Simulating protein evolution in sequence and structure space

Current Opinion in Structural Biology

Volumn 14, Issue 2, 2004, Pages 202-207

  Xia, Yu ^a   Levitt, Michael ^b  

^a YALE UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; ANALYTIC METHOD; ATOM; METHODOLOGY; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MOLECULAR MODEL; POINT MUTATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; REVIEW; SIMULATION; STOCHASTIC MODEL; STRUCTURE ANALYSIS; THERMODYNAMICS; WILD TYPE;

ALGORITHMS; AMINO ACID SEQUENCE; COMPUTER SIMULATION; EVOLUTION, MOLECULAR; PROTEIN FOLDING; PROTEINS; SEQUENCE ANALYSIS, PROTEIN;

EID: 1842839788     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2004.03.001     Document Type: Review

References (71)

1. Onuchic J.N., Wolynes P.G. Theory of protein folding. Curr Opin Struct Biol. 14:2004;70-75.
2. Fontana W. Modelling 'evo-devo' with RNA. Bioessays. 24:2002;1164-1177.
3. Voigt C.A., Kauffman S., Wang Z.G. Rational evolutionary design: the theory of in vitro protein evolution. Adv Protein Chem. 55:2000;79-160.
4. Arnold F.H. Combinatorial and computational challenges for biocatalyst design. Nature. 409:2001;253-257.
5. Bryngelson J.D., Wolynes P.G. Spin glasses and the statistical mechanics of protein folding. Proc Natl Acad Sci USA. 84:1987;7524-7528.
6. Dill K.A., Bromberg S., Yue K., Fiebig K.M., Yee D.P., Thomas P.D., Chan H.S. Principles of protein folding - a perspective from simple exact models. Protein Sci. 4:1995;561-602.
7. Shakhnovich E.I. Theoretical studies of protein-folding thermodynamics and kinetics. Curr Opin Struct Biol. 7:1997;29-40.
8. Chan H.S., Bornberg-Bauer E. Perspectives on protein evolution from simple exact models. Appl Bioinformatics. 1:2002;121-144 An in-depth and comprehensive review of the use of simple exact models to study protein evolution.
9. Bornberg-Bauer E. How are model protein structures distributed in sequence space? Biophys J. 73:1997;2393-2403.
10. Bornberg-Bauer E., Chan H.S. Modeling evolutionary landscapes: mutational stability, topology, and superfunnels in sequence space. Proc Natl Acad Sci USA. 96:1999;10689-10694.
11. Xia Y., Levitt M. Funnel-like organization in sequence space determines the distributions of protein stability and folding rate preferred by evolution. Proteins. 55:2004;107-114 Using a two-dimensional HP-like model, the authors calculated the stability and folding rate of all sequences that fold to the same 24-mer structure. It was found that the distributions of stability and folding rate in sequence space are different, but both distributions are funnel like. The existence of stability and folding rate funnels in sequence space limits the range of possible dynamic behavior of protein evolution.
12. Bornberg-Bauer E. Randomness, structural uniqueness, modularity, and neutral evolution in sequence space of model proteins. Z Phys Chem. 216:2002;139-154.
13. Cui Y., Wong W.H., Bornberg-Bauer E., Chan H.S. Recombinatoric exploration of novel folded structures: a heteropolymer-based model of protein evolutionary landscapes. Proc Natl Acad Sci USA. 99:2002;809-814.
14. Grishin N.V. Fold change in evolution of protein structures. J Struct Biol. 134:2001;167-185.
15. Li H., Helling R., Tang C., Wingreen N. Emergence of preferred structures in a simple model of protein folding. Science. 273:1996;666-669.
16. Wang T., Miller J., Wingreen N.S., Tang C., Dill K.A. Symmetry and designability for lattice protein models. J Chem Phys. 113:2000;8329-8336.
17. Melin R., Li H., Wingreen N., Tang C. Designability, thermodynamic stability, and dynamics in protein folding: a lattice model study. J Chem Phys. 110:1999;1252-1262.
18. Li H., Tang C., Wingreen N.S. Are protein folds atypical? Proc Natl Acad Sci USA. 95:1998;4987-4990.
19. Buchler N.E.G., Goldstein R.A. Surveying determinants of protein structure designability across different energy models and amino-acid alphabets: a consensus. J Chem Phys. 112:2000;2533-2547.
20. Li H., Tang C., Wingreen N.S. Designability of protein structures: a lattice-model study using the Miyazawa-Jernigan matrix. Proteins. 49:2002;403-412.
21. Helling R., Li H., Melin R., Miller J., Wingreen N., Zeng C., Tang C. The designability of protein structures. J Mol Graph Model. 19:2001;157-167.
22. Hirst J.D. The evolutionary landscape of functional model proteins. Protein Eng. 12:1999;721-726.
23. Blackburne B.P., Hirst J.D. Evolution of functional model proteins. J Chem Phys. 115:2001;1935-1942.
24. Blackburne B.P., Hirst J.D. Three-dimensional functional model proteins: structure, function and evolution. J Chem Phys. 119:2003;3453-3460.
25. Hinds D.A., Levitt M. From structure to sequence and back again. J Mol Biol. 258:1996;201-209.
26. Bastolla U., Roman H.E., Vendruscolo M. Neutral evolution of model proteins: diffusion in sequence space and overdispersion. J Theor Biol. 200:1999;49-64.
27. Bastolla U., Vendruscolo M., Roman H.E. Structurally constrained protein evolution: results from a lattice simulation. Eur Phys J B. 15:2000;385-397.
28. Tiana G., Broglia R.A., Shakhnovich E.I. Hiking in the energy landscape in sequence space: a bumpy road to good folders. Proteins. 39:2000;244-251.
29. Tiana G., Broglia R.A., Shakhnovich E.I. Energy profile of the space of model protein sequences. J Biol Phys. 27:2001;147-159.
30. Babajide A., Farber R., Hofacker I.L., Inman J., Lapedes A.S., Stadler P.F. Exploring protein sequence space using knowledge-based potentials. J Theor Biol. 212:2001;35-46.
31. Aita T., Ota M., Husimi Y. An in silico exploration of the neutral network in protein sequence space. J Theor Biol. 221:2003;599-613.
32. Eigen M. Self-organization of matter and the evolution of biological macromolecules. Naturwissenschaften. 58:1971;465-523.
33. Fontana W., Schuster P. Continuity in evolution: on the nature of transitions. Science. 280:1998;1451-1455.
34. Wilke C.O., Wang J.L., Ofria C., Lenski R.E., Adami C. Evolution of digital organisms at high mutation rates leads to survival of the flattest. Nature. 412:2001;331-333.
35. Mirny L.A., Abkevich V.I., Shakhnovich E.I. How evolution makes proteins fold quickly. Proc Natl Acad Sci USA. 95:1998;4976-4981.
36. Govindarajan S., Goldstein R.A. On the thermodynamic hypothesis of protein folding. Proc Natl Acad Sci USA. 95:1998;5545-5549.
37. Taverna D.M., Goldstein R.A. Why are proteins so robust to site mutations? J Mol Biol. 315:2002;479-484 The authors studied two models of protein sequence evolution. In the first model, a viable sequence diffuses randomly over the range of allowed sequences. In the second model, a sequence population evolves over the range of allowed sequences via mutation, selection and reproduction. It was found that evolved proteins in the second model are more robust to site mutations than those in the first model. This result suggests that mutational robustness is a population dynamics effect.
38. Xia Y., Levitt M. Roles of mutation and recombination in the evolution of protein thermodynamics. Proc Natl Acad Sci USA. 99:2002;10382-10387.
39. Sasaki T.N., Sasai M. Correlation between the conformation space and the sequence space of peptide chain. J Biol Phys. 28:2002;483-492.
40. Taverna D.M., Goldstein R.A. Why are proteins marginally stable? Proteins. 46:2002;105-109.
41. Taverna D.M., Goldstein R.A. The distribution of structures in evolving protein populations. Biopolymers. 53:2000;1-8.
42. Williams P.D., Pollock D.D., Goldstein R.A. Evolution of functionality in lattice proteins. J Mol Graph Model. 19:2001;150-156.
43. Bastolla U., Porto M., Roman H.E., Vendruscolo M. Lack of self-averaging in neutral evolution of proteins. Phys Rev Lett. 89:2002;208101.
44. Bastolla U., Porto M., Eduardo Roman M.H., Vendruscolo M.H. Connectivity of neutral networks, overdispersion, and structural conservation in protein evolution. J Mol Evol. 56:2003;243-254.
45. Kuhlman B., Dantas G., Ireton G.C., Varani G., Stoddard B.L., Baker D. Design of a novel globular protein fold with atomic-level accuracy. Science. 302:2003;1364-1368 Computational protein design was used to create a new protein sequence with a novel topology. The subsequent X-ray structure of the protein is very close to the design model, with a root mean square difference of 1.2 Å for 93 residues.
46. Kuhlman B., Baker D. Exploring folding free energy landscapes using computational protein design. Curr Opin Struct Biol. 14:2004;89-95.
47. Koehl P., Levitt M. De novo protein design. II. Plasticity in sequence space. J Mol Biol. 293:1999;1183-1193.
48. Kuhlman B., Baker D. Native protein sequences are close to optimal for their structures. Proc Natl Acad Sci USA. 97:2000;10383-10388.
49. Dokholyan N.V., Shakhnovich E.I. Understanding hierarchical protein evolution from first principles. J Mol Biol. 312:2001;289-307.
50. Koehl P., Levitt M. Protein topology and stability define the space of allowed sequences. Proc Natl Acad Sci USA. 99:2002;1280-1285 Using all-atom computational protein design and a physical energy function, the authors estimated the size of sequence space compatible with a fold using multiple alignments of the designed sequences. It was found that the volume of sequence space compatible with a fold is similar in size to that observed in nature. This is a promising method for identifying highly designable folds.
51. Larson S.M., England J.L., Desjarlais J.R., Pande V.S. Thoroughly sampling sequence space: large-scale protein design of structural ensembles. Protein Sci. 11:2002;2804-2813.
52. Jaramillo A., Wernisch L., Hery S., Wodak S.J. Folding free energy function selects native-like protein sequences in the core but not on the surface. Proc Natl Acad Sci USA. 99:2002;13554-13559.
53. Larson S.M., Pande V.S. Sequence optimization for native state stability determines the evolution and folding kinetics of a small protein. J Mol Biol. 332:2003;275-286.
54. Gillespie B., Vu D.M., Shah P.S., Marshall S.A., Dyer R.B., Mayo S.L., Plaxco K.W. NMR and temperature-jump measurements of de novo designed proteins demonstrate rapid folding in the absence of explicit selection for kinetics. J Mol Biol. 330:2003;813-819.
55. Kussell E.L., Shakhnovich E.I. Analytical approach to the protein design problem. Phys Rev Lett. 83:1999;4437-4440.
56. Emberly E.G., Miller J., Zeng C., Wingreen N.S., Tang C. Identifying proteins of high designability via surface-exposure patterns. Proteins. 47:2002;295-304.
57. England J.L., Shakhnovich E.I. Structural determinant of protein designability. Phys Rev Lett. 90:2003;218101.
58. England J.L., Shakhnovich B.E., Shakhnovich E.I. Natural selection of more designable folds: a mechanism for thermophilic adaptation. Proc Natl Acad Sci USA. 100:2003;8727-8731.
59. Yahyanejad M., Kardar M., Tang C. Structure space of model proteins: a principal component analysis. J Chem Phys. 118:2003;4277-4284.
60. Miller J., Zeng C., Wingreen N.S., Tang C. Emergence of highly designable protein-backbone conformations in an off-lattice model. Proteins. 47:2002;506-512.
61. Emberly E.G., Wingreen N.S., Tang C. Designability of alpha-helical proteins. Proc Natl Acad Sci USA. 99:2002;11163-11168 The authors extensively sampled structure space for all compact four-helix bundles connected by short turns. Highly designable structures were identified from this ensemble, most of which resemble known four-helix-bundle folds. The few novel ones can serve as targets for protein design.
62. Huynen M.A., van Nimwegen E. The frequency distribution of gene family sizes in complete genomes. Mol Biol Evol. 15:1998;583-589.
63. Yanai I., Camacho C.J., DeLisi C. Predictions of gene family distributions in microbial genomes: evolution by gene duplication and modification. Phys Rev Lett. 85:2000;2641-2644.
64. Qian J., Luscombe N.M., Gerstein M. Protein family and fold occurrence in genomes: power-law behaviour and evolutionary model. J Mol Biol. 313:2001;673-681.
65. Koonin E.V., Wolf Y.I., Karev G.P. The structure of the protein universe and genome evolution. Nature. 420:2002;218-223.
66. Dokholyan N.V., Shakhnovich B., Shakhnovich E.I. Expanding protein universe and its origin from the biological Big Bang. Proc Natl Acad Sci USA. 99:2002;14132-14136.
67. Deeds E.J., Dokholyan N.V., Shakhnovich E.I. Protein evolution within a structural space. Biophys J. 85:2003;2962-2972.
68. Chothia C., Gough J., Vogel C., Teichmann S.A. Evolution of the protein repertoire. Science. 300:2003;1701-1703.
69. Wingreen N.S., Li H., Tang C. Designability and thermal stability of protein structures. Polymer. 45:2004;699-705.
70. Tiana G., Shakhnovich B.E., Dokholyan N.V., Shakhnovich E.I. Imprint of evolution on protein structures. Proc Natl Acad Sci USA. 101:2004;2846-2851.
71. Bloom JD, Wilke CO, Arnold FH, Adami C: Stability and the evolvability of function in a model protein. Biophys J 2004, in press.