1932

Abstract

The properties of unfolded proteins have long been of interest because of their importance to the protein folding process. Recently, the surprising prevalence of unstructured regions or entirely disordered proteins under physiological conditions has led to the realization that such intrinsically disordered proteins can be functional even in the absence of a folded structure. However, owing to their broad conformational distributions, many of the properties of unstructured proteins are difficult to describe with the established concepts of structural biology. We have thus seen a reemergence of polymer physics as a versatile framework for understanding their structure and dynamics. An important driving force for these developments has been single-molecule spectroscopy, as it allows structural heterogeneity, intramolecular distance distributions, and dynamics to be quantified over a wide range of timescales and solution conditions. Polymer concepts provide an important basis for relating the physical properties of unstructured proteins to folding and function.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-062215-010915
2016-07-05
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/biophys/45/1/annurev-biophys-062215-010915.html?itemId=/content/journals/10.1146/annurev-biophys-062215-010915&mimeType=html&fmt=ahah

Literature Cited

  1. Aigrain L, Crawford R, Torella J, Plochowietz A, Kapanidis A. 1.  2012. Single-molecule FRET measurements in bacterial cells. FEBS J. 279:Suppl. s1513 [Google Scholar]
  2. Alonso DO, Dill KA. 2.  1991. Solvent denaturation and stabilization of globular proteins. Biochemistry 30:5974–85 [Google Scholar]
  3. Ansari A, Jones CM, Henry ER, Hofrichter J, Eaton WA. 3.  1992. The role of solvent viscosity in the dynamics of protein conformational changes. Science 256:1796–98 [Google Scholar]
  4. Aznauryan M, Nettels D, Holla A, Hofmann H, Schuler B. 4.  2013. Single-molecule spectroscopy of cold denaturation and the temperature-induced collapse of unfolded proteins. J. Am. Chem. Soc. 135:14040–43 [Google Scholar]
  5. Babu MM, Kriwacki RW, Pappu RV. 5.  2012. Structural biology. Versatility from protein disorder. Science 337:1460–61 [Google Scholar]
  6. Barsegov V, Morrison G, Thirumalai D. 6.  2008. Role of internal chain dynamics on the rupture kinetic of adhesive contacts. Phys. Rev. Lett. 100:248102 [Google Scholar]
  7. Bazua ER, Williams MC. 7.  1973. Molecular formulation of internal viscosity in polymer dynamics, and stress symmetry. J. Chem. Phys. 59:2858–68 [Google Scholar]
  8. Benke S, Roderer D, Wunderlich B, Nettels D, Glockshuber R, Schuler B. 8.  2015. The assembly dynamics of the cytolytic pore toxin ClyA. Nat. Commun. 6:6198 [Google Scholar]
  9. Bernado P, Svergun DI. 9.  2012. Structural analysis of intrinsically disordered proteins by small-angle X-ray scattering. Mol. BioSyst. 8:151–67 [Google Scholar]
  10. Best RB, Hofmann H, Nettels D, Schuler B. 10.  2015. Quantitative interpretation of FRET experiments via molecular simulation: force field and validation. Biophys. J. 108:2721–31 [Google Scholar]
  11. Best RB, Merchant K, Gopich IV, Schuler B, Bax A, Eaton WA. 11.  2007.. Effect of flexibility and cis residues in single molecule FRET studies of polyproline. PNAS 104:18964–69 [Google Scholar]
  12. Best RB, Mittal J. 12.  2010. Protein simulations with an optimized water model: cooperative helix formation and temperature-induced unfolded state collapse. J. Phys. Chem. B 114:14916–23 [Google Scholar]
  13. Best RB, Zheng W, Mittal J. 13.  2014. Balanced protein-water interactions improve properties of disordered proteins and non-specific protein association. J. Chem. Theory Comput. 10:5113–24 [Google Scholar]
  14. Borgia A, Wensley BG, Soranno A, Nettels D, Borgia M. 14.  et al. 2012. Localizing internal friction along the reaction coordinate of protein folding by combining ensemble and single molecule fluorescence spectroscopy. Nat. Commun. 3:1195 [Google Scholar]
  15. Brucale M, Schuler B, Samori B. 15.  2014. Single-molecule studies of intrinsically disordered proteins. Chem. Rev. 114:3281–317 [Google Scholar]
  16. Bungenberg de Jong HL, Klaar WJ. 16.  1932. Colloid chemistry of gliadin separation phenomena. Trans. Faraday Soc. 28:27–68 [Google Scholar]
  17. Camacho CJ, Thirumalai D. 17.  1993. Kinetics and thermodynamics of folding in model proteins. PNAS 90:6369–72 [Google Scholar]
  18. Cellmer T, Henry ER, Hofrichter J, Eaton WA. 18.  2008. Measuring internal friction of an ultrafast-folding protein. PNAS 105:18320–25 [Google Scholar]
  19. Cerf R.19.  1958. Mécanique statistique des macromolécules en chaines dans un champ de vitesses. J. Phys. Radium 19:122–34 [Google Scholar]
  20. Chan HS, Dill KA. 20.  1991. Polymer principles in protein structure and stability. Annu. Rev. Biophys. Biophys. Chem. 20:447–90 [Google Scholar]
  21. Chattopadhyay K, Elson EL, Frieden C. 21.  2005. The kinetics of conformational fluctuations in an unfolded protein measured by fluorescence methods. PNAS 102:2385–89 [Google Scholar]
  22. Chen H, Rhoades E. 22.  2008. Fluorescence characterization of denatured proteins. Curr. Opin. Struct. Biol. 18:516–24 [Google Scholar]
  23. Cheng RR, Hawk AT, Makarov DE. 23.  2013. Exploring the role of internal friction in the dynamics of unfolded proteins using simple polymer models. J. Chem. Phys. 138:074112 [Google Scholar]
  24. Choi UB, McCann JJ, Weninger KR, Bowen ME. 24.  2011. Beyond the random coil: stochastic conformational switching in intrinsically disordered proteins. Structure 19:566–76 [Google Scholar]
  25. Chung HS, Gopich IV, McHale K, Cellmer T, Louis JM, Eaton WA. 25.  2011. Extracting rate coefficients from single-molecule photon trajectories and FRET efficiency histograms for a fast-folding protein. J. Phys. Chem. A 115:3642–56 [Google Scholar]
  26. Chung HS, McHale K, Louis JM, Eaton WA. 26.  2012. Single-molecule fluorescence experiments determine protein folding transition path times. Science 335:981–84 [Google Scholar]
  27. Crick SL, Jayaraman M, Frieden C, Wetzel R, Pappu RV. 27.  2006. Fluorescence correlation spectroscopy shows that monomeric polyglutamine molecules form collapsed structures in aqueous solutions. PNAS 103:16764–69 [Google Scholar]
  28. Das A, Sin BK, Mohazab AR, Plotkin SS. 28.  2013. Unfolded protein ensembles, folding trajectories, and refolding rate prediction. J. Chem. Phys. 139:121925 [Google Scholar]
  29. Das RK, Pappu RV. 29.  2013. Conformations of intrinsically disordered proteins are influenced by linear sequence distributions of oppositely charged residues. PNAS 110:13392–97 [Google Scholar]
  30. de Gennes PG. 30.  1979. Scaling Concepts in Polymer Physics Ithaca, NY: Cornell Univ. Press
  31. de Sancho D, Sirur A, Best RB. 31.  2014. Molecular origins of internal friction effects on protein-folding rates. Nat. Commun. 5:4307 [Google Scholar]
  32. Dedmon MM, Patel CN, Young GB, Pielak GJ. 32.  2002. FlgM gains structure in living cells. PNAS 99:12681–84 [Google Scholar]
  33. Deniz AA, Laurence TA, Beligere GS, Dahan M, Martin AB. 33.  et al. 2000. Single-molecule protein folding: diffusion fluorescence resonance energy transfer studies of the denaturation of chymotrypsin inhibitor 2. PNAS 97:5179–84 [Google Scholar]
  34. Deniz AA, Laurence TA, Dahan M, Chemla DS, Schultz PG, Weiss S. 34.  2001. Ratiometric single-molecule studies of freely diffusing biomolecules. Annu. Rev. Phys. Chem. 52:233–53 [Google Scholar]
  35. Dill KA.35.  1985. Theory for the folding and stability of globular proteins. Biochemistry 24:1501–9 [Google Scholar]
  36. Dima RI, Thirumalai D. 36.  2004. Asymmetry in the shapes of folded and denatured states of proteins. J. Phys. Chem. B 108:6564–70 [Google Scholar]
  37. Dobrynin AV, Colby RH, Rubinstein M. 37.  2004. Polyampholytes. J. Pol. Sci. B 42:3513–38 [Google Scholar]
  38. Doi M, Edwards SF. 38.  1988. The Theory of Polymer Dynamics New York: Oxford Univ. Press
  39. Doose S, Neuweiler H, Sauer M. 39.  2009. Fluorescence quenching by photoinduced electron transfer: a reporter for conformational dynamics of macromolecules. ChemPhysChem 10:1389–98 [Google Scholar]
  40. Eaton WA.40.  1999. Searching for “downhill scenarios” in protein folding. PNAS 96:5897–99 [Google Scholar]
  41. Eaton WA, Muñoz V, Thompson PA, Chan CK, Hofrichter J. 41.  1997. Submillisecond kinetics of protein folding. Curr. Opin. Struct. Biol. 7:10–14 [Google Scholar]
  42. Echeverria I, Makarov DE, Papoian GA. 42.  2014. Concerted dihedral rotations give rise to internal friction in unfolded proteins. J. Am. Chem. Soc. 136:8708–13 [Google Scholar]
  43. Edwards SF.43.  1966. Theory of polymer solutions at intermediate concentration. Proc. Phys. Soc. 88:265 [Google Scholar]
  44. Elbaum-Garfinkle S, Rhoades E. 44.  2012. Identification of an aggregation-prone structure of tau. J. Am. Chem. Soc. 134:16607–13 [Google Scholar]
  45. Ferreiro DU, Komives EA, Wolynes PG. 45.  2014. Frustration in biomolecules. Q. Rev. Biophys. 47:285–363 [Google Scholar]
  46. Ferreon AC, Moran CR, Gambin Y, Deniz AA. 46.  2010. Single-molecule fluorescence studies of intrinsically disordered proteins. Methods Enzymol. 472:179–204 [Google Scholar]
  47. Ferreon ACM, Gambin Y, Lemke EA, Deniz AA. 47.  2009. Interplay of α-synuclein binding and conformational switching probed by single-molecule fluorescence. PNAS 106:5645–50 [Google Scholar]
  48. Fitzkee NC, Rose GD. 48.  2004. Reassessing random-coil statistics in unfolded proteins. PNAS 101:12497–502 [Google Scholar]
  49. Flory PJ.49.  1953. Principles of Polymer Chemistry Ithaca, NY: Cornell Univ. Press
  50. Flory PJ.50.  1969. Statistical Mechanics of Chain Molecules New York: Wiley
  51. Förster T.51.  1948. Zwischenmolekulare Energiewanderung und Fluoreszenz. Ann. Phys. 6:55–75 [Google Scholar]
  52. Gambin Y, Deniz AA. 52.  2010. Multicolor single-molecule FRET to explore protein folding and binding. Mol. Biosyst. 6:1540–47 [Google Scholar]
  53. Gast K, Modler AJ. 53.  2005. Studying protein folding and aggregation by laser light scattering. Protein Folding Handbook J Buchner, T Kiefhaber 673–709 Weinheim, Ger: Wiley-VCH [Google Scholar]
  54. Gnutt D, Gao M, Brylski O, Heyden M, Ebbinghaus S. 54.  2015. Excluded-volume effects in living cells. Angew. Chem. Int. Ed. Engl. 54:2548–51 [Google Scholar]
  55. Gopich IV, Nettels D, Schuler B, Szabo A. 55.  2009. Protein dynamics from single-molecule fluorescence intensity correlation functions. J. Chem. Phys. 131:095102 [Google Scholar]
  56. Gopich IV, Szabo A. 56.  2003. Single-macromolecule fluorescence resonance energy transfer and free-energy profiles. J. Phys. Chem. B 107:5058–63 [Google Scholar]
  57. Gopich IV, Szabo A. 57.  2005. Theory of photon statistics in single-molecule Förster resonance energy transfer. J. Chem. Phys. 122:014707 [Google Scholar]
  58. Gopich IV, Szabo A. 58.  2010. FRET efficiency distributions of multistate single molecules. J. Phys. Chem. B 114:15221–26 [Google Scholar]
  59. Gopich IV, Szabo A. 59.  2012. Theory of the energy transfer efficiency and fluorescence lifetime distribution in single-molecule FRET. PNAS 109:7747–52 [Google Scholar]
  60. Grinvald A, Haas E, Steinberg I. 60.  1972. Evaluation of distribution of distances between energy donors and acceptors by fluorescence decay. PNAS 69:2273–2277 [Google Scholar]
  61. Grosberg AY, Kuznetsov DV. 61.  1992. Quantitative theory of the globule-to-coil transition. 1. Link density distribution in a globule and its Radius of gyration. Macromolecules 25:1970–79 [Google Scholar]
  62. Ha BY, Thirumalai D. 62.  1992. Conformations of a polyelectrolyte chain. Phys. Rev. A 46:R3012–15 [Google Scholar]
  63. Haas E, Katchalskikatzir E, Steinberg IZ. 63.  1978. Brownian motion of ends of oligopeptide chains in solution as estimated by energy transfer between chain ends. Biopolymers 17:11–31 [Google Scholar]
  64. Hagen SJ.64.  2010. Solvent viscosity and friction in protein folding dynamics. Curr. Protein Pept. Sci. 11:385–95 [Google Scholar]
  65. Haran G.65.  2012. How, when and why proteins collapse: the relation to folding. Curr. Opin. Struct. Biol. 22:14–20 [Google Scholar]
  66. Higgs PG, Joanny JF. 66.  1991. Theory of polyampholyte solutions. J. Chem. Phys. 94:1543–54 [Google Scholar]
  67. Hoffmann A, Kane A, Nettels D, Hertzog DE, Baumgärtel P. 67.  et al. 2007. Mapping protein collapse with single-molecule fluorescence and kinetic synchrotron radiation circular dichroism spectroscopy. PNAS 104:105–10 [Google Scholar]
  68. Hoffmann A, Nettels D, Clark J, Borgia A, Radford SE. 68.  et al. 2011. Quantifying heterogeneity and conformational dynamics from single molecule FRET of diffusing molecules: recurrence analysis of single particles (RASP). Phys. Chem. Chem. Phys. 13:1857–71 [Google Scholar]
  69. Hofmann H, Golbik RP, Ott M, Hübner CG, Ulbrich-Hofmann R. 69.  2008. Coulomb forces control the density of the collapsed unfolded state of barstar. J. Mol. Biol. 376:597–605 [Google Scholar]
  70. Hofmann H, Soranno A, Borgia A, Gast K, Nettels D, Schuler B. 70.  2012. Polymer scaling laws of unfolded and intrinsically disordered proteins quantified with single-molecule spectroscopy. PNAS 109:16155–60 [Google Scholar]
  71. Holehouse AS, Garai K, Lyle N, Vitalis A, Pappu RV. 71.  2015. Quantitative assessments of the distinct contributions of polypeptide backbone amides versus side chain groups to chain expansion via chemical denaturation. J. Am. Chem. Soc. 137:2984–95 [Google Scholar]
  72. Hong JA, Gierasch LM. 72.  2010. Macromolecular crowding remodels the energy landscape of a protein by favoring a more compact unfolded state. J. Am. Chem. Soc. 132:10445–52 [Google Scholar]
  73. Hyeon C, Thirumalai D. 73.  2011. Capturing the essence of folding and functions of biomolecules using coarse-grained models. Nat. Commun. 2:487 [Google Scholar]
  74. Hyman AA, Weber CA, Jülicher F. 74.  2014. Liquid-liquid phase separation in biology. Annu. Rev. Cell Dev. Biol. 30:39–58 [Google Scholar]
  75. Jensen MR, Zweckstetter M, Huang JR, Backledge M. 75.  2014. Exploring free-energy landscapes of intrinsically disordered proteins at atomic resolution using NMR spectroscopy. Chem. Rev. 114:6632–60 [Google Scholar]
  76. Joanny JF, Grant P, Pincus P, Turkevich LA. 76.  1981. Conformations of polydisperse polymer solutions: bimodal distribution. J. Appl. Phys. 52:5943–48 [Google Scholar]
  77. Johansen D, Jeffries CM, Hammouda B, Trewhella J, Goldenberg DP. 77.  2011. Effects of macromolecular crowding on an intrinsically disordered protein characterized by small-angle neutron scattering with contrast matching. Biophys. J. 100:1120–28 [Google Scholar]
  78. Kalinin S, Valeri A, Antonik M, Felekyan S, Seidel CA. 78.  2010. Detection of structural dynamics by FRET: a photon distribution and fluorescence lifetime analysis of systems with multiple states. J. Phys. Chem. B 114:7983–95 [Google Scholar]
  79. Kang H, Pincus PA, Hyeon C, Thirumalai D. 79.  2015. Effects of macromolecular crowding on the collapse of biopolymers. Phys. Rev. Lett. 114:068303 [Google Scholar]
  80. Kauzmann W.80.  1959. Some factors in the interpretation of protein denaturation. Adv. Protein Chem. 14:1–63 [Google Scholar]
  81. Kellner R, Hofmann H, Barducci A, Wunderlich B, Nettels D, Schuler B. 81.  2014. Single-molecule spectroscopy reveals chaperone-mediated expansion of substrate protein. PNAS 111:13355–60 [Google Scholar]
  82. Khatri BS, McLeish TCB. 82.  2007. Rouse model with internal friction: a coarse grained framework for single biopolymer dynamics. Macromolecules 40:6770–77 [Google Scholar]
  83. Koenig I, Zarrine-Afsar A, Aznauryan M, Soranno A, Wunderlich B. 83.  et al. 2015. Single-molecule spectroscopy of protein conformational dynamics in live eukaryotic cells. Nat. Methods 12:773–79 [Google Scholar]
  84. Kohn JE, Millett IS, Jacob J, Zagrovic B, Dillon TM. 84.  et al. 2004. Random-coil behavior and the dimensions of chemically unfolded proteins. PNAS 101:12491–96 [Google Scholar]
  85. Kuhn W, Kuhn H. 85.  1945. Bedeutung beschränkt freier Drehbarkeit für die Viskosität und Strömungsdoppelbrechung von Fadenmolekellösungen 1. Helv. Chim. Acta 28:1533–79 [Google Scholar]
  86. Kumar R, Kundagrami A, Muthukumar M. 86.  2009. Counterion adsorption on flexible polyelectrolytes: comparison of theories. Macromolecules 42:1370–79 [Google Scholar]
  87. Kuzmenkina EV, Heyes CD, Nienhaus GU. 87.  2005. Single-molecule Förster resonance energy transfer study of protein dynamics under denaturing conditions. PNAS 102:15471–76 [Google Scholar]
  88. Lamboy JA, Kim H, Lee KS, Ha T, Komives EA. 88.  2011. Visualization of the nanospring dynamics of the IκBα ankyrin repeat domain in real time. PNAS 108:10178–83 [Google Scholar]
  89. Lapidus LJ, Eaton WA, Hofrichter J. 89.  2000. Measuring the rate of intramolecular contact formation in polypeptides. PNAS 97:7220–25 [Google Scholar]
  90. Laurence TA, Kong XX, Jäger M, Weiss S. 90.  2005. Probing structural heterogeneities and fluctuations of nucleic acids and denatured proteins. PNAS 102:17348–53 [Google Scholar]
  91. Li P, Banjade S, Cheng HC, Kim S, Chen B. 91.  et al. 2012. Phase transitions in the assembly of multivalent signalling proteins. Nature 483:336–40 [Google Scholar]
  92. Li Y, Shan B, Raleigh DP. 92.  2007. The cold denatured state is compact but expands at low temperatures: hydrodynamic properties of the cold denatured state of the C-terminal domain of L9. J. Mol. Biol. 368:256–62 [Google Scholar]
  93. Liu B, Chia D, Csizmok V, Farber P, Forman-Kay JD, Gradinaru CC. 93.  2014. The effect of intrachain electrostatic repulsion on conformational disorder and dynamics of the Sic1 protein. J. Phys. Chem. B 118:4088–97 [Google Scholar]
  94. Magg C, Kubelka J, Holtermann G, Haas E, Schmid FX. 94.  2006. Specificity of the initial collapse in the folding of the cold shock protein. J. Mol. Biol. 360:1067–80 [Google Scholar]
  95. Makarov DE.95.  2010. Spatiotemporal correlations in denatured proteins: the dependence of fluorescence resonance energy transfer (FRET)-derived protein reconfiguration times on the location of the FRET probes. J. Chem. Phys. 132:035104 [Google Scholar]
  96. Makhatadze GI, Privalov PL. 96.  1992. Protein interactions with urea and guanidinium chloride: a calorimetric study. J. Mol. Biol. 226:491–505 [Google Scholar]
  97. Mao AH, Crick SL, Vitalis A, Chicoine CL, Pappu RV. 97.  2010. Net charge per residue modulates conformational ensembles of intrinsically disordered proteins. PNAS 107:8183–88 [Google Scholar]
  98. McCarney ER, Werner JH, Bernstein SL, Ruczinski I, Makarov DE. 98.  et al. 2005. Site-specific dimensions across a highly denatured protein; a single molecule study. J. Mol. Biol. 352:672–82 [Google Scholar]
  99. McNulty BC, Young GB, Pielak GJ. 99.  2006. Macromolecular crowding in the Escherichia coli periplasm maintains α-synuclein disorder. J. Mol. Biol. 355:893–97 [Google Scholar]
  100. Merchant KA, Best RB, Louis JM, Gopich IV, Eaton WA. 100.  2007. Characterizing the unfolded states of proteins using single-molecule FRET spectroscopy and molecular simulations. PNAS 104:1528–33 [Google Scholar]
  101. Mikaelsson T, Ad én J, Johansson LBA, Wittung-Stafshede P. 101.  2013. Direct observation of protein unfolded state compaction in the presence of macromolecular crowding. Biophys. J. 104:694–704 [Google Scholar]
  102. Milles S, Koehler C, Gambin Y, Deniz AA, Lemke EA. 102.  2012. Intramolecular three-colour single pair FRET of intrinsically disordered proteins with increased dynamic range. Mol. Biosyst. 8:2531–34 [Google Scholar]
  103. Milles S, Lemke EA. 103.  2011. Single molecule study of the intrinsically disordered FG-repeat nucleoporin 153. Biophys. J. 101:1710–19 [Google Scholar]
  104. Minton AP.104.  2005. Models for excluded volume interaction between an unfolded protein and rigid macromolecular cosolutes: macromolecular crowding and protein stability revisited. Biophys. J. 88971–85
  105. Minton AP.105.  2013. Quantitative assessment of the relative contributions of steric repulsion and chemical interactions to macromolecular crowding. Biopolymers 99:239–44 [Google Scholar]
  106. Mittal J, Best RB. 106.  2010. Dependence of protein folding stability and dynamics on the density and composition of macromolecular crowders. Biophys. J. 98:315–20 [Google Scholar]
  107. Möglich A, Joder K, Kiefhaber T. 107.  2006. End-to-end distance distributions and intrachain diffusion constants in unfolded polypeptide chains indicate intramolecular hydrogen bond formation. PNAS 103:12394–99 [Google Scholar]
  108. Mukhopadhyay S, Krishnan R, Lemke EA, Lindquist S, Deniz AA. 108.  2007. A natively unfolded yeast prion monomer adopts an ensemble of collapsed and rapidly fluctuating structures. PNAS 104:2649–54 [Google Scholar]
  109. Müller-Späth S, Soranno A, Hirschfeld V, Hofmann H, Rüegger S. 109.  et al. 2010. Charge interactions can dominate the dimensions of intrinsically disordered proteins. PNAS 107:14609–14 [Google Scholar]
  110. Nath A, Sammalkorpi M, DeWitt DC, Trexler AJ, Elbaum-Garfinkle S. 110.  et al. 2012. The conformational ensembles of α-synuclein and tau: combining single-molecule FRET and simulations. Biophys. J. 103:1940–49 [Google Scholar]
  111. Nerenberg PS, Jo B, So C, Tripathy A, Head-Gordon T. 111.  2012. Optimizing solute-water van der Waals interactions to reproduce solvation free energies. J. Phys. Chem. B. 116:4524–34 [Google Scholar]
  112. Nettels D, Gopich IV, Hoffmann A, Schuler B. 112.  2007. Ultrafast dynamics of protein collapse from single-molecule photon statistics. PNAS 104:2655–60 [Google Scholar]
  113. Nettels D, Hoffmann A, Schuler B. 113.  2008. Unfolded protein and peptide dynamics investigated with single-molecule FRET and correlation spectroscopy from picoseconds to seconds. J. Phys. Chem. B 112:6137–46 [Google Scholar]
  114. Nettels D, Müller-Späth S, Küster F, Hofmann H, Haenni D. 114.  et al. 2009. Single molecule spectroscopy of the temperature-induced collapse of unfolded proteins. PNAS 106:20740–45 [Google Scholar]
  115. Neuweiler H, Johnson CM, Fersht AR. 115.  2009. Direct observation of ultrafast folding and denatured state dynamics in single protein molecules. PNAS 106:18569–74 [Google Scholar]
  116. O'Brien EP, Morrison G, Brooks BR, Thirumalai D. 116.  2009. How accurate are polymer models in the analysis of Förster resonance energy transfer experiments on proteins. ? J. Chem. Phys. 130:124903 [Google Scholar]
  117. O'Brien EP, Ziv G, Haran G, Brooks BR, Thirumalai D. 117.  2008. Effects of denaturants and osmolytes on proteins are accurately predicted by the molecular transfer model. PNAS 105:13403–8 [Google Scholar]
  118. Oosawa F.118.  1971. Polyelectrolytes New York: Marcel Dekker
  119. Phillip Y, Kiss V, Schreiber G. 119.  2012. Protein-binding dynamics imaged in a living cell. PNAS 109:1461–66 [Google Scholar]
  120. Piana S, Donchev AG, Robustelli P, Shaw DE. 120.  2015. Water dispersion interactions strongly influence simulated structural properties of disordered protein states. J. Phys. Chem. B. 119:5113–23 [Google Scholar]
  121. Pirchi M, Ziv G, Riven I, Cohen SS, Zohar N. 121.  et al. 2011. Single-molecule fluorescence spectroscopy maps the folding landscape of a large protein. Nat. Commun. 2:493 [Google Scholar]
  122. Portman JJ, Takada S, Wolynes PG. 122.  2001. Microscopic theory of protein folding rates. II. Local reaction coordinates and chain dynamics. J. Chem. Phys. 114:5082–96 [Google Scholar]
  123. Ptitsyn OB.123.  1995. Molten globule and protein folding. Adv. Protein Chem. 47:83–229 [Google Scholar]
  124. Rhoades E, Cohen M, Schuler B, Haran G. 124.  2004. Two-state folding observed in individual protein molecules. J. Am. Chem. Soc. 126:14686–87 [Google Scholar]
  125. Rhoades E, Gussakovsky E, Haran G. 125.  2003. Watching proteins fold one molecule at a time. PNAS 100:3197–202 [Google Scholar]
  126. Ritchie DB, Woodside MT. 126.  2015. Probing the structural dynamics of proteins and nucleic acids with optical tweezers. Curr. Opin. Struct. Biol. 34:43–51 [Google Scholar]
  127. Robinson DR, Jencks WP. 127.  1963. Effect of denaturing agents of the urea-guanidinium class on the solubility of acetyltetraglycine ethyl ester and related compounds. J. Biol. Chem. 238:1558–60 [Google Scholar]
  128. Rouse PE.128.  1953. A theory of the linear viscoelastic properties of dilute solutions of coiling polymers. J. Chem. Phys. 21:1272–80 [Google Scholar]
  129. Sadqi M, Lapidus LJ, Muñoz V. 129.  2003. How fast is protein hydrophobic collapse. ? PNAS 100:12117–22 [Google Scholar]
  130. Sakon JJ, Weninger KR. 130.  2010. Detecting the conformation of individual proteins in live cells. Nat. Methods 7:203–5 [Google Scholar]
  131. Sanchez IC.131.  1979. Phase transition behavior of the isolated polymer chain. Macromolecules 12:980–88 [Google Scholar]
  132. Sawle L, Ghosh K. 132.  2015. A theoretical method to compute sequence dependent configurational properties in charged polymers and proteins. J. Chem. Phys. 143:085101 [Google Scholar]
  133. Schäfer L.133.  1999. Excluded Volume Effects in Polymer Solutions as Explained by the Renormalization Group Berlin: Springer
  134. Schäfer L, Kappeler C. 134.  1993. Interaction effects on the size of a polymer chain in ternary solutions: a renormalization group study. J. Chem. Phys. 99:6135–54 [Google Scholar]
  135. Schröder GF, Alexiev U, Grubmüller H. 135.  2005. Simulation of fluorescence anisotropy experiments: probing protein dynamics. Biophys. J. 89:3757–70 [Google Scholar]
  136. Schuler B.136.  2013. Single-molecule FRET of protein structure and dynamics—a primer. J. Nanobiotechnol. 11:Suppl. 1S2 [Google Scholar]
  137. Schuler B, Hofmann H. 137.  2013. Single-molecule spectroscopy of protein folding dynamics—expanding scope and timescales. Curr. Opin. Struct. Biol. 23:36–47 [Google Scholar]
  138. Schuler B, Lipman EA, Eaton WA. 138.  2002. Probing the free-energy surface for protein folding with single-molecule fluorescence spectroscopy. Nature 419:743–47 [Google Scholar]
  139. Schuler B, Lipman EA, Steinbach PJ, Kumke M, Eaton WA. 139.  2005. Polyproline and the “spectroscopic ruler” revisited with single molecule fluorescence. PNAS 102:2754–59 [Google Scholar]
  140. Schulz JC, Schmidt L, Best RB, Dzubiella J, Netz RR. 140.  2012. Peptide chain dynamics in light and heavy water: zooming in on internal friction. J. Am. Chem. Soc. 134:6273–79 [Google Scholar]
  141. Shakhnovich EI.141.  1997. Theoretical studies of protein-folding thermodynamics and kinetics. Curr. Opin. Struct. Biol. 7:29–40 [Google Scholar]
  142. Sherman E, Haran G. 142.  2006. Coil–globule transition in the denatured state of a small protein. PNAS 103:11539–43 [Google Scholar]
  143. Sherman E, Haran G. 143.  2011. Fluorescence correlation spectroscopy of fast chain dynamics within denatured protein L. ChemPhysChem 12:696–703 [Google Scholar]
  144. Sherman E, Itkin A, Kuttner YY, Rhoades E, Amir D. 144.  et al. 2008. Using fluorescence correlation spectroscopy to study conformational changes in denatured proteins. Biophys. J. 94:4819–27 [Google Scholar]
  145. Sickmeier M, Hamilton JA, LeGall T, Vacic V, Cortese MS. 145.  et al. 2007. DisProt: the database of disordered proteins. Nucleic Acids Res. 35:D786–93 [Google Scholar]
  146. Sisamakis E, Valeri A, Kalinin S, Rothwell PJ, Seidel CAM. 146.  2010. Accurate single-molecule FRET studies using multiparameter fluorescence detection. Methods Enzymol. 475:455–514 [Google Scholar]
  147. Soranno A, Buchli B, Nettels D, Müller-Späth S, Cheng RR. 147.  et al. 2012. Quantifying internal friction in unfolded and intrinsically disordered proteins with single molecule spectroscopy. PNAS 109:17800–6 [Google Scholar]
  148. Soranno A, Koenig I, Borgia MB, Hofmann H, Zosel F. 148.  et al. 2014. Single-molecule spectroscopy reveals polymer effects of disordered proteins in crowded environments. PNAS 111:4874–79 [Google Scholar]
  149. Sun ST, Nishio I, Swislow G, Tanaka T. 149.  1980. The coil–globule transition: radius of gyration of polystyrene in cyclohexane. J. Chem. Phys. 73:5971–75 [Google Scholar]
  150. Szabo A, Schulten K, Schulten Z. 150.  1980. First passage time approach to diffusion controlled reactions. J. Chem. Phys. 72:4350–57 [Google Scholar]
  151. Szasz C, Alexa A, Toth K, Rakacs M, Langowski J, Tompa P. 151.  2011. Protein disorder prevails under crowded conditions. Biochemistry 50:5834–44 [Google Scholar]
  152. Talaga DS, Lau WL, Roder H, Tang J, Jia Y. 152.  et al. 2000. Dynamics and folding of single two-stranded coiled-coil peptides studied by fluorescent energy transfer confocal microscopy. PNAS 97:13021–26 [Google Scholar]
  153. Tanford C.153.  1964. Isothermal unfolding of globular proteins in aqueous urea solutions. J. Am. Chem. Soc. 86:2050–59 [Google Scholar]
  154. Tanford C.154.  1968. Protein denaturation. Adv. Protein Chem. 23:121–282 [Google Scholar]
  155. Tcherkasskaya O, Uversky VN. 155.  2001. Denatured collapsed states in protein folding: example of apomyoglobin. Proteins 44:244–54 [Google Scholar]
  156. Teufel DP, Johnson CM, Lum JK, Neuweiler H. 156.  2011. Backbone-driven collapse in unfolded protein chains. J. Mol. Biol. 409:250–62 [Google Scholar]
  157. Tompa P, Fuxreiter M. 157.  2008. Fuzzy complexes: polymorphism and structural disorder in protein–protein interactions. Trends Biochem. Sci. 33:2–8 [Google Scholar]
  158. Udgaonkar JB.158.  2008. Multiple routes and structural heterogeneity in protein folding. Annu. Rev. Biophys. 37:489–510 [Google Scholar]
  159. Uversky VN.159.  1993. Use of fast protein size-exclusion liquid chromatography to study the unfolding of proteins which denature through the molten globule. Biochemistry 32:13288–98 [Google Scholar]
  160. Uversky VN.160.  2002. Natively unfolded proteins: a point where biology waits for physics. Protein Sci. 11:739–56 [Google Scholar]
  161. Uversky VN, Dunker AK. 161.  2012. Intrinsically Disordered Protein Analysis New York: Springer
  162. Uversky VN, Gillespie JR, Fink AL. 162.  2000. Why are “natively unfolded” proteins unstructured under physiologic conditions?. Proteins 41:415–27 [Google Scholar]
  163. Uzawa T, Kimura T, Ishimori K, Morishima I, Matsui T. 163.  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 [Google Scholar]
  164. van der Lee R, Buljan M, Lang B, Weatheritt RJ, Daughdrill GW. 164.  et al. 2014. Classification of intrinsically disordered regions and proteins. Chem. Rev. 114:6589–631 [Google Scholar]
  165. Vendruscolo M.165.  2007. Determination of conformationally heterogeneous states of proteins. Curr. Opin. Struct. Biol. 17:15–20 [Google Scholar]
  166. Vitalis A, Pappu RV. 166.  2009. ABSINTH: a new continuum solvation model for simulations of polypeptides in aqueous solutions. J. Comput. Chem. 30:673–99 [Google Scholar]
  167. Wang ZS, Makarov DE. 167.  2003. Nanosecond dynamics of single polypeptide molecules revealed by photoemission statistics of fluorescence resonance energy transfer: a theoretical study. J. Phys. Chem. B 107:5617–22 [Google Scholar]
  168. Wilkins DK, Grimshaw SB, Receveur V, Dobson CM, Jones JA, Smith LJ. 168.  1999. Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques. Biochemistry 38:16424–31 [Google Scholar]
  169. Wisniewski JR, Hein MY, Cox J, Mann M. 169.  2014. A “proteomic ruler” for protein copy number and concentration estimation without spike-in standards. Mol. Cell. Proteomics 13:3497–506 [Google Scholar]
  170. Wozniak AK, Schröder GF, Grubmüller H, Seidel CA, Oesterhelt F. 170.  2008. Single-molecule FRET measures bends and kinks in DNA. PNAS 105:18337–42 [Google Scholar]
  171. Wright PE, Dyson HJ. 171.  2009. Linking folding and binding. Curr. Opin. Struct. Biol. 19:31–38 [Google Scholar]
  172. Wuttke R, Hofmann H, Nettels D, Borgia MB, Mittal J. 172.  et al. 2014. Temperature-dependent solvation modulates the dimensions of disordered proteins. PNAS 111:5213–18 [Google Scholar]
  173. Yang WY, Gruebele M. 173.  2003. Folding at the speed limit. Nature 423:193–97 [Google Scholar]
  174. Yasin UM, Sashi P, Bhuyan AK. 174.  2013. Expansion and internal friction in unfolded protein chain. J. Phys. Chem. B 117:12059–64 [Google Scholar]
  175. Yoo TY, Meisburger SP, Hinshaw J, Pollack L, Haran G. 175.  et al. 2012. Small-angle X-ray scattering and single-molecule FRET spectroscopy produce highly divergent views of the low-denaturant unfolded state. J. Mol. Biol. 418:226–36 [Google Scholar]
  176. Zhou HX.176.  2004. Polymer models of protein stability, folding, and interactions. Biochemistry 43:2141–54 [Google Scholar]
  177. Zhou HX, Rivas GN, Minton AP. 177.  2008. Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences. Annu. Rev. Biophys. 37:375–97 [Google Scholar]
  178. Zimm BH.178.  1956. Dynamics of polymer molecules in dilute solution: viscoelasticity, flow birefringence and dielectric loss. J. Chem. Phys. 24:269–78 [Google Scholar]
  179. Zimmerman SB, Trach SO. 179.  1991. Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli. J. Mol. Biol. 222:599–620 [Google Scholar]
  180. Ziv G, Haran G. 180.  2009. Protein folding, protein collapse, and Tanford's transfer model: lessons from single-molecule FRET. J. Am. Chem. Soc. 131:2942–47 [Google Scholar]
  181. Ziv G, Thirumalai D, Haran G. 181.  2009. Collapse transition in proteins. Phys. Chem. Chem. Phys. 11:83–93 [Google Scholar]
  182. Zoldak G, Rief M. 182.  2013. Force as a single molecule probe of multidimensional protein energy landscapes. Curr. Opin. Struct. Biol. 23:48–57 [Google Scholar]
/content/journals/10.1146/annurev-biophys-062215-010915
Loading
/content/journals/10.1146/annurev-biophys-062215-010915
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error