Home LiteratureArticle Details
PMID: 12237457 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The origins of asymmetry in the folding transition states of protein L and protein G.

Protein science : a publication of the Protein Society ·Vol. 11 ·No. 10 ·2002-10-00 ·Pages 2351-61

Karanicolas J, Brooks CL

Abstract

Topology has been shown to be an important determinant of many features of protein folding; however, the delineation of sequence effects on folding remains obscure. Furthermore, differentiation between the two influences proves difficult due to their intimate relationship. To investigate the effect of sequence in the absence of significant topological differences, we examined the folding mechanisms of segment B1 peptostreptococcal protein L and segment B1 of streptococcal protein G. These proteins share the same highly symmetrical topology. Despite this symmetry, neither protein folds through a symmetrical transition state. We analyzed the origins of this difference using theoretical models. We found that the strength of the interactions present in the N-terminal hairpin of protein L causes this hairpin to form ahead of the C-terminal hairpin. The difference in chain entropy associated with the formation of the hairpins of protein G proves sufficient to beget initiation of folding at the shorter C-terminal hairpin. Our findings suggest that the mechanism of folding may be understood by examination of the free energy associated with the formation of partially folded microstates.

MeSH Terms
Algorithms Bacterial Proteins Computational Biology DNA-Binding Proteins/metabolism Models, Molecular Nerve Tissue Proteins/metabolism Protein Folding Protein Structure, Tertiary/physiology Thermodynamics
Chemicals
Bacterial Proteins DNA-Binding Proteins G-substrate L-protein, Peptococcus magnus Nerve Tissue Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Karanicolas John
Department of Molecular Biology, The Scripps Research Institute, La Jolla, California 92037, USA.
Brooks Charles L
References (52)
52 references, click to expand
  1. Contrasting roles for symmetrically disposed beta-turns in the folding of a small protein.
    J Mol Biol. 1997 Dec 12;274(4):588-96 PMID: 9417937
  2. Molecular picture of folding of a small alpha/beta protein.
    Proc Natl Acad Sci U S A. 1998 Feb 17;95(4):1562-7 PMID: 9465055
  3. A theoretical search for folding/unfolding nuclei in three-dimensional protein structures.
    Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11299-304 PMID: 10500171
  4. Mutational analysis of acylphosphatase suggests the importance of topology and contact order in protein folding.
    Nat Struct Biol. 1999 Nov;6(11):1005-9 PMID: 10542090
  5. Computer-based redesign of a protein folding pathway.
    Nat Struct Biol. 2001 Jul;8(7):602-5 PMID: 11427890
  6. Obligatory steps in protein folding and the conformational diversity of the transition state.
    Nat Struct Biol. 1998 Aug;5(8):721-9 PMID: 9699637
  7. Interpreting the folding kinetics of helical proteins.
    Nature. 1999 Sep 23;401(6751):400-3 PMID: 10517642
  8. Characterization of the free energy spectrum of peptostreptococcal protein L.
    Fold Des. 1997;2(5):271-80 PMID: 9377710
  9. Structural and dynamic characterization of the urea denatured state of the immunoglobulin binding domain of streptococcal protein G by multidimensional heteronuclear NMR spectroscopy.
    Protein Sci. 1995 Dec;4(12):2605-15 PMID: 8580852
  10. Critical role of beta-hairpin formation in protein G folding.
    Nat Struct Biol. 2000 Aug;7(8):669-73 PMID: 10932252
  11. Proton nuclear magnetic resonance sequential assignments and secondary structure of an immunoglobulin light chain-binding domain of protein L.
    Biochemistry. 1993 Apr 6;32(13):3381-6 PMID: 8461301
  12. Roles of native topology and chain-length scaling in protein folding: a simulation study with a Go-like model.
    J Mol Biol. 2001 Oct 12;313(1):171-80 PMID: 11601854
  13. Calculations on folding of segment B1 of streptococcal protein G.
    J Mol Biol. 1998 May 1;278(2):439-56 PMID: 9571063
  14. Studies on protein folding, unfolding and fluctuations by computer simulation. I. The effect of specific amino acid sequence represented by specific inter-unit interactions.
    Int J Pept Protein Res. 1975;7(6):445-59 PMID: 1201909
  15. Viewing protein folding from many perspectives.
    Proc Natl Acad Sci U S A. 2002 Feb 5;99(3):1099-100 PMID: 11830648
  16. Contact order, transition state placement and the refolding rates of single domain proteins.
    J Mol Biol. 1998 Apr 10;277(4):985-94 PMID: 9545386
  17. Structure of the transition state in the folding process of human procarboxypeptidase A2 activation domain.
    J Mol Biol. 1998 Nov 13;283(5):1027-36 PMID: 9799641
  18. Monte Carlo simulations of protein folding. I. Lattice model and interaction scheme.
    Proteins. 1994 Apr;18(4):338-52 PMID: 8208726
  19. Experiment and theory highlight role of native state topology in SH3 folding.
    Nat Struct Biol. 1999 Nov;6(11):1016-24 PMID: 10542092
  20. The single helix in protein L is largely disrupted at the rate-limiting step in folding.
    J Mol Biol. 1998 Dec 4;284(3):807-15 PMID: 9826517
  21. Barriers in protein folding reactions.
    Adv Protein Chem. 2000;53:153-207 PMID: 10751945
  22. The environmental dependency of protein folding best explains prion and amyloid diseases.
    Proc Natl Acad Sci U S A. 1998 Feb 3;95(3):930-2 PMID: 9448261
  23. Identifying the protein folding nucleus using molecular dynamics.
    J Mol Biol. 2000 Mar 10;296(5):1183-8 PMID: 10698625
  24. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features.
    Biopolymers. 1983 Dec;22(12):2577-637 PMID: 6667333
  25. Mechanisms of protein folding.
    Curr Opin Struct Biol. 2001 Feb;11(1):70-82 PMID: 11179895
  26. From folding theories to folding proteins: a review and assessment of simulation studies of protein folding and unfolding.
    Annu Rev Phys Chem. 2001;52:499-535 PMID: 11326073
  27. Structure-derived potentials and protein simulations.
    Curr Opin Struct Biol. 1996 Apr;6(2):195-209 PMID: 8728652
  28. Protein folding in the landscape perspective: chevron plots and non-Arrhenius kinetics.
    Proteins. 1998 Jan;30(1):2-33 PMID: 9443337
  29. Structural transitions in the protein L denatured state ensemble.
    Biochemistry. 1999 Nov 30;38(48):15927-35 PMID: 10625459
  30. How do small single-domain proteins fold?
    Fold Des. 1998;3(4):R81-91 PMID: 9710577
  31. Conformational analysis of peptides corresponding to all the secondary structure elements of protein L B1 domain: secondary structure propensities are not conserved in proteins with the same fold.
    Protein Sci. 1997 Jan;6(1):162-74 PMID: 9007989
  32. Structure and dynamics of an acid-denatured protein G mutant.
    Biochemistry. 2000 Feb 8;39(5):965-77 PMID: 10653640
  33. Kinetics of folding of the IgG binding domain of peptostreptococcal protein L.
    Biochemistry. 1997 Mar 18;36(11):3373-82 PMID: 9116017
  34. Prediction of protein-folding mechanisms from free-energy landscapes derived from native structures.
    Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11305-10 PMID: 10500172
  35. Folding dynamics of the B1 domain of protein G explored by ultrarapid mixing.
    Nat Struct Biol. 1999 Oct;6(10):943-7 PMID: 10504729
  36. The Protein Data Bank: a computer-based archival file for macromolecular structures.
    J Mol Biol. 1977 May 25;112(3):535-42 PMID: 875032
  37. Fast folding of a prototypic polypeptide: the immunoglobulin binding domain of streptococcal protein G.
    Protein Sci. 1994 Nov;3(11):1945-52 PMID: 7703841
  38. Optimized Monte Carlo data analysis.
    Phys Rev Lett. 1989 Sep 18;63(12):1195-1198 PMID: 10040500
  39. Folding of protein G B1 domain studied by the conformational characterization of fragments comprising its secondary structure elements.
    Eur J Biochem. 1995 Jun 1;230(2):634-49 PMID: 7607238
  40. Protein folding mediated by solvation: water expulsion and formation of the hydrophobic core occur after the structural collapse.
    Proc Natl Acad Sci U S A. 2002 Jan 22;99(2):685-90 PMID: 11805324
  41. NMR characterization of residual structure in the denatured state of protein L.
    J Mol Biol. 2000 Jun 23;299(5):1341-51 PMID: 10873457
  42. The complexity and accuracy of discrete state models of protein structure.
    J Mol Biol. 1995 Jun 2;249(2):493-507 PMID: 7783205
  43. A simple model for calculating the kinetics of protein folding from three-dimensional structures.
    Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11311-6 PMID: 10500173
  44. Folding funnels and frustration in off-lattice minimalist protein landscapes.
    Proc Natl Acad Sci U S A. 1998 May 26;95(11):5921-8 PMID: 9600893
  45. The fundamentals of protein folding: bringing together theory and experiment.
    Curr Opin Struct Biol. 1999 Feb;9(1):92-101 PMID: 10047588
  46. A breakdown of symmetry in the folding transition state of protein L.
    J Mol Biol. 2000 May 19;298(5):971-84 PMID: 10801362
  47. The SH3-fold family: experimental evidence and prediction of variations in the folding pathways.
    J Mol Biol. 2000 Dec 15;304(5):967-82 PMID: 11124040
  48. Exploring the origins of topological frustration: design of a minimally frustrated model of fragment B of protein A.
    Proc Natl Acad Sci U S A. 1999 Oct 26;96(22):12512-7 PMID: 10535953
  49. A novel, highly stable fold of the immunoglobulin binding domain of streptococcal protein G.
    Science. 1991 Aug 9;253(5020):657-61 PMID: 1871600
  50. Residue-residue potentials with a favorable contact pair term and an unfavorable high packing density term, for simulation and threading.
    J Mol Biol. 1996 Mar 1;256(3):623-44 PMID: 8604144
  51. Kinetic analysis of folding and unfolding the 56 amino acid IgG-binding domain of streptococcal protein G.
    Biochemistry. 1992 Aug 18;31(32):7243-8 PMID: 1510916
  52. Topology, stability, sequence, and length: defining the determinants of two-state protein folding kinetics.
    Biochemistry. 2000 Sep 19;39(37):11177-83 PMID: 10985762
Article Info
Journal
Protein science : a publication of the Protein Society
Abbr.
Protein Sci
ISSN
0961-8368
Published
2002-10-00
Pages
2351-61
Language
English
Region
United States
NLM ID
9211750
PMCID
PMC2373711
Subset
IM
Grants
NCRR NIH HHS · P41 RR012255 · United States
NIGMS NIH HHS · R01 GM048807 · United States
NIGMS NIH HHS · GM48807 · United States
NCRR NIH HHS · RR12255 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com