FRET-based dynamic structural biology: Challenges, perspectives and an appeal for open-science practices

Lerner, Eitan; Barth, Anders; Hendrix, Jelle; Ambrose, Benjamin; Birkedal, Victoria; Blanchard, Scott C.; Börner, Richard; Sung Chung, Hoi; Cordes, Thorben; Craggs, Timothy D.; Deniz, Ashok A.; Diao, Jiajie; Fei, Jingyi; Gonzalez, Ruben L.; Gopich, Irina V.; Ha, Taekjip; Hanke, Christian A.; Haran, Gilad; Hatzakis, Nikos S.; Hohng, Sungchul; Hong, Seok-Cheol; Hugel, Thorsten; Ingargiola, Antonino; Joo, Chirlmin; Kapanidis, Achillefs N.; Kim, Harold D.; Laurence, Ted; Lee, Nam Ki; Lee, Tae-Hee; Lemke, Edward A.; Margeat, Emmanuel; Michaelis, Jens; Michalet, Xavier; Myong, Sua; Nettels, Daniel; Peulen, Thomas-Otavio; Ploetz, Evelyn; Razvag, Yair; Robb, Nicole C.; Schuler, Benjamin; Soleimaninejad, Hamid; Tang, Chun; Vafabakhsh, Reza; Lamb, Don C.; Seidel, Claus A.M.; Weiss, Shimon

doi:10.7554/elife.60416

Title: FRET-based dynamic structural biology: Challenges, perspectives and an appeal for open-science practices

Abstract

Single-molecule FRET (smFRET) has become a mainstream technique for studying biomolecular structural dynamics. The rapid and wide adoption of smFRET experiments by an ever-increasing number of groups has generated significant progress in sample preparation, measurement procedures, data analysis, algorithms and documentation. Several labs that employ smFRET approaches have joined forces to inform the smFRET community about streamlining how to perform experiments and analyze results for obtaining quantitative information on biomolecular structure and dynamics. The recent efforts include blind tests to assess the accuracy and the precision of smFRET experiments among different labs using various procedures. These multi-lab studies have led to the development of smFRET procedures and documentation, which are important when submitting entries into the archiving system for integrative structure models, PDB-Dev. This position paper describes the current ‘state of the art’ from different perspectives, points to unresolved methodological issues for quantitative structural studies, provides a set of ‘soft recommendations’ about which an emerging consensus exists, and lists openly available resources for newcomers and seasoned practitioners. To make further progress, we strongly encourage ‘open science’ practices.

Authors:

^[1];

^[2];

^[3]; Ambrose, Benjamin ^[4]; Birkedal, Victoria ^[5];

^[6];

^[7]; Sung Chung, Hoi ^[8];

^[9];

^[4]; Deniz, Ashok A. ^[10]; Diao, Jiajie ^[11];

^[12];

^[13]; Gopich, Irina V. ^[8];

^[14]; Hanke, Christian A. ^[2];

^[15]; Hatzakis, Nikos S. ^[16]; Hohng, Sungchul ^[17] more »

Hebrew Univ. of Jerusalem (Israel)
Heinrich-Heine-Univ., Düsseldorf (Germany)
Hasselt Univ., Diepenbeek (Belgium)
Univ. of Sheffield (United Kingdom)
Aarhus Univ. (Denmark)
St. Jude Children's Research Hospital, Memphis, TN (United States)
Univ. of Applied Science, Mittweida (Germany)
National Institutes of Health (NIH), Bethesda, MD (United States)
Ludwig-Maximilians-Univ. München, Planegg-Martinsried (Germany)
The Scripps Research Inst., La Jolla, CA (United States)
Univ. of Cincinnati, OH (United States)
Univ. of Chicago, IL (United States)
Columbia Univ., New York, NY (United States)
Johns Hopkins Univ., Baltimore, MD (United States)
Weizmann Inst. of Science, Rehovot (Israel)
Univ. of Copenhagen (Denmark)
Seoul National Univ. (Korea, Republic of)
Korea Univ., Seoul, (Korea, Republic of)
Univ. of Freiburg (Germany)
Univ. of California, Los Angeles, CA (United States)
Delft Univ. of Technology (Netherlands)
Univ. of Oxford (United Kingdom)
Georgia Institute of Technology, Atlanta, GA (United States)
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Pennsylvania State Univ., University Park, PA (United States)
Johannes Gutenberg Univ., Mainz (Germany)
Univ. of Montpellier (France)
Ulm Univ. (Germany)
Univ. of Zurich (Switzerland)
Univ. of California, San Francisco, CA (United States)
Ludwig-Maximilians-Univ., München (Germany)
Univ. of Warwick, Coventry (United Kingdom)
Univ. of Melbourne, Parkville (Australia)
Peking Univ., Beijing (China)
Northwestern Univ., Evanston, IL (United States)

Publication Date:: Mon Mar 29 00:00:00 EDT 2021

Research Org.:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Org.:: USDOE National Nuclear Security Administration (NNSA); National Institutes of Health (NIH); National Science Foundation (NSF); European Research Council (ERC); German Research Foundation (DFG); Wellcome Trust; Swiss National Science Foundation (SNSF); UK Biotechnology and Biological Sciences Research Council; Royal Society; Agence Nationale de la Recherche; Israel Science Foundation (ISF); National Research Foundation of Korea (NRF); Independent Fund Denmark; Ministry of Science and Technology of China; Villum Foundation Center for Excellence BIONEC; Novo Nordisk Foundation

OSTI Identifier:: 1822617

Report Number(s):: LLNL-JRNL-822117
Journal ID: ISSN 2050-084X; 1032929

Grant/Contract Number:: AC52-07NA27344; R01 GM084288; R01 GM137608; R01 GM112882; R01 GM123164; R01 GM130793; R01 GM140272; R35 GM130375; 1DP2M128185-01; MCB-1818147; MCB-1842951; CHE-2004016; RGP0061/2019; 638536; 860954; 671208; 819299; GRK2062; SFB863; PL696/4-1; SPP2191 402723784; SFB 1129 240245660; SE 1195/21/1; 110164/Z/15/Z; BB/S008896/1; BB/T008032/1; RGS/R2/180405; DKR00620; RGF/R1/180054; ANR-17-CE0-0026-02; ANR-18-CE11-0004-02; ANR-19-CE44-0009-02; 1250/19; 3565/20; 2019R1A2C2090896; NRF-2019R1A2C2005209; NRF-2019R1A2C1089808; 6110-00623B; 2018YFA0507700; C14/16/053; NNF14CC0001

Resource Type:: Accepted Manuscript

Journal Name:: eLife

Additional Journal Information:: Journal Volume: 10; Journal Issue: na; Journal ID: ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; biological and medical sciences

Citation Formats


                    Lerner, Eitan, Barth, Anders, Hendrix, Jelle, Ambrose, Benjamin, Birkedal, Victoria, Blanchard, Scott C., Börner, Richard, Sung Chung, Hoi, Cordes, Thorben, Craggs, Timothy D., Deniz, Ashok A., Diao, Jiajie, Fei, Jingyi, Gonzalez, Ruben L., Gopich, Irina V., Ha, Taekjip, Hanke, Christian A., Haran, Gilad, Hatzakis, Nikos S., Hohng, Sungchul, Hong, Seok-Cheol, Hugel, Thorsten, Ingargiola, Antonino, Joo, Chirlmin, Kapanidis, Achillefs N., Kim, Harold D., Laurence, Ted, Lee, Nam Ki, Lee, Tae-Hee, Lemke, Edward A., Margeat, Emmanuel, Michaelis, Jens, Michalet, Xavier, Myong, Sua, Nettels, Daniel, Peulen, Thomas-Otavio, Ploetz, Evelyn, Razvag, Yair, Robb, Nicole C., Schuler, Benjamin, Soleimaninejad, Hamid, Tang, Chun, Vafabakhsh, Reza, Lamb, Don C., Seidel, Claus A.M., and Weiss, Shimon. FRET-based dynamic structural biology: Challenges, perspectives and an appeal for open-science practices.  United States: N. p., 2021. 
Web.  doi:10.7554/elife.60416.

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                    Lerner, Eitan, Barth, Anders, Hendrix, Jelle, Ambrose, Benjamin, Birkedal, Victoria, Blanchard, Scott C., Börner, Richard, Sung Chung, Hoi, Cordes, Thorben, Craggs, Timothy D., Deniz, Ashok A., Diao, Jiajie, Fei, Jingyi, Gonzalez, Ruben L., Gopich, Irina V., Ha, Taekjip, Hanke, Christian A., Haran, Gilad, Hatzakis, Nikos S., Hohng, Sungchul, Hong, Seok-Cheol, Hugel, Thorsten, Ingargiola, Antonino, Joo, Chirlmin, Kapanidis, Achillefs N., Kim, Harold D., Laurence, Ted, Lee, Nam Ki, Lee, Tae-Hee, Lemke, Edward A., Margeat, Emmanuel, Michaelis, Jens, Michalet, Xavier, Myong, Sua, Nettels, Daniel, Peulen, Thomas-Otavio, Ploetz, Evelyn, Razvag, Yair, Robb, Nicole C., Schuler, Benjamin, Soleimaninejad, Hamid, Tang, Chun, Vafabakhsh, Reza, Lamb, Don C., Seidel, Claus A.M., & Weiss, Shimon. FRET-based dynamic structural biology: Challenges, perspectives and an appeal for open-science practices.  United States.  https://doi.org/10.7554/elife.60416

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                    Lerner, Eitan, Barth, Anders, Hendrix, Jelle, Ambrose, Benjamin, Birkedal, Victoria, Blanchard, Scott C., Börner, Richard, Sung Chung, Hoi, Cordes, Thorben, Craggs, Timothy D., Deniz, Ashok A., Diao, Jiajie, Fei, Jingyi, Gonzalez, Ruben L., Gopich, Irina V., Ha, Taekjip, Hanke, Christian A., Haran, Gilad, Hatzakis, Nikos S., Hohng, Sungchul, Hong, Seok-Cheol, Hugel, Thorsten, Ingargiola, Antonino, Joo, Chirlmin, Kapanidis, Achillefs N., Kim, Harold D., Laurence, Ted, Lee, Nam Ki, Lee, Tae-Hee, Lemke, Edward A., Margeat, Emmanuel, Michaelis, Jens, Michalet, Xavier, Myong, Sua, Nettels, Daniel, Peulen, Thomas-Otavio, Ploetz, Evelyn, Razvag, Yair, Robb, Nicole C., Schuler, Benjamin, Soleimaninejad, Hamid, Tang, Chun, Vafabakhsh, Reza, Lamb, Don C., Seidel, Claus A.M., and Weiss, Shimon. Mon .  
"FRET-based dynamic structural biology: Challenges, perspectives and an appeal for open-science practices".  United States.  https://doi.org/10.7554/elife.60416.  https://www.osti.gov/servlets/purl/1822617.

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@article{osti_1822617,

  title        = {FRET-based dynamic structural biology: Challenges, perspectives and an appeal for open-science practices},

  author       = {Lerner, Eitan and Barth, Anders and Hendrix, Jelle and Ambrose, Benjamin and Birkedal, Victoria and Blanchard, Scott C. and Börner, Richard and Sung Chung, Hoi and Cordes, Thorben and Craggs, Timothy D. and Deniz, Ashok A. and Diao, Jiajie and Fei, Jingyi and Gonzalez, Ruben L. and Gopich, Irina V. and Ha, Taekjip and Hanke, Christian A. and Haran, Gilad and Hatzakis, Nikos S. and Hohng, Sungchul and Hong, Seok-Cheol and Hugel, Thorsten and Ingargiola, Antonino and Joo, Chirlmin and Kapanidis, Achillefs N. and Kim, Harold D. and Laurence, Ted and Lee, Nam Ki and Lee, Tae-Hee and Lemke, Edward A. and Margeat, Emmanuel and Michaelis, Jens and Michalet, Xavier and Myong, Sua and Nettels, Daniel and Peulen, Thomas-Otavio and Ploetz, Evelyn and Razvag, Yair and Robb, Nicole C. and Schuler, Benjamin and Soleimaninejad, Hamid and Tang, Chun and Vafabakhsh, Reza and Lamb, Don C. and Seidel, Claus A.M. and Weiss, Shimon},

  abstractNote = {Single-molecule FRET (smFRET) has become a mainstream technique for studying biomolecular structural dynamics. The rapid and wide adoption of smFRET experiments by an ever-increasing number of groups has generated significant progress in sample preparation, measurement procedures, data analysis, algorithms and documentation. Several labs that employ smFRET approaches have joined forces to inform the smFRET community about streamlining how to perform experiments and analyze results for obtaining quantitative information on biomolecular structure and dynamics. The recent efforts include blind tests to assess the accuracy and the precision of smFRET experiments among different labs using various procedures. These multi-lab studies have led to the development of smFRET procedures and documentation, which are important when submitting entries into the archiving system for integrative structure models, PDB-Dev. This position paper describes the current ‘state of the art’ from different perspectives, points to unresolved methodological issues for quantitative structural studies, provides a set of ‘soft recommendations’ about which an emerging consensus exists, and lists openly available resources for newcomers and seasoned practitioners. To make further progress, we strongly encourage ‘open science’ practices.},

  doi          = {10.7554/elife.60416},

  journal      = {eLife},

  number       = na,

  volume       = 10,

  place        = {United States},

  year         = {Mon Mar 29 00:00:00 EDT 2021},

  month        = {Mon Mar 29 00:00:00 EDT 2021}

}

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Current Opinion in Structural Biology, Vol. 23, Issue 1
DOI: 10.1016/j.sbi.2012.10.008

Effect of flexibility and cis residues in single-molecule FRET studies of polyproline
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Best, R. B.; Merchant, K. A.; Gopich, I. V.
Proceedings of the National Academy of Sciences, Vol. 104, Issue 48
DOI: 10.1073/pnas.0709567104

Effect of the orientation of donor and acceptor on the probability of energy transfer involving electronic transitions of mixed polarization
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Haas, Elisha; Katchalski-Katzir, Ephraim; Steinberg, Izchak Z.
Biochemistry, Vol. 17, Issue 23
DOI: 10.1021/bi00616a032

Detection of Structural Dynamics by FRET: A Photon Distribution and Fluorescence Lifetime Analysis of Systems with Multiple States
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Kalinin, Stanislav; Valeri, Alessandro; Antonik, Matthew
The Journal of Physical Chemistry B, Vol. 114, Issue 23
DOI: 10.1021/jp102156t

Single-molecule FRET–derived model of the synaptotagmin 1–SNARE fusion complex
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Choi, Ucheor B.; Strop, Pavel; Vrljic, Marija
Nature Structural & Molecular Biology, Vol. 17, Issue 3
DOI: 10.1038/nsmb.1763

Single-molecule protein folding: Diffusion fluorescence resonance energy transfer studies of the denaturation of chymotrypsin inhibitor 2
journal, May 2000

Deniz, A. A.; Laurence, T. A.; Beligere, G. S.
Proceedings of the National Academy of Sciences, Vol. 97, Issue 10
DOI: 10.1073/pnas.090104997

Experimental determination of upper bound for transition path times in protein folding from single-molecule photon-by-photon trajectories
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Chung, H. S.; Louis, J. M.; Eaton, W. A.
Proceedings of the National Academy of Sciences, Vol. 106, Issue 29
DOI: 10.1073/pnas.0901178106

Single-Molecule Fluorescence Experiments Determine Protein Folding Transition Path Times
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Chung, Hoi Sung; McHale, Kevin; Louis, John M.
Science, Vol. 335, Issue 6071
DOI: 10.1126/science.1215768

Double fluorescence resonance energy transfer to explore multicomponent binding interactions: a case study of DNA mismatches
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Horsey, Imogen; Furey, W. Scott; Harrison, Joseph G.
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Nature Communications, Vol. 10, Issue 1
DOI: 10.1038/s41467-019-10490-9

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Nettels, Daniel; Hoffmann, Armin; Schuler, Benjamin
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DOI: 10.1021/jp076971j

Fluorescence Lifetime Correlation Spectroscopy
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Kapusta, Peter; Wahl, Michael; Benda, Aleš
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Chizhik, Alexey I.; Chizhik, Anna M.; Khoptyar, Dmitry
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DOI: 10.1021/nl200215v

Fluorescence resonance energy transfer analysis of the structure of the four-way DNA junction
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Clegg, Robert M.; Murchie, Alastair I. H.; Zechel, Annelies
Biochemistry, Vol. 31, Issue 20
DOI: 10.1021/bi00135a016

The contribution of modern EPR to structural biology
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Jeschke, Gunnar
Emerging Topics in Life Sciences, Vol. 2, Issue 1
DOI: 10.1042/ETLS20170143

Highly Efficient FRET from a Single Nitrogen-Vacancy Center in Nanodiamonds to a Single Organic Molecule
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Tisler, Julia; Reuter, Rolf; Lämmle, Anke
ACS Nano, Vol. 5, Issue 10
DOI: 10.1021/nn2021259

Multidomain structure and correlated dynamics determined by self-consistent FRET networks
journal, December 2016

Hellenkamp, Björn; Wortmann, Philipp; Kandzia, Florian
Nature Methods, Vol. 14, Issue 2
DOI: 10.1038/nmeth.4081

A DNA Origami Platform for Single-Pair Förster Resonance Energy Transfer Investigation of DNA–DNA Interactions and Ligation
journal, December 2019

Bartnik, Kira; Barth, Anders; Pilo-Pais, Mauricio
Journal of the American Chemical Society, Vol. 142, Issue 2
DOI: 10.1021/jacs.9b09093

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journal, March 2016

Hadi-Alijanvand, Hamid; Proctor, Elizabeth A.; Ding, Feng
Proteins: Structure, Function, and Bioinformatics, Vol. 84, Issue 5
DOI: 10.1002/prot.25011

Polyproline and the "spectroscopic ruler" revisited with single-molecule fluorescence
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Schuler, B.; Lipman, E. A.; Steinbach, P. J.
Proceedings of the National Academy of Sciences, Vol. 102, Issue 8
DOI: 10.1073/pnas.0408164102

The Dynamic Multisite Interactions between Two Intrinsically Disordered Proteins
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Wu, Shaowen; Wang, Dongdong; Liu, Jin
Angewandte Chemie International Edition, Vol. 56, Issue 26
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Application of dual-focus fluorescence correlation spectroscopy to microfluidic flow-velocity measurement
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Arbour, Tyler J.; Enderlein, Jörg
Lab on a Chip, Vol. 10, Issue 10
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Fluorescent proteins for single-molecule fluorescence applications
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Journal of Biophotonics, Vol. 1, Issue 1
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Kappa-squared: from nuisance to new sense
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van der Meer, B. W.
Reviews in Molecular Biotechnology, Vol. 82, Issue 3
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An Introduction to Infinite HMMs for Single-Molecule Data Analysis
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Sgouralis, Ioannis; Pressé, Steve
Biophysical Journal, Vol. 112, Issue 10
DOI: 10.1016/j.bpj.2017.04.027

Integrated NMR, Fluorescence, and Molecular Dynamics Benchmark Study of Protein Mechanics and Hydrodynamics
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Möckel, Christina; Kubiak, Jakub; Schillinger, Oliver
The Journal of Physical Chemistry B, Vol. 123, Issue 7
DOI: 10.1021/acs.jpcb.8b08903

Correlative Fluorescence and Electron Microscopy
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Schirra, Randall T.; Zhang, Peijun
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Extreme Fuzziness: Direct Interactions between Two IDPs
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Wang, Wenning; Wang, Dongdong
Biomolecules, Vol. 9, Issue 3
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Photon Counting Histograms for Diffusing Fluorophores
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Gopich, Irina V.; Szabo, Attila
The Journal of Physical Chemistry B, Vol. 109, Issue 37
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Protein folding transition path times from single molecule FRET
journal, February 2018

Chung, Hoi Sung; Eaton, William A.
Current Opinion in Structural Biology, Vol. 48
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Crystal Structures of Cyanine Fluorophores Stacked onto the End of Double-Stranded RNA
journal, December 2017

Liu, Yijin; Lilley, David M. J.
Biophysical Journal, Vol. 113, Issue 11
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Physical Principles Underlying the Complex Biology of Intracellular Phase Transitions
journal, May 2020

Choi, Jeong-Mo; Holehouse, Alex S.; Pappu, Rohit V.
Annual Review of Biophysics, Vol. 49, Issue 1
DOI: 10.1146/annurev-biophys-121219-081629

Photobleaching Pathways in Single-Molecule FRET Experiments
journal, April 2007

Kong, Xiangxu; Nir, Eyal; Hamadani, Kambiz
Journal of the American Chemical Society, Vol. 129, Issue 15
DOI: 10.1021/ja068002s

Substrate conformational dynamics facilitate structure-specific recognition of gapped DNA by DNA polymerase
journal, September 2019

Craggs, Timothy D.; Sustarsic, Marko; Plochowietz, Anne
Nucleic Acids Research, Vol. 47, Issue 20
DOI: 10.1093/nar/gkz797

Real-time analysis of single influenza virus replication complexes reveals large promoter-dependent differences in initiation dynamics
journal, April 2019

Robb, Nicole C.; te Velthuis, Aartjan J. W.; Fodor, Ervin
Nucleic Acids Research, Vol. 47, Issue 12
DOI: 10.1093/nar/gkz313

Transport dynamics in a glutamate transporter homologue
journal, June 2013

Akyuz, Nurunisa; Altman, Roger B.; Blanchard, Scott C.
Nature, Vol. 502, Issue 7469
DOI: 10.1038/nature12265

Nanocavity-Based Determination of Absolute Values of Photoluminescence Quantum Yields
journal, January 2013

Chizhik, Alexey I.; Gregor, Ingo; Ernst, Benedikt
ChemPhysChem, Vol. 14, Issue 3
DOI: 10.1002/cphc.201200931

Architecture of an RNA Polymerase II Transcription Pre-Initiation Complex
journal, September 2013

Murakami, K.; Elmlund, H.; Kalisman, N.
Science, Vol. 342, Issue 6159
DOI: 10.1126/science.1238724

Two New Concepts to Measure Fluorescence Resonance Energy Transfer via Fluorescence Correlation Spectroscopy: Theory and Experimental Realizations
journal, June 2001

Widengren, Jerker; Schweinberger, Enno; Berger, Sylvia
The Journal of Physical Chemistry A, Vol. 105, Issue 28
DOI: 10.1021/jp010301a

AMBER-DYES: Characterization of Charge Fluctuations and Force Field Parameterization of Fluorescent Dyes for Molecular Dynamics Simulations
journal, December 2014

Graen, Timo; Hoefling, Martin; Grubmüller, Helmut
Journal of Chemical Theory and Computation, Vol. 10, Issue 12
DOI: 10.1021/ct500869p

Deciphering Complexity in Molecular Biophysics with Single-Molecule Resolution
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Deniz, Ashok A.
Journal of Molecular Biology, Vol. 428, Issue 2
DOI: 10.1016/j.jmb.2015.12.011

Microsecond ALEX FRET analysis notebook using FRETbursts - corrections, FRET burst analysis of recurring molecules, FCS, 2CDE & BVA
dataset, January 2020

Lerner, Eitan
Zenodo
DOI: 10.5281/zenodo.3630473

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Abstract

Citation Formats

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Allosteric control of the ribosome by small-molecule antibiotics journal, August 2012

Performance of Fluorescence Correlation Spectroscopy for Measuring Diffusion and Concentration journal, November 2005

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NMR-STAR: comprehensive ontology for representing, archiving and exchanging data from nuclear magnetic resonance spectroscopic experiments journal, December 2018

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Tunable microsecond dynamics of an allosteric switch regulate the activity of a AAA+ disaggregation machine journal, March 2019

Resolving Heterogeneity on the Single Molecular Level with the Photon-Counting Histogram journal, January 2000

Theory, Practice, and Applications of Paramagnetic Relaxation Enhancement for the Characterization of Transient Low-Population States of Biological Macromolecules and Their Complexes journal, September 2009

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A photoprotection strategy for microsecond-resolution single-molecule fluorescence spectroscopy journal, January 2011

Super-resolution Imaging of Energy Transfer by Intensity-Based STED-FRET journal, February 2021

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Evidence of a Folding Intermediate in RNase H from Single‐Molecule FRET Experiments journal, November 2010

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Insights into the conformations and dynamics of intrinsically disordered proteins using single-molecule fluorescence journal, November 2017

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Testing the use of molecular dynamics to simulate fluorophore motions and FRET journal, January 2011

A Method for Extracting the Free Energy Surface and Conformational Dynamics of Fast-Folding Proteins from Single Molecule Photon Trajectories journal, June 2015

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An Oxygen Scavenging System for Improvement of Dye Stability in Single-Molecule Fluorescence Experiments journal, March 2008

Structure-Guided Design of a Peptide Lock for Modular Peptide Binders journal, January 2020

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Identification of Two Distinct Hybrid State Intermediates on the Ribosome journal, February 2007

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Dynamics of the nucleosomal histone H3 N-terminal tail revealed by high precision single-molecule FRET journal, January 2020

Conformational and dynamic plasticity in substrate-binding proteins underlies selective transport in ABC importers journal, March 2019

Identifying Molecular Dynamics in Single-Molecule FRET Experiments with Burst Variance Analysis journal, March 2011

Conformational Sampling of Aminoacyl-tRNA during Selection on the Bacterial Ribosome journal, June 2010

Evaluation of the Distribution of Distances Between Energy Donors and Acceptors by Fluorescence Decay journal, August 1972

Conformational dynamics of the ABC transporter McjD seen by single‐molecule FRET
journal, September 2018

Allosteric control of the ribosome by small-molecule antibiotics
journal, August 2012

Performance of Fluorescence Correlation Spectroscopy for Measuring Diffusion and Concentration
journal, November 2005

Toward Complete Sequence Flexibility of Nucleic Acid Base Analogue FRET
journal, June 2017

NMR-STAR: comprehensive ontology for representing, archiving and exchanging data from nuclear magnetic resonance spectroscopic experiments
journal, December 2018

Excluded-Volume Effects in Living Cells
journal, December 2014

Identification of Single Molecules in Aqueous Solution by Time-Resolved Fluorescence Anisotropy
journal, January 1999

Probing the interaction between two single molecules: fluorescence resonance energy transfer between a single donor and a single acceptor.
journal, June 1996

Specific Conformational Dynamics and Expansion Underpin a Multi-Step Mechanism for Specific Binding of p27 with Cdk2/Cyclin A
journal, April 2020

rFRET: A comprehensive, Matlab-based program for analyzing intensity-based ratiometric microscopic FRET experiments: Ratiometric FRET Analysis
journal, March 2016

Detecting the conformation of individual proteins in live cells
journal, January 2010

Single-Molecule Analysis beyond Dwell Times: Demonstration and Assessment in and out of Equilibrium
journal, October 2016

New electron microscopy database and deposition system
journal, November 2002

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journal, September 2020

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journal, November 2019

Intrinsically disordered proteins in cellular signalling and regulation
journal, December 2014

Inhibition Assay of Biomolecules based on Fluorescence Resonance Energy Transfer (FRET) between Quantum Dots and Gold Nanoparticles
journal, March 2005

Tunable microsecond dynamics of an allosteric switch regulate the activity of a AAA+ disaggregation machine
journal, March 2019

Resolving Heterogeneity on the Single Molecular Level with the Photon-Counting Histogram
journal, January 2000

Theory, Practice, and Applications of Paramagnetic Relaxation Enhancement for the Characterization of Transient Low-Population States of Biological Macromolecules and Their Complexes
journal, September 2009

Learning Rates and States from Biophysical Time Series: A Bayesian Approach to Model Selection and Single-Molecule FRET Data
journal, December 2009

Distribution of end-to-end distances of oligopeptides in solution as estimated by energy transfer.
journal, May 1975

Protein induced fluorescence enhancement as a single molecule assay with short distance sensitivity
journal, April 2011

Single-Molecule FRET Spectroscopy and the Polymer Physics of Unfolded and Intrinsically Disordered Proteins
journal, July 2016

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journal, January 2015

Probing DNA Dynamics: Stacking‐Induced Fluorescence Increase (SIFI) versus FRET
journal, May 2020

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journal, July 2014

A photoprotection strategy for microsecond-resolution single-molecule fluorescence spectroscopy
journal, January 2011

Super-resolution Imaging of Energy Transfer by Intensity-Based STED-FRET
journal, February 2021

Single-molecule Forster resonance energy transfer study of protein dynamics under denaturing conditions
journal, October 2005

Protein folding stability and dynamics imaged in a living cell
journal, February 2010

Ultrahigh-resolution multicolor colocalization of single fluorescent probes
journal, August 2000

Evidence of a Folding Intermediate in RNase H from Single‐Molecule FRET Experiments
journal, November 2010

Visualizing transient dark states by NMR spectroscopy
journal, January 2015

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journal, November 2017

Microfluidic Device for Single-Molecule Experiments with Enhanced Photostability
journal, September 2009

Stability of local secondary structure determines selectivity of viral RNA chaperones
journal, May 2018

48-spot single-molecule FRET setup with periodic acceptor excitation
journal, March 2018

Sensing DNA Opening in Transcription Using Quenchable Förster Resonance Energy Transfer
journal, October 2010

Testing the use of molecular dynamics to simulate fluorophore motions and FRET
journal, January 2011

A Method for Extracting the Free Energy Surface and Conformational Dynamics of Fast-Folding Proteins from Single Molecule Photon Trajectories
journal, June 2015

Diphenylhexatrienes as Photoprotective Agents for Ultrasensitive Fluorescence Detection
journal, March 2010

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journal, March 2011

A practical guide to single-molecule FRET
journal, May 2008

Conformational landscapes of DNA polymerase I and mutator derivatives establish fidelity checkpoints for nucleotide insertion
journal, July 2013

Single-molecule dynamics of gating in a neurotransmitter transporter homologue
journal, May 2010

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journal, February 2018

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journal, February 2011

High-throughput single-molecule optofluidic analysis
journal, February 2011

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journal, February 2014

An Oxygen Scavenging System for Improvement of Dye Stability in Single-Molecule Fluorescence Experiments
journal, March 2008

Structure-Guided Design of a Peptide Lock for Modular Peptide Binders
journal, January 2020

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journal, April 2001

Pulsed IR Heating Studies of Single-Molecule DNA Duplex Dissociation Kinetics and Thermodynamics
journal, January 2014

Functional Dynamics within the Human Ribosome Regulate the Rate of Active Protein Synthesis
journal, November 2015

Trapping intermediates in the crystal: ligand binding to myoglobin
journal, December 2000

Integrative Structure Modeling: Overview and Assessment
journal, June 2019

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journal, May 2006

Minute negative superhelicity is sufficient to induce the B-Z transition in the presence of low tension
journal, March 2010

Polyelectrolyte interactions enable rapid association and dissociation in high-affinity disordered protein complexes
journal, November 2020

Relationship between Absorption Intensity and Fluorescence Lifetime of Molecules
journal, August 1962

Simulation of FRET dyes allows quantitative comparison against experimental data
journal, March 2018

Self-assembled nanoscale biosensors based on quantum dot FRET donors
journal, August 2003

Identification of Two Distinct Hybrid State Intermediates on the Ribosome
journal, February 2007

Single-Molecule Detection and Identification of Multiple Species by Multiparameter Fluorescence Detection
journal, February 2006

Mass spectrometry analysis of the structural proteome
journal, February 2020

On the Mechanism of Trolox as Antiblinking and Antibleaching Reagent
journal, April 2009

Time-resolved X-ray crystallographic study of the conformational change in Ha-Ras p21 protein on GTP hydrolysis
journal, May 1990

CHARMM-DYES: Parameterization of Fluorescent Dyes for Use with the CHARMM Force Field
journal, November 2020

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journal, May 2007

Multiparameter single-molecule fluorescence spectroscopy reveals heterogeneity of HIV-1 reverse transcriptase:primer/template complexes
journal, February 2003

DNA bipedal motor walking dynamics: an experimental and theoretical study of the dependency on step size
journal, December 2017

Dynamics of the nucleosomal histone H3 N-terminal tail revealed by high precision single-molecule FRET
journal, January 2020

Conformational and dynamic plasticity in substrate-binding proteins underlies selective transport in ABC importers
journal, March 2019

Identifying Molecular Dynamics in Single-Molecule FRET Experiments with Burst Variance Analysis
journal, March 2011

Conformational Sampling of Aminoacyl-tRNA during Selection on the Bacterial Ribosome
journal, June 2010

Evaluation of the Distribution of Distances Between Energy Donors and Acceptors by Fluorescence Decay
journal, August 1972

Proton-powered subunit rotation in single membrane-bound F0F1-ATP synthase
journal, January 2004

Single‐molecule studies of conformational states and dynamics in the ABC importer OpuA
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Förster resonance energy transfer and protein-induced fluorescence enhancement as synergetic multi-scale molecular rulers
journal, September 2016