Polymer scaling laws of unfolded and intrinsically disordered proteins quantified with single-molecule spectroscopy

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 40, 2012, Pages 16155-16160

  Hofmann, Hagen ^a   Soranno, Andrea ^a   Borgia, Alessandro ^a   Gast, Klaus ^b   Nettels, Daniel ^a   Schuler, Benjamin ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF POTSDAM   (Germany)

Author keywords

Coil globule transition; Polymer theory; Protein folding; Single molecule FRET

Indexed keywords

POLYMER; WATER;

AMINO ACID SEQUENCE; ARTICLE; CELLULAR PARAMETERS; FLUORESCENCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; UNFOLDED PROTEIN RESPONSE;

AMINO ACID SEQUENCE; CYCLOPHILIN A; HUMANS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; POLYMERS; PROTEIN FOLDING; PROTEINS; SPECTROMETRY, FLUORESCENCE; WATER;

EID: 84867048390     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1207719109     Document Type: Article

References (61)

1. Hagen SJ, Hofrichter J, Szabo A, Eaton WA (1996) Diffusion-limited contact formation in unfolded cytochrome c: Estimating the maximum rate of protein folding. Proc Natl Acad Sci USA 93:11615-11617. (Pubitemid 26347170)
2. Bieri O, et al. (1999) The speed limit for protein folding measured by triplet-triplet energy transfer. Proc Natl Acad Sci USA 96:9597-9601. (Pubitemid 29398776)
3. Schuler B, Lipman E, Eaton W (2002) Probing the free-energy surface for protein folding with single-molecule fluorescence spectroscopy. Nature 419:743-747. (Pubitemid 35177962)
4. Müller-Späth S, et al. (2010) Charge interactions can dominate the dimensions of intrinsically disordered proteins. Proc Natl Acad Sci USA 107:14609-14614.
5. Shoemaker B, Portman J, Wolynes P (2000) Speeding molecular recognition by using the folding funnel: The fly-casting mechanism. Proc Natl Acad Sci USA 97:8868-8873. (Pubitemid 30626639)
6. Sugase K, Dyson H, Wright PE (2007) Mechanism of coupled folding and binding of an intrinsically disordered protein. Nature 447:1021-1025. (Pubitemid 46975749)
7. Chan HS, Dill KA (1991) Polymer principles in protein structure and stability. Annu Rev Biophys Biophys Chem 20:447-490.
8. Onuchic JN, Luthey-Schulten Z, Wolynes PG (1997) Theory of protein folding: The energy landscape perspective. Annu Rev Phys Chem 48:545-600. (Pubitemid 127443918)
9. Thirumalai D, O'Brien E, Morrison G, Hyeon C (2010) Theoretical perspectives on protein folding. Annu Rev Biophys 39:159-183.
10. Sherman E, Haran G (2006) Coil-globule transition in the denatured state of a small protein. Proc Natl Acad Sci USA 103:11539-11543. (Pubitemid 44182487)
11. Ziv G, Haran G (2009) Protein folding, protein collapse, and Tanford's transfer model: Lessons from single-molecule FRET. J Am Chem Soc 131:2942-2947.
12. Bryngelson J, Wolynes P (1990) A simple statistical field-theory of heteropolymer collapse with application to protein folding. Biopolymers 30:177-188. (Pubitemid 20263101)
13. Alonso DO, Dill KA (1991) Solvent denaturation and stabilization of globular proteins. Biochemistry 30:5974-5985.
14. O'Brien E, Ziv G, Haran G, Brooks B, Thirumalai D (2008) Effects of denaturants and osmolytes on proteins are accurately predicted by the molecular transfer model. Proc Natl Acad Sci USA 105:13403-13408.
15. Haran G (2012) How, when, and why proteins collapse: The relation to folding. Curr Opin Struct Biol 22:14-20.
16. Waldauer S, Bakajin O, Lapidus L (2010) Extremely slow intramolecular diffusion in unfolded protein L. Proc Natl Acad Sci USA 107:13713-13717.
17. Nettels D, Gopich I, Hoffmann A, Schuler B (2007) Ultrafast dynamics of protein collapse from single-molecule photon statistics. Proc Natl Acad Sci USA 104:2655-2660. (Pubitemid 46327935)
18. Nettels D, et al. (2009) Single-molecule spectroscopy of the temperature-induced collapse of unfolded proteins. Proc Natl Acad Sci USA 106:20740-20745.
19. Schuler B, Eaton W (2008) Protein folding studied by single-molecule FRET. Curr Opin Struct Biol 18:16-26.
20. Grosberg A, Kuznetsov D (1992) Quantitative theory of the globule-to-coil transition. 4. Comparison of theoretical results with experimental data. Macromolecules 25:1996-2003.
21. Sanchez I (1979) Phase transition behavior of the isolated polymer chain. Macromolecules 12:980-988.
22. Flory P (1949) The configuration of real polymer chains. J Chem Phys 17:303-310.
23. de Gennes P-G (1979) Scaling Concepts in Polymer Physics (Cornell Univ Press, Ithaca, NY and London), pp 113-123.
24. Ha B-Y, Thirumalai D (1992) Conformations of a polyelectrolyte chain. Phys Rev A 46: R3012-R3015.
25. Camacho C, Thirumalai D (1993) Kinetics and thermodynamics of folding in model proteins. Proc Natl Acad Sci USA 90:6369-6372. (Pubitemid 23191517)
26. Thirumalai D (1995) From minimal models to real proteins: Time scales for proteinfolding kinetics. J Phys (Paris) 5:1457-1467.
27. Uversky VN (2002) Natively unfolded proteins: A point where biology waits for physics. Protein Sci 11:739-756.
28. Crick SL, Jayaraman M, Frieden C, Wetzel R, Pappu RV (2006) Fluorescence correlation spectroscopy shows that monomeric polyglutamine molecules form collapsed structures in aqueous solutions. Proc Natl Acad Sci USA 103:16764-16769. (Pubitemid 44737327)
29. Tran HT, Mao A, Pappu RV (2008) Role of backbone-solvent interactions in determining conformational equilibria of intrinsically disordered proteins. J Am Chem Soc 130:7380-7392. (Pubitemid 351813231)
30. Uzawa T, et al. (2006) Time-resolved small-angle X-ray scattering investigation of the folding dynamics of heme oxygenase: Implication of the scaling relationship for the submillisecond intermediates of protein folding. J Mol Biol 357:997-1008.
31. Kallen J, et al. (1991) Structure of human cyclophilin and its binding site for cyclosporin A determined by X-ray crystallography and NMR spectroscopy. Nature 353:276-279. (Pubitemid 21896773)
32. Wensley B, et al. (2010) Experimental evidence for a frustrated energy landscape in a three-helix-bundle protein family. Nature 463:685-688.
33. Möglich A, Joder K, Kiefhaber T (2006) End-to-end distance distributions and intrachain diffusion constants in unfolded polypeptide chains indicate intramolecular hydrogen bond formation. Proc Natl Acad Sci USA 103:12394-12399. (Pubitemid 44267270)
34. Flory P (1989) Statistical Mechanics of Chain Molecules (Carl Hanser Verlag, Munich, Vienna, and New York).
35. Dima R, Thirumalai D (2004) Asymmetry in the shapes of folded and denatured states of proteins. J Phys Chem B 108:6564-6570.
36. Theodorou DN, Suter UW (1985) Shape of unperturbed linear-polymers: Polypropylene. Macromolecules 18:1206-1214.
37. Tran HT, Pappu RV (2006) Toward an accurate theoretical framework for describing ensembles for proteins under strongly denaturing conditions. Biophys J 91:1868-1886. (Pubitemid 44352450)
38. Hammouda B (1993) SANS from homogeneous polymer mixtures: A unified overview. Adv Polymer Sci 106:87-133.
39. Zhou H (2004) Polymer models of protein stability, folding, and interactions. Biochemistry 43:2141-2154.
40. Kohn J, et al. (2004) Random-coil behavior and the dimensions of chemically unfolded proteins. Proc Natl Acad Sci USA 101:12491-12496. (Pubitemid 39122051)
41. Wilkins D, et al. (1999) Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques. Biochemistry 38:16424-16431.
42. Goldenberg D (2003) Computational simulation of the statistical properties of unfolded proteins. J Mol Biol 326:1615-1633.
43. Vitalis A, Wang X, Pappu R (2007) Quantitative characterization of intrinsic disorder in polyglutamine: Insights from analysis based on polymer theories. Biophys J 93:1923-1937. (Pubitemid 47437577)
44. Fitzkee N, Rose G (2004) Reassessing random-coil statistics in unfolded proteins. Proc Natl Acad Sci USA 101:12497-12502. (Pubitemid 39122052)
45. Zhou H (2002) Dimensions of denatured protein chains from hydrodynamic data. J Phys Chem B 106:5769-5775.
46. Damaschun G, Damaschun H, Gast K, Zirwer D (1998) Denatured states of yeast phosphoglycerate kinase. Biochemistry (Moscow) 63:259-275. (Pubitemid 128588264)
47. Tanford C, Kawahara K, Lapanje S (1966) Proteins in 6M guanidine hydrochloride: Demonstration of random coil behavior. J Biol Chem 241:1921-1923.
48. Uversky V, Gillespie J, Fink A (2000) Why are "natively unfolded" proteins unstructured under physiologic conditions. Proteins 41:415-427.
49. O'Brien E, Dima R, Brooks B, Thirumalai D (2007) Interactions between hydrophobic and ionic solutes in aqueous guanidinium chloride and urea solutions: Lessons for protein denaturation mechanism. J Am Chem Soc 129:7346-7353. (Pubitemid 46980813)
50. Wu C, Zhou S (1996) First observation of the molten globule state of a single homopolymer chain. Phys Rev Lett 77:3053-3055. (Pubitemid 126624205)
51. Dertinger T, et al. (2007) Two-focus fluorescence correlation spectroscopy: A new tool for accurate and absolute diffusion measurements. Chemphyschem 8:433-443.
52. Steinhauser MO (2005) A molecular dynamics study on universal properties of polymer chains in different solvent qualities. Part I. A review of linear chain properties. J Chem Phys 122:94901-94913.
53. Schellman J (2002) Fifty years of solvent denaturation. Biophys Chem 96:91-101.
54. Nozaki Y, Tanford C (1970) The solubility of amino acids, diglycine, and triglycine in aqueous guanidine hydrochloride solutions. J Biol Chem 245:1648-1652.
55. Mao AH, Crick SL, Vitalis A, Chicoine CL, Pappu RV (2010) Net charge per residue modulates conformational ensembles of intrinsically disordered proteins. Proc Natl Acad Sci USA 107:8183-8188.
56. Teufel DP, Johnson CM, Lum JK, Neuweiler H (2011) Backbone-driven collapse in unfolded protein chains. J Mol Biol 409:250-262.
57. Gutin A, Abkevich V (1995) Is burst hydrophobic collapse necessary for protein folding? Biochemistry 34:3066-3076.
58. Soranno A, et al. (2012) Quantifying internal friction in unfolded and intrinsically disordered proteins with single molecule spectroscopy. Proc Natl Acad Sci USA, doi:10.1073/pnas.1117368109.
59. Plaxco K, Simons K, Baker D (1998) Contact order, transition state placement and the refolding rates of single domain proteins. J Mol Biol 277:985-994. (Pubitemid 28195995)
60. Jordan IK, et al. (2005) A universal trend of amino acid gain and loss in protein evolution. Nature 433:633-638. (Pubitemid 40282996)
61. Hoffmann A, et al. (2007) Mapping protein collapse with single-molecule fluorescence and kinetic synchrotron radiation circular dichroism spectroscopy. Proc Natl Acad Sci USA 104:105-110. (Pubitemid 46067992)