DOI: 10.7554/elife.03600. Structure of catalase determined by MicroED

Structure of catalase determined by MicroED

10.7554/elife.03600

Crossref journal-article

eLife Sciences Publications, Ltd

eLife (4374)

Abstract

MicroED is a recently developed method that uses electron diffraction for structure determination from very small three-dimensional crystals of biological material. Previously we used a series of still diffraction patterns to determine the structure of lysozyme at 2.9 Å resolution with MicroED (<xref ref-type="bibr" rid="bib26">Shi et al., 2013</xref>). Here we present the structure of bovine liver catalase determined from a single crystal at 3.2 Å resolution by MicroED. The data were collected by continuous rotation of the sample under constant exposure and were processed and refined using standard programs for X-ray crystallography. The ability of MicroED to determine the structure of bovine liver catalase, a protein that has long resisted atomic analysis by traditional electron crystallography, demonstrates the potential of this method for structure determination.

Bibliography

Nannenga, B. L., Shi, D., Hattne, J., Reyes, F. E., & Gonen, T. (2014). Structure of catalase determined by MicroED. ELife, 3. CLOCKSS.

Authors 5

Brent L Nannenga (first)
Dan Shi (additional)
Johan Hattne (additional)
Francis E Reyes (additional)
Tamir Gonen (additional)

References 32 Referenced 112

10.1107/S0907444909052925 / Acta Crystallographica Section D, Biological Crystallography / PHENIX: a comprehensive Python-based system for macromolecular structure solution by Adams (2010)
10.1016/J.Jsb.2009.11.014 / Journal of Structural Biology / The resolution dependence of optimal exposures in liquid nitrogen temperature electron cryomicroscopy of catalase crystals by Baker (2010)
10.1107/S0907444910048675 / Acta Crystallographica Section D, Biological Crystallography / iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM by Battye (2011)
10.1107/S0907444904016427 / Acta Crystallographica Section D, Biological Crystallography / Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT by Blanc (2004)
10.1107/S0907444909042073 / Acta Crystallographica Section D, Biological Crystallography / MolProbity: all-atom structure validation for macromolecular crystallography by Chen (2010)
10.1107/S0907444906022116 / Acta Crystallographica Section D, Biological Crystallography / The Buccaneer software for automated model building. 1. Tracing protein chains by Cowtan (2006)
10.1107/S0567739475000423 / Acta Crystallographica Section D, Biological Crystallography / Electron-diffraction from single, fully-hydrated, ox liver catalase microcrystals by Dorset (1975a)
10.1107/S0021889875009430 / Journal of Applied Crystallography / Thickness measurements of wet protein crystals in electron-microscope by Dorset (1975b)
10.1107/S0907444910007493 / Acta Crystallographica Section D, Biological Crystallography / Features and development of Coot by Emsley (2010)
10.1107/S0907444905036693 / Acta Crystallographica Section D, Biological Crystallography / Scaling and assessment of data quality by Evans (2006)
10.1107/S090744491003982x / Acta Crystallographica Section D, Biological Crystallography / An introduction to data reduction: space-group determination, scaling and intensity statistics by Evans (2011)
10.1107/S0907444913000061 / Acta Crystallographica Section D, Biological Crystallography / How good are my data and what is the resolution? by Evans (2013)
10.1073/pnas.82.6.1604 / Proceedings of the National Academy of Sciences of USA / The NADPH binding site on beef liver catalase by Fita (1985)
10.1021/Cg101518f / Crystal Growth and Design / Polymer-induced heteronucleation for protein single crystal growth: structural elucidation of bovine liver catalase and concanavalin a forms by Foroughi (2011)
10.1016/0304-3991(89)90021-1 / Ultramicroscopy / 3-Dimensional reconstructions from incomplete data - interpretability of density maps at atomic resolution by Glaeser (1989)
10.1007/978-1-62703-176-9_9 / Methods in Molecular Biology / The collection of high-resolution electron diffraction data by Gonen (2013)
10.1073/pnas.81.14.4343 / Proceedings of the National Academy of Sciences of USA / Catalase: a tetrameric enzyme with four tightly bound molecules of NADPH by Kirkman (1984)
10.1107/S0907444999007052 / Acta Crystallographica Section D, Biological Crystallography / Structure of orthorhombic crystals of beef liver catalase by Ko (1999)
10.1007/978-1-4020-6316-9_4 / NATO Science Series II: Mathematics, Physics and Chemistry / Processing diffraction data with MOSFLM by Leslie (2007)
10.1016/S0022-2836(67)80042-1 / Journal of Molecular Biology / Crystal structure of bovine liver catalase - a combined study by x-ray diffraction and electron microscopy by Longley (1967)
10.1126/Science.177.4045.268 / Science / Electron-diffraction of wet proteins - catalase by Matricardi (1972)
10.1107/S0907444996012255 / Acta Crystallographica Section D, Biological Crystallography / Refinement of macromolecular structures by the maximum-likelihood method by Murshudov (1997)
10.1038/nmeth.3043 / Nature Methods / High-resolution structure determination by continuous-rotation data collection in MicroED by Nannenga (2014)
10.1002/jcc.20084 / Journal of Computational Chemistry / UCSF Chimera–a visualization system for exploratory research and analysis by Pettersen (2004)
10.1021/bi200130r / Biochemistry / Interaction of nitric oxide with catalase: structural and kinetic analysis by Purwar (2011)
10.7554/eLife.01345 / eLife / Three-dimensional electron crystallography of protein microcrystals by Shi (2013)
10.1016/S0021-9258(18)74274-9 / The Journal of Biological Chemistry / Crystalline catalase by Sumner (1937)
10.1107/S0907444906046233 / Acta Crystallographica Section D, Biological Crystallography / Ligand identification using electron-density map correlations by Terwilliger (2007)
10.1107/S0907444906017161 / Acta Crystallographica Section D, Biological Crystallography / Automated ligand fitting by core-fragment fitting and extension into density by Terwilliger (2006)
10.1016/S0022-2836(75)80111-2 / Journal of Molecular Biology / Beef liver catalase structure: interpretation of electron micrographs by Unwin (1975)
10.1016/0022-2836(75)90212-0 / Journal of Molecular Biology / Molecular structure determination by electron microscopy of unstained crystalline specimens by Unwin (1975)
10.1107/S0021889897006766 / Journal of Applied Crystallography / MOLREP: an automated program for molecular replacement by Vagin (1997)

Dates

Type	When
Created	10 years, 10 months ago (Oct. 10, 2014, 5:30 a.m.)
Deposited	1 year, 10 months ago (Oct. 11, 2023, 8:47 p.m.)
Indexed	3 weeks, 1 day ago (July 30, 2025, 1:08 p.m.)
Issued	10 years, 10 months ago (Oct. 10, 2014)
Published	10 years, 10 months ago (Oct. 10, 2014)
Published Online	10 years, 10 months ago (Oct. 10, 2014)

Funders 2

Howard Hughes Medical Institute 10.13039/100000011
Region: Americas
pri (Research institutes and centers)
Labels2
1. Howard Hughes Medical Institute Inc
2. HHMI
Howard Hughes Medical Institute 10.13039/100000011
Region: Americas
pri (Research institutes and centers)
Labels2
1. Howard Hughes Medical Institute Inc
2. HHMI

BibTeX

@article{Nannenga_2014, title={Structure of catalase determined by MicroED}, volume={3}, ISSN={2050-084X}, url={http://dx.doi.org/10.7554/elife.03600}, DOI={10.7554/elife.03600}, journal={eLife}, publisher={eLife Sciences Publications, Ltd}, author={Nannenga, Brent L and Shi, Dan and Hattne, Johan and Reyes, Francis E and Gonen, Tamir}, year={2014}, month=oct }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        30
      ]
    ],
    "date-time": "2025-07-30T17:08:21Z",
    "timestamp": 1753895301516,
    "version": "3.41.2"
  },
  "reference-count": 32,
  "publisher": "eLife Sciences Publications, Ltd",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2014,
            10,
            10
          ]
        ],
        "date-time": "2014-10-10T00:00:00Z",
        "timestamp": 1412899200000
      },
      "content-version": "vor",
      "delay-in-days": 0,
      "URL": "http://creativecommons.org/licenses/by/4.0/"
    },
    {
      "start": {
        "date-parts": [
          [
            2014,
            10,
            10
          ]
        ],
        "date-time": "2014-10-10T00:00:00Z",
        "timestamp": 1412899200000
      },
      "content-version": "am",
      "delay-in-days": 0,
      "URL": "http://creativecommons.org/licenses/by/4.0/"
    },
    {
      "start": {
        "date-parts": [
          [
            2014,
            10,
            10
          ]
        ],
        "date-time": "2014-10-10T00:00:00Z",
        "timestamp": 1412899200000
      },
      "content-version": "tdm",
      "delay-in-days": 0,
      "URL": "http://creativecommons.org/licenses/by/4.0/"
    },
    {
      "start": {
        "date-parts": [
          [
            2014,
            10,
            10
          ]
        ],
        "date-time": "2014-10-10T00:00:00Z",
        "timestamp": 1412899200000
      },
      "content-version": "vor",
      "delay-in-days": 0,
      "URL": "http://creativecommons.org/licenses/by/4.0/"
    },
    {
      "start": {
        "date-parts": [
          [
            2014,
            10,
            10
          ]
        ],
        "date-time": "2014-10-10T00:00:00Z",
        "timestamp": 1412899200000
      },
      "content-version": "am",
      "delay-in-days": 0,
      "URL": "http://creativecommons.org/licenses/by/4.0/"
    },
    {
      "start": {
        "date-parts": [
          [
            2014,
            10,
            10
          ]
        ],
        "date-time": "2014-10-10T00:00:00Z",
        "timestamp": 1412899200000
      },
      "content-version": "tdm",
      "delay-in-days": 0,
      "URL": "http://creativecommons.org/licenses/by/4.0/"
    }
  ],
  "funder": [
    {
      "DOI": "10.13039/100000011",
      "name": "Howard Hughes Medical Institute",
      "doi-asserted-by": "publisher",
      "id": [
        {
          "id": "10.13039/100000011",
          "id-type": "DOI",
          "asserted-by": "publisher"
        }
      ]
    },
    {
      "DOI": "10.13039/100000011",
      "name": "Howard Hughes Medical Institute",
      "doi-asserted-by": "publisher",
      "id": [
        {
          "id": "10.13039/100000011",
          "id-type": "DOI",
          "asserted-by": "publisher"
        }
      ]
    }
  ],
  "content-domain": {
    "domain": [
      "www.elifesciences.org"
    ],
    "crossmark-restriction": false
  },
  "abstract": "<jats:p>MicroED is a recently developed method that uses electron diffraction for structure determination from very small three-dimensional crystals of biological material. Previously we used a series of still diffraction patterns to determine the structure of lysozyme at 2.9 \u00c5 resolution with MicroED (&lt;xref ref-type=\"bibr\" rid=\"bib26\"&gt;Shi et al., 2013&lt;/xref&gt;). Here we present the structure of bovine liver catalase determined from a single crystal at 3.2 \u00c5 resolution by MicroED. The data were collected by continuous rotation of the sample under constant exposure and were processed and refined using standard programs for X-ray crystallography. The ability of MicroED to determine the structure of bovine liver catalase, a protein that has long resisted atomic analysis by traditional electron crystallography, demonstrates the potential of this method for structure determination.</jats:p>",
  "DOI": "10.7554/elife.03600",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2014,
        10,
        10
      ]
    ],
    "date-time": "2014-10-10T09:30:25Z",
    "timestamp": 1412933425000
  },
  "source": "Crossref",
  "is-referenced-by-count": 112,
  "title": "Structure of catalase determined by MicroED",
  "prefix": "10.7554",
  "volume": "3",
  "author": [
    {
      "given": "Brent L",
      "family": "Nannenga",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States"
        }
      ]
    },
    {
      "given": "Dan",
      "family": "Shi",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States"
        }
      ]
    },
    {
      "ORCID": "https://orcid.org/0000-0002-8936-0912",
      "authenticated-orcid": true,
      "given": "Johan",
      "family": "Hattne",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States"
        }
      ]
    },
    {
      "given": "Francis E",
      "family": "Reyes",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States"
        }
      ]
    },
    {
      "given": "Tamir",
      "family": "Gonen",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States"
        }
      ]
    }
  ],
  "member": "4374",
  "published-online": {
    "date-parts": [
      [
        2014,
        10,
        10
      ]
    ]
  },
  "reference": [
    {
      "key": "bib1",
      "doi-asserted-by": "publisher",
      "first-page": "213",
      "DOI": "10.1107/S0907444909052925",
      "article-title": "PHENIX: a comprehensive Python-based system for macromolecular structure solution",
      "volume": "66",
      "author": "Adams",
      "year": "2010",
      "journal-title": "Acta Crystallographica Section D, Biological Crystallography"
    },
    {
      "key": "bib2",
      "doi-asserted-by": "publisher",
      "first-page": "431",
      "DOI": "10.1016/J.Jsb.2009.11.014",
      "article-title": "The resolution dependence of optimal exposures in liquid nitrogen temperature electron cryomicroscopy of catalase crystals",
      "volume": "169",
      "author": "Baker",
      "year": "2010",
      "journal-title": "Journal of Structural Biology"
    },
    {
      "key": "bib3",
      "doi-asserted-by": "publisher",
      "first-page": "271",
      "DOI": "10.1107/S0907444910048675",
      "article-title": "iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM",
      "volume": "67",
      "author": "Battye",
      "year": "2011",
      "journal-title": "Acta Crystallographica Section D, Biological Crystallography"
    },
    {
      "key": "bib4",
      "doi-asserted-by": "publisher",
      "first-page": "2210",
      "DOI": "10.1107/S0907444904016427",
      "article-title": "Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT",
      "volume": "60",
      "author": "Blanc",
      "year": "2004",
      "journal-title": "Acta Crystallographica Section D, Biological Crystallography"
    },
    {
      "key": "bib5",
      "doi-asserted-by": "publisher",
      "first-page": "12",
      "DOI": "10.1107/S0907444909042073",
      "article-title": "MolProbity: all-atom structure validation for macromolecular crystallography",
      "volume": "66",
      "author": "Chen",
      "year": "2010",
      "journal-title": "Acta Crystallographica Section D, Biological Crystallography"
    },
    {
      "key": "bib6",
      "doi-asserted-by": "publisher",
      "first-page": "1002",
      "DOI": "10.1107/S0907444906022116",
      "article-title": "The Buccaneer software for automated model building. 1. Tracing protein chains",
      "volume": "62",
      "author": "Cowtan",
      "year": "2006",
      "journal-title": "Acta Crystallographica Section D, Biological Crystallography"
    },
    {
      "key": "bib7",
      "doi-asserted-by": "publisher",
      "first-page": "210",
      "DOI": "10.1107/S0567739475000423",
      "article-title": "Electron-diffraction from single, fully-hydrated, ox liver catalase microcrystals",
      "volume": "31",
      "author": "Dorset",
      "year": "1975a",
      "journal-title": "Acta Crystallographica Section D, Biological Crystallography"
    },
    {
      "key": "bib8",
      "doi-asserted-by": "publisher",
      "first-page": "12",
      "DOI": "10.1107/S0021889875009430",
      "article-title": "Thickness measurements of wet protein crystals in electron-microscope",
      "volume": "8",
      "author": "Dorset",
      "year": "1975b",
      "journal-title": "Journal of Applied Crystallography"
    },
    {
      "key": "bib9",
      "doi-asserted-by": "publisher",
      "first-page": "486",
      "DOI": "10.1107/S0907444910007493",
      "article-title": "Features and development of Coot",
      "volume": "66",
      "author": "Emsley",
      "year": "2010",
      "journal-title": "Acta Crystallographica Section D, Biological Crystallography"
    },
    {
      "key": "bib10",
      "doi-asserted-by": "publisher",
      "first-page": "72",
      "DOI": "10.1107/S0907444905036693",
      "article-title": "Scaling and assessment of data quality",
      "volume": "62",
      "author": "Evans",
      "year": "2006",
      "journal-title": "Acta Crystallographica Section D, Biological Crystallography"
    },
    {
      "key": "bib11",
      "doi-asserted-by": "publisher",
      "first-page": "282",
      "DOI": "10.1107/S090744491003982x",
      "article-title": "An introduction to data reduction: space-group determination, scaling and intensity statistics",
      "volume": "67",
      "author": "Evans",
      "year": "2011",
      "journal-title": "Acta Crystallographica Section D, Biological Crystallography"
    },
    {
      "key": "bib12",
      "doi-asserted-by": "publisher",
      "first-page": "1204",
      "DOI": "10.1107/S0907444913000061",
      "article-title": "How good are my data and what is the resolution?",
      "volume": "69",
      "author": "Evans",
      "year": "2013",
      "journal-title": "Acta Crystallographica Section D, Biological Crystallography"
    },
    {
      "key": "bib13",
      "doi-asserted-by": "publisher",
      "first-page": "1604",
      "DOI": "10.1073/pnas.82.6.1604",
      "article-title": "The NADPH binding site on beef liver catalase",
      "volume": "82",
      "author": "Fita",
      "year": "1985",
      "journal-title": "Proceedings of the National Academy of Sciences of USA"
    },
    {
      "key": "bib14",
      "doi-asserted-by": "publisher",
      "first-page": "1294",
      "DOI": "10.1021/Cg101518f",
      "article-title": "Polymer-induced heteronucleation for protein single crystal growth: structural elucidation of bovine liver catalase and concanavalin a forms",
      "volume": "11",
      "author": "Foroughi",
      "year": "2011",
      "journal-title": "Crystal Growth and Design"
    },
    {
      "key": "bib15",
      "doi-asserted-by": "publisher",
      "first-page": "307",
      "DOI": "10.1016/0304-3991(89)90021-1",
      "article-title": "3-Dimensional reconstructions from incomplete data - interpretability of density maps at atomic resolution",
      "volume": "27",
      "author": "Glaeser",
      "year": "1989",
      "journal-title": "Ultramicroscopy"
    },
    {
      "key": "bib16",
      "doi-asserted-by": "publisher",
      "first-page": "153",
      "DOI": "10.1007/978-1-62703-176-9_9",
      "article-title": "The collection of high-resolution electron diffraction data",
      "volume": "955",
      "author": "Gonen",
      "year": "2013",
      "journal-title": "Methods in Molecular Biology"
    },
    {
      "key": "bib17",
      "doi-asserted-by": "publisher",
      "first-page": "4343",
      "DOI": "10.1073/pnas.81.14.4343",
      "article-title": "Catalase: a tetrameric enzyme with four tightly bound molecules of NADPH",
      "volume": "81",
      "author": "Kirkman",
      "year": "1984",
      "journal-title": "Proceedings of the National Academy of Sciences of USA"
    },
    {
      "key": "bib18",
      "doi-asserted-by": "publisher",
      "first-page": "1383",
      "DOI": "10.1107/S0907444999007052",
      "article-title": "Structure of orthorhombic crystals of beef liver catalase",
      "volume": "55",
      "author": "Ko",
      "year": "1999",
      "journal-title": "Acta Crystallographica Section D, Biological Crystallography"
    },
    {
      "key": "bib19",
      "doi-asserted-by": "publisher",
      "first-page": "41",
      "DOI": "10.1007/978-1-4020-6316-9_4",
      "article-title": "Processing diffraction data with MOSFLM",
      "volume": "245",
      "author": "Leslie",
      "year": "2007",
      "journal-title": "NATO Science Series II: Mathematics, Physics and Chemistry"
    },
    {
      "key": "bib20",
      "doi-asserted-by": "publisher",
      "first-page": "323",
      "DOI": "10.1016/S0022-2836(67)80042-1",
      "article-title": "Crystal structure of bovine liver catalase - a combined study by x-ray diffraction and electron microscopy",
      "volume": "30",
      "author": "Longley",
      "year": "1967",
      "journal-title": "Journal of Molecular Biology"
    },
    {
      "key": "bib21",
      "doi-asserted-by": "publisher",
      "first-page": "268",
      "DOI": "10.1126/Science.177.4045.268",
      "article-title": "Electron-diffraction of wet proteins - catalase",
      "volume": "177",
      "author": "Matricardi",
      "year": "1972",
      "journal-title": "Science"
    },
    {
      "key": "bib22",
      "doi-asserted-by": "publisher",
      "first-page": "240",
      "DOI": "10.1107/S0907444996012255",
      "article-title": "Refinement of macromolecular structures by the maximum-likelihood method",
      "volume": "53",
      "author": "Murshudov",
      "year": "1997",
      "journal-title": "Acta Crystallographica Section D, Biological Crystallography"
    },
    {
      "key": "bib23",
      "doi-asserted-by": "publisher",
      "first-page": "927",
      "DOI": "10.1038/nmeth.3043",
      "article-title": "High-resolution structure determination by continuous-rotation data collection in MicroED",
      "volume": "11",
      "author": "Nannenga",
      "year": "2014",
      "journal-title": "Nature Methods"
    },
    {
      "key": "bib24",
      "doi-asserted-by": "publisher",
      "first-page": "1605",
      "DOI": "10.1002/jcc.20084",
      "article-title": "UCSF Chimera\u2013a visualization system for exploratory research and analysis",
      "volume": "25",
      "author": "Pettersen",
      "year": "2004",
      "journal-title": "Journal of Computational Chemistry"
    },
    {
      "key": "bib25",
      "doi-asserted-by": "publisher",
      "first-page": "4491",
      "DOI": "10.1021/bi200130r",
      "article-title": "Interaction of nitric oxide with catalase: structural and kinetic analysis",
      "volume": "50",
      "author": "Purwar",
      "year": "2011",
      "journal-title": "Biochemistry"
    },
    {
      "key": "bib26",
      "doi-asserted-by": "publisher",
      "first-page": "e01345",
      "DOI": "10.7554/eLife.01345",
      "article-title": "Three-dimensional electron crystallography of protein microcrystals",
      "volume": "2",
      "author": "Shi",
      "year": "2013",
      "journal-title": "eLife"
    },
    {
      "key": "bib27",
      "doi-asserted-by": "crossref",
      "first-page": "417",
      "DOI": "10.1016/S0021-9258(18)74274-9",
      "article-title": "Crystalline catalase",
      "volume": "121",
      "author": "Sumner",
      "year": "1937",
      "journal-title": "The Journal of Biological Chemistry"
    },
    {
      "key": "bib28",
      "doi-asserted-by": "publisher",
      "first-page": "101",
      "DOI": "10.1107/S0907444906046233",
      "article-title": "Ligand identification using electron-density map correlations",
      "volume": "63",
      "author": "Terwilliger",
      "year": "2007",
      "journal-title": "Acta Crystallographica Section D, Biological Crystallography"
    },
    {
      "key": "bib29",
      "doi-asserted-by": "publisher",
      "first-page": "915",
      "DOI": "10.1107/S0907444906017161",
      "article-title": "Automated ligand fitting by core-fragment fitting and extension into density",
      "volume": "62",
      "author": "Terwilliger",
      "year": "2006",
      "journal-title": "Acta Crystallographica Section D, Biological Crystallography"
    },
    {
      "key": "bib30",
      "doi-asserted-by": "publisher",
      "first-page": "235",
      "DOI": "10.1016/S0022-2836(75)80111-2",
      "article-title": "Beef liver catalase structure: interpretation of electron micrographs",
      "volume": "98",
      "author": "Unwin",
      "year": "1975",
      "journal-title": "Journal of Molecular Biology"
    },
    {
      "key": "bib31",
      "doi-asserted-by": "publisher",
      "first-page": "425",
      "DOI": "10.1016/0022-2836(75)90212-0",
      "article-title": "Molecular structure determination by electron microscopy of unstained crystalline specimens",
      "volume": "94",
      "author": "Unwin",
      "year": "1975",
      "journal-title": "Journal of Molecular Biology"
    },
    {
      "key": "bib32",
      "doi-asserted-by": "publisher",
      "first-page": "1022",
      "DOI": "10.1107/S0021889897006766",
      "article-title": "MOLREP: an automated program for molecular replacement",
      "volume": "30",
      "author": "Vagin",
      "year": "1997",
      "journal-title": "Journal of Applied Crystallography"
    }
  ],
  "container-title": "eLife",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://cdn.elifesciences.org/articles/03600/elife-03600-v1.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://cdn.elifesciences.org/articles/03600/elife-03600-v1.xml",
      "content-type": "application/xml",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://elifesciences.org/articles/03600",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        10,
        12
      ]
    ],
    "date-time": "2023-10-12T00:47:00Z",
    "timestamp": 1697071620000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://elifesciences.org/articles/03600"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2014,
        10,
        10
      ]
    ]
  },
  "references-count": 32,
  "alternative-id": [
    "10.7554/eLife.03600"
  ],
  "URL": "http://dx.doi.org/10.7554/eLife.03600",
  "relation": {
    "references": [
      {
        "id-type": "uri",
        "id": "http://www.pdb.org/pdb/explore/explore.do?structureId=3nwl",
        "asserted-by": "subject"
      },
      {
        "id-type": "uri",
        "id": "http://www.pdb.org/pdb/explore/explore.do?structureId=4blc",
        "asserted-by": "subject"
      },
      {
        "id-type": "uri",
        "id": "http://www.pdb.org/pdb/explore/explore.do?structureId=3rgp",
        "asserted-by": "subject"
      }
    ],
    "has-review": [
      {
        "id-type": "doi",
        "id": "10.7554/eLife.03600.012",
        "asserted-by": "object"
      },
      {
        "id-type": "doi",
        "id": "10.7554/eLife.03600.011",
        "asserted-by": "object"
      }
    ]
  },
  "ISSN": [
    "2050-084X"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        2014,
        10,
        10
      ]
    ]
  },
  "assertion": [
    {
      "value": "2014-06-06",
      "order": 0,
      "name": "received",
      "label": "Received",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "2014-09-28",
      "order": 1,
      "name": "accepted",
      "label": "Accepted",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "2014-10-10",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ],
  "article-number": "e03600"
}