Data publication with the structural biology data grid supports live analysis

Peter A Meyer¹, Stephanie Socias¹, Jason Key¹, Elizabeth Ransey¹, Emily C Tjon¹, Alejandro Buschiazzo^{2

3}, Ming Lei⁴, Chris Botka⁵, James Withrow⁶, David Neau⁶, Kanagalaghatta Rajashankar⁶, Karen S Anderson⁷, Richard H Baxter⁸, Stephen C Blacklow¹, Titus J Boggon⁷, Alexandre M J J Bonvin⁹, Dominika Borek¹⁰, Tom J Brett¹¹, Amedeo Caflisch¹², Chung-I Chang¹³, Walter J Chazin¹⁴, Kevin D Corbett^{15

16}, Michael S Cosgrove¹⁷, Sean Crosson¹⁸, Sirano Dhe-Paganon¹⁹, Enrico Di Cera²⁰, Catherine L Drennan²¹, Michael J Eck^{1

19}, Brandt F Eichman²², Qing R Fan²³, Adrian R Ferré-D'Amaré²⁴, J Christopher Fromme²⁵, K Christopher Garcia^{26

27

28}, Rachelle Gaudet²⁹, Peng Gong³⁰, Stephen C Harrison^{1

31

32}, Ekaterina E Heldwein³³, Zongchao Jia³⁴, Robert J Keenan¹⁸, Andrew C Kruse¹, Marc Kvansakul³⁵, Jason S McLellan³⁶, Yorgo Modis³⁷, Yunsun Nam³⁸, Zbyszek Otwinowski¹⁰, Emil F Pai^{39

40}, Pedro José Barbosa Pereira⁴¹, Carlo Petosa⁴², C S Raman⁴³, Tom A Rapoport⁴⁴, Antonina Roll-Mecak^{45

46}, Michael K Rosen⁴⁷, Gabby Rudenko⁴⁸, Joseph Schlessinger⁴⁹, Thomas U Schwartz⁵⁰, Yousif Shamoo⁵¹, Holger Sondermann⁵², Yizhi J Tao⁵¹, Niraj H Tolia⁵³, Oleg V Tsodikov⁵⁴, Kenneth D Westover⁵⁵, Hao Wu^{1

56}, Ian Foster⁵⁷, James S Fraser⁵⁸, Filipe R N C Maia^{59

60}, Tamir Gonen⁶¹, Tom Kirchhausen^{62

63}, Kay Diederichs⁶⁴, Mercè Crosas⁶⁵, Piotr Sliz¹

Affiliations

¹ Department of Biological Chemistry and Molecular Pharmacology, Boston, Massachusetts 02115, USA.
² Laboratory of Molecular &Structural Microbiology, Institut Pasteur de Montevideo, Montevideo 11400, Uruguay.
³ Department of Structural Biology &Chemistry, Institut Pasteur, 75015 Paris, France.
⁴ Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China.
⁵ Harvard Medical School, Boston, Massachusetts 02115, USA.
⁶ NE-CAT and Department of Chemistry and Chemical Biology, Cornell University, Building 436E, Argonne National Laboratory, 9700S. Cass Avenue, Argonne, Illinois 60439, USA.
⁷ Departments of Pharmacology and Molecular Biophysics and Biochemistry, Yale University School of Medicine, New Haven, Connecticut 06520, USA.
⁸ Department of Chemistry, Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520, USA.
⁹ Bijvoet Center, Faculty of Science, Utrecht University, 3584 CH Utrecht, The Netherlands.
¹⁰ Departments of Biophysics and Biochemistry, University of Texas Southwestern Medical Center, Dallas, Texas 75390, USA.
¹¹ Department of Internal Medicine, Washington University School of Medicine, St Louis, Missouri 63110, USA.
¹² Department of Biochemistry, University of Zurich, CH-8057 Zurich, Switzerland.
¹³ Institute of Biological Chemistry, Academia Sinica, Taipei 11529, Taiwan.
¹⁴ Departments of Biochemistry and Chemistry, Center for Structural Biology, Vanderbilt University, Nashville, Tennessee 37232, USA.
¹⁵ Ludwig Institute for Cancer Research, San Diego Branch, La Jolla, California 92093, USA.
¹⁶ Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, California 92093, USA.
¹⁷ Department of Biochemistry and Molecular Biology, SUNY Upstate Medical University, Syracuse, New York 13210, USA.
¹⁸ Department of Biochemistry and Molecular Biology, University of Chicago, Chicago, Illinois 60637, USA.
¹⁹ Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, Massachusetts 02115, USA.
²⁰ Edward A. Doisy Department of Biochemistry and Molecular Biology, Saint Louis University School of Medicine, St Louis, Missouri 63104, USA.
²¹ Departments of Chemistry and Biology and the Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA.
²² Department of Biological Sciences and Center for Structural Biology, Vanderbilt University, Nashville, Tennessee 37235, USA.
²³ Departments of Pharmacology and Pathology and Cell Biology, Columbia University, New York, New York 10032, USA.
²⁴ Laboratory of RNA Biophysics, National Heart, Lung and Blood Institute, NIH, Bethesda, Maryland 20892, USA.
²⁵ Department of Molecular Biology and Genetics, Weill Institute for Cell and Molecular Biology, Cornell University, Ithaca, New York 14853, USA.
²⁶ Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, California 94305, USA.
²⁷ Department of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, California 94305, USA.
²⁸ Department of Structural Biology, Stanford University School of Medicine, Stanford, California 94305, USA.
²⁹ Department of Molecular and Cellular Biology, Harvard University, Cambridge, Massachusetts 02138, USA.
³⁰ Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China.
³¹ Howard Hughes Medical Institute, Harvard Medical School, Boston, Massachusetts 02115, USA.
³² Laboratory of Molecular Medicine, Boston Children's Hospital, Harvard Medical School, Boston, Massachusetts 02115, USA.
³³ Department of Molecular Biology and Microbiology, Tufts University School of Medicine, Boston, Massachusetts 02111, USA.
³⁴ Department of Biomedical and Molecular Sciences, Queen's University, Kingston, Ontario, Canada K7M 3G5.
³⁵ Department of Biochemistry and Genetics, La Trobe University, Melbourne, Victoria 3086, Australia.
³⁶ Department of Biochemistry, Geisel School of Medicine at Dartmouth, Hanover, New Hampshire 03755, USA.
³⁷ Department of Medicine, University of Cambridge, MRC Laboratory of Molecular Biology, Francis Crick Avenue, Cambridge CB2 0QH, UK.
³⁸ University of Texas, Southwestern Medical Center, Dallas, Texas 75390, USA.
³⁹ Departments of Biochemistry, Medical Biophysics and Molecular Genetics, University of Toronto, Toronto, Ontario, Canada M5S 1A8.
⁴⁰ Campbell Family Institute for Cancer Research, Ontario Cancer Institute/University Health Network, Toronto, Ontario, Canada M5G 2M9.
⁴¹ IBMC-Instituto de Biologia Molecular e Celular and Instituto de Investigação e Inovação em Saúde, Universidade do Porto, 4150 Porto, Portugal.
⁴² Université Grenoble Alpes/CNRS/CEA, Institut de Biologie Structurale, 38027 Grenoble, France.
⁴³ Department of Pharmaceutical Sciences, University of Maryland, Baltimore, Maryland 21201, USA.
⁴⁴ Howard Hughes Medical Institute and Harvard Medical School, Department of Cell Biology, Boston, Massachusetts 02115, USA.
⁴⁵ Cell Biology and Biophysics Unit, Porter Neuroscience Research Center, National Institute of Neurological Disorders and Stroke, Bethesda, Maryland 20892, USA.
⁴⁶ National Heart, Lung and Blood Institute, Bethesda, Maryland 20892, USA.
⁴⁷ Department of Biophysics and Howard Hughes Medical Institute, University of Texas Southwestern Medical Center, Dallas, Texas 75390, USA.
⁴⁸ Department of Pharmacology and Toxicology, Sealy Center for Structural Biology and Molecular Biophysics, University of Texas Medical Branch, Galveston, Texas 77555, USA.
⁴⁹ Department of Pharmacology, Yale University School of Medicine, New Haven, Connecticut 06520, USA.
⁵⁰ Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA.
⁵¹ Department of BioSciences, Rice University, Houston, Texas 77005, USA.
⁵² Department of Molecular Medicine, College of Veterinary Medicine, Cornell University, Ithaca, New York 14853, USA.
⁵³ Department of Molecular Microbiology, Washington University School of Medicine, St Louis, Missouri 63110, USA.
⁵⁴ Department of Pharmaceutical Sciences, College of Pharmacy, University of Kentucky, Lexington, Kentucky 40536, USA.
⁵⁵ Departments of Biochemistry and Radiation Oncology, University of Texas, Southwestern Medical Center, Dallas, Texas 75390, USA.
⁵⁶ Program in Cellular and Molecular Medicine, Boston Children's Hospital, Boston, Massachusetts 02115, USA.
⁵⁷ Mathematics and Computer Science Division, Argonne National Laboratory, Argonne, Illinois, and Department of Computer Science, University of Chicago, Chicago, Illinois 60637, USA.
⁵⁸ Department of Bioengineering and Therapeutic Sciences, University of California San Francisco, San Francisco, California 94158, USA.
⁵⁹ Laboratory of Molecular Biophysics, Department of Cell and Molecular Biology, Uppsala University, Husargatan 3 (Box 596), SE-751 24 Uppsala, Sweden.
⁶⁰ NERSC, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA.
⁶¹ Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia 20147 USA.
⁶² Program in Cellular and Molecular Medicine and Department of Pediatrics, Boston Children's Hospital, Boston, Massachusetts 02115, USA.
⁶³ Departments of Cell Biology, Harvard Medical School, Boston, Massachusetts 02115, USA.
⁶⁴ Department of Biology, University of Konstanz, D-78457 Konstanz, Germany.
⁶⁵ Institute for Quantitative Social Science, Harvard University, Cambridge, Massachusetts, 02138, USA.

PMID: 26947396
PMCID: PMC4786681
DOI: 10.1038/ncomms10882

Data publication with the structural biology data grid supports live analysis

Peter A Meyer et al. Nat Commun. 2016.

. 2016 Mar 7:7:10882.

doi: 10.1038/ncomms10882.

Authors

Affiliations

¹ Department of Biological Chemistry and Molecular Pharmacology, Boston, Massachusetts 02115, USA.
² Laboratory of Molecular &Structural Microbiology, Institut Pasteur de Montevideo, Montevideo 11400, Uruguay.
³ Department of Structural Biology &Chemistry, Institut Pasteur, 75015 Paris, France.
⁴ Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China.
⁵ Harvard Medical School, Boston, Massachusetts 02115, USA.
⁶ NE-CAT and Department of Chemistry and Chemical Biology, Cornell University, Building 436E, Argonne National Laboratory, 9700S. Cass Avenue, Argonne, Illinois 60439, USA.
⁷ Departments of Pharmacology and Molecular Biophysics and Biochemistry, Yale University School of Medicine, New Haven, Connecticut 06520, USA.
⁸ Department of Chemistry, Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520, USA.
⁹ Bijvoet Center, Faculty of Science, Utrecht University, 3584 CH Utrecht, The Netherlands.
¹⁰ Departments of Biophysics and Biochemistry, University of Texas Southwestern Medical Center, Dallas, Texas 75390, USA.
¹¹ Department of Internal Medicine, Washington University School of Medicine, St Louis, Missouri 63110, USA.
¹² Department of Biochemistry, University of Zurich, CH-8057 Zurich, Switzerland.
¹³ Institute of Biological Chemistry, Academia Sinica, Taipei 11529, Taiwan.
¹⁴ Departments of Biochemistry and Chemistry, Center for Structural Biology, Vanderbilt University, Nashville, Tennessee 37232, USA.
¹⁵ Ludwig Institute for Cancer Research, San Diego Branch, La Jolla, California 92093, USA.
¹⁶ Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, California 92093, USA.
¹⁷ Department of Biochemistry and Molecular Biology, SUNY Upstate Medical University, Syracuse, New York 13210, USA.
¹⁸ Department of Biochemistry and Molecular Biology, University of Chicago, Chicago, Illinois 60637, USA.
¹⁹ Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, Massachusetts 02115, USA.
²⁰ Edward A. Doisy Department of Biochemistry and Molecular Biology, Saint Louis University School of Medicine, St Louis, Missouri 63104, USA.
²¹ Departments of Chemistry and Biology and the Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA.
²² Department of Biological Sciences and Center for Structural Biology, Vanderbilt University, Nashville, Tennessee 37235, USA.
²³ Departments of Pharmacology and Pathology and Cell Biology, Columbia University, New York, New York 10032, USA.
²⁴ Laboratory of RNA Biophysics, National Heart, Lung and Blood Institute, NIH, Bethesda, Maryland 20892, USA.
²⁵ Department of Molecular Biology and Genetics, Weill Institute for Cell and Molecular Biology, Cornell University, Ithaca, New York 14853, USA.
²⁶ Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, California 94305, USA.
²⁷ Department of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, California 94305, USA.
²⁸ Department of Structural Biology, Stanford University School of Medicine, Stanford, California 94305, USA.
²⁹ Department of Molecular and Cellular Biology, Harvard University, Cambridge, Massachusetts 02138, USA.
³⁰ Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China.
³¹ Howard Hughes Medical Institute, Harvard Medical School, Boston, Massachusetts 02115, USA.
³² Laboratory of Molecular Medicine, Boston Children's Hospital, Harvard Medical School, Boston, Massachusetts 02115, USA.
³³ Department of Molecular Biology and Microbiology, Tufts University School of Medicine, Boston, Massachusetts 02111, USA.
³⁴ Department of Biomedical and Molecular Sciences, Queen's University, Kingston, Ontario, Canada K7M 3G5.
³⁵ Department of Biochemistry and Genetics, La Trobe University, Melbourne, Victoria 3086, Australia.
³⁶ Department of Biochemistry, Geisel School of Medicine at Dartmouth, Hanover, New Hampshire 03755, USA.
³⁷ Department of Medicine, University of Cambridge, MRC Laboratory of Molecular Biology, Francis Crick Avenue, Cambridge CB2 0QH, UK.
³⁸ University of Texas, Southwestern Medical Center, Dallas, Texas 75390, USA.
³⁹ Departments of Biochemistry, Medical Biophysics and Molecular Genetics, University of Toronto, Toronto, Ontario, Canada M5S 1A8.
⁴⁰ Campbell Family Institute for Cancer Research, Ontario Cancer Institute/University Health Network, Toronto, Ontario, Canada M5G 2M9.
⁴¹ IBMC-Instituto de Biologia Molecular e Celular and Instituto de Investigação e Inovação em Saúde, Universidade do Porto, 4150 Porto, Portugal.
⁴² Université Grenoble Alpes/CNRS/CEA, Institut de Biologie Structurale, 38027 Grenoble, France.
⁴³ Department of Pharmaceutical Sciences, University of Maryland, Baltimore, Maryland 21201, USA.
⁴⁴ Howard Hughes Medical Institute and Harvard Medical School, Department of Cell Biology, Boston, Massachusetts 02115, USA.
⁴⁵ Cell Biology and Biophysics Unit, Porter Neuroscience Research Center, National Institute of Neurological Disorders and Stroke, Bethesda, Maryland 20892, USA.
⁴⁶ National Heart, Lung and Blood Institute, Bethesda, Maryland 20892, USA.
⁴⁷ Department of Biophysics and Howard Hughes Medical Institute, University of Texas Southwestern Medical Center, Dallas, Texas 75390, USA.
⁴⁸ Department of Pharmacology and Toxicology, Sealy Center for Structural Biology and Molecular Biophysics, University of Texas Medical Branch, Galveston, Texas 77555, USA.
⁴⁹ Department of Pharmacology, Yale University School of Medicine, New Haven, Connecticut 06520, USA.
⁵⁰ Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA.
⁵¹ Department of BioSciences, Rice University, Houston, Texas 77005, USA.
⁵² Department of Molecular Medicine, College of Veterinary Medicine, Cornell University, Ithaca, New York 14853, USA.
⁵³ Department of Molecular Microbiology, Washington University School of Medicine, St Louis, Missouri 63110, USA.
⁵⁴ Department of Pharmaceutical Sciences, College of Pharmacy, University of Kentucky, Lexington, Kentucky 40536, USA.
⁵⁵ Departments of Biochemistry and Radiation Oncology, University of Texas, Southwestern Medical Center, Dallas, Texas 75390, USA.
⁵⁶ Program in Cellular and Molecular Medicine, Boston Children's Hospital, Boston, Massachusetts 02115, USA.
⁵⁷ Mathematics and Computer Science Division, Argonne National Laboratory, Argonne, Illinois, and Department of Computer Science, University of Chicago, Chicago, Illinois 60637, USA.
⁵⁸ Department of Bioengineering and Therapeutic Sciences, University of California San Francisco, San Francisco, California 94158, USA.
⁵⁹ Laboratory of Molecular Biophysics, Department of Cell and Molecular Biology, Uppsala University, Husargatan 3 (Box 596), SE-751 24 Uppsala, Sweden.
⁶⁰ NERSC, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA.
⁶¹ Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia 20147 USA.
⁶² Program in Cellular and Molecular Medicine and Department of Pediatrics, Boston Children's Hospital, Boston, Massachusetts 02115, USA.
⁶³ Departments of Cell Biology, Harvard Medical School, Boston, Massachusetts 02115, USA.
⁶⁴ Department of Biology, University of Konstanz, D-78457 Konstanz, Germany.
⁶⁵ Institute for Quantitative Social Science, Harvard University, Cambridge, Massachusetts, 02138, USA.

PMID: 26947396
PMCID: PMC4786681
DOI: 10.1038/ncomms10882

Abstract

Access to experimental X-ray diffraction image data is fundamental for validation and reproduction of macromolecular models and indispensable for development of structural biology processing methods. Here, we established a diffraction data publication and dissemination system, Structural Biology Data Grid (SBDG; data.sbgrid.org), to preserve primary experimental data sets that support scientific publications. Data sets are accessible to researchers through a community driven data grid, which facilitates global data access. Our analysis of a pilot collection of crystallographic data sets demonstrates that the information archived by SBDG is sufficient to reprocess data to statistics that meet or exceed the quality of the original published structures. SBDG has extended its services to the entire community and is used to develop support for other types of biomedical data sets. It is anticipated that access to the experimental data sets will enhance the paradigm shift in the community towards a much more dynamic body of continuously improving data analysis.

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Figures

**Figure 1. Data collection statistics for the pilot subset of 112 data sets.**
(a,b) Data sets were collected from synchrotrons on four continents (in addition to laboratory sources, which are not broken down geographically) and originate from eleven synchrotron facilities: Advanced Light Source, Advanced Photon Source, Australian Synchrotron, Cornell High Energy Synchrotron Source, Canadian Light Source, European Synchrotron Radiation Facility, National Synchrotron Light Source, National Synchrotron Radiation Research Center, Swiss Light Source, Shanghai Synchrotron Radiation Facility, and Stanford Synchrotron Radiation Lightsource. World map image courtesy of the U.S. Geological Survey. (c) Breakdown of data sets collected at the Advanced Photon Source beamlines. (d) Data sets cover a range of detector types, including Area Detector Systems Corporation M300, Q210 and Q315, Rayonix MarMosaic, Dectris Pilatus 2M and 6M, R-AXIS HTC, and MAR345.

**Figure 2. Estimation of storage requirements for different stages of the structural biology pipeline, based on the SBDG pilot collection.**
For structure factor amplitudes and PDB models file sizes were obtained from a subset of 96 PDB depositions derived from the pilot data sets. On average, SBDG stores 1.26 data sets per PDB file. Numbers in red indicated the estimated storage requirements to accommodate data sets for 100,000 structures. We estimate that for each primary data set, additional 100 data sets are collected at national facilities. Primary data refers to original experimental diffraction images supporting the derived structural model, as distinguished from all experimental data (screening images, inferior quality data sets, and so on). For crystallographic experiments, reduced data refers to the integrated intensities (or amplitudes, which do not materially affect storage requirements).

**Figure 3. Organized display of data collections at SBDG.**
(a) Graphical view of Laboratory and Institutional Collections within the SBDG; (b) PV structure viewer, displaying a published model with links to its two primary deposited data sets.

**Figure 4. SBDG persistent data set landing page (the target of a DOI resolver for a published data set).**
Data set metadata are displayed, as are instructions for downloading and verifying the data set.

**Figure 5. Experimental data flow and publication.**
(a) Flow of Primary Experimental Data. Data sets collected at synchrotrons are moved to end-users' computers for processing and structure determination. Subsequently refined macromolecular models are deposited at PDB and primary data is uploaded to SBDG. From SBDG, data sets are replicated to DAA centres and eventually copied to DAA Satellites. End-users can access data sets by downloading from DAA centres and by direct access from Satellites. (b) Flowchart for data publication.

**Figure 6. DataCite metadata schema used for primary data sets within the SBDG.**
Information associated with the DOI record for a primary data set through the EZID system.

**Figure 7. Data publication guidelines.**
(a) Flowchart illustrating publication guidelines incorporating software and data citations. (b) Data Citation guidelines, adapted from Dataverse Best Practices Guidelines that were developed based on Force 11 Joint Declaration of Data Citation Principles.

**Figure 8. Reprocessing of X-ray diffraction data sets.**
(a) Analysis of 110 X-ray diffraction data sets that supported previously published PDB coordinates. Most of the failures (represented in red) were due to inaccurate or incomplete image-header information. In several of these cases, depositors provided annotations correcting this information; (b) Comparison of resolution determined by automated *xia2* reprocessing with published resolution. Includes data sets not used for final refinement of published structures; (c) Shift in direct beam position from image headers and refined value following successful reprocessing with *xia2*.

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References

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Data publication with the structural biology data grid supports live analysis

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Data publication with the structural biology data grid supports live analysis

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