2x5q Citations

The Scottish Structural Proteomics Facility: targets, methods and outputs.


The Scottish Structural Proteomics Facility was funded to develop a laboratory scale approach to high throughput structure determination. The effort was successful in that over 40 structures were determined. These structures and the methods harnessed to obtain them are reported here. This report reflects on the value of automation but also on the continued requirement for a high degree of scientific and technical expertise. The efficiency of the process poses challenges to the current paradigm of structural analysis and publication. In the 5 year period we published ten peer-reviewed papers reporting structural data arising from the pipeline. Nevertheless, the number of structures solved exceeded our ability to analyse and publish each new finding. By reporting the experimental details and depositing the structures we hope to maximize the impact of the project by allowing others to follow up the relevant biology.

Articles - 2x5q mentioned but not cited (2)

  1. Structure and mechanism of the CMR complex for CRISPR-mediated antiviral immunity. Zhang J, Rouillon C, Kerou M, Reeks J, Brugger K, Graham S, Reimann J, Cannone G, Liu H, Albers SV, Naismith JH, Spagnolo L, White MF. Mol. Cell 45 303-313 (2012)
  2. The Scottish Structural Proteomics Facility: targets, methods and outputs. Oke M, Carter LG, Johnson KA, Liu H, McMahon SA, Yan X, Kerou M, Weikart ND, Kadi N, Sheikh MA, Schmelz S, Dorward M, Zawadzki M, Cozens C, Falconer H, Powers H, Overton IM, van Niekerk CA, Peng X, Patel P, Garrett RA, Prangishvili D, Botting CH, Coote PJ, Dryden DT, Barton GJ, Schwarz-Linek U, Challis GL, Taylor GL, White MF, Naismith JH. J. Struct. Funct. Genomics 11 167-180 (2010)

Reviews citing this publication (9)

  1. Targeting adenylate-forming enzymes with designed sulfonyladenosine inhibitors. Lux MC, Standke LC, Tan DS. J. Antibiot. 72 325-349 (2019)
  2. Ironing out siderophore biosynthesis: a review of non-ribosomal peptide synthetase (NRPS)-independent siderophore synthetases. Carroll CS, Moore MM. Crit. Rev. Biochem. Mol. Biol. 53 356-381 (2018)
  3. Type I restriction enzymes and their relatives. Loenen WA, Dryden DT, Raleigh EA, Wilson GG. Nucleic Acids Res. 42 20-44 (2014)
  4. A survey of protein structures from archaeal viruses. Dellas N, Lawrence CM, Young MJ. 3 118-130 (2013)
  5. Genomics and biology of Rudiviruses, a model for the study of virus-host interactions in Archaea. Prangishvili D, Koonin EV, Krupovic M. Biochem. Soc. Trans. 41 443-450 (2013)
  6. Host and viral transcriptional regulators in Sulfolobus: an overview. Contursi P, Fusco S, Limauro D, Fiorentino G. Extremophiles 17 881-895 (2013)
  7. Post-translation modification in Archaea: lessons from Haloferax volcanii and other haloarchaea. Eichler J, Maupin-Furlow J. FEMS Microbiol. Rev. 37 583-606 (2013)
  8. Genomics of bacterial and archaeal viruses: dynamics within the prokaryotic virosphere. Krupovic M, Prangishvili D, Hendrix RW, Bamford DH. Microbiol. Mol. Biol. Rev. 75 610-635 (2011)
  9. Intramolecular isopeptide bonds: protein crosslinks built for stress? Kang HJ, Baker EN. Trends Biochem. Sci. 36 229-237 (2011)

Articles citing this publication (51)

  1. Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin. Zakeri B, Fierer JO, Celik E, Chittock EC, Schwarz-Linek U, Moy VT, Howarth M. Proc. Natl. Acad. Sci. U.S.A. 109 E690-7 (2012)
  2. JLigand: a graphical tool for the CCP4 template-restraint library. Lebedev AA, Young P, Isupov MN, Moroz OV, Vagin AA, Murshudov GN. Acta Crystallogr. D Biol. Crystallogr. 68 431-440 (2012)
  3. Structural and functional characterization of an archaeal clustered regularly interspaced short palindromic repeat (CRISPR)-associated complex for antiviral defense (CASCADE). Lintner NG, Kerou M, Brumfield SK, Graham S, Liu H, Naismith JH, Sdano M, Peng N, She Q, Copié V, Young MJ, White MF, Lawrence CM. J. Biol. Chem. 286 21643-21656 (2011)
  4. The CRISPR associated protein Cas4 Is a 5' to 3' DNA exonuclease with an iron-sulfur cluster. Zhang J, Kasciukovic T, White MF. PLoS ONE 7 e47232 (2012)
  5. A highly unusual thioester bond in a pilus adhesin is required for efficient host cell interaction. Pointon JA, Smith WD, Saalbach G, Crow A, Kehoe MA, Banfield MJ. J. Biol. Chem. 285 33858-33866 (2010)
  6. Structural analysis and optimization of the covalent association between SpyCatcher and a peptide Tag. Li L, Fierer JO, Rapoport TA, Howarth M. J. Mol. Biol. 426 309-317 (2014)
  7. Massive activation of archaeal defense genes during viral infection. Quax TE, Voet M, Sismeiro O, Dillies MA, Jagla B, Coppée JY, Sezonov G, Forterre P, van der Oost J, Lavigne R, Prangishvili D. J. Virol. 87 8419-8428 (2013)
  8. A dimeric Rep protein initiates replication of a linear archaeal virus genome: implications for the Rep mechanism and viral replication. Oke M, Kerou M, Liu H, Peng X, Garrett RA, Prangishvili D, Naismith JH, White MF. J. Virol. 85 925-931 (2011)
  9. De novo missense mutations in the NAA10 gene cause severe non-syndromic developmental delay in males and females. Popp B, Støve SI, Endele S, Myklebust LM, Hoyer J, Sticht H, Azzarello-Burri S, Rauch A, Arnesen T, Reis A. Eur. J. Hum. Genet. 23 602-609 (2015)
  10. NMR spectroscopic and theoretical analysis of a spontaneously formed Lys-Asp isopeptide bond. Hagan RM, Björnsson R, McMahon SA, Schomburg B, Braithwaite V, Bühl M, Naismith JH, Schwarz-Linek U. Angew. Chem. Int. Ed. Engl. 49 8421-8425 (2010)
  11. A ketosynthase homolog uses malonyl units to form esters in cervimycin biosynthesis. Bretschneider T, Zocher G, Unger M, Scherlach K, Stehle T, Hertweck C. Nat. Chem. Biol. 8 154-161 (2012)
  12. Evolution of insect arylalkylamine N-acetyltransferases: structural evidence from the yellow fever mosquito, Aedes aegypti. Han Q, Robinson H, Ding H, Christensen BM, Li J. Proc. Natl. Acad. Sci. U.S.A. 109 11669-11674 (2012)
  13. Multiple nucleic acid cleavage modes in divergent type III CRISPR systems. Zhang J, Graham S, Tello A, Liu H, White MF. Nucleic Acids Res. 44 1789-1799 (2016)
  14. Structure of a dimeric crenarchaeal Cas6 enzyme with an atypical active site for CRISPR RNA processing. Reeks J, Sokolowski RD, Graham S, Liu H, Naismith JH, White MF. Biochem. J. 452 223-230 (2013)
  15. A novel method for synthetic vaccine construction based on protein assembly. Liu Z, Zhou H, Wang W, Tan W, Fu YX, Zhu M. Sci Rep 4 7266 (2014)
  16. Structural insights into the mechanism and inhibition of the β-hydroxydecanoyl-acyl carrier protein dehydratase from Pseudomonas aeruginosa. Moynié L, Leckie SM, McMahon SA, Duthie FG, Koehnke A, Taylor JW, Alphey MS, Brenk R, Smith AD, Naismith JH. J. Mol. Biol. 425 365-377 (2013)
  17. Prespacer processing and specific integration in a Type I-A CRISPR system. Rollie C, Graham S, Rouillon C, White MF. Nucleic Acids Res. 46 1007-1020 (2018)
  18. An internal thioester in a pathogen surface protein mediates covalent host binding. Walden M, Edwards JM, Dziewulska AM, Bergmann R, Saalbach G, Kan SY, Miller OK, Weckener M, Jackson RJ, Shirran SL, Botting CH, Florence GJ, Rohde M, Banfield MJ, Schwarz-Linek U. Elife 4 (2015)
  19. Archaeal Viruses: Diversity, Replication, and Structure. Dellas N, Snyder JC, Bolduc B, Young MJ. Annu Rev Virol 1 399-426 (2014)
  20. Displacement of the canonical single-stranded DNA-binding protein in the Thermoproteales. Paytubi S, McMahon SA, Graham S, Liu H, Botting CH, Makarova KS, Koonin EV, Naismith JH, White MF. Proc. Natl. Acad. Sci. U.S.A. 109 E398-405 (2012)
  21. Functional and structural analysis of the siderophore synthetase AsbB through reconstitution of the petrobactin biosynthetic pathway from Bacillus anthracis. Nusca TD, Kim Y, Maltseva N, Lee JY, Eschenfeldt W, Stols L, Schofield MM, Scaglione JB, Dixon SD, Oves-Costales D, Challis GL, Hanna PC, Pfleger BF, Joachimiak A, Sherman DH. J. Biol. Chem. 287 16058-16072 (2012)
  22. Structure of the archaeal Cascade subunit Csa5: relating the small subunits of CRISPR effector complexes. Reeks J, Graham S, Anderson L, Liu H, White MF, Naismith JH. RNA Biol 10 762-769 (2013)
  23. Disruption of the siderophore-binding desE receptor gene in Streptomyces coelicolor A3(2) results in impaired growth in spite of multiple iron-siderophore transport systems. Tierrafría VH, Ramos-Aboites HE, Gosset G, Barona-Gómez F. Microb Biotechnol 4 275-285 (2011)
  24. Functional characterization of a conserved archaeal viral operon revealing single-stranded DNA binding, annealing and nuclease activities. Guo Y, Kragelund BB, White MF, Peng X. J. Mol. Biol. 427 2179-2191 (2015)
  25. Salt bridges regulate both dimer formation and monomeric flexibility in HdeB and may have a role in periplasmic chaperone function. Wang W, Rasmussen T, Harding AJ, Booth NA, Booth IR, Naismith JH. J. Mol. Biol. 415 538-546 (2012)
  26. Staphylococcus aureus DinG, a helicase that has evolved into a nuclease. McRobbie AM, Meyer B, Rouillon C, Petrovic-Stojanovska B, Liu H, White MF. Biochem. J. 442 77-84 (2012)
  27. Structure of WbdD: a bifunctional kinase and methyltransferase that regulates the chain length of the O antigen in Escherichia coli O9a. Hagelueken G, Huang H, Clarke BR, Lebl T, Whitfield C, Naismith JH. Mol. Microbiol. 86 730-742 (2012)
  28. Structural and functional studies of a 50 kDa antigenic protein from Salmonella enterica serovar Typhi. Choong YS, Lim TS, Chew AL, Aziah I, Ismail A. J. Mol. Graph. Model. 29 834-842 (2011)
  29. Protein-protein interactions leading to recruitment of the host DNA sliding clamp by the hyperthermophilic Sulfolobus islandicus rod-shaped virus 2. Gardner AF, Bell SD, White MF, Prangishvili D, Krupovic M. J. Virol. 88 7105-7108 (2014)
  30. Kinetic Controlled Tag-Catcher Interactions for Directed Covalent Protein Assembly. Tan LL, Hoon SS, Wong FT. PLoS ONE 11 e0165074 (2016)
  31. Computational approaches to selecting and optimising targets for structural biology. Overton IM, Barton GJ. Methods 55 3-11 (2011)
  32. Kinetic Landscape of a Peptide Bond-Forming Prolyl Oligopeptidase. Czekster CM, Naismith JH. Biochemistry 56 2086-2095 (2017)
  33. DNA-Interacting Characteristics of the Archaeal Rudiviral Protein SIRV2_Gp1. Peeters E, Boon M, Rollie C, Willaert RG, Voet M, White MF, Prangishvili D, Lavigne R, Quax TEF. Viruses 9 (2017)
  34. Unraveling the specific regulation of the central pathway for anaerobic degradation of 3-methylbenzoate. Juárez JF, Liu H, Zamarro MT, McMahon S, Liu H, Naismith JH, Eberlein C, Boll M, Carmona M, Díaz E. J. Biol. Chem. 290 12165-12183 (2015)
  35. Coenzyme Q Biosynthesis: Evidence for a Substrate Access Channel in the FAD-Dependent Monooxygenase Coq6. Ismail A, Leroux V, Smadja M, Gonzalez L, Lombard M, Pierrel F, Mellot-Draznieks C, Fontecave M. PLoS Comput. Biol. 12 e1004690 (2016)
  36. Dynamics-function relationship in the catalytic domains of N-terminal acetyltransferases. Abboud A, Bédoucha P, Byška J, Arnesen T, Reuter N. Comput Struct Biotechnol J 18 532-547 (2020)
  37. SpyTag/SpyCatcher Cyclization Enhances the Thermostability of Firefly Luciferase. Si M, Xu Q, Jiang L, Huang H. PLoS ONE 11 e0162318 (2016)
  38. Structure of Thermoplasma volcanium Ard1 belongs to N-acetyltransferase family member suggesting multiple ligand binding modes with acetyl coenzyme A and coenzyme A. Ma C, Pathak C, Jang S, Lee SJ, Nam M, Kim SJ, Im H, Lee BJ. Biochim. Biophys. Acta 1844 1790-1797 (2014)
  39. Structure-activity relationship-based screening of antibiotics against Gram-negative Acinetobacter baumannii. Lee JY, Jeong MC, Jeon D, Lee Y, Lee WC, Kim Y. Bioorg. Med. Chem. 25 372-380 (2017)
  40. Synthetic Biology: A New Tool for the Trade. Zakeri B. Chembiochem 16 2277-2282 (2015)
  41. Characterization of a dual function macrocyclase enables design and use of efficient macrocyclization substrates. Czekster CM, Ludewig H, McMahon SA, Naismith JH. Nat Commun 8 1045 (2017)
  42. New insights about pilus formation in gut-adapted Lactobacillus rhamnosus GG from the crystal structure of the SpaA backbone-pilin subunit. Chaurasia P, Pratap S, von Ossowski I, Palva A, Krishnan V. Sci Rep 6 28664 (2016)
  43. PqsL uses reduced flavin to produce 2-hydroxylaminobenzoylacetate, a preferred PqsBC substrate in alkyl quinolone biosynthesis in Pseudomonas aeruginosa. Drees SL, Ernst S, Belviso BD, Jagmann N, Hennecke U, Fetzner S. J. Biol. Chem. 293 9345-9357 (2018)
  44. An unconventional ligand-binding mechanism of substrate-binding proteins: MD simulation and Markov state model analysis of BtuF. Wang D, Weng J, Wang W. J Comput Chem 40 1440-1448 (2019)
  45. Desferrioxamine biosynthesis: diverse hydroxamate assembly by substrate-tolerant acyl transferase DesC. Ronan JL, Kadi N, McMahon SA, Naismith JH, Alkhalaf LM, Challis GL. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 373 (2018)
  46. Probing the potential of CnaB-type domains for the design of tag/catcher systems. Pröschel M, Kraner ME, Horn AHC, Schäfer L, Sonnewald U, Sticht H. PLoS ONE 12 e0179740 (2017)
  47. Structural analysis and mutant growth properties reveal distinctive enzymatic and cellular roles for the three major L-alanine transaminases of Escherichia coli. Peña-Soler E, Fernandez FJ, López-Estepa M, Garces F, Richardson AJ, Quintana JF, Rudd KE, Coll M, Vega MC. PLoS ONE 9 e102139 (2014)
  48. The rhizoferrin biosynthetic gene in the fungal pathogen Rhizopus delemar is a novel member of the NIS gene family. Carroll CS, Grieve CL, Murugathasan I, Bennet AJ, Czekster CM, Liu H, Naismith J, Moore MM. Int. J. Biochem. Cell Biol. 89 136-146 (2017)
  49. Approaching infinite affinity through engineering of peptide-protein interaction. Keeble AH, Turkki P, Stokes S, Khairil Anuar INA, Rahikainen R, Hytönen VP, Howarth M. Proc. Natl. Acad. Sci. U.S.A. (2019)
  50. Structural insight into substrate and product binding in an archaeal mevalonate kinase. Miller BR, Kung Y. PLoS ONE 13 e0208419 (2018)
  51. The Siderophore Synthetase IucA of the Aerobactin Biosynthetic Pathway Uses an Ordered Mechanism. Mydy LS, Bailey DC, Patel KD, Rice MR, Gulick AM. Biochemistry 59 2143-2153 (2020)