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

Author:

Lerner Eitan1ORCID,Barth Anders2ORCID,Hendrix Jelle3ORCID,Ambrose Benjamin4,Birkedal Victoria5,Blanchard Scott C6ORCID,Börner Richard7ORCID,Sung Chung Hoi8,Cordes Thorben9ORCID,Craggs Timothy D4ORCID,Deniz Ashok A10,Diao Jiajie11,Fei Jingyi12ORCID,Gonzalez Ruben L13ORCID,Gopich Irina V8,Ha Taekjip14ORCID,Hanke Christian A2,Haran Gilad15ORCID,Hatzakis Nikos S1617,Hohng Sungchul18,Hong Seok-Cheol19,Hugel Thorsten20ORCID,Ingargiola Antonino21ORCID,Joo Chirlmin22,Kapanidis Achillefs N23,Kim Harold D24,Laurence Ted25,Lee Nam Ki26ORCID,Lee Tae-Hee27,Lemke Edward A2829ORCID,Margeat Emmanuel30,Michaelis Jens31,Michalet Xavier21ORCID,Myong Sua32,Nettels Daniel33,Peulen Thomas-Otavio34,Ploetz Evelyn35ORCID,Razvag Yair1,Robb Nicole C36,Schuler Benjamin33ORCID,Soleimaninejad Hamid37,Tang Chun38,Vafabakhsh Reza39,Lamb Don C35ORCID,Seidel Claus AM2ORCID,Weiss Shimon2140ORCID

Affiliation:

1. Department of Biological Chemistry, The Alexander Silberman Institute of Life Sciences, and The Center for Nanoscience and Nanotechnology, Faculty of Mathematics & Science, The Edmond J. Safra Campus, The Hebrew University of Jerusalem, Jerusalem, Israel

2. Lehrstuhl für Molekulare Physikalische Chemie, Heinrich-Heine-Universität, Düsseldorf, Germany

3. Dynamic Bioimaging Lab, Advanced Optical Microscopy Centre and Biomedical Research Institute (BIOMED), Hasselt University, Diepenbeek, Belgium

4. Department of Chemistry, University of Sheffield, Sheffield, United Kingdom

5. Department of Chemistry and iNANO center, Aarhus University, Aarhus, Denmark

6. Department of Structural Biology, St. Jude Children's Research Hospital, Memphis, United States

7. Laserinstitut HS Mittweida, University of Applied Science Mittweida, Mittweida, Germany

8. Laboratory of Chemical Physics, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, United States

9. Physical and Synthetic Biology, Faculty of Biology, Ludwig-Maximilians-Universität München, Planegg-Martinsried, Germany

10. Department of Integrative Structural and Computational Biology, The Scripps Research Institute, La Jolla, United States

11. Department of Cancer Biology, University of Cincinnati School of Medicine, Cincinnati, United States

12. Department of Biochemistry and Molecular Biology and The Institute for Biophysical Dynamics, University of Chicago, Chicago, United States

13. Department of Chemistry, Columbia University, New York, United States

14. Department of Biophysics and Biophysical Chemistry, Department of Biomedical Engineering, Johns Hopkins University School of Medicine, Howard Hughes Medical Institute, Baltimore, United States

15. Department of Chemical and Biological Physics, Weizmann Institute of Science, Rehovot, Israel

16. Department of Chemistry & Nanoscience Centre, University of Copenhagen, Copenhagen, Denmark

17. Denmark Novo Nordisk Foundation Centre for Protein Research, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark

18. Department of Physics and Astronomy, and Institute of Applied Physics, Seoul National University, Seoul, Republic of Korea

19. Center for Molecular Spectroscopy and Dynamics, Institute for Basic Science and Department of Physics, Korea University, Seoul, Republic of Korea

20. Institute of Physical Chemistry and Signalling Research Centres BIOSS and CIBSS, University of Freiburg, Freiburg, Germany

21. Department of Chemistry and Biochemistry, and Department of Physiology, University of California, Los Angeles, Los Angeles, United States

22. Department of BioNanoScience, Kavli Institute of Nanoscience, Delft University of Technology, Delft, Netherlands

23. Biological Physics Research Group, Clarendon Laboratory, Department of Physics, University of Oxford, Oxford, United Kingdom

24. School of Physics, Georgia Institute of Technology, Atlanta, United States

25. Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, United States

26. School of Chemistry, Seoul National University, Seoul, Republic of Korea

27. Department of Chemistry, Pennsylvania State University, University Park, United States

28. Departments of Biology and Chemistry, Johannes Gutenberg University, Mainz, Germany

29. Institute of Molecular Biology (IMB), Mainz, Germany

30. Centre de Biologie Structurale (CBS), CNRS, INSERM, Universitié de Montpellier, Montpellier, France

31. Institüt of Biophysics, Ulm University, Ulm, Germany

32. Department of Biophysics, Johns Hopkins University, Baltimore, United States

33. Department of Biochemistry and Department of Physics, University of Zurich, Zurich, Switzerland

34. Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, United States

35. Physical Chemistry, Department of Chemistry, Center for Nanoscience (CeNS), Center for Integrated Protein Science Munich (CIPSM) and Nanosystems Initiative Munich (NIM), Ludwig-Maximilians-Universität, München, Germany

36. Warwick Medical School, University of Warwick, Coventry, United Kingdom

37. Biological Optical Microscopy Platform (BOMP), University of Melbourne, Parkville, Australia

38. College of Chemistry and Molecular Engineering, PKU-Tsinghua Center for Life Sciences, Beijing National Laboratory for Molecular Sciences, Peking University, Beijing, China

39. Department of Molecular Biosciences, Northwestern University, Evanston, United States

40. Department of Physiology, CaliforniaNanoSystems Institute, University of California, Los Angeles, Los Angeles, United States

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.

Funder

National Institutes of Health

National Institute of Diabetes and Digestive and Kidney Diseases

National Science Foundation

Human Frontier Science Program

European Research Council

Deutsche Forschungsgemeinschaft

Wellcome Trust

Swiss National Science Foundation

Biotechnology and Biological Sciences Research Council

Royal Society

Agence Nationale de la Recherche

Israel Science Foundation

National Research Foundation of Korea

Independent Fund Denmark

National Key Research and Development Program of China

UHasselt BOF fund

Milner Fund

KU Leuven Special Research Fund

Carlsbergfondet

Villum Fonden

Novo Nordisk

Ludwig-Maximilians-Universität München

Carolina Cancer Center of Nanotechnology Excellence

University of Melbourne

Searle Scholars Program

University of Zurich

EPSRC

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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