Funnel-Like Organization in Sequence Space Determines the Distributions of Protein Stability and Folding Rate Preferred by Evolution

Proteins: Structure, Function and Genetics

Volumn 55, Issue 1, 2004, Pages 107-114

  Xia, Yu ^a   Levitt, Michael ^b  

^a YALE UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Hydrophobic polar; Lattice model; Protein evolution; Protein folding; Protein sequence structure relationships

Indexed keywords

ARTICLE; COMPARATIVE STUDY; HYDROPHOBICITY; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; THERMODYNAMICS;

EVOLUTION; HYDROPHOBICITY; KINETICS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEINS; SEQUENCE ANALYSIS, PROTEIN; THERMODYNAMICS;

EID: 1442324641     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/prot.10563     Document Type: Article

References (36)

1. Bryngelson JD, Wolynes PG. Spin glasses and the statistical mechanics of protein folding. Proc Natl Acad Sci USA 1987;84:7524-7528.
2. Lau KF, Dill KA. A lattice statistical-mechanics model of the conformational and sequence-spaces of proteins. Macromolecules 1989;22:3986-3997.
3. Sali A, Shakhnovich E, Karplus M. How does a protein fold? Nature 1994;369:248-251.
4. Levinthal C. Are there pathways for protein folding? J Chim Phys 1968;65:44-45.
5. Shakhnovich EI, Gutin AM. Implications of thermodynamics of protein folding for evolution of primary sequences. Nature 1990;346:773-775.
6. Shakhnovich EI, Gutin AM. A new approach to the design of stable proteins. Protein Eng 1993;6:793-800.
7. Wolynes PG, Onuchic JN, Thirumalai D. Navigating the folding routes. Science 1995;267:1619-1620.
8. Dill KA, Chan HS. From Levinthal to pathways to funnels. Nat Struct Biol 1997;4:10-19.
9. Pande VS, Grosberg AY, Tanaka T, Rokhsar DS. Pathways for protein folding: is a new view needed? Curr Opin Struct Biol 1998;8:68-79.
10. Dobson CM, Karplus M. The fundamentals of protein folding: bringing together theory and experiment. Curr Opin Struct Biol 1999;9:92-101.
11. Wright S. The roles of mutation, inbreeding, crossbreeding and selection in evolution. Proceedings of the Sixth International Congress on Genetics 1932;1:356-366.
12. Maynard Smith J. Natural selection and the concept of a protein space. Nature 1970;225:563-564.
13. Mirny LA, Abkevich VI, Shakhnovich EI. How evolution makes proteins fold quickly. Proc Natl Acad Sci USA 1998;95:4976-4981.
14. Tiana G, Broglia RA, Shakhnovich EI. Hiking in the energy landscape in sequence space: a bumpy road to good folders. Proteins 2000;39:244-251.
15. Govindarajan S, Goldstein RA. Evolution of model proteins on a foldability landscape. Proteins 1997;29:461-466.
16. Bornberg-Bauer E, Chan HS. Modeling evolutionary landscapes: mutational stability, topology, and superfunnels in sequence space. Proc Natl Acad Sci USA 1999;96:10689-10694.
17. Taverna DM, Goldstein RA. The distribution of structures in evolving protein populations. Biopolymers 2000;53:1-8.
18. Taverna DM, Goldstein RA. Why are proteins so robust to site mutations? J Mol Biol 2002;315:479-484.
19. Taverna DM, Goldstein RA. Why are proteins marginally stable? Proteins 2002;46:105-109.
20. Cui Y, Wong WH, Bornberg-Bauer E, Chan HS. Recombinatoric exploration of novel folded structures: a heteropolymer-based model of protein evolutionary landscapes. Proc Natl Acad Sci USA 2002;99:809-814.
21. Xia Y, Levitt M. Roles of mutation and recombination in the evolution of protein thermodynamics. Proc Natl Acad Sci USA 2002;99:10382-10387.
22. Voigt CA, Mayo SL, Arnold FH, Wang ZG. Computational method to reduce the search space for directed protein evolution. Proc Natl Acad Sci USA 2001;98:3778-3783.
23. Eigen M. Self-organization of matter and the evolution of biological macromolecules. Naturwissenschaften 1971;58:465-523.
24. Fontana W, Schuster P. Shaping space: the possible and the attainable in RNA genotype-phenotype mapping. Science 1998;280:1451-1455.
25. Li H, Tang C, Wingreen NS. Are protein folds atypical? Proc Natl Acad Sci USA 1998;95:4987-4990.
26. Li H, Helling R, Tang C, Wingreen N. Emergence of preferred structures in a simple model of protein folding. Science 1996;273:666-669.
27. Dill KA, Bromberg S, Yue KZ, Fiebig KM, Yee DP, Thomas PD, Chan HS. Principles of protein-folding: a perspective from simple exact models. Protein Sci 1995;4:561-602.
28. Irbäck A, Troein C. Enumerating designing sequences in the HP model. J Biol Phys 2002;28:1-15.
29. Chan HS, Dill KA. Transition-states and folding dynamics of proteins and heteropolymers. J Chem Phys 1994;100:9238-9257.
30. Tenenbaum JB, de Silva V, Langford JC. A global geometric framework for nonlinear dimensionality reduction. Science 2000;290:2319-2323.
31. Kimura M. The neutral theory of molecular evolution: a review of recent evidence. Jpn J Genet 1991;66:367-386.
32. Goldenberg DP. Finding the right fold. Nat Struct Biol 1999;6:987-990.
33. Kim DE, Gu H, Baker D. The sequences of small proteins are not extensively optimized for rapid folding by natural selection. Proc Natl Acad Sci USA 1998;95:4982-4986.
34. Williams PD, Pollock DD, Goldstein RA. Evolution of functionality in lattice proteins. J Mol Graph Mod 2001;19:150-156.
35. Abkevich VI, Gutin AM, Shakhnovich EI. Impact of local and nonlocal interactions on thermodynamics and kinetics of protein folding. J Mol Biol 1995;252:460-471.
36. Chan HS. Modeling protein density of states: additive hydrophobic effects are insufficient for calorimetric two-state cooperativity. Proteins 2000;40:543-571.