Skip to main content Accessibility help

Anticipating innovations in structural biology

  • Helen M. Berman (a1), Catherine L. Lawson (a1), Brinda Vallat (a1) and Margaret J. Gabanyi (a1)


In this review, we describe how the interplay among science, technology and community interests contributed to the evolution of four structural biology data resources. We present the method by which data deposited by scientists are prepared for worldwide distribution, and argue that data archiving in a trusted repository must be an integral part of any scientific investigation.


Corresponding author

Author for correspondence: Helen M. Berman, E-mail:


Hide All
Alber, F et al. (2007 a) Determining the architectures of macromolecular assemblies. Nature 450, 683694.
Alber, F et al. (2007 b) The molecular architecture of the nuclear pore complex. Nature 450, 695701.
Allen, FH et al. (1973) Cambridge crystallographic data centre. II. Structural data file. Journal of Chemical Documentation 13, 119123.
Arnold, E and Rossmann, MG (1988) The use of molecular-replacement phases for the refinement of the human rhinovirus 14 structure. Acta Crystallographica Section A 44, 270282.
Ban, N et al. (2000) The complete atomic structure of the large ribosomal subunit at a 2·4 Å resolution. Science 289, 905920.
Barinaga, M (1989) The missing crystallography data. Science 245, 11791181.
Belsom, A et al. (2016) Serum albumin domain structures in human blood serum by mass spectrometry and computational biology. Molecular and Cellular Proteomics 15, 11051116.
Berman, HM, Henrick, K and Nakamura, H (2003) Announcing the worldwide Protein Data Bank. Nature Structural Biology 10, 980.
Berman, HM et al. (2000) The Protein Data Bank. Nucleic Acids Research 28, 235242.
Berman, HM et al. (2009) The protein structure initiative structural genomics knowledgebase. Nucleic Acids Research 37, D365D368.
Berman, HM et al. (2016) A data dictionary for archiving integrative/hybrid models. In 66th Annual Meeting of the American Crystallographic Association, Denver, CO, USA, pp. 85-SA.
Blake, CCF et al. (1965) Structure of hen egg-white lysozyme. A three dimensional Fourier synthesis at 2 Å resolution. Nature 206, 757761.
Bordoli, L and Schwede, T (2012) Automated protein structure modeling with SWISS-MODEL workspace and the Protein Model Portal. Methods in Molecular Biology 857, 107136.
Bruno, IJ et al. (2004) Retrieval of crystallographically-derived molecular geometry information. Journal of Chemical Information and Computer Sciences 44, 21332144.
Burley, SK et al. (2017) PDB-Dev: a prototype system for depositing integrative/hybrid structural models. Structure 25, 13171318.
Carter, AP et al. (2000) Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 407, 340348.
Chen, VB et al. (2010) Molprobity: all-atom structure validation for macromolecular crystallography. Acta Crystallographica Section D: Biological Crystallography 66, 1221.
Chiu, W et al. (2005) Electron cryomicroscopy of biological machines at subnanometer resolution. Structure 13, 363372.
Dessailly, BH et al. (2009) PSI-2: structural genomics to cover protein domain family space. Structure 17, 869881.
Dickerson, RE et al. (1982) The anatomy of a-DNA, B-DNA, and Z-DNA. Science 216, 475485.
Dominguez, C, Boelens, R and Bonvin, AM (2003) HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. Journal of the American Chemical Society 125, 17311737.
Dong, Y et al. (2017) Antibody-induced uncoating of human rhinovirus B14. Proceedings of the National Academy of Sciences of the United States of America 114, 80178022.
Dutta, S et al. (2014) Improving the representation of peptide-like inhibitor and antibiotic molecules in the Protein Data Bank. Biopolymers 101, 659668.
Editorial (2003) A database for ’em. Nature Structural Biology 10(5), 313.
Erickson, JW et al. (1985) The structure of a T = 1 icosahedral empty particle from southern bean mosaic virus. Science 229, 625629.
Fitzgerald, PMD et al. (2005) 4·5 macromolecular dictionary (mmCIF). In Hall, SR and McMahon, B (eds), International Tables for Crystallography G. Definition and Exchange of Crystallographic Data. Dordrecht, The Netherlands: Springer, pp. 295443.
Flippen-Andersen, J, Gabanyi, MJ, Chen, L, Sala, R, Westbrook, JD and Berman, HM (2010) BioSync: a structural biologist's guide to high energy data collection facilities,
Gabanyi, MJ et al. (2011) The Structural Biology Knowledgebase: a portal to protein structures, sequences, functions, and methods. Journal of Structural and Functional Genomics 12, 4554.
Gifford, LK et al. (2012) The protein structure initiative structural biology knowledgebase technology portal: a structural biology web resource. Journal of Structural and Functional Genomics 13, 5762.
Goddard, TD et al. (2018) UCSF chimerax: meeting modern challenges in visualization and analysis. Protein Science 27, 1425.
Goodsell, D (2000a) Nucleosome. PDB-101 Molecule of the Month series. doi:10.2210/rcsb_pdb/mom_2000_7.
Goodsell, D (2000b) Ribosomal subunits. PDB-101 Molecule of the Month series. doi:10.2210/rcsb_pdb/mom_2000_10.
Goodsell, D (2001) DNA. PDB-101 Molecule of the Month series. doi:10.2210/rcsb_pdb/mom_2001_11.
Goodsell, DS et al. (2015) The RCSB PDB “molecule of the month”: inspiring a molecular view of biology. PLoS Biology 13, e1002140.
Gore, S et al. (2017) Validation of the structures in the Protein Data Bank. Structure 25, 19161927.
Grabowski, M et al. (2016) The impact of structural genomics: the first quindecennial. Journal of Structural and Functional Genomics 17, 116.
Haas, J and Schwede, T (2013) Model Archive.
Haas, J et al. (2013) The Protein Model Portal – a comprehensive resource for protein structure and model information. Database (Oxford) 2013, bat031.
Hall, SR, Allen, FH and Brown, ID (1991) The Crystallographic Information File (Cif) – a new standard archive file for crystallography. Acta Crystallographica Section A 47, 655685.
Hamlin, RC (1985) Multiwire area X-ray diffractometers. Methods in Enzymology 114, 416452.
Harmsen, A, Leberman, R and Schulz, GE (1976) Comparison of protein crystal diffraction patterns and absolute intensities from synchrotron and conventional x-ray sources. Journal of Molecular Biology 104, 311314.
Henderson, R et al. (1990) Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. Journal of Molecular Biology 213, 899929.
Henderson, R et al. (2012) Outcome of the first electron microscopy validation task force meeting. Structure 20, 205214.
Hendrickson, WA, Smith, JL and Sheriff, S (1985) Direct phase determination based on anomalous scattering. Methods in Enzymology 115, 4155.
Henrick, K et al. (2003) EMDep: a web-based system for the deposition and validation of high-resolution electron microscopy macromolecular structural information. Journal of Structural Biology 144, 228237.
Henrick, K et al. (2008) Remediation of the Protein Data Bank archive. Nucleic Acids Research 36(Database issue), D426D433.
Hope, H (1988) Cryocrystallography of biological macromolecules: a generally applicable method. Acta Crystallographica Section B: Structural Science 44, 2226.
Hopper, P, Harrison, SC and Sauer, RT (1984) Structure of tomato bushy stunt virus. V. Coat protein sequence determination and its structural implications. Journal of Molecular Biology 177, 701713.
Horst, R et al. (2001) NMR structure reveals intramolecular regulation mechanism for pheromone binding and release. Proceedings of the National Academy of Sciences of the United States of America 98, 1437414379.
Howard Hughes Medical Institute (2017).
Hufton, AL (2014) Sharing the structures. In Nature Milestones: Crystallography. (1970s) Open software and crystallographic databases. Nature, Scientific Data.
International Union of Crystallography (1989) Commission on Biological Macromolecules. Acta Crystallographica Section A 45, 658.
Jones, TA (1978) FRODO: a graphic model building and refinement system for macromolecules. Journal of Applied Crystallography 11, 268272.
Kartha, G, Bello, J and Harker, D (1967) Tertiary structure of ribonuclease. Nature 213, 862865.
Kelly, JA et al. (1979) X-ray crystallography of the binding of the bacterial cell wall trisaccharide NAM-NAG-NAM to lysozyme. Nature 282, 875878.
Kendrew, JC et al. (1958) A three-dimensional model of the myoglobin molecule obtained by X-ray analysis. Nature 181, 662666.
Kim, SJ et al. (2014) Integrative structure-function mapping of the nucleoporin nup133 suggests a conserved mechanism for membrane anchoring of the nuclear pore complex. Molecular and Cellular Proteomics 13, 29112926.
Kinjo, AR et al. (2017) Protein Data Bank Japan (PDBj): updated user interfaces, resource description framework, analysis tools for large structures. Nucleic Acids Research 45, D282D288.
Kopp, J and Schwede, T (2004) The SWISS-MODEL Repository of annotated three-dimensional protein structure homology models. Nucleic Acids Research 32, D230D234.
Kuller, A et al. (2002) A biologist's guide to synchrotron facilities: the BioSync web resource. TIBS 27, 213215.
Lawson, CL et al. (2008) Representation of viruses in the remediated PDB archive. Acta Crystallographica Section D: Biological Crystallography 64, 874882.
Lawson, CL et al. (2011) unified data resource for CryoEM. Nucleic Acids Research. 39, D456D464.
Lawson, CL et al. (2016) EMDatabank unified data resource for 3DEM. Nucleic Acids Research 44, D396D403.
Leaver-Fay, A et al. (2011) ROSETTA3: an object-oriented software suite for the simulation and design of macromolecules. Methods in Enzymology 487, 545574.
Liang, YL et al. (2017) Phase-plate cryo-EM structure of a class B GPCR-G-protein complex. Nature 546, 118123.
Liu, Z et al. (2018) Characterizing protein dynamics with integrative use of bulk and single-molecule techniques. Biochemistry 57, 305313.
Loquet, A et al. (2012) Atomic model of the type III secretion system needle. Nature 486, 276279.
Luger, K et al. (1997) Crystal structure of the nucleosome core particle at 2·8 A resolution. Nature 389, 251260.
Matthews, BW (1996) Structural and genetic analysis of the folding and function of T4 lysozyme. FASEB Journal 10, 3541.
Meyer, EF (1997) The first years of the Protein Data Bank. Protein Science 6(7), 15911597.
Montelione, GT et al. (2013) Recommendations of the wwPDB NMR validation task force. Structure 21, 15631570.
Norvell, JC and Berg, JM (2007) Update on the protein structure initiative. Structure 15, 15191522.
Ostrom, E (1990) Governing the Commons: The Evolution of Institutions for Collective Action. Cambridge University Press, Cambridge, United Kingdom.
Patikoglou, GA et al. (1999) TATA element recognition by the TATA box-binding protein has been conserved throughout evolution. Genes and Development 13, 32173230.
Perutz, MF et al. (1960) Structure of haemoglobin: a three-dimensional Fourier synthesis at 5.5 Å resolution, obtained by X-ray analysis. Nature 185, 416422.
Pettersen, EF et al. (2004) UCSF Chimera--a visualization system for exploratory research and analysis. Journal of Computational Chemistry 25, 16051612.
Phillips, DC (1972) Protein crystallography 1971: coming of age. In Cold Spring Harbor Symposia on Quantitative Biology, Cold Spring Harbor: Cold Spring Harbor Laboratory Press 36, 589592.
Pieper, U et al. (2009) MODBASE, a database of annotated comparative protein structure models and associated resources. Nucleic Acids Research 37, D347D354.
Pieper, U et al. (2013) Coordinating the impact of structural genomics on the human alpha-helical transmembrane proteome. Nature Structural and Molecular Biology 20, 135138.
Politis, A et al. (2014) A mass spectrometry-based hybrid method for structural modeling of protein complexes. Nature Methods 11, 403406.
Protein Data Bank. (1971) Crystallography: Protein Data Bank. Nature: New Biology 233, 223223.
Quiocho, FA and Lipscomb, WN (1971) Carboxypeptidase A: a protein and an enzyme. Advances in Protein Chemistry 25, 178.
Read, RJ et al. (2011) A new generation of crystallographic validation tools for the Protein Data Bank. Structure 19, 13951412.
Rich, A and Kim, S-H (1978) The three-dimensional structure of transfer RNA. Scientific American 238, 5262.
Richards, FM (1968) The matching of physical models to three-dimensional electron-density maps: a simple optical device. Journal of Molecular Biology 37, 225230.
Robertus, JD et al. (1974) Structure of yeast phenylalanine tRNA at 3 Å resolution. Nature 250, 546551.
Robinson, PJ et al. (2015) Molecular architecture of the yeast Mediator complex. Elife 4, pii: e08719.
Roh, SH et al. (2017) Subunit conformational variation within individual GroEL oligomers resolved by Cryo-EM. Proceedings of the National Academy of Sciences of the United States of America 114, 82598264.
Rose, PW et al. (2017) The RCSB Protein Data Bank: integrative view of protein, gene and 3D structural information. Nucleic Acids Research 45, D271D281.
Rossmann, MG et al. (2005) Combining X-ray crystallography and electron microscopy. Structure 13, 355362.
Russel, D et al. (2012) Putting the pieces together: integrative modeling platform software for structure determination of macromolecular assemblies. PLoS Biology 10, e1001244.
Sali, A et al. (2015) Outcome of the first wwPDB hybrid/integrative methods task force workshop. Structure 23, 11561167.
Schluenzen, F et al. (2000) Structure of functionally activated small ribosomal subunit at 3·3 Å resolution. Cell 102, 615623.
Schwieters, CD, Bermejo, GA and Clore, GM (2018) Xplor-NIH for molecular structure determination from NMR and other data sources. Protein Science 27, 2640.
Seiler, CY et al. (2014) DNASU plasmid and PSI:Biology-Materials repositories: resources to accelerate biological research. Nucleic Acids Research 42, D1253D1260.
Serra, F et al. (2017) Automatic analysis and 3D-modelling of Hi-C data using TADbit reveals structural features of the fly chromatin colors. PLoS Computational Biology 13, e1005665.
Sharif, H et al. (2017) Cryo-EM structure of the DNA-PK holoenzyme. Proceedings of the National Academy of Sciences of the United States of America 114, 73677372.
Shi, Y et al. (2014) Structural characterization by cross-linking reveals the detailed architecture of a coatomer-related heptameric module from the nuclear pore complex. Molecular and Cellular Proteomics 13, 29272943.
Shi, Y et al. (2015) A strategy for dissecting the architectures of native macromolecular assemblies. Nature Methods 12, 11351138.
Trussart, M et al. (2015) Assessing the limits of restraint-based 3D modeling of genomes and genomic domains. Nucleic Acids Research 43, 34653477.
Twomey, EC et al. (2017) Channel opening and gating mechanism in AMPA-subtype glutamate receptors. Nature 549, 6065.
Ulrich, EL et al. (2008) Biomagresbank. Nucleic Acids Research 36, D402D408.
Vallat, B et al. (2017) A Data Dictionary For Archiving Integrative/Hybrid Models. In 24th IUCr Congress and General Assembly. International Union of Crystallography, Hyderabad, India.
Vallat, B, Webb, B, Westbrook, JD, Sali, A and Berman, HM (2018) Development of a Prototype System for Archiving Integrative/Hybrid Structure Models of Biological Macromolecules. Structure 26 894904.
Van Zundert, GCP, Melquiond, ASJ and Bonvin, A (2015) Integrative modeling of biomolecular complexes: HADDOCKing with cryo-electron microscopy data. Structure 23, 949960.
Velankar, S et al. (2016) PDBe: improved accessibility of macromolecular structure data from PDB and EMDB. Nucleic Acids Research 44, D385D395.
Vinothkumar, KR and Henderson, R (2016). Single particle electron cryomicroscopy: trends, issues and future perspective. Quarterly Reviews of Biophysics 49, e13.
Wan, R et al. (2016). Structure of a yeast catalytic step I spliceosome at 3·4 A resolution. Science 353, 895904.
Ward, AB, Sali, A and Wilson, IA (2013). Biochemistry. Integrative structural biology. Science 339, 913915.
Watson, HC (1969). The stereochemistry of the protein myoglobin. Progress in Stereochemistry 4, 299.
Westbrook, JD and Fitzgerald, PM D. (2009). Chapter 10 The PDB format, mmCIF formats, and other data formats. In Bourne, PE and Gu, J (eds), Structural Bioinformatics, 2nd Edn. Hoboken, NJ: John Wiley & Sons, Inc., pp. 271291.
Wilkinson, MD et al. (2016) The FAIR Guiding Principles for scientific data management and stewardship. Scientific Data 3, 160018.
Wlodawer, A (2002) Rational approach to AIDS drug design through structural biology. Annual Review of Medicine 53, 595614.
Wlodawer, A et al. (2008) Protein crystallography for non-crystallographers, or how to get the best (but not more) from published macromolecular structures. FEBS Journal 275, 121.
Wyckoff, HW et al. (1967) The structure of ribonuclease-S at 6 Å resolution. Journal of Biological Chemistry 242, 37493753.
Young, JY et al. (2017) Onedep: unified wwPDB system for deposition, biocuration, and validation of macromolecular structures in the PDB archive. Structure 25, 536545.


Anticipating innovations in structural biology

  • Helen M. Berman (a1), Catherine L. Lawson (a1), Brinda Vallat (a1) and Margaret J. Gabanyi (a1)


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed