Dynamics of unfolded polypeptide chains in crowded environment studied by fluorescence correlation spectroscopy

Neuweiler H, Löllmann M, Doose S, Sauer M (2007)
JOURNAL OF MOLECULAR BIOLOGY 365(3): 856-869.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
Download
Es wurden keine Dateien hochgeladen. Nur Publikationsnachweis!
Autor*in
Neuweiler, Hannes; Löllmann, MarcUniBi; Doose, Sören; Sauer, MarkusUniBi
Abstract / Bemerkung
Proteins have evolved to fold and function within a cellular environment that is characterized by high macromolecular content. The earliest step of protein folding represents intrachain contact formation of amino acid residues within an unfolded polypeptide chain. It has been proposed that macromolecular crowding can have significant effects on rates and equilibria of biomolecular processes. However, the kinetic consequences on intrachain diffusion of polypeptides, have not been tested experimentally, yet. Here, we demonstrate that selective fluorescence quenching of the oxazine fluorophore MR121 by the amino acid tryptophan (Trp) in combination with fast fluorescence correlation spectroscopy (FCS) can be used to monitor end-to-end contact formation rates of unfolded polypeptide chains. MR121 and Trp were incorporated at the terminal ends of polypeptides. consisting of repetitive units of glycine (G) and serine (S) residues. End-to-end contact formation and dissociation result in "off" and "on" switching of MR121 fluorescence and underlying kinetics can be revealed in FCS experiments with nanosecond time resolution. We revisit previous experimental studies concerning the dependence of end-to-end contact formation rates on polypeptide chain length, showing that kinetics can be described by Gaussian chain theory. We further investigate effects of solvent viscosity and temperature on contact formation rates demonstrating that intrachain diffusion represents a purely diffusive, entropy-controlled process. Finally, we study the influence of macromolecular crowding on polypepticle chain dynamics. The data presented demonstrate that intrachain diffusion is fast in spite of hindered diffusion caused by repulsive interactions with macromolecules. Findings can be explained by effects of excluded volume reducing chain entropy and therefore accelerating the loop search process. Our results suggest that within a cellular environment the early formation of structural elements in k unfolded proteins can still proceed quite efficiently in spite of hindered L diffusion caused by high macromolecular content. (c) 2006 Elsevier Ltd. All rights reserved.
Stichworte
unfolded polypeptides; molecular crowding; fluorescence quenching; fluorescence correlation spectroscopy; intrachain diffusion
Erscheinungsjahr
2007
Zeitschriftentitel
JOURNAL OF MOLECULAR BIOLOGY
Band
365
Ausgabe
3
Seite(n)
856-869
ISSN
0022-2836
Page URI
https://pub.uni-bielefeld.de/record/1596078

Zitieren

Neuweiler H, Löllmann M, Doose S, Sauer M. Dynamics of unfolded polypeptide chains in crowded environment studied by fluorescence correlation spectroscopy. JOURNAL OF MOLECULAR BIOLOGY. 2007;365(3):856-869.
Neuweiler, H., Löllmann, M., Doose, S., & Sauer, M. (2007). Dynamics of unfolded polypeptide chains in crowded environment studied by fluorescence correlation spectroscopy. JOURNAL OF MOLECULAR BIOLOGY, 365(3), 856-869. https://doi.org/10.1016/j.jmb.2006.10.021
Neuweiler, Hannes, Löllmann, Marc, Doose, Sören, and Sauer, Markus. 2007. “Dynamics of unfolded polypeptide chains in crowded environment studied by fluorescence correlation spectroscopy”. JOURNAL OF MOLECULAR BIOLOGY 365 (3): 856-869.
Neuweiler, H., Löllmann, M., Doose, S., and Sauer, M. (2007). Dynamics of unfolded polypeptide chains in crowded environment studied by fluorescence correlation spectroscopy. JOURNAL OF MOLECULAR BIOLOGY 365, 856-869.
Neuweiler, H., et al., 2007. Dynamics of unfolded polypeptide chains in crowded environment studied by fluorescence correlation spectroscopy. JOURNAL OF MOLECULAR BIOLOGY, 365(3), p 856-869.
H. Neuweiler, et al., “Dynamics of unfolded polypeptide chains in crowded environment studied by fluorescence correlation spectroscopy”, JOURNAL OF MOLECULAR BIOLOGY, vol. 365, 2007, pp. 856-869.
Neuweiler, H., Löllmann, M., Doose, S., Sauer, M.: Dynamics of unfolded polypeptide chains in crowded environment studied by fluorescence correlation spectroscopy. JOURNAL OF MOLECULAR BIOLOGY. 365, 856-869 (2007).
Neuweiler, Hannes, Löllmann, Marc, Doose, Sören, and Sauer, Markus. “Dynamics of unfolded polypeptide chains in crowded environment studied by fluorescence correlation spectroscopy”. JOURNAL OF MOLECULAR BIOLOGY 365.3 (2007): 856-869.

50 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Enzyme leaps fuel antichemotaxis.
Jee AY, Dutta S, Cho YK, Tlusty T, Granick S., Proc Natl Acad Sci U S A 115(1), 2018
PMID: 29255047
Dynamic Optical Contrast Imaging.
Kim IA, Taylor ZD, Cheng H, Sebastian C, Maccabi A, Garritano J, Tajudeen B, Razfar A, Palma Diaz F, Yeh M, Stafsudd O, Grundfest W, St John M., Otolaryngol Head Neck Surg 156(3), 2017
PMID: 28116982
Integrated view of internal friction in unfolded proteins from single-molecule FRET, contact quenching, theory, and simulations.
Soranno A, Holla A, Dingfelder F, Nettels D, Makarov DE, Schuler B., Proc Natl Acad Sci U S A 114(10), 2017
PMID: 28223518
The roughness of the protein energy landscape results in anomalous diffusion of the polypeptide backbone.
Volk M, Milanesi L, Waltho JP, Hunter CA, Beddard GS., Phys Chem Chem Phys 17(2), 2015
PMID: 25412176
Microsecond protein dynamics observed at the single-molecule level.
Otosu T, Ishii K, Tahara T., Nat Commun 6(), 2015
PMID: 26151767
β-Structure within the Denatured State of the Helical Protein Domain BBL.
Thukral L, Schwarze S, Daidone I, Neuweiler H., J Mol Biol 427(19), 2015
PMID: 26281710
Effects of Mutations on the Reconfiguration Rate of α-Synuclein.
Acharya S, Saha S, Ahmad B, Lapidus LJ., J Phys Chem B 119(50), 2015
PMID: 26572968
On the cellular uptake and membrane effect of the multifunctional peptide, TatLK15.
Alkotaji M, Pluen A, Zindy E, Hamrang Z, Aojula H., J Pharm Sci 103(1), 2014
PMID: 24218116
The crowd you're in with: effects of different types of crowding agents on protein aggregation.
Breydo L, Reddy KD, Piai A, Felli IC, Pierattelli R, Uversky VN., Biochim Biophys Acta 1844(2), 2014
PMID: 24252314
Photophysical processes in single molecule organic fluorescent probes.
Stennett EM, Ciuba MA, Levitus M., Chem Soc Rev 43(4), 2014
PMID: 24141280
Physicochemical properties of cells and their effects on intrinsically disordered proteins (IDPs).
Theillet FX, Binolfi A, Frembgen-Kesner T, Hingorani K, Sarkar M, Kyne C, Li C, Crowley PB, Gierasch L, Pielak GJ, Elcock AH, Gershenson A, Selenko P., Chem Rev 114(13), 2014
PMID: 24901537
Mutational definition of binding requirements of an hnRNP-like protein in Arabidopsis using fluorescence correlation spectroscopy.
Leder V, Lummer M, Tegeler K, Humpert F, Lewinski M, Schüttpelz M, Staiger D., Biochem Biophys Res Commun 453(1), 2014
PMID: 25251471
Single-molecule spectroscopy of protein folding dynamics--expanding scope and timescales.
Schuler B, Hofmann H., Curr Opin Struct Biol 23(1), 2013
PMID: 23312353
Direct observation of protein unfolded state compaction in the presence of macromolecular crowding.
Mikaelsson T, Adén J, Johansson LB, Wittung-Stafshede P., Biophys J 104(3), 2013
PMID: 23442920
Effects of macromolecular crowding agents on protein folding in vitro and in silico.
Christiansen A, Wang Q, Cheung MS, Wittung-Stafshede P., Biophys Rev 5(2), 2013
PMID: 28510156
Systematic evaluation of fluorescence correlation spectroscopy data analysis on the nanosecond time scale.
Steger K, Bollmann S, Noé F, Doose S., Phys Chem Chem Phys 15(25), 2013
PMID: 23685745
Sequence and temperature dependence of the end-to-end collision dynamics of single-stranded DNA.
Uzawa T, Isoshima T, Ito Y, Ishimori K, Makarov DE, Plaxco KW., Biophys J 104(11), 2013
PMID: 23746521
Identification of slow molecular order parameters for Markov model construction.
Pérez-Hernández G, Paul F, Giorgino T, De Fabritiis G, Noé F., J Chem Phys 139(1), 2013
PMID: 23822324
Determining serpin conformational distributions with single molecule fluorescence.
Mushero N, Gershenson A., Methods Enzymol 501(), 2011
PMID: 22078542
Unfolding dynamics of cytochrome c revealed by single-molecule and ensemble-averaged spectroscopy.
Choi J, Kim S, Tachikawa T, Fujitsuka M, Majima T., Phys Chem Chem Phys 13(13), 2011
PMID: 21305089
Dynamical fingerprints for probing individual relaxation processes in biomolecular dynamics with simulations and kinetic experiments.
Noé F, Doose S, Daidone I, Löllmann M, Sauer M, Chodera JD, Smith JC., Proc Natl Acad Sci U S A 108(12), 2011
PMID: 21368203
Backbone-driven collapse in unfolded protein chains.
Teufel DP, Johnson CM, Lum JK, Neuweiler H., J Mol Biol 409(2), 2011
PMID: 21497607
Dimer formation of organic fluorophores reports on biomolecular dynamics under denaturing conditions.
Bollmann S, Löllmann M, Sauer M, Doose S., Phys Chem Chem Phys 13(28), 2011
PMID: 21687885
Conformational flexibility of glycosylated peptides.
Bollmann S, Burgert A, Plattner C, Nagel L, Sewald N, Löllmann M, Sauer M, Doose S., Chemphyschem 12(16), 2011
PMID: 21922630
Hydrogen-bond driven loop-closure kinetics in unfolded polypeptide chains.
Daidone I, Neuweiler H, Doose S, Sauer M, Smith JC., PLoS Comput Biol 6(1), 2010
PMID: 20098498
Building blocks for protein interaction devices.
Grünberg R, Ferrar TS, van der Sloot AM, Constante M, Serrano L., Nucleic Acids Res 38(8), 2010
PMID: 20215443
Kinetics of chain motions within a protein-folding intermediate.
Neuweiler H, Banachewicz W, Fersht AR., Proc Natl Acad Sci U S A 107(51), 2010
PMID: 21135210
Polymers and single molecule fluorescence spectroscopy, what can we learn?
Wöll D, Braeken E, Deres A, De Schryver FC, Uji-i H, Hofkens J., Chem Soc Rev 38(2), 2009
PMID: 19169450
The length and viscosity dependence of end-to-end collision rates in single-stranded DNA.
Uzawa T, Cheng RR, Cash KJ, Makarov DE, Plaxco KW., Biophys J 97(1), 2009
PMID: 19580758
Effect of macromolecular crowding on protein folding dynamics at the secondary structure level.
Mukherjee S, Waegele MM, Chowdhury P, Guo L, Gai F., J Mol Biol 393(1), 2009
PMID: 19682997
Estimating the sampling error: distribution of transition matrices and functions of transition matrices for given trajectory data.
Metzner P, Noé F, Schütte C., Phys Rev E Stat Nonlin Soft Matter Phys 80(2 pt 1), 2009
PMID: 19792076
Direct observation of ultrafast folding and denatured state dynamics in single protein molecules.
Neuweiler H, Johnson CM, Fersht AR., Proc Natl Acad Sci U S A 106(44), 2009
PMID: 19841261
Protein folding in confined and crowded environments.
Zhou HX., Arch Biochem Biophys 469(1), 2008
PMID: 17719556
Nonequilibrium single molecule protein folding in a coaxial mixer.
Hamadani KM, Weiss S., Biophys J 95(1), 2008
PMID: 18339751
Fluorescence characterization of denatured proteins.
Chen H, Rhoades E., Curr Opin Struct Biol 18(4), 2008
PMID: 18675353
Thermodynamics and kinetics of protein folding under confinement.
Mittal J, Best RB., Proc Natl Acad Sci U S A 105(51), 2008
PMID: 19073911
Ultrafast dynamics of protein collapse from single-molecule photon statistics.
Nettels D, Gopich IV, Hoffmann A, Schuler B., Proc Natl Acad Sci U S A 104(8), 2007
PMID: 17301233
Polymer properties of polythymine as revealed by translational diffusion.
Doose S, Barsch H, Sauer M., Biophys J 93(4), 2007
PMID: 17513377

59 References

Daten bereitgestellt von Europe PubMed Central.

The present view of the mechanism of protein folding.
Daggett V, Fersht A., Nat. Rev. Mol. Cell Biol. 4(6), 2003
PMID: 12778129
Early events in protein folding.
Ferguson N, Fersht AR., Curr. Opin. Struct. Biol. 13(1), 2003
PMID: 12581663
Fast kinetics and mechanisms in protein folding.
Eaton WA, Munoz V, Hagen SJ, Jas GS, Lapidus LJ, Henry ER, Hofrichter J., Annu Rev Biophys Biomol Struct 29(), 2000
PMID: 10940252
Kinetic role of early intermediates in protein folding.
Roder H, Colon W., Curr. Opin. Struct. Biol. 7(1), 1997
PMID: 9032062
The speed limit for protein folding measured by triplet-triplet energy transfer.
Bieri O, Wirz J, Hellrung B, Schutkowski M, Drewello M, Kiefhaber T., Proc. Natl. Acad. Sci. U.S.A. 96(17), 1999
PMID: 10449738
Dynamics of unfolded polypeptide chains as model for the earliest steps in protein folding.
Krieger F, Fierz B, Bieri O, Drewello M, Kiefhaber T., J. Mol. Biol. 332(1), 2003
PMID: 12946363
Brownian-motion of ends of oligopeptide chains in solution as estimated by energy-transfer between chain ends
Haas, Biopolymers 17(), 1978
Diffusion-limited contact formation in unfolded cytochrome c: estimating the maximum rate of protein folding.
Hagen SJ, Hofrichter J, Szabo A, Eaton WA., Proc. Natl. Acad. Sci. U.S.A. 93(21), 1996
PMID: 8876184
Effects of chain stiffness on the dynamics of loop formation in polypeptides. Appendix: testing a 1-dimensional diffusion model for peptide dynamics
Lapidus, J. Phys. Chem. B 106(), 2002
Measuring the rate of intramolecular contact formation in polypeptides.
Lapidus LJ, Eaton WA, Hofrichter J., Proc. Natl. Acad. Sci. U.S.A. 97(13), 2000
PMID: 10860987
A conformational flexibility scale for amino acids in peptides.
Huang F, Nau WM., Angew. Chem. Int. Ed. Engl. 42(20), 2003
PMID: 12772159
Measurement of submicrosecond intramolecular contact formation in peptides at the single-molecule level.
Neuweiler H, Schulz A, Bohmer M, Enderlein J, Sauer M., J. Am. Chem. Soc. 125(18), 2003
PMID: 12720444
How crowded is the cytoplasm?
Fulton AB., Cell 30(2), 1982
PMID: 6754085
Implications of macromolecular crowding for protein assembly.
Minton AP., Curr. Opin. Struct. Biol. 10(1), 2000
PMID: 10679465
Macromolecular crowding: obvious but underappreciated.
Ellis RJ., Trends Biochem. Sci. 26(10), 2001
PMID: 11590012
Molecular crowding enhances native state stability and refolding rates of globular proteins.
Cheung MS, Klimov D, Thirumalai D., Proc. Natl. Acad. Sci. U.S.A. 102(13), 2005
PMID: 15781864
Macromolecular crowding: biochemical, biophysical, and physiological consequences.
Zimmerman SB, Minton AP., Annu Rev Biophys Biomol Struct 22(), 1993
PMID: 7688609
Detection of individual p53-autoantibodies by using quenched peptide-based molecular probes.
Neuweiler H, Schulz A, Vaiana AC, Smith JC, Kaul S, Wolfrum J, Sauer M., Angew. Chem. Int. Ed. Engl. 41(24), 2002
PMID: 12481354
Fluorescence quenching of dyes by tryptophan: interactions at atomic detail from combination of experiment and computer simulation.
Vaiana AC, Neuweiler H, Schulz A, Wolfrum J, Sauer M, Smith JC., J. Am. Chem. Soc. 125(47), 2003
PMID: 14624606
A close look at fluorescence quenching of organic dyes by tryptophan
Doose, Chem. Phys. Chem. 6(), 2005

Lakowicz, 1983
Fluorescence correlation spectroscopy with high count rate and low background: analysis of translational diffusion
Rigler, Eur. Biophys. J. 22(), 1993
Fluorescence correlation spectroscopy. II. An experimental realization.
Magde D, Elson EL, Webb WW., Biopolymers 13(1), 1974
PMID: 4818131
Biological and chemical applications of fluorescence correlation spectroscopy: a review.
Hess ST, Huang S, Heikal AA, Webb WW., Biochemistry 41(3), 2002
PMID: 11790090
The kinetics of conformational fluctuations in an unfolded protein measured by fluorescence methods.
Chattopadhyay K, Elson EL, Frieden C., Proc. Natl. Acad. Sci. U.S.A. 102(7), 2005
PMID: 15701687
A microscopic view of miniprotein folding: enhanced folding efficiency through formation of an intermediate.
Neuweiler H, Doose S, Sauer M., Proc. Natl. Acad. Sci. U.S.A. 102(46), 2005
PMID: 16269542
Two-state models of protein folding kinetics.
Zwanzig R., Proc. Natl. Acad. Sci. U.S.A. 94(1), 1997
PMID: 8990176
Intramolecular reaction in polycondensation. I. The theory of linear systems
Jacobsen, J. Phys. Chem. 18(), 1950
First passage time approach to diffusion controlled reactions
Szabo, J. Chem. Phys. 72(), 1980
Diffusion-controlled intrachain reactions of polymers. II Results for a pair of terminal reactive groups
Wilemski, J. Chem. Phys. 60(), 1973
Non-Gaussian dynamics from a simulation of a short peptide: loop closure rates and effective diffusion coefficients
Portman, J. Chem. Phys. 118(), 2003
Diffusion limited first contact of the ends of a polymer: comparison of theory with simulation
Pastor, J. Chem. Phys. 105(), 1996

Flory, 1969
Random coil configurations of polypeptide chains
Miller, J. Mol. Biol. 23(), 1967
Brownian motion in a field of force and the diffusion model of chemical reactions
Kramers, Physica (The Hague) 7(), 1940
Reaction-rate theory: fifty years after Kramers
Hänggi, Rev. Mod. Phys. 62(), 1990
Viscosity dependence of the folding rates of proteins
Klimov, Phys. Rev. Letters 79(), 1997
The role of solvent viscosity in the dynamics of protein conformational changes.
Ansari A, Jones CM, Henry ER, Hofrichter J, Eaton WA., Science 256(5065), 1992
PMID: 1615323
Diffusional limits to the speed of protein folding: fact or friction?
Hagen, J. Phys.: Condens. Matter 18(), 2005
A limiting speed for protein folding at low solvent viscosity.
Qiu L, Hagen SJ., J. Am. Chem. Soc. 126(11), 2004
PMID: 15025447
Effects of denaturants on the dynamics of loop formation in polypeptides.
Buscaglia M, Lapidus LJ, Eaton WA, Hofrichter J., Biophys. J. 91(1), 2006
PMID: 16617069

Lide, 1994
Crowding effects on EcoRV kinetics and binding.
Wenner JR, Bloomfield VA., Biophys. J. 77(6), 1999
PMID: 10585945
Effects of macromolecular crowding on protein folding and aggregation.
van den Berg B, Ellis RJ, Dobson CM., EMBO J. 18(24), 1999
PMID: 10601015
Microscopic viscosity and rotational diffusion of proteins in a macromolecular environment.
Lavalette D, Tetreau C, Tourbez M, Blouquit Y., Biophys. J. 76(5), 1999
PMID: 10233089
Anomalous diffusion of proteins due to molecular crowding.
Banks DS, Fradin C., Biophys. J. 89(5), 2005
PMID: 16113107
Separating the contribution of translational and rotational diffusion to protein association.
Kuttner YY, Kozer N, Segal E, Schreiber G, Haran G., J. Am. Chem. Soc. 127(43), 2005
PMID: 16248654
The hydrodynamic radii of macromolecules and their effect on red blood cell aggregation.
Armstrong JK, Wenby RB, Meiselman HJ, Fisher TC., Biophys. J. 87(6), 2004
PMID: 15361408
Sub-microsecond protein folding.
Kubelka J, Chiu TK, Davies DR, Eaton WA, Hofrichter J., J. Mol. Biol. 359(3), 2006
PMID: 16643946
Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®
Quellen

PMID: 17084857
PubMed | Europe PMC

Suchen in

Google Scholar