A kinetic mechanism for in vivo protein folding

• Autorzy: Cruzeiro L.

Identyfikatory

DOI

10.1515/bams-2014-0010

• Języki publikacji: EN

Abstrakty

EN

For many decades now, the solution to the protein folding problem has been sought within the thermodynamic hypothesis of Anfinsen. Instead, the work discussed here is concerned with protein folding in vivo and assumes that the solution lies within a generalization of the kinetic, nonequilibrium mechanism first proposed by Levinthal. Accordingly, two different initial conditions, namely, a fully extended and a helical chain, are tested and pathways to the native state are generated via targeted molecular dynamics. The energetic and structural analysis indicates that a helical initial condition is to be preferred over an extended one. These results are set against the broader context of in vitro protein refolding experiments and theories and are found to be in agreement with the recent experimental observations about the influence of the ribosome on the structure of, and on the folding from, nascent chains.

Słowa kluczowe

EN

kinetic mechanism; protein folding; VES hypothesis

• Wydawca: Uniwersytet Jagielloński - Collegium Medicum ; Index Copernicus Sp. z o.o.
• Czasopismo: Bio-Algorithms and Med-Systems
• Rocznik: 2014
• Tom: Vol. 10, no. 3
• Strony: 117--127
• Opis fizyczny: Bibliogr. 70 poz., rys., wykr.

Twórcy

autor

Cruzeiro L.

• CCMAR and Physics, FCT, Universidade do Algarve, Campus de Gambelas, 8005-139 Faro, Portugal

Bibliografia

• 1. Anfinsen CB. Principles that govern the folding of protein chains. Science 1973;181:223–30.
• 2. Gutte B, Merrifield RB. The synthesis of ribonuclease A. J Biol Chem 1971;246:1922–40.
• 3. Merrifiel B. The chemical synthesis of proteins. Protein Sci 1996;5:1947–51.
• 4. Nilsson BL, Soellner MB, Raines RT. Chemical synthesis of proteins. Annu Rev Biophys Biomol Struct 2005;34:91–118.
• 5. Lau KF, Dill KA. A lattice statistical mechanics model of the conformational and sequence spaces of proteins. Macromolecules 1989;22:3986–97.
• 6. Shakhnovich E, Gutin A. Enumeration of all compact conformation of copolymers with random sequence of links. J Chem Phys 1990;93:5967–71.
• 7. Pande VS, Joerg C, Grosberg AY, Tanaka T. Enumerations of the Hamiltonian walks on a cubic sublattice. J Phys A Math Gen 1994;27:6231–6.
• 8. Dill KA, Bromberg S, Yue K, Fiebig KM, Yee DP, Thomas PD, et al. Principles of protein folding – a perspective from simple exact models. Protein Sci 1995;4:561–602.
• 9. Bryngelson JD, Onuchic JN, Socci ND, Wolynes PG. Funnels, pathways, and the energy landscape of protein folding: a synthesis. Proteins 1995;21:167–95.
• 10. Onuchic JN, Luthey-Schulten Z, Wolynes PG. Theory of protein folding: the energy landscape perspective. Annu Rev Phys Chem 1997;48:545–600.
• 11. Schram RD, Schiessel H. Exact enumeration of Hamiltonian walks on the 4 x 4 x 4 cube and applications to protein folding. J Phys A Math Gen 2013;46:485001.
• 12. Lazaridis T, Karplus M. “New view” of protein folding reconciled with the old through multiple unfolding simulations. Science 1997;278:1928–31.
• 13. Cruzeiro L. Protein’s multi-funnel energy landscape and misfolding diseases. J Phys Org Chem 2008;21:549–54.
• 14. Cruzeiro L, Lopes PA. Are the native states of proteins kinetic traps? Mol Phys 2009;107:1485–93.
• 15. Cruzeiro L. Protein folding. In: Springborg M, editor. Specialist periodical reports, chemical modelling, Vol. 7. London, UK: Royal Society of Chemistry, 2010:89–114.
• 16. Hecht MH, Richardson JS, Richardson DC, Ogden RC. De novo design, expression, and characterization of Felix: a four-helix bundle protein of native-like sequence. Science 1990;249: 884–91.
• 17. Kuhlman B, Dantas G, Ireton GC, Varani G, Stoddard BL, Baker D. Design of a novel globular protein fold with atomic-level accuracy. Science 2003;302:1364–8.
• 18. Shaw DE, Maragakis P, Lindorff-Larsen K, Piana S, Dror RO, Eastwood MP, et al. Atomic-level characterization of the structural dynamics of proteins. Science 2010;330:341–6.
• 19. Sanchez-Ruiz JM. Protein kinetic stability. Biophys Chem 2010;148:1–15.
• 20. Levinthal C. Are there pathways for protein folding? J Chem Phys 1968;65:44–5.
• 21. Baker D, Sohl JL, Agard DA. A protein-folding reaction under kinetic control. Nature 1992;356:263–5.
• 22. Sohl JL, Jaswal SS, Agard DA. Unfolded conformations of alphalytic protease are more stable than its native state. Nature 1998;395:817–9.
• 23. Gettins PGW. Serpin structure, mechanism, and function. Chem Rev 2002;102:4751–803.
• 24. Luo X, Tang Z, Xia G, Wassmann K, Matsumoto T, Rizo J, et al. The Mad2 spindle checkpoint protein has two distinct natively folded states. Nat Struct Mol Biol 2004;11:338–45.
• 25. Tuinstra RL, Peterson FC, Kutlesa S, Elgin ES, Kron MA, Volkman BF. Interconversion between two unrelated protein folds in the lymphotactin native state. Proc Natl Acad Sci USA 2008;105:5057–62.
• 26. Murzin AG. Metamorphic proteins. Science 2008;320: 1725–26.
• 27. Burmann BM, Knauer SH, Sevostyanova A, Schweimer K, Mooney RA, Landick R, et al. An a helix to β barrel domain switch transforms the transcription factor RfaH into a translation factor. Cell 2012;150:291–303.
• 28. Prusiner SB. Novel proteinaceous infectious particles cause scrapie. Science 1982;216:136–44.
• 29. Prusiner SB. Molecular biology of prion diseases. Science 1991;252:1515–22.
• 30. Braselmann E, Chaney JL, Clark PL. Folding the proteome. TIBS 2013;38:337–44.
• 31. Bhushan S, Gartmann M, Halic M, Armache JP, Jarasch A, Mielke T, et al. Alpha-helical nascent polypeptide chains visualized within distinct regions of the ribosomal exit tunnel. Nat Struct Mol Biol 2010;17:313–7.
• 32. Wilson DN, Beckmann R. The ribosomal tunnel as a functional environment for nascent polypeptide folding and translational stalling. Curr Opin Struct Biol 2011;21:274–82.
• 33. Zhang G, Ignatova Z. Folding at the birth of the nascent chain: coordinating translation with co-translational folding. Curr Opin Struct Biol 2011;21:25–31.
• 34. Fedyukina DV, Cavagnero S. Protein folding at the exit tunnel. Annu Rev Biophys 2011;40:337–59.
• 35. Kaiser CM, Goldman DH, Chodera JD, Tinoco Jr I, Bustamante C. The ribosome modulates nascent protein folding. Science 2011;334:1723–7.
• 36. Sander IM, Chaney JL, Clark PL. Expanding Anfinsen’s principle: contributions of synonymous codon selection to rational protein design. J Am Chem Soc 2014;136:858–61.
• 37. Levinthal C. How to fold graciously. In: Mossbauer spectroscopy in biological systems: proceedings of a meeting held at Allerton House, Monticello, Illinois, 1969;22–24.
• 38. Cruzeiro L. Nonlinear models for protein folding and function. In: Rubio RG, Ryazantsev YS, Starov VM, Huang G-X, Chetverikov AP, Arena P, editors. Without bounds: a scientific canvas of nonlinearity and complex dynamics. Heidelberg, New York, Dordrecht, London: Springer, 2013:635–46.
• 39. Ellis JP, Culviner PH, Cavagnero S. Confined dynamics of a ribosome-bound nascent globin: cone angle analysis of fluorescent depolarization decays in the presence of two local motions. Prot Sci 2009;18:2003–15.
• 40. Orengo, CA, Michie AD, Jones S, Jones DT, Swindells MB, Thornton JM. CATH – a hierarchic classification of protein domain structures. Structure 1997;5:1093–108.
• 41. Schlitter J, Engels M, Krüger P, Jacoby E, Wollmer A. Targeted molecular dynamics simulation of conformational change: application to the T to R transition in insulin. Mol Simul 1994;10:291–309.
• 42. Apostolakis J, Ferrara P, Caflisch A. Calculation of conformational transitions and barriers in solvated systems: application to the alanine dipeptide in water. J Chem Phys 1999;110:2099–108.
• 43. Ovchinnikov V, Trout BL, Karplus M. Mechanical coupling in myosin V: a simulation study. J Mol Biol 2010;395:815–33.
• 44. Negri A, Rodríguez-Larrea D, Marco E, Jiménez-Ruiz A, Sánchez-Ruiz JM, Gago F. Protein-protein interactions at an enzymesubstrate interface: characterization of transient reaction intermediates throughout a full catalytic cycle of Escherichia coli thioredoxin reductase. Proteins Struct Funct Bioinf 2010;78:36–51.
• 45. Apostolakis J, Ferrara P, Caflisch A. Computer simulations of protein folding by targeted molecular dynamics. Proteins Struct Funct Gen 2000;39:252–60.
• 46. Gouda H, Torigoe H, Saito A, Sato M, Arata Y, Shimada I. Threedimensional solution structure of the b domain of staphylococcal protein a: comparisons of the solution and crystal structures. Biochemistry 1992;31:9665–72.
• 47. Gallagher T, Alexander P, Bryan P, Gillilan GL. Two crystal structures of the B1 immunoglobulin-binding domain of streptococcal protein G and comparison with NMR. Biochemistry 1994;33:4721–9.
• 48. Hornak V, Abel R, Okur A, Strockbine B, Roitberg A, Simmerling C. Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 2006;65:712–25.
• 49. Case DA, Darden TA, Cheatham III TE, Simmerling CL, Wang J, Duke RE, et al. AMBER 9, 2006; University of California, San Francisco.
• 50. Wickstrom L, Okur A, Simmerling C. Evaluating the performance of the ff99SB force field based on NMR scalar coupling data. Biophys J 2009;97:853–6.
• 51. Weiser J, Shenkin PS, Still WC. Approximate atomic surfaces from linear combinations of pairwise overlaps (LCPO). J Comput Chem 1999;20:217–30.
• 52. Humphrey W, Dalke A, Schulten K. VMD – Visual Molecular Dynamics. J Mol Graphics 1996;14:33–8.
• 53. Dill KA, Chan H-S. From Levinthal to pathways to funnels. Nat Struct Biol 1997;4:10–9.
• 54. Dill KA, Ozkan SB, Shell MS, Weikl TR. The protein folding problem. Annu Rev Biophys 2008;37:289–316.
• 55. Christen M, Hünenberger PH, Bakowies D, Baron R, Bürgi R, Geerke DP, et al. The GROMOS software for biomolecular simulation: GROMOS05. J Comput Chem. 2005;26:1719–51.
• 56. Brooks BR, Brooks III CL, Mackerell Jr AD, Nilsson L, Petrella RJ, Roux B, et al. CHARMM: the biomolecular simulation program. J Comput Chem 2009;30:1545–614.
• 57. Allen F, Almasi G, Andreoni W, Beece D, Berne BJ, Bright A, et al. Blue Gene: a vision for protein science using a petaflop computer. IBM Syst J 2001;40:310–27.
• 58. Berendsen HJC. A glimpse of the Holy Grail? Science 1998;282:642–3.
• 59. Horowitz PM. Ironing out the protein folding problem? Nat Biotechnol 1999;17:136–7.
• 60. Service RF. Problem Solved (sort of). Science 2008;321:784–6.
• 61. Pan KM, Baldwin M, Nguyen J, Gasset M, Serban A, Groth D, et al. Conversion of -helices into -sheets features in the formation of the scrapie prion proteins. Proc Natl Acad Sci USA 1993;90:10962–6.
• 62. Booth DR, Sunde M, Bellotti V, Robinson C.V, Hutchinson WL, Fraser PE, et al. Instability, unfolding and aggregation of human lysozyme variants underlying amyloid fibrillogenesis. Nature 1997;385:787–93.
• 63. Fändrich M, Fletcher MA, Dobson CM. Amyloid fibrils from muscle myoglobin. Nature 2001;410:165–6.
• 64. Cruzeiro-Hansson L, Silva PAS. Protein folding: thermodynamic versus kinetic control. J Biol Phys 2001;27:S6–9.
• 65. Cruzeiro L. Why are proteins with glutamine- and asparaginerich regions associated with protein misfolding diseases? J Phys Condens Matter 2005;17:7833–44.
• 66. Kohn JE, Millett IS, Jacob J, Zagrovic B, Dillon TM, Cingel N, et al. Random-coil behavior and the dimensions of chemically unfolded proteins. Proc Natl Acad Sci 2004;34:12491–6.
• 67. Bowler BE. Residual structure in unfolded proteins. Curr Opin Struct Biol 2012;22:4–13.
• 68. Ziv G, Haran G, Thirumalai D. Ribosome exit tunnel can entropically stabilize alpha-helices. Proc Natl Acad Sci USA 2005;102:18956–61.
• 69. Silva PAS, Cruzeiro-Hansson L. A reduced set of exact equations of motion for a non-number-conserving Hamiltonian. Phys Lett A 2003;315/6:447–51.
• 70. Silva PAS, Cruzeiro L. Dynamics of a nonconserving Davydov monomer. Phys Rev E 2006;74:021920.