Time-resolved multirotational dynamics of single solution-phase tau proteins reveals details of conformational variation

Foote, Alexander K.; Manger, Lydia H.; Holden, Michael R.; Margittai, Martin; Goldsmith, Randall H.

doi:10.1039/C8CP06971A

Title: Time-resolved multirotational dynamics of single solution-phase tau proteins reveals details of conformational variation

Journal Article · 22 January 2019 · Physical Chemistry Chemical Physics. PCCP

DOI: https://doi.org/10.1039/C8CP06971A · OSTI ID:1490550

Foote, Alexander K. ^[1];

^[1]; Holden, Michael R. ^[2]; Margittai, Martin ^[2];

^[1]

Department of Chemistry, University of Wisconsin-Madison, 1101 University Ave, Madison, USA
Department of Chemistry & Biochemistry, University of Denver, 2190 E. Iliff Ave., Denver, USA

Time-resolved fluorescence anisotropy reveals conformational variation of single tau proteins in solution.

View Accepted Manuscript (Publisher)

Cite

Export

Save

Sponsoring Organization:: USDOE

OSTI ID:: 1490550

Journal Information:: Physical Chemistry Chemical Physics. PCCP, Journal Name: Physical Chemistry Chemical Physics. PCCP Journal Issue: 4 Vol. 21; ISSN 1463-9076; ISSN PPCPFQ

Publisher:: Royal Society of Chemistry (RSC)Copyright Statement

Country of Publication:: United Kingdom

Language:: English

References (45)

Asymmetric Modulation of Protein Order-Disorder Transitions by Phosphorylation and Partner Binding Banerjee, Priya R.; Mitrea, Diana M.; Kriwacki, Richard W. Angewandte Chemie International Edition, Vol. 55, Issue 5 https://doi.org/10.1002/anie.201507728	journal	December 2015
Revealing Conformational Variants of Solution-Phase Intrinsically Disordered Tau Protein at the Single-Molecule Level Manger, Lydia H.; Foote, Alexander K.; Wood, Sharla L. Angewandte Chemie International Edition, Vol. 56, Issue 49 https://doi.org/10.1002/anie.201708242	journal	November 2017
Confined dynamics of a ribosome-bound nascent globin: Cone angle analysis of fluorescence depolarization decays in the presence of two local motions Ellis, Jamie P.; Culviner, Peter H.; Cavagnero, Silvia Protein Science, Vol. 18, Issue 10 https://doi.org/10.1002/pro.196	journal	October 2009
Characterizing the conformational ensemble of monomeric polyglutamine Wang, Xiaoling; Vitalis, Andreas; Wyczalkowski, Matthew A. Proteins: Structure, Function, and Bioinformatics, Vol. 63, Issue 2 https://doi.org/10.1002/prot.20761	journal	November 2005
Abnormal Tau-Containing Filaments in Neurodegenerative Diseases Crowther, R. A.; Goedert, M. Journal of Structural Biology, Vol. 130, Issue 2-3 https://doi.org/10.1006/jsbi.2000.4270	journal	June 2000
Are Tangles as Toxic as They Look? Spires-Jones, Tara L.; Kopeikina, Katherine J.; Koffie, Robert M. Journal of Molecular Neuroscience, Vol. 45, Issue 3 https://doi.org/10.1007/s12031-011-9566-7	journal	June 2011
Effect of librational motion on fluorescence depolarization and nuclear magnetic resonance relaxation in macromolecules and membranes Lipari, G.; Szabo, A. Biophysical Journal, Vol. 30, Issue 3 https://doi.org/10.1016/S0006-3495(80)85109-5	journal	June 1980
On the wobbling-in-cone analysis of fluorescence anisotropy decay Kinosita, K.; Ikegami, A.; Kawato, S. Biophysical Journal, Vol. 37, Issue 2 https://doi.org/10.1016/S0006-3495(82)84692-4	journal	February 1982
Tau in Alzheimer's disease Mandelkow, E. Trends in Cell Biology, Vol. 8, Issue 11 https://doi.org/10.1016/S0962-8924(98)01368-3	journal	November 1998
An Experimental Comparison of the Maximum Likelihood Estimation and Nonlinear Least-Squares Fluorescence Lifetime Analysis of Single Molecules Maus, Michael; Cotlet, Mircea; Hofkens, Johan Analytical Chemistry, Vol. 73, Issue 9 https://doi.org/10.1021/ac000877g	journal	May 2001
Resolving Mixtures in Solution by Single-Molecule Rotational Diffusivity Yang, Hsiang-Yu; Moerner, W. E. Nano Letters, Vol. 18, Issue 8 https://doi.org/10.1021/acs.nanolett.8b02280	journal	July 2018
Probing Single Biomolecules in Solution Using the Anti-Brownian Electrokinetic (ABEL) Trap Wang, Quan; Goldsmith, Randall H.; Jiang, Yan Accounts of Chemical Research, Vol. 45, Issue 11 https://doi.org/10.1021/ar200304t	journal	March 2012
Domains of tau Protein and Interactions with Microtubules Gustke, N.; Trinczek, B.; Biernat, J. Biochemistry, Vol. 33, Issue 32 https://doi.org/10.1021/bi00198a017	journal	October 1994
Single-Molecule Studies of Intrinsically Disordered Proteins Brucale, Marco; Schuler, Benjamin; Samorì, Bruno Chemical Reviews, Vol. 114, Issue 6 https://doi.org/10.1021/cr400297g	journal	January 2014
Identification of an Aggregation-Prone Structure of Tau Elbaum-Garfinkle, Shana; Rhoades, Elizabeth Journal of the American Chemical Society, Vol. 134, Issue 40 https://doi.org/10.1021/ja305206m	journal	October 2012
Single-Molecule Nanosecond Anisotropy Dynamics of Tethered Protein Motions Hu, Dehong; Lu, H. Peter The Journal of Physical Chemistry B, Vol. 107, Issue 2 https://doi.org/10.1021/jp0213654	journal	January 2003
Detection of Intensity Change Points in Time-Resolved Single-Molecule Measurements Watkins, Lucas P.; Yang, Haw The Journal of Physical Chemistry B, Vol. 109, Issue 1 https://doi.org/10.1021/jp0467548	journal	January 2005
Lifetime and Spectrally Resolved Characterization of the Photodynamics of Single Fluorophores in Solution Using the Anti-Brownian Electrokinetic Trap Wang, Quan; Moerner, W. E. The Journal of Physical Chemistry B, Vol. 117, Issue 16 https://doi.org/10.1021/jp308949d	journal	November 2012
Identification of Single Molecules in Aqueous Solution by Time-Resolved Fluorescence Anisotropy Schaffer, J.; Volkmer, A.; Eggeling, C. The Journal of Physical Chemistry A, Vol. 103, Issue 3 https://doi.org/10.1021/jp9833597	journal	January 1999
Electron Spin Resonance of Nitrogen-Vacancy Defects Embedded in Single Nanodiamonds in an ABEL Trap Kayci, Metin; Chang, Huan-Cheng; Radenovic, Aleksandra Nano Letters, Vol. 14, Issue 9 https://doi.org/10.1021/nl5023964	journal	August 2014
An Adaptive Anti-Brownian Electrokinetic Trap with Real-Time Information on Single-Molecule Diffusivity and Mobility Wang, Quan; Moerner, W. E. ACS Nano, Vol. 5, Issue 7 https://doi.org/10.1021/nn2014968	journal	June 2011
Cryo-EM structures of tau filaments from Alzheimer’s disease Fitzpatrick, Anthony W. P.; Falcon, Benjamin; He, Shaoda Nature, Vol. 547, Issue 7662 https://doi.org/10.1038/nature23002	journal	July 2017
Extreme disorder in an ultrahigh-affinity protein complex Borgia, Alessandro; Borgia, Madeleine B.; Bugge, Katrine Nature, Vol. 555, Issue 7694 https://doi.org/10.1038/nature25762	journal	February 2018
Watching conformational- and photodynamics of single fluorescent proteins in solution Goldsmith, Randall H.; Moerner, W. E. Nature Chemistry, Vol. 2, Issue 3 https://doi.org/10.1038/nchem.545	journal	January 2010
Single-molecule motions enable direct visualization of biomolecular interactions in solution Wang, Quan; Moerner, W. E. Nature Methods, Vol. 11, Issue 5 https://doi.org/10.1038/nmeth.2882	journal	March 2014
Tau in physiology and pathology Wang, Yipeng; Mandelkow, Eckhard Nature Reviews Neuroscience, Vol. 17, Issue 1 https://doi.org/10.1038/nrn.2015.1	journal	December 2015
Amyloid-β and tau — a toxic pas de deux in Alzheimer's disease Ittner, Lars M.; Götz, Jürgen Nature Reviews Neuroscience, Vol. 12, Issue 2 https://doi.org/10.1038/nrn2967	journal	December 2010
Effects of surface tethering on protein folding mechanisms Friedel, M.; Baumketner, A.; Shea, J. -E. Proceedings of the National Academy of Sciences, Vol. 103, Issue 22 https://doi.org/10.1073/pnas.0601210103	journal	May 2006
Fluorescence correlation spectroscopy shows that monomeric polyglutamine molecules form collapsed structures in aqueous solutions Crick, S. L.; Jayaraman, M.; Frieden, C. Proceedings of the National Academy of Sciences, Vol. 103, Issue 45 https://doi.org/10.1073/pnas.0608175103	journal	October 2006
Principal-components analysis of shape fluctuations of single DNA molecules Cohen, A. E.; Moerner, W. E. Proceedings of the National Academy of Sciences, Vol. 104, Issue 31 https://doi.org/10.1073/pnas.0610396104	journal	May 2007
A natively unfolded yeast prion monomer adopts an ensemble of collapsed and rapidly fluctuating structures Mukhopadhyay, S.; Krishnan, R.; Lemke, E. A. Proceedings of the National Academy of Sciences, Vol. 104, Issue 8 https://doi.org/10.1073/pnas.0611503104	journal	February 2007
Charge interactions can dominate the dimensions of intrinsically disordered proteins Muller-Spath, S.; Soranno, A.; Hirschfeld, V. Proceedings of the National Academy of Sciences, Vol. 107, Issue 33 https://doi.org/10.1073/pnas.1001743107	journal	July 2010
Electrokinetic trapping at the one nanometer limit Fields, A. P.; Cohen, A. E. Proceedings of the National Academy of Sciences, Vol. 108, Issue 22 https://doi.org/10.1073/pnas.1103554108	journal	May 2011
Sensing cooperativity in ATP hydrolysis for single multisubunit enzymes in solution Jiang, Y.; Douglas, N. R.; Conley, N. R. Proceedings of the National Academy of Sciences, Vol. 108, Issue 41 https://doi.org/10.1073/pnas.1112244108	journal	September 2011
Single-molecule spectroscopy reveals photosynthetic LH2 complexes switch between emissive states Schlau-Cohen, G. S.; Wang, Q.; Southall, J. Proceedings of the National Academy of Sciences, Vol. 110, Issue 27 https://doi.org/10.1073/pnas.1310222110	journal	June 2013
Dissecting pigment architecture of individual photosynthetic antenna complexes in solution Wang, Quan; Moerner, W. E. Proceedings of the National Academy of Sciences, Vol. 112, Issue 45 https://doi.org/10.1073/pnas.1514027112	journal	October 2015
Direct single-molecule measurements of phycocyanobilin photophysics in monomeric C-phycocyanin Squires, Allison H.; Moerner, W. E. Proceedings of the National Academy of Sciences, Vol. 114, Issue 37 https://doi.org/10.1073/pnas.1705435114	journal	August 2017
Assembly of tau protein into Alzheimer paired helical filaments depends on a local sequence motif (306VQIVYK311) forming beta structure von Bergen, M.; Friedhoff, P.; Biernat, J. Proceedings of the National Academy of Sciences, Vol. 97, Issue 10 https://doi.org/10.1073/pnas.97.10.5129	journal	May 2000
Dynamics and folding of single two-stranded coiled-coil peptides studied by fluorescent energy transfer confocal microscopy Talaga, D. S.; Lau, W. L.; Roder, H. Proceedings of the National Academy of Sciences, Vol. 97, Issue 24 https://doi.org/10.1073/pnas.97.24.13021	journal	November 2000
Identification of key amino acids responsible for the distinct aggregation properties of microtubule-associated protein 2 and tau Xie, Ce; Soeda, Yoshiyuki; Shinzaki, Yuki Journal of Neurochemistry, Vol. 135, Issue 1 https://doi.org/10.1111/jnc.13228	journal	August 2015
Propagation of Tau Aggregates and Neurodegeneration Goedert, Michel; Eisenberg, David S.; Crowther, R. Anthony Annual Review of Neuroscience, Vol. 40, Issue 1 https://doi.org/10.1146/annurev-neuro-072116-031153	journal	July 2017
The role of tau in neurodegeneration Gendron, Tania F.; Petrucelli, Leonard Molecular Neurodegeneration, Vol. 4, Issue 1 https://doi.org/10.1186/1750-1326-4-13	journal	January 2009
Time-resolved fluorescence anisotropy imaging applied to live cells Suhling, Klaus; Siegel, Jan; Lanigan, Peter M. P. Optics Letters, Vol. 29, Issue 6 https://doi.org/10.1364/OL.29.000584	journal	January 2004
Structural Polymorphism of 441-Residue Tau at Single Residue Resolution Mukrasch, Marco D.; Bibow, Stefan; Korukottu, Jegannath PLoS Biology, Vol. 7, Issue 2 https://doi.org/10.1371/journal.pbio.1000034	journal	February 2009
Soluble forms of tau are toxic in Alzheimer’s disease Kopeikina, Katherine; Hyman, Bradley; Spires-Jones, Tara Translational Neuroscience, Vol. 3, Issue 3 https://doi.org/10.2478/s13380-012-0032-y	journal	January 2012

Similar Records

Single-Molecule Protein Conformational Dynamics in Cell Signaling

Conference · 2004 · OSTI ID:15020318

Lu, H PETER

Single-Molecule Nanosecond Anisotropy Dynamics of Tethered Protein Motions

Journal Article · 2003 · Journal of Physical Chemistry B: Materials, Surfaces, Interfaces, amp Biophysical · OSTI ID:15003529

Hu, Dehong; Lu, H Peter

Probing Conformational Dynamics of Tau Protein by Hydrogen/Deuterium Exchange Mass Spectrometry

Journal Article · 2018 · Journal of the American Society for Mass Spectrometry · OSTI ID:22776809

Huang, Richard Y.-C.; Iacob, Roxana E.; Sankaranarayanan, Sethu; +5 more

Title: Time-resolved multirotational dynamics of single solution-phase tau proteins reveals details of conformational variation

Citation Formats

References (45)

Similar Records

Related Subjects