Universally conserved positions in protein folds: Reading evolutionary signals about stability, folding kinetics and function

Journal of Molecular Biology

Volumn 291, Issue 1, 1999, Pages 177-196

  Mirny, Leonid A ^a   Shakhnovich, Eugene I ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

Conservatism; Protein evolution; Protein folding; Protein stability; Super site kinetics

Indexed keywords

IMMUNOGLOBULIN; OLIGONUCLEOTIDE;

AMINO ACID SEQUENCE; ARTICLE; MOLECULAR EVOLUTION; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; STATISTICAL ANALYSIS; STRUCTURE ACTIVITY RELATION; THERMODYNAMICS;

EID: 0345062357     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.2911     Document Type: Article

References (62)

1. Abkevich V., Gutin A., Shakhnovich E. Specific nucleus as the transition state for protein folding: evidence from the lattice model. Biochemistry. 33:1994;10026-10036.
2. Altschuh D., Vernet T., Berti P., Moras D., Nagai K. Coordinated amino acid changes in homologous protein families. Protein Eng. 2:1988;193-199.
3. Bahar I., Jernigan R. Inter-residue potentials in globular proteins and the dominance of highly specific hydrophilic interactions at close separation. J. Mol. Biol. 266:1997;195-214.
4. Bellsolell L., Cronet P., Majolero M., Serrano L., Coll M. The three-dimensional structure of two mutants of the signal transduction protein chey suggest its molecular activation mechanism. J. Mol. Biol. 257:1996;116-128.
5. Bork P., Holm L., Sander C. The immunoglobulin fold. Structural classification, sequence patterns and common core. J. Mol. Biol. 242:1994;309-320.
6. Branden C., Tooze J. Introduction to Protein Structure. 1998;Garland Publishing, Inc. New York.
7. Bryngelson J., Wolynes P. A simple statistical field theory of heteropolymer collapse with application to protein folding. Biopolymers. 30:1990;177-188.
8. Dodge C., Schneider R., Sander C. The hssp database of protein structure-sequence alignments and family profiles. Nucl. Acids Res. 26:1998;313-315.
9. Feller W. An Introduction to Probability Theory and its Applications. 1970;Wiley, New York.
10. Gilis D., Rooman M. Predicting protein stability changes upon mutation using database-derived potentials: solvent accessibility determines the importance of local versus non-local interactions along the sequence. J. Mol. Biol. 272:1997;276-290.
11. Goldstein R., Luthey-Schulten Z., Wolynes P. Optimal protein-folding codes from spin-glass theory. Proc. Natl Acad. Sci. USA. 89:1992;4918-4922.
12. Govindarajan S., Goldstein R. Why are some protein structures so common? Proc. Natl Acad. Sci. USA. 93:1995;3341-3345.
13. Guo Z., Thirumalai D. Nucleation mechanism for protein folding and theoretical predictions for hydrogen-exchange labelling experiments. Biopolymers. 35:1995;137-139.
14. Gutin A., Abkevich V., Shakhnovich E. A protein engineering analysis of the transition state for protein folding: simulation in the lattice model. Fold. Design. 3:1998;183-194.
15. Hamill S., Meekhof A., Clarke J. The effect of boundary selection on the stability and folding of the third fibronectin type iii domain from human tenascin. Biochemistry. 37:1998;8071-8079.
16. Hao M.-H., Scheraga H. Monte-Carlo simulation of a first order transition for protein folding. J. Phys. Chem. 98:1994a;4940-4945.
17. Hao M.-H., Scheraga H. Statistical thermodynamics of protein folding: sequence dependence. J. Phys. Chem. 98:1994b;9882-9886.
18. Henikoff S., Henikoff J. Position-based sequence weights. J. Mol. Biol. 243:1994;574-578.
19. Holm L., Sander C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233:1993;123-138.
20. Itzhaki L., Otzen D., Fersht A. The structure of the transition state for folding of chymotrypsin inhibitor 2 analyzed by protein engineering methods: evidence for a nucleation-condensation mechanism for protein folding. J. Mol. Biol. 254:1995;260-288.
21. Jackson S. How do small single-domain proteins fold? Fold. Design. 3:1998;R81-R91.
22. Koshi J., Goldstein R. Mutation matrices and physical-chemical properties: correlations and implications. Proteins: Struct. Funct. Genet. 27:1997;336-344.
23. Kraulis P. Molscript: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
24. Liaw S., Jun G., Eisenberg D. Interactions of nucleotides with fully unadenylylated glutamine synthetase from salmonella typhimurium. Biochemistry. 33:1994;11184-11188.
25. Lopez-Hernandez E., Serrano L. Structure of the transition state for folding of the 129 aa protein chey resembles that of a smaller protein, ci2. Fold. Design. 1:1996;43-55.
26. Lorch M., Mason J., Clarke A., Parker M. Effects of core mutations on the folding of a beta-sheet protein: implications for backbone organization in the i-state. Biochemistry. 38:1999;1377-1385.
27. Martinez J., Pissabarro T., Serrano L. Obligatory steps in protein folding and the conformational diversity of the transition state. Nature Struct. Biol. 5:1998;721-729.
28. Meekhof A., Freund S. Probing residual structure and backbone dynamics on the milli- to picosecond timescale in a urea-denatured fibronectin type III domain. J. Mol. Biol. 286:1999;579-592.
29. Merritt E., Bacon D. Raster3D: phosorealistic molecular graphics. Methods Enzymol. 277:1997;505-524.
30. Mirny L., Shakhnovich E. Protein structure prediction by threading. Why it works and why it does not. J. Mol. Biol. 283:1998;507-526.
31. Mirny L., Abkevich V., Shakhnovich E. How evolution makes proteins fold quickly. Proc. Natl Acad. Sci. USA. 95:1998;4976-4981.
32. Newkirk K., Feng W., Jiang W., Tejero R., Emerson S., Inouye M., Montelione G. Solution nmr structure of the major cold shock protein (cspa) from Escherichia coli: identification of a binding epitope for DNA. Proc. Natl Acad. Sci. USA. 91:1994;5114-5118.
33. Pande V., Grosberg A., Tanaka T. How accurate must potentials be for successful modeling of protein folding? J. Chem. Phys. 103:1995;1-10.
34. Pande V., Grosberg A., Rokshar D., Tanaka T. Pathways for protein folding: is a "new view" needed? Curr. Opin. Struct. Biol. 8:1998;68-79.
35. Parker M., Dempsey C., Hosszu L., Waltho J., Clarke A. Topology, sequence evolution and folding dynamics of an immunoglobulin domain. Nature Struct. Biol. 5:1998;194-198.
36. Pelletier H., Sawaya M., Wolfle W., Wilson S., Kraut J. Crystal structures of human DNA polymerase beta complexed with DNA: implications for catalytic mechanism, processivity, and fidelity. Biochemistry. 35:1996;12742-12761.
37. Perl D., Welker C., Schindler T., Schroder K., Marahiel M., Jaenicke R., Schmid F. Conservation of rapid two-state folding in mesophilic, thermophilic and hyperthermophilic cold shock proteins. Nature Struct. Biol. 5:1998;229-235.
38. Plaxco K., Soitzfaden C., Campbell I., Dobson C. Rapid refolding of a proline-rich all β-sheet fibronectin type III module. Proc. Natl Acad. Sci. USA. 93:1996;10703-10706.
39. Ptitsyn O. Protein folding and protein evolution: common folding nucleus in different subfamilies of c -type cytochromes? J. Mol. Biol. 278:1998;655-666.
40. Reid K., Rodriguez H., Hillier B., Gregoret L. Stability and folding properties of a model beta-sheet protein, Escherichia coli CSPA [published erratum appears in protein Sci 1998]. Protein Sci. 7:1998;470-479.
41. Russell R., Sasieni P., Sternberg M. Supersites within superfolds. Binding site similarity in the absence of homology. J. Mol. Biol. 282:1998;903-918.
42. Sali A., Shakhnovich E., Karplus M. Kinetics of protein folding. A lattice model study for the requirements for folding to the native state. J. Mol. Biol. 235:1994;1614-1636.
43. Schindelin H., Jiang W., Inouye M., Heinemann U. Crystal structure of cspa, the major cold shock protein of Escherichia coli. Proc. Natl Acad. Sci. USA. 91:1994;5119-5123.
44. Schindler T., Perl D., Graumann P., Sieber V., Marahiel M., Schmid F. Surface-exposed phenylalanines in the rnp1/rnp2 motif stabilize the cold-shock protein cspb from Bacillus subtilis. Proteins: Struct. Funct. Genet. 30:1998;401-406.
45. Schindler T., Graumann P., Perl D., Ma S., Schmid F., Marahiel M. The family of cold shock proteins of Bacillus subtilis. Stability and dynamics in vitro and in vivo. J. Biol. Chem. 274:1999;3407-3413.
46. Schuller D., Grant G., Banaszak L. The allosteric ligand site in the vmax-type cooperative enzyme phosphoglycerate dehydrogenase. Nature Struct. Biol. 2:1995;69-76.
47. Shakhnovich E. Proteins with selected sequences fold to their unique native conformation. Phys. Rev. Letters. 72:1994;3907-3910.
48. Shakhnovich E. Theoretical studies of protein-folding thermodynamics and kinetics. Curr. Opin. Struct. Biol. 7:1997;29-40.
49. Shakhnovich E. Folding nucleus: specific of multiple? Insights from simulations and comparison with experiment. Fold. Design. 3:1998a;R108-R111.
50. Shakhnovich E. Protein design: a perspective from simple tractable models. Fold. Design. 3:1998b;R45-R58.
51. Shakhnovich E., Gutin A. Engineering of stable and fast-folding sequences of model proteins. Proc. Natl Acad. Sci. USA. 90:1993a;7195-7199.
52. Shakhnovich E., Gutin A. A novel approach to design of stable proteins. Protein Eng. 6:1993b;793-800.
53. Shakhnovich E., Abkevich V., Ptitsyn O. Conserved residues and the mechanism of protein folding. Nature. 379:1996;96-98.
54. Thomas D., Casari G., Sander C. The prediction of protein contacts from multiple sequence alignments. Protein Eng. 9:1996;941-948.
55. Tiana G., Broglia R., Roman H., Vigezzi E., Shakhnovich E. Folding and misfolding of designed protein like chains with mutations. J. Chem. Phys. 108:1998;757-761.
56. van Nuland H., Chiti F., Taddei N., Raugei G., Ramponi G., Dobson C. Slow folding of muscle acylphosphatase in the absence of intermediates. J. Mol. Biol. 283:1998a;883-891.
57. van Nuland H., Meijberg W., Warner J., Forge V., Scheek R., Robillard G., Dobson C. Slow cooperative folding of a small globular protein hpr. Biochemistry. 37:1998b;622-637.
58. Viguera A., Serrano L., Wilmanns M. Different folding transition states may result in the same native structure. Nature Struct. Biol. 4:1997;939-946.
59. Villegas V., Martinez J., Aviles F., Serrano L. Structure of the transition state in the folding process of human procarboxypeptidase a2 activation domain. J. Mol. Biol. 283:1998;1027-1036.
60. 2+, and conformation of the chemotaxis protein chey on its binding to the flagellar switch protein flim. Biochemistry. 33:1994;10470-10476.
61. Wilcock D., Pisabarro M., Lopez-Hernandez E., Serrano L., Coll M. Structure analysis of two chey mutants: importance of the hydrogen-bond contribution to protein stability. Acta Crystallog. sect. D. 54:1998;378-385.
62. Wilson K., Shewchuk L., Brennan R., Otsuka A., Matthews B. Escherichia coli biotin holoenzyme synthetase/bio repressor crystal structure delineates the biotin- and DNA-binding domains. Proc. Natl Acad. Sci. USA. 89:1992;9257-9261.