A microscopic view of miniprotein folding: Enhanced folding efficiency through formation of an intermediate

Neuweiler H, Doose S, Sauer M (2005)
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 102(46): 16650-16655.

Download
Es wurde kein Volltext hochgeladen. Nur Publikationsnachweis!
Zeitschriftenaufsatz | Veröffentlicht | Englisch
Autor
; ;
Abstract / Bemerkung
The role of polypeptide collapse and formation of intermediates in protein folding is still under debate. Miniproteins, small globular peptide structures, serve as ideal model systems to study the basic principles that govern folding. Experimental investigations of folding dynamics of such small systems, however, turn out to be challenging, because requirements for high temporal and spatial resolution have to be met simultaneously. Here, we demonstrate how selective quenching of an extrinsic fluorescent label by the amino acid tryptophan (Trp) can be used to probe folding dynamics of Trp-cage (TC), the smallest protein known to date. Using fluorescence correlation spectroscopy, we monitor folding transitions as well as conformational flexibility in the denatured state of the 20-residue protein under thermodynamic equilibrium conditions with nanosecond time resolution. Besides microsecond folding kinetics, we reveal hierarchical folding of TC, hidden to previous experimental studies. We show that specific collapse of the peptide to a molten globule-like intermediate enhances folding efficiency considerably. A single point mutation destabilizes the intermediate, switching the protein to two-state folding behavior and slowing down the folding process. Our results underscore the importance of preformed structure in the denatured state for folding of even the smallest globular structures. A unique method emerges for monitoring conformational dynamics and ultrafast folding events of polypeptides at the nanometer scale.
Erscheinungsjahr
Zeitschriftentitel
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Band
102
Ausgabe
46
Seite(n)
16650-16655
ISSN
eISSN
PUB-ID

Zitieren

Neuweiler H, Doose S, Sauer M. A microscopic view of miniprotein folding: Enhanced folding efficiency through formation of an intermediate. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 2005;102(46):16650-16655.
Neuweiler, H., Doose, S., & Sauer, M. (2005). A microscopic view of miniprotein folding: Enhanced folding efficiency through formation of an intermediate. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 102(46), 16650-16655. doi:10.1073/pnas.0507351102
Neuweiler, H., Doose, S., and Sauer, M. (2005). A microscopic view of miniprotein folding: Enhanced folding efficiency through formation of an intermediate. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 102, 16650-16655.
Neuweiler, H., Doose, S., & Sauer, M., 2005. A microscopic view of miniprotein folding: Enhanced folding efficiency through formation of an intermediate. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 102(46), p 16650-16655.
H. Neuweiler, S. Doose, and M. Sauer, “A microscopic view of miniprotein folding: Enhanced folding efficiency through formation of an intermediate”, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, vol. 102, 2005, pp. 16650-16655.
Neuweiler, H., Doose, S., Sauer, M.: A microscopic view of miniprotein folding: Enhanced folding efficiency through formation of an intermediate. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 102, 16650-16655 (2005).
Neuweiler, H, Doose, S, and Sauer, Markus. “A microscopic view of miniprotein folding: Enhanced folding efficiency through formation of an intermediate”. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 102.46 (2005): 16650-16655.

83 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Mixed Macromolecular Crowding: A Protein and Solvent Perspective.
Biswas S, Kundu J, Mukherjee SK, Chowdhury PK., ACS Omega 3(4), 2018
PMID: 30023892
Evidence for the residual tertiary structure in the urea-unfolded form of bacteriophage T5 endolysin.
Kutyshenko VP, Prokhorov DA, Mikoulinskaia GV, Molochkov NV, Paskevich SI, Uversky VN., J Biomol Struct Dyn 35(6), 2017
PMID: 27109308
An adaptive bias - hybrid MD/kMC algorithm for protein folding and aggregation.
Peter EK, Shea JE., Phys Chem Chem Phys 19(26), 2017
PMID: 28650060
A hydrodynamic view of the first-passage folding of Trp-cage miniprotein.
Andryushchenko VA, Chekmarev SF., Eur Biophys J 45(3), 2016
PMID: 26559408
Itinerary profiling to analyze a large number of protein-folding trajectories.
Ota M, Ikeguchi M, Kidera A., Biophys Physicobiol 13(), 2016
PMID: 28409081
Comparison of hydration behavior and conformational preferences of the Trp-cage mini-protein in different rigid-body water models.
Gupta M, Nayar D, Chakravarty C, Bandyopadhyay S., Phys Chem Chem Phys 18(48), 2016
PMID: 27878168
Systematic characterization of protein folding pathways using diffusion maps: application to Trp-cage miniprotein.
Kim SB, Dsilva CJ, Kevrekidis IG, Debenedetti PG., J Chem Phys 142(8), 2015
PMID: 25725756
Folding and unfolding thermodynamics of the TC10b Trp-cage miniprotein.
English CA, García AE., Phys Chem Chem Phys 16(7), 2014
PMID: 24448113
Photophysical processes in single molecule organic fluorescent probes.
Stennett EM, Ciuba MA, Levitus M., Chem Soc Rev 43(4), 2014
PMID: 24141280
A hybrid MD-kMC algorithm for folding proteins in explicit solvent.
Peter EK, Shea JE., Phys Chem Chem Phys 16(14), 2014
PMID: 24499973
Sampling the equilibrium kinetic network of Trp-cage in explicit solvent.
Du W, Bolhuis PG., J Chem Phys 140(19), 2014
PMID: 24852564
Folding dynamics and pathways of the trp-cage miniproteins.
Byrne A, Williams DV, Barua B, Hagen SJ, Kier BL, Andersen NH., Biochemistry 53(38), 2014
PMID: 25184759
Cosolvent effects on protein stability.
Canchi DR, García AE., Annu Rev Phys Chem 64(), 2013
PMID: 23298246
Structural insights into the Trp-cage folding intermediate formation.
Rovó P, Stráner P, Láng A, Bartha I, Huszár K, Nyitray L, Perczel A., Chemistry 19(8), 2013
PMID: 23319425
Dynamic folding pathway models of the Trp-cage protein.
Lee IH, Kim SY., Biomed Res Int 2013(), 2013
PMID: 23865078
Using D-Amino Acids to Delineate the Mechanism of Protein Folding: Application to Trp-cage.
Culik RM, Annavarapu S, Nanda V, Gai F., Chem Phys 422(), 2013
PMID: 24307748
Effect of an ionic liquid on the unfolding of human serum albumin: a fluorescence correlation spectroscopy study.
Das DK, Kumar Das A, Kumar Mandal A, Mondal T, Bhattacharyya K., Chemphyschem 13(7), 2012
PMID: 21922626
Spectroscopic studies of protein folding: linear and nonlinear methods.
Serrano AL, Waegele MM, Gai F., Protein Sci 21(2), 2012
PMID: 22109973
Panorama of DNA hairpin folding observed via diffusion-decelerated fluorescence correlation spectroscopy.
Yin Y, Wang P, Yang XX, Li X, He C, Zhao XS., Chem Commun (Camb) 48(59), 2012
PMID: 22715462
Crystal and NMR structures of a Trp-cage mini-protein benchmark for computational fold prediction.
Scian M, Lin JC, Le Trong I, Makhatadze GI, Stenkamp RE, Andersen NH., Proc Natl Acad Sci U S A 109(31), 2012
PMID: 22802678
Atomic-level structure characterization of an ultrafast folding mini-protein denatured state.
Rogne P, Ozdowy P, Richter C, Saxena K, Schwalbe H, Kuhn LT., PLoS One 7(7), 2012
PMID: 22848459
Backbone-driven collapse in unfolded protein chains.
Teufel DP, Johnson CM, Lum JK, Neuweiler H., J Mol Biol 409(2), 2011
PMID: 21497607
Markov models of molecular kinetics: generation and validation.
Prinz JH, Wu H, Sarich M, Keller B, Senne M, Held M, Chodera JD, Schütte C, Noé F., J Chem Phys 134(17), 2011
PMID: 21548671
Optimal use of data in parallel tempering simulations for the construction of discrete-state Markov models of biomolecular dynamics.
Prinz JH, Chodera JD, Pande VS, Swope WC, Smith JC, Noé F., J Chem Phys 134(24), 2011
PMID: 21721613
Binding of organic dyes with human serum albumin: a single-molecule study.
Das DK, Mondal T, Mandal AK, Bhattacharyya K., Chem Asian J 6(11), 2011
PMID: 21751404
Protonation/deprotonation effects on the stability of the Trp-cage miniprotein.
Jimenez-Cruz CA, Makhatadze GI, Garcia AE., Phys Chem Chem Phys 13(38), 2011
PMID: 21773639
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
Intrinsic property of flavin mononucleotide controls its optical spectra in three redox states.
Ai YJ, Tian G, Liao RZ, Liao RZ, Zhang Q, Fang WH, Luo Y., Chemphyschem 12(16), 2011
PMID: 21954157
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
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
Super-resolution imaging with small organic fluorophores.
Heilemann M, van de Linde S, Mukherjee A, Sauer M., Angew Chem Int Ed Engl 48(37), 2009
PMID: 19670280
Multicolor photoswitching microscopy for subdiffraction-resolution fluorescence imaging.
van de Linde S, Endesfelder U, Mukherjee A, Schüttpelz M, Wiebusch G, Wolter S, Heilemann M, Sauer M., Photochem Photobiol Sci 8(4), 2009
PMID: 19337659
Observing proteins as single molecules encapsulated in surface-tethered polymeric nanocontainers.
Rosenkranz T, Katranidis A, Atta D, Gregor I, Enderlein J, Grzelakowski M, Rigler P, Meier W, Fitter J., Chembiochem 10(4), 2009
PMID: 19191249
Analysis of the free-energy surface of proteins from reversible folding simulations.
Allen LR, Krivov SV, Paci E., PLoS Comput Biol 5(7), 2009
PMID: 19593364
A kinetic model of trp-cage folding from multiple biased molecular dynamics simulations.
Marinelli F, Pietrucci F, Laio A, Piana S., PLoS Comput Biol 5(8), 2009
PMID: 19662155
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
Folding versus aggregation: polypeptide conformations on competing pathways.
Jahn TR, Radford SE., Arch Biochem Biophys 469(1), 2008
PMID: 17588526
Single-molecule studies of protein folding.
Borgia A, Williams PM, Clarke J., Annu Rev Biochem 77(), 2008
PMID: 18412537
The Trp-cage: optimizing the stability of a globular miniprotein.
Barua B, Lin JC, Williams VD, Kummler P, Neidigh JW, Andersen NH., Protein Eng Des Sel 21(3), 2008
PMID: 18203802
Design of an optical switch for studying conformational dynamics in individual molecules of GroEL.
Frank GA, Kipnis Y, Smolensky E, Daube SS, Horovitz A, Haran G., Bioconjug Chem 19(7), 2008
PMID: 18572960
Rate constant and reaction coordinate of Trp-cage folding in explicit water.
Juraszek J, Bolhuis PG., Biophys J 95(9), 2008
PMID: 18676648
The structure of a folding intermediate provides insight into differences in immunoglobulin amyloidogenicity.
Feige MJ, Groscurth S, Marcinowski M, Yew ZT, Truffault V, Paci E, Kessler H, Buchner J., Proc Natl Acad Sci U S A 105(36), 2008
PMID: 18768806
Computing the stability diagram of the Trp-cage miniprotein.
Paschek D, Hempel S, García AE., Proc Natl Acad Sci U S A 105(46), 2008
PMID: 19004791
VCD spectroscopic and molecular dynamics analysis of the Trp-cage miniprotein TC5b.
Copps J, Murphy RF, Lovas S., Biopolymers 88(3), 2007
PMID: 17326200
Ultrafast and downhill protein folding.
Dyer RB., Curr Opin Struct Biol 17(1), 2007
PMID: 17223539
Intermediates: ubiquitous species on folding energy landscapes?
Brockwell DJ, Radford SE., Curr Opin Struct Biol 17(1), 2007
PMID: 17239580
A natively unfolded yeast prion monomer adopts an ensemble of collapsed and rapidly fluctuating structures.
Mukhopadhyay S, Krishnan R, Lemke EA, Lindquist S, Deniz AA., Proc Natl Acad Sci U S A 104(8), 2007
PMID: 17299036
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
A pre-existing hydrophobic collapse in the unfolded state of an ultrafast folding protein.
Mok KH, Kuhn LT, Goez M, Day IJ, Lin JC, Andersen NH, Hore PJ., Nature 447(7140), 2007
PMID: 17429353
Calculation of the free energy and cooperativity of protein folding.
Kentsis A, Gindin T, Mezei M, Osman R., PLoS One 2(5), 2007
PMID: 17505540
Dynamics of equilibrium structural fluctuations of apomyoglobin measured by fluorescence correlation spectroscopy.
Chen H, Rhoades E, Butler JS, Loh SN, Webb WW., Proc Natl Acad Sci U S A 104(25), 2007
PMID: 17556539
The initial step of DNA hairpin folding: a kinetic analysis using fluorescence correlation spectroscopy.
Kim J, Doose S, Neuweiler H, Sauer M., Nucleic Acids Res 34(9), 2006
PMID: 16687657
Molecular fluorescence, phosphorescence, and chemiluminescence spectrometry.
Fletcher KA, Fakayode SO, Lowry M, Tucker SA, Neal SL, Kimaru IW, McCarroll ME, Patonay G, Oldham PB, Rusin O, Strongin RM, Warner IM., Anal Chem 78(12), 2006
PMID: 16771540
Sampling the multiple folding mechanisms of Trp-cage in explicit solvent.
Juraszek J, Bolhuis PG., Proc Natl Acad Sci U S A 103(43), 2006
PMID: 17035504
Shot-noise limited single-molecule FRET histograms: comparison between theory and experiments.
Nir E, Michalet X, Hamadani KM, Laurence TA, Neuhauser D, Kovchegov Y, Weiss S., J Phys Chem B 110(44), 2006
PMID: 17078646

39 References

Daten bereitgestellt von Europe PubMed Central.

Protein folding and misfolding.
Dobson CM., Nature 426(6968), 2003
PMID: 14685248
Early events in protein folding.
Ferguson N, Fersht AR., Curr. Opin. Struct. Biol. 13(1), 2003
PMID: 12581663
Kinetic role of early intermediates in protein folding.
Roder H, Colon W., Curr. Opin. Struct. Biol. 7(1), 1997
PMID: 9032062

AUTHOR UNKNOWN, 1998
The protein folding 'speed limit'.
Kubelka J, Hofrichter J, Eaton WA., Curr. Opin. Struct. Biol. 14(1), 2004
PMID: 15102453
The complete folding pathway of a protein from nanoseconds to microseconds.
Mayor U, Guydosh NR, Johnson CM, Grossmann JG, Sato S, Jas GS, Freund SM, Alonso DO, Daggett V, Fersht AR., Nature 421(6925), 2003
PMID: 12594518
The present view of the mechanism of protein folding.
Daggett V, Fersht A., Nat. Rev. Mol. Cell Biol. 4(6), 2003
PMID: 12778129
Absolute comparison of simulated and experimental protein-folding dynamics.
Snow CD, Nguyen H, Pande VS, Gruebele M., Nature 420(6911), 2002
PMID: 12422224
Designing a 20-residue protein.
Neidigh JW, Fesinmeyer RM, Andersen NH., Nat. Struct. Biol. 9(6), 2002
PMID: 11979279
Smaller and faster: the 20-residue Trp-cage protein folds in 4 micros.
Qiu L, Pabit SA, Roitberg AE, Hagen SJ., J. Am. Chem. Soc. 124(44), 2002
PMID: 12405814
Determination of ultrafast protein folding rates from loop formation dynamics.
Buscaglia M, Kubelka J, Eaton WA, Hofrichter J., J. Mol. Biol. 347(3), 2005
PMID: 15755457
A close look at fluorescence quenching of organic dyes by tryptophan.
Doose S, Neuweiler H, Sauer M., Chemphyschem 6(11), 2005
PMID: 16224752
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

AUTHOR UNKNOWN, 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

AUTHOR UNKNOWN, 2001
Measurement of microsecond dynamic motion in the intestinal fatty acid binding protein by using fluorescence correlation spectroscopy.
Chattopadhyay K, Saffarian S, Elson EL, Frieden C., Proc. Natl. Acad. Sci. U.S.A. 99(22), 2002
PMID: 12381795
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
Protein conformational dynamics probed by single-molecule electron transfer.
Yang H, Luo G, Karnchanaphanurach P, Louie TM, Rech I, Cova S, Xun L, Xie XS., Science 302(5643), 2003
PMID: 14551431
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
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
The Trp cage: folding kinetics and unfolded state topology via molecular dynamics simulations.
Snow CD, Zagrovic B, Pande VS., J. Am. Chem. Soc. 124(49), 2002
PMID: 12465960
Ab initio folding simulation of the Trp-cage mini-protein approaches NMR resolution.
Chowdhury S, Lee MC, Xiong G, Duan Y., J. Mol. Biol. 327(3), 2003
PMID: 12634063
Trp-cage: folding free energy landscape in explicit water.
Zhou R., Proc. Natl. Acad. Sci. U.S.A. 100(23), 2003
PMID: 14581616

AUTHOR UNKNOWN, 2004
UV-resonance raman thermal unfolding study of Trp-cage shows that it is not a simple two-state miniprotein.
Ahmed Z, Beta IA, Mikhonin AV, Asher SA., J. Am. Chem. Soc. 127(31), 2005
PMID: 16076200
Molten globule and protein folding.
Ptitsyn OB., Adv. Protein Chem. 47(), 1995
PMID: 8561052

AUTHOR UNKNOWN, 2000
Fast events in protein folding initiated by nanosecond laser photolysis.
Jones CM, Henry ER, Hu Y, Chan CK, Luck SD, Bhuyan A, Roder H, Hofrichter J, Eaton WA., Proc. Natl. Acad. Sci. U.S.A. 90(24), 1993
PMID: 8265638
Fast events in protein folding: the time evolution of primary processes.
Callender RH, Dyer RB, Gilmanshin R, Woodruff WH., Annu Rev Phys Chem 49(), 1998
PMID: 9933907
The fast protein folding problem.
Gruebele M., Annu Rev Phys Chem 50(), 1999
PMID: 15012420
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
The renaissance of fluorescence resonance energy transfer.
Selvin PR., Nat. Struct. Biol. 7(9), 2000
PMID: 10966639

Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

Quellen

PMID: 16269542
PubMed | Europe PMC

Suchen in

Google Scholar