppl 4):S5.
37. Kalodimos, C. G.. 2012. Protein function and allostery: a dynamic relationship. Annals of the New York Academy of Sciences 1260:81-86.
38. Kamerlin, S. C., and A. Warshel . 2010. At the dawn of the 21st century: Is dynamics the missing link for understanding enzyme catalysis? Proteins: Structure, Function and Bioinformatics 78:1339-1375.
39. Kellogg, E. H., A. Leaver-Fay, and D. Baker . 2011. Role of conformational sampling in computing mutation-induced changes in protein structure and stability. Proteins: Structure, Function and Bioinformatics 79:830-838.
40. Kent, W. J., C. W. Sugnet, T. S. Furey, K. M. Roskin, T. H. Pringle, A. M. Zahler, and D. Haussler . 2002. The human genome browser at UCSC. Genome Research 12:996-1006.
41. Kumar, S., M. P. Suleski, G. J. Markov, S. Lawrence, A. Marco, and A. J. Filipski . 2009. Positional conservation and amino acids shape the correct diagnosis and population frequencies of benign and damaging personal amino acid mutations. Genome Research 19:1562-1569.
42. Kumar, S., J. T. Dudley, L. Liu, and A. J. Filipski . 2011. Phylomedicine: an evolutionary telescope to explore and diagnose the universe of disease mutations. Trends in Genetics 27:377-386.
43. Kurkcuoglu, O., Z. Kurkcuoglu, P. Doruker, and R. L. Jernigan . 2009. Collective dynamics of the ribosomal tunnel revealed by elastic network modeling. Proteins: Structure, Function and Bioinformatics 75:837-845.
44. Laskowski, R. A.. 2009. PDBsum new things. Nucleic Acids Research 37(Database issue):D355-D359.
45. Laskowski, R. A., E. G. Hutchinson, A. D. Michie, A. C. Wallace, M. L. Jones, and J. M. Thornton . 1997. PDBsum: a Web-based database of summaries and analyses of all PDB structures. Trends in Biochemical Sciences 22:488-490.
46. Lebard, D. N., and D. V. Matyushov . 2009. Energetics of bacterial photosynthesis. Journal of Physical Chemistry B 113:12424-12437.
47. Leo-Macias, A., P. Lopez-Romero, D. Lupyan, D. Zerbino, and A. R. Ortiz . 2005. An analysis of core deformations in protein superfamilies. Biophysical Journal 88:1291-1299.
48. Lin, C. P., S. W. Huang, Y. L. Lai, S. C. Yen, C. H. Shih, C. H. Lu, C. C. Huang et al. 2008. Deriving protein dynamical properties from weighted protein contact number. Proteins: Structure, Function and Bioinformatics 72:929-935.
49. Liu, Y., and I. Bahar . 2012. Sequence evolution correlates with structural dynamics. Molecular Biology and Evolution 29:2253-2263.
50. Liu, Y., L. M. Gierasch, and I. Bahar . 2010. Role of Hsp70 ATPase domain intrinsic dynamics and sequence evolution in enabling its functional interactions with NEFs. PLoS Computational Biology 6:e1000931.
51. Ma, B., C. J. Tsai, T. Haliloglu, and R. Nussinov . 2011. Dynamic allostery: linkers are not merely flexible. Structure 19:907-917.
52. Martin, A. J., M. Vidotto, F. Boscariol, T. Di Domenico, I. Walsh, and S. C. Tosatto . 2011. RING: networking interacting residues, evolutionary information and energetics in protein structures. Bioinformatics 27:2003-2005.
53. Miller, M. P., and S. Kumar . 2001. Understanding human disease mutations through the use of interspecific genetic variation. Human Molecular Genetics 10:2319-2328.
54. Mittermaier, A., A. R. Davidson, and L. E. Kay . 2003. Correlation between 2H NMR side-chain order parameters and sequence conservation in globular proteins. Journal of the American Chemical Society 125:9004-9005.
55. Ozkan, S. B., G. A. Wu, J. D. Chodera, and K. A. Dill . 2007. Protein folding by zipping and assembly. Proceedings of the National Academy of Sciences of the United States of America 104:11987-11992.
56. Potapov, V., M. Cohen, and G. Schreiber . 2009. Assessing computational methods for predicting protein stability upon mutation: good on average but not in the details. Protein Engineering Design & Selection 22:553-560.
57. Ramensky, V., P. Bork, and S. Sunyaev . 2002. Human non-synonymous SNPs: server and survey. Nucleic Acids Research 30:3894-3900.
58. Smock, R. G., and L. M. Gierasch . 2009. Sending signals dynamically. Science 324:198-203.
59. Tama, F., and Y. H. Sanejouand . 2001. Conformational change of proteins arising from normal mode calculations. Protein Engineering 14:1-6.
60. Teilum, K., J. G. Olsen, and B. B. Kragelund . 2009. Functional aspects of protein flexibility. Cellular and Molecular Life Sciences 66:2231-2247.
61. Tirion, M. M.. 1996. Large Amplitude Elastic Motions in Proteins from a Single-Parameter, Atomic Analysis. Physical Review Letters 77:1905-1908.
62. Toth-Petroczy, A., and D. S. Tawfik . 2011. Slow protein evolutionary rates are dictated by surface-core association. Proceedings of the National Academy of Sciences of the United States of America 108:11151-11156.
63. Tsai, C. J., A. del Sol, and R. Nussinov . 2008. Allostery: absence of a change in shape does not imply that allostery is not at play. Journal of Molecular Biology 378:1-11.
64. Tsodikov, O. V., M. T. Record Jr, and Y. V. Sergeev . 2002. Novel computer program for fast exact calculation of accessible and molecular surface areas and average surface curvature. Journal of Computational Chemistry 23:600-609.
65. Tzeng, S. R., and C. G. Kalodimos . 2011. Protein dynamics and allostery: an NMR view. Current Opinion in Structural Biology 21:62-67.
66. Velazquez-Muriel, J. A., M. Rueda, I. Cuesta, A. Pascual-Montano, M. Orozco, and J. M. Carazo . 2009. Comparison of molecular dynamics and superfamily spaces of protein domain deformation. BMC Structural Biology 9:6.
67. Villali, J., and D. Kern . 2010. Choreographing an enzyme's dance. Current Opinion in Chemical Biology 14:636-643.
68. Wang, Y., A. J. Rader, I. Bahar, and R. L. Jernigan . 2004. Global ribosome motions revealed with elastic network model. Journal of Structural Biology 147:302-314.
69. Wei, Q., Q. Xu, and R. L. Dunbrack Jr. 2013. Prediction of phenotypes of missense mutations in human proteins from biological assemblies. Proteins: Structure, Function and Bioinformatics: 81:199-213.
70. Wickstrom, L., E. Gallicchio, and R. M. Levy . 2012. The linear interaction energy method for the prediction of protein stability changes upon mutation. Proteins: Structure, Function and Bioinformatics 80:111-125.
71. Wilke, C. O., and D. A. Drummond . 2010. Signatures of protein biophysics in coding sequence evolution. Current Opinion in Structural Biology 20:385-389.
72. Yang, L. W., and I. Bahar . 2005. Coupling between catalytic site and collective dynamics: a requirement for mechanochemical activity of enzymes. Structure 13:893-904.
73. Yang, L., G. Song, and R. L. Jernigan . 2009. Protein elastic network models and the ranges of cooperativity. Proceedings of the National Academy of Sciences of the United States of America 106:12347-12352.
74. Yue, P., Z. Li, and J. Moult . 2005. Loss of protein structure stability as a major causative factor in monogenic disease. Journal of Molecular Biology 353:459-473.
75. Zheng, W., B. R. Brooks, and D. Thirumalai . 2006. Low-frequency normal modes that describe allosteric transitions in biological nanomachines are robust to sequence variations. Proceedings of the National Academy of Sciences of the United States of America 103:7664-7669.
76. Zheng, W., B. R. Brooks, and D. Thirumalai . 2007. Allosteric transitions in the chaperonin GroEL are captured by a dominant normal mode that is most robust to sequence variations. Biophysical Journal 93:2289-2299.