Crystal structure of the integral membrane diacylglycerol kinase

Nature

Volumn 497, Issue 7450, 2013, Pages 521-524

  Li, Dianfan ^a   Lyons, Joseph A ^a   Pye, Valerie E ^a,c   Vogeley, Lutz ^a   Aragão, David ^a,d   Kenyon, Colin P ^b   Shah, Syed T A ^a   Doherty, Christine ^a,e   Aherne, Margaret ^a   Caffrey, Martin ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b DSI CSIR Nanotechnology Innovation Centre   (South Africa)

^c IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^d AUSTRALIAN SYNCHROTRON   (Australia)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; DIACYLGLYCEROL KINASE;

ALCOHOL; BACTERIUM; CELL ORGANELLE; CRYSTAL STRUCTURE; ENZYME ACTIVITY; MEMBRANE; PHOSPHORITE; POLYSACCHARIDE; PROTEIN; SOLUBILIZATION;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BIOPHYSICS; CRYSTAL STRUCTURE; CRYSTALLIZATION; CYTOSOL; ENZYME CONFORMATION; ENZYME STRUCTURE; MOLECULAR DOCKING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN PHOSPHORYLATION; PROTEIN QUATERNARY STRUCTURE;

ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEINS; CATALYTIC DOMAIN; CELL MEMBRANE; CRYSTALLOGRAPHY, X-RAY; DIACYLGLYCEROL KINASE; ENZYME ACTIVATION; ENZYME STABILITY; LIPIDS; MAGNESIUM; MEMBRANE PROTEINS; MODELS, MOLECULAR; MUTANT PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; ZINC;

NEGIBACTERIA;

EID: 84878145235     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12179     Document Type: Article

References (50)

1. Van Horn, W. D. & Sanders, C. R. Prokaryotic diacylglycerol kinase and undecaprenol kinase. Annu. Rev. Biophys. 41, 81-101 (2012).
2. Schneider, E. G. & Kennedy, E. P. Phosphorylation of ceramide by diglyceride kinase preparations from Escherichia coli. J. Biol. Chem. 248, 3739-3741 (1973).
3. Badola, P.&Sanders, C. R. Escherichia coli diacylglycerol kinase is an evolutionarily optimized membrane enzyme and catalyzes direct phosphoryl transfer. J. Biol. Chem. 272, 24176-24182 (1997).
4. Lau, F. W., Chen, X. & Bowie, J. U. Active sites of diacylglycerol kinase from Escherichia coli are shared between subunits. Biochemistry 38, 5521-5527 (1999).
5. Pilot, J. D., East, J. M. & Lee, A. G. Effects of bilayer thickness on the activity of diacylglycerol kinase of Escherichia coli. Biochemistry 40, 8188-8195 (2001).
6. Lahiri, S., Brehs, M., Olschewski, D. & Becker, C. F. Total chemical synthesis of an integral membrane enzyme: diacylglycerol kinase from Escherichia coli. Angew. Chem. Int. Edn Engl. 50, 3988-3992 (2011).
7. Sanders, C. R. et al. Escherichia coli diacylglycerol kinase is an alpha-helical polytopic membrane protein and can spontaneously insert into preformed lipid vesicles. Biochemistry 35, 8610-8618 (1996).
8. Gorzelle, B. M. et al. Reconstitutive refolding of diacylglycerol kinase, an integral membrane protein. Biochemistry 38, 16373-16382 (1999).
9. Vinogradova, O.,Badola,P., Czerski, L.,Sonnichsen, F. D.&Sanders, C. R. Escherichia coli diacylglycerol kinase: a case study in the application of solutionNMR methods to an integral membrane protein. Biophys. J. 72, 2688-2701 (1997).
10. Nagy, J. K., Lau, F. W., Bowie, J. U.&Sanders, C. R.Mapping the oligomeric interface of diacylglycerol kinase by engineered thiol cross-linking: homologous sites in the transmembrane domain. Biochemistry 39, 4154-4164 (2000).
11. Wen, J., Chen, X. & Bowie, J. U. Exploring the allowed sequence space of a membrane protein. Nature Struct. Biol. 3, 141-148 (1996).
12. Smith, R. L., O'Toole, J. F., Maguire, M. E. & Sanders, C. R. Membrane topology of Escherichia coli diacylglycerol kinase. J. Bacteriol. 176, 5459-5465 (1994).
13. Zhou, Y. & Bowie, J. U. Building a thermostable membrane protein. J. Biol. Chem. 275, 6975-6979 (2000).
14. Van Horn, W. D. et al. Solution nuclear magnetic resonance structure of membrane-integral diacylglycerol kinase. Science 324, 1726-1729 (2009).
15. Lorch, M. et al. How to prepare membrane proteins for solid-state NMR: A case study onthe a-helical integralmembrane protein diacylglycerol kinase fromE. coli. ChemBioChem 6, 1693-1700 (2005).
16. Caffrey, M., Li, D. & Dukkipati, A. Membrane protein structure determination using crystallography and lipidic mesophases: recent advances and successes. Biochemistry 51, 6266-6288 (2012).
17. Caffrey, M., Lyons, J., Smyth, T. & Hart, D. J. Monoacylglycerols: The workhorse lipids for crystallizing membrane proteins in mesophases. Curr. Top. Membr. 63, 83-108 (2009).
18. Li, D., Shah, S. T. A.&Caffrey, M.Host lipid and temperature asimportant screening variables for crystallizingintegralmembraneproteins in lipidicmesophases. Trials with diacylglycerol kinase. Cryst. Growth Des. http://dx.doi.org/10.1021/cg400254v (2013).
19. Walsh, J. P., Fahrner, L. & Bell, R. M. sn-1,2-diacylglycerol kinase of Escherichia coli. Diacylglycerol analogues define specificity and mechanism. J. Biol. Chem. 265, 4374-4381 (1990).
20. Bohnenberger, E. & Sandermann, H. Jr. Lipid dependence of diacylglycerol kinase from Escherichia coli. Eur. J. Biochem. 132, 645-650 (1983).
21. Li, D. & Caffrey, M. Lipid cubic phase as a membrane mimetic for integral membrane protein enzymes. Proc. Natl Acad. Sci. USA 108, 8639-8644 (2011).
22. Matte, A. & Delbaere, L. T. J. ATP-binding motifs. eLS http://dx.doi.org/10.1002/9780470015902.a0003050.pub2 (2010).
23. Krissinel, E. On the relationship between sequence and structure similarities in proteomics. Bioinformatics 23, 717-723 (2007).
24. Ullrich, S. J., Hellmich, U. A., Ullrich, S.&Glaubitz, C. Interfacial enzymekinetics of a membrane bound kinase analyzed by real-time MAS-NMR. Nature Chem. Biol. 7, 263-270 (2011).
25. Walsh, J. P. & Bell, R. M. sn-1,2-diacylglycerol kinase of Escherichia coli. Mixed micellar analysis of the phospholipid cofactor requirement and divalent cation dependence. J. Biol. Chem. 261, 6239-6247 (1986).
26. Martin, J. W., Yan, A. K., Bailey-Kellogg, C., Zhou, P. & Donald, B. R. A geometric arrangement algorithm for structure determination of symmetric protein homooligomers from NOEs and RDCs. J. Comput. Biol. 18, 1507-1523 (2011).
27. Martin, J. W., Yan, A. K., Bailey-Kellogg, C., Zhou, P. & Donald, B. R. A graphical method for analyzing distance restraints using residual dipolar couplings for structure determination of symmetric protein homo-oligomers. Protein Sci. 20, 970-985 (2011).
28. Lomize, M. A., Pogozheva, I. D., Joo, H.,Mosberg, H. I.& Lomize, A. L. OPMdatabase andPPMweb server: resources for positioning of proteins inmembranes. Nucleic Acids Res. 40, 370-376 (2012).
29. Doublié, S. Production of selenomethionyl proteins in prokaryotic and eukaryotic expression systems. Methods Mol. Biol. 363, 91-108 (2007).
30. Caffrey, M. & Porter, C. Crystallizing membrane proteins for structure determination using lipidic mesophases. J. Vis. Exp. 45, e1712 (2010).
31. Li, D., Boland, C., Walsh, K. & Caffrey, M. Use of a robot for high-throughput crystallization of membrane proteins in lipidic mesophases. J. Vis. Exp. 67, e4000 (2012).
32. Li, D., Boland, C., Aragao, D., Walsh, K. & Caffrey, M. Harvesting and cryo-cooling crystals of membrane proteins grown in lipidic mesophases for structure determination by macromolecular crystallography. J. Vis. Exp. 67, e4001 (2012).
33. Fischetti, R. F. et al. Mini-beam collimator enables microcrystallography experiments on standard beamlines. J. Synchrotron Radiat. 16, 217-225 (2009).
34. Evans, G., Axford, D. & Owen, R. L. The design of macromolecular crystallography diffraction experiments. Acta Crystallogr. D 67, 261-270 (2011).
35. Cherezov, V. et al. Rastering strategy for screening and centring of microcrystal samples of human membrane proteins with a sub-10 mm size X-ray synchrotron beam. J. R. Soc. Interface 6 (suppl. 5), S587-S597 (2009).
36. Winter, G. xia2: an expert system for macromolecular crystallography data reduction. J. Appl. Crystallogr. 43, 186-190 (2010).
37. Kabsch, W. XDS. Acta Crystallogr. D 66, 125-132 (2010).
38. Evans, P. Scaling and assessment of data quality. Acta Crystallogr. D 62, 72-82 (2006).
39. Stokes-Rees, I. & Sliz, P. Protein structure determination by exhaustive search of Protein Data Bank derived databases. Proc. Natl. Acad. Sci. USA 107, 21476-21481 (2010).
40. Long, F., Vagin, A. A., Young, P. & Murshudov, G. N. BALBES: a molecularreplacement pipeline. Acta Crystallogr. D 64, 125-132 (2008).
41. Hendrickson, W. A., Horton, J. R. & LeMaster, D. M. Selenomethionyl proteins produced for analysis by multiwavelength anomalous diffraction (MAD): a vehicle for direct determination of three-dimensional structure. EMBO J. 9, 1665-1672 (1990).
42. Sheldrick, G. M. Experimental phasing withSHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr. D 66, 479-485 (2010).
43. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221 (2010).
44. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486-501 (2010).
45. Painter, J. & Merritt, E. A. TLSMD web server for the generation of multi-group TLS models. J. Appl. Crystallogr. 39, 109-111 (2006).
46. McCoy, A. J. et al.Phaser crystallographic software. J.Appl. Crystallogr.40, 658-674 (2007).
47. Jones, T. A., Zou, J.-Y.,Cowan, S. W.&Kjeldgaard,M.Improvedmethodsfor building proteinmodels in electron densitymaps and the location of errors in thesemodels. Acta Crystallogr. A 47, 110-119 (1991).
48. Blanc, E. et al. Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr. D 60, 2210-2221 (2004).
49. Baker, N. A., Sept, D., Joseph, S., Holst, M. J. & McCammon, J. A. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl Acad. Sci. USA 98, 10037-10041 (2001).
50. Diller, D. J. & Merz, K. M. Jr. High throughput docking for library design and library prioritization. Proteins 43, 113-124 (2001).