Protein Crystallography from the Perspective of Technology Developments

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Protein Crystallography from the Perspective of Technology Developments Crystallography Reviews ISSN: 0889-311X (Print) 1476-3508 (Online) Journal homepage: http://www.tandfonline.com/loi/gcry20 Protein crystallography from the perspective of technology developments Xiao-Dong Su, Heng Zhang, Thomas C. Terwilliger, Anders Liljas, Junyu Xiao & Yuhui Dong To cite this article: Xiao-Dong Su, Heng Zhang, Thomas C. Terwilliger, Anders Liljas, Junyu Xiao & Yuhui Dong (2015) Protein crystallography from the perspective of technology developments, Crystallography Reviews, 21:1-2, 122-153, DOI: 10.1080/0889311X.2014.973868 To link to this article: http://dx.doi.org/10.1080/0889311X.2014.973868 Published online: 13 Dec 2014. Submit your article to this journal Article views: 304 View related articles View Crossmark data Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=gcry20 Download by: [Peking University] Date: 18 November 2015, At: 02:19 Crystallography Reviews, 2015 Vol. 21, Nos. 1–2, 122–153, http://dx.doi.org/10.1080/0889311X.2014.973868 REVIEW ARTICLE Protein crystallography from the perspective of technology developments Xiao-Dong Sua∗, Heng Zhanga, Thomas C. Terwilligerb, Anders Liljasc, Junyu Xiaoa and Yuhui Dongd aState Key Laboratory of Protein and Plant Gene Research, and Biodynamic Optical Imaging Center (BIOPIC), School of Life Sciences, Peking University, Beijing 100871, People’s Republic of China; bBioscience Division, Los Alamos National Laboratory, Mail Stop M888, Los Alamos, NM 87545, USA; cDepartment of Biochemistry and Structural Biology, Lund University, Lund, Sweden; d Beijing Synchrotron Radiation Facility, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing 100049, People’s Republic of China (Received 2 October 2014; accepted 3 October 2014) Early on, crystallography was a domain of mineralogy and mathematics and dealt mostly with symmetry properties and imaginary crystal lattices. This changed when Wilhelm Conrad Rönt- gen discovered X-rays in 1895, and in 1912, Max von Laue and his associates discovered that X-ray irradiated salt crystals would produce diffraction patterns that could reveal the inter- nal atomic periodicity of the crystals. In the same year, the father-and-son team, Henry and Lawrence Bragg successfully solved the first crystal structure of sodium chloride and the era of modern crystallography began. Protein crystallography (PX) started some 20 years later with the pioneering work of British crystallographers. In the past 50–60 years, the achievements of modern crystallography and particularly those in PX have been due to breakthroughs in theoretical and technical advancements such as phasing and direct methods; to more powerful X-ray sources such as synchrotron radiation; to more sensitive and efficient X-ray detectors; to ever faster computers and to improvements in software. The exponential development of PX has been accelerated by the invention and applications of recombinant DNA technology that can yield nearly any protein of interest in large amounts and with relative ease. Novel meth- ods, informatics platforms and technologies for automation and high-throughput have allowed the development of large-scale, high-efficiency macromolecular crystallography efforts in the field of structural genomics. Very recently, the X-ray free-electron laser sources and its appli- cations in PX have shown great potential for revolutionizing the whole field again in the near future. Keywords: X-ray crystallography; protein crystallization; computer programs and graphics; recombinant DNA techniques; synchrotron radiation (SR); structural genomics (SG); X-ray Downloaded by [Peking University] at 02:19 18 November 2015 free-electron laser (XFEL) Contents PAGE Technology developments for PX 129 Soft technology 129 Theoretical foundations, computational algorithm and software development 129 Theoretical background 129 Computational algorithm 130 Phasing and computational developments 130 Solvent flattening/flipping and density-modification programs 132 *Corresponding author. Email: [email protected] c 2014 Taylor & Francis Crystallography Reviews 123 Computer graphics 132 Structure refinement and structure validation programs 133 Hardware technology 133 Light sources, detectors and computer hardware 133 X-ray light sources 133 SR and XFEL 134 Data collection: detectors and methods 134 Cryo-crystallography 136 Wet-lab technology 136 Protein purification, crystallization and recombinant DNA techniques 136 The developments of wet-lab technologies: protein production and purification 137 Recent and future perspectives 137 SG and XFEL 137 SG 2000–2015 137 Technologies from SG 138 XFEL applications 140 Acknowledgements 143 Funding 143 Notes on contributors 143 References 145 Subject index 153 2014 is celebrated as the International Year of Crystallography (IYCr-2014). About 100 years ago, Max von Laue in Germany and the father-and-son Bragg team (William Henry Bragg and William Lawrence Bragg) in England pioneered the use of X-ray to irradiate crystals for atomic structure determination, and for those pioneering investigations, they were awarded Nobel prizes for physics in the years 1914 and 1915 [1–5] (Table 1). This was the birth of X-ray crystallog- Downloaded by [Peking University] at 02:19 18 November 2015 raphy which has profoundly changed the way we perceive the atomic structures of the world built of organic and inorganic materials and molecules. With the X-ray crystal diffraction tech- nique, one can really ‘see’ the atomic arrangements in a crystal lattice and accurately measure atomic bond distances, bond and dihedral angels and other parameters. This paper will review some important technical developments relevant to crystallography in general and in particular focus on the application of X-ray crystallography to study the structure and function of pro- teins and other bio-macromolecule complexes. X-ray crystallography, though a very specialized field, has received very significant attention from the Nobel committees compared with other similar scientific fields. Table 1 lists the milestone discoveries and technique developments rec- ognized by Nobel prizes related to protein crystallography (PX) and protein structures (X-ray, electron and neutron crystallography). This list does not contain all important contributions that made crystallography as it is today, of course. A recent review on the Nobel-crystallography topics has covered the work of most of the Nobel laureates who made major contributions to crystallography.[6] Our paper will pay attention to other important contributors to PX as well. X-ray crystallography has emerged as one of the most important scientific and technical tools in the twentieth century. Most solid-state matter (rocks and soils) on earth is in the crystalline 124 X.-D. Su et al. Table 1. Nobel prizes as milestones of discoveries and technique developments relevant to PX (including X-ray, electron and neutron crystallography), and to protein structure–function relationships. Year Sub. Nobel laureates Reasons for the prizes 1901 P Germany Wilhelm Conrad Röntgen Discovery of the remarkable rays (X-ray) 1914 P Germany Max von Laue Discovery of the diffraction of X-rays by crystals 1915 P UK Sir William Henry Bragg Analysis of crystal structure by means of X-rays UK: William Lawrence Bragg 1917 P UK Charles Glover Barkla Discovery of the characteristic Röntgen (X-ray) radiation of the elements 1924 P Sweden Karl Manne Georg Siegbahn Discoveries and research in the field of X-ray spectroscopy 1926 C Sweden Theodor Svedberg Development of the analytical ultracentrifuge 1937 P USA Clinton Joseph Davisson Discovery of the diffraction of electrons by crystals UK George Paget Thomson 1939a P USA Ernest Lawrence Invention and development of the cyclotron 1946b C USA James B. Sumner Discovery that enzymes are proteins that can be purified and crystallized and so can viruses USA John Howard Northrop USA Wendell Meredith Stanley 1954 C USA Linus Carl Pauling Research into the nature of the chemical bond 1958 C UK Frederick Sanger Protein sequencing 1962b C UK John Charles Kendrew Protein structure determination UK Max Ferdinand Perutz 1962 PM UK Francis Harry Compton Crick Discovery of DNA double helix USA James Watson UK Maurice Hugh Frederick Wilkins Downloaded by [Peking University] at 02:19 18 November 2015 1964 C UK Dorothy Crowfoot Hodgkin Determination of the structures of penicillin and vitamin B12 1972 C USA Christian Borhmer Anfinsen Principles that govern the folding of protein USA Stanford Moore Principles related to the biological activity of the enzyme USA William Howard Stein 1976 C USA William Nunn Lipscomb Jr. Studies on the structure of boranes 1980 C UK Frederick Sanger Fundamental studies of the biochemistry of nucleic acids and determination of base sequences in nucleic acids (Continued) Crystallography Reviews 125 Table 1. Continued. Year Sub. Nobel laureates Reasons for the prizes USA Paul Berg USA Walter Gilbert 1982 C UK Aaron Klug Development of crys- tallographic electron microscopy 1985 C USA Herbert Aaron Direct methods for the Hauptman determination of crystal structures USA Jerome Karle 1986 P Germany Ernst Ruska Design of the first electron microscope and design of the scanning tunnelling microscope Germany Gerd Binnig Switzerland Heinrich Rohrer 1988 C Germany Johann Determination of the three- Deisenhofer dimensional structure of a photosynthetic reaction centre Germany Robert Huber Germany Hartmut Michel 1992 P Switzerland Georges Charpak Invention
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