Fast folding of the two-domain Semliki Forest virus capsid protein explains co-translational proteolytic activity

Journal of Molecular Biology

Volumn 338, Issue 1, 2004, Pages 159-167

  Sánchez, Ignacio E ^a   Morillas, Manuel ^b   Zobeley, Eva ^b   Kiefhaber, Thomas ^a   Glockshuber, Rudi ^b  

^a UNIVERSITY OF BASEL   (Switzerland)

^b ETH ZURICH   (Switzerland)

Author keywords

Co translational folding; Prolyl isomerization; Protein folding; Semliki Forest virus protease; SFV, Semliki Forest virus; SFVP, a 149 residue serine protease module; Two domain proteins

Indexed keywords

CAPSID PROTEIN; POLYPEPTIDE; RECOMBINANT PROTEIN; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL COMPOSITION; IN VITRO STUDY; MOLECULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; SEMLIKI FOREST ALPHAVIRUS;

RABBIT FIBROMA VIRUS; SEMLIKI FOREST VIRUS;

EID: 17344384932     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.02.037     Document Type: Article

References (43)

1. Jaenicke R. Folding and association of proteins. Prog. Biophys. Mol. Biol. 49:1987;117-237.
2. Creighton T.E. Protein folding coupled to disulphide bond formation. Biol. Chem. 378:1997;731-744.
3. Fischer G., Schmid F.X. The mechanism of protein folding. Implications of in vitro refolding models for de novo protein folding and translocation in the cell. Biochemistry. 29:1990;2205-2212.
4. Walter S., Buchner J. Molecular chaperones - cellular machines for protein folding. Angew. Chem. Int. Ed. Engl. 41:2003;1098-1113.
5. Nicola A.V., Chen W., Helenius A. Co-translational folding of an alphavirus capsid protein in the cytosol of living cells. Nature Cell. Biol. 1:1999;341-345.
6. Kolb V.A., Makeyev E.V., Spirin A.S. Co-translational folding of an eukaryotic multidomain protein in a prokaryotic translation system. J. Biol. Chem. 275:2000;16597-16601.
7. Boege U., Wengler G., Wittmann-Liebold B. Primary structures of the core proteins of the alphaviruses Semliki Forest virus and Sindbis virus. Virology. 113:1981;293-303.
8. Strauss J.H., Strauss E.G. The alphaviruses: gene expression, replication, and evolution. Microbiol. Rev. 58:1994;491-562.
9. Choi H.K., Lu G., Lee S., Wengler G., Rossmann M.G. Structure of Semliki Forest virus core protein. Proteins: Struct. Funct. Genet. 27:1997;345-359.
10. Kowarik M., Küng S., Martoglio B., Helenius A. Protein folding during cotranslational translocation in the endoplasmic reticulum. Mol. Cell. 10:2002;769-778.
11. Braakmann I., Hoover-Litty H., Wagner K.R., Helenius A. Folding of influenza hemagglutinin in the endoplasmic reticulum. J. Cell. Biol. 114:1991;401-411.
12. Chrunyk B.A., Matthews C.R. Role of diffusion in the folding of the α subunit of tryptophan synthase from Escherichia coli. Biochemistry. 29:1990;2149-2154.
13. Rudolph R., Siebendritt R., Nesslauer G., Sharma A.K., Jaenicke R. Folding of an all-beta protein: independent domain folding in gamma II-crystallin from calf eye lens. Proc. Natl Acad. Sci. USA. 87:1990;4625-4629.
14. Jaenicke R. Stability and folding of domain proteins. Prog. Biophys. Mol. Biol. 71:1999;155-241.
15. Martin A., Schmid F.X. The folding mechanism of a two-domain protein: folding kinetics and domain docking of the gene-3 protein of phage fd. J. Mol. Biol. 329:2003;599-610.
16. Parker M.J., Spencer J., Jackson G.S., Burston S.G., Hosszu L.L., Craven C.J., et al. Domain behavior during the folding of a thermostable phosphoglycerate kinase. Biochemistry. 35:1996;15740-15752.
17. Myers J.K., Pace C.N., Scholtz J.M. Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding. Protein Sci. 4:1995;2138-2148.
18. Ikai A., Tanford C. Kinetics of unfolding and refolding of proteins. I. Mathematical analysis. J. Mol. Biol. 73:1973;145-163.
19. Sánchez I.E., Kiefhaber T. Non-linear rate-equilibrium free energy relationships and Hammond behavior in protein folding. Biophys. Chem. 100:2003;397-407.
20. Sánchez I.E., Kiefhaber T. Evidence for sequential barriers and obligatory intermediates in apparent two-state protein folding. J. Mol. Biol. 325:2003;367-376.
21. Schmid F.X. Mechanism of folding of ribonuclease A. Slow refolding is a sequential reaction via structural intermediates. Biochemistry. 22:1983;4690-4696.
22. Kiefhaber T. Protein folding kinetics. Shirley B.A. Methods in Molecular Biology, Protein Stability and Folding Protocols. 1995;313-341 Humana Press, Totowa, NJ.
23. Kiefhaber T. Kinetic traps in lysozyme folding. Proc. Natl Acad. Sci. USA. 92:1995;9029-9033.
24. Moore J.W., Pearson R.G. Kinetics and Mechanisms. 1981;John Wiley & Sons, New York.
25. Brandts J.F., Halvorson H.R., Brennan M. Consideration of the possibility that the slow step in protein denaturation reactions is due to cis-trans isomerism of proline residues. Biochemistry. 14:1975;4953-4963.
26. Hagerman P.J., Baldwin R.L. A quantitative treatment of the kinetics of the folding transition of ribonuclease A. Biochemistry. 15:1976;1462-1473.
27. Schmid F.X. Kinetics of unfolding and refolding of single-domain proteins. Creighton T.E. Protein Folding. 1992;197-239 W. H. Freeman and Company, New York.
28. Pappenberger G., Aygün H., Engels J.W., Reimer U., Fischer G., Kiefhaber T. Nonprolyl cis peptide bonds in unfolded proteins cause complex folding kinetics. Nature Struct. Biol. 8:2001;452-458.
29. Reimer U., Scherer G., Drewello M., Kruber S., Schutkowski M., Fischer G. Side-chain effects on peptidyl-prolyl cis/trans isomerization. J. Mol. Biol. 279:1998;449-460.
30. Szabo Z.G. Kinetic characterization of complex reaction systems. Bamford C.H., Tipper C.F.H. Comprehensive Chemical Kinetics. Comprehensive Chemical Kinetics. vol. 2:1969;1-80 Elsevier Publishing Company, Amsterdam.
31. Bieri O., Kiefhaber T. Kinetic models in protein folding. Pain R. Protein Folding: Frontiers in Molecular Biology. 2nd edit. 2000;34-64 Oxford University Press, Oxford.
32. Balbach J., Schmid F.X. Proline isomerization and its catalysis in protein folding. Pain R. Protein Folding: Frontiers in Molecular Biology. 2nd edit. 2000;212-249 Oxford University Press, Oxford.
33. Scherer G., Kramer M.L., Schutkowski M., Reimer U., Fischer G. Barriers to rotation of secondary amide peptide bonds. J. Am. Chem. Soc. 120:1998;5568-5574.
34. Jackson S.E. How do small single-domain proteins fold? Fold. Des. 3:1998;R81-R91.
35. Kubelka J., Hofrichter J., Eaton W.A. The protein folding speed limit. Curr. Opin. Struct. Biol. 14:2004;76-88.
36. Schiene-Fischer C., Habazettl J., Schmid F.X., Fischer G. The hsp70 chaperone DnaK is a secondary amide peptide bond cis-trans isomerase. Nature Struct. Biol. 9:2002;419-424.
37. Martin A., Schmid F.X. A proline switch controls folding and domain interacxtions in the gene-3-protein of the filamentous phage fd. J. Mol. Biol. 331:2003;1131-1140.
38. Demeler B., Saber H. Determination of molecular parameters by fitting sedimentation data to finite-element solutions of the Lamm equation. Biophys. J. 74:1998;444.
39. Golbik R., Fischer G., Fersht A.R. Folding of barstar C40A/C82A/P27A and catalysis of the peptidyl-prolyl cis/trans isomerization by human cytosolic cyclophilin (Cyp18). Protein Sci. 8:1999;1505-1514.
40. Aune K.C., Tanford C. Thermodynamics of denaturation of lysozyme by guanidine hydrochloride. II. Dependence on denaturant concentration at 25 °C. Biochemistry. 8:1969;4586-4590.
41. Kiefhaber T., Kohler H.H., Schmid F.X. Kinetic coupling between protein folding and prolyl isomerization. I. Theoretical models. J. Mol. Biol. 224:1992;217-229.
42. Koradi R., Billeter M., Wüthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14:1996;51-55.
43. Santoro M.M., Bolen D.W. Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants. Biochemistry. 27:1988;8063-8068.