Design of a molecular support for cryo-EM structure determination

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 47, 2016, Pages E7456-E7463

  Martin, Thomas G ^a   Bharat, Tanmay A M ^a,b   Joerger, Andreas C ^a,c   Bai, Xiao Chen ^a   Praetorius, Florian ^d   Fersht, Alan R ^a   Dietz, Hendrik ^d   Scheres, Sjors H W ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c GOETHE UNIVERSITY   (Germany)

^d WALTER SCHOTTKY INSTITUT   (Germany)

Author keywords

Cryo EM; DNA origami; P53; Single particle analysis; Structural biology

Indexed keywords

DOUBLE STRANDED DNA; PROTEIN P53; TETRAMER; WATER; DNA; TP53 PROTEIN, HUMAN;

CONFERENCE PAPER; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; DNA SEQUENCE; ESCHERICHIA COLI; ESCHERICHIA COLI BL21; FILM; MACROMOLECULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DNA BINDING; PROTEIN STRUCTURE; CHEMISTRY; HUMAN; METABOLISM; PROCEDURES; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; THREE DIMENSIONAL IMAGING;

CRYOELECTRON MICROSCOPY; DNA; HUMANS; IMAGING, THREE-DIMENSIONAL; MACROMOLECULAR SUBSTANCES; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; TUMOR SUPPRESSOR PROTEIN P53; WATER;

EID: 84996525816     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1612720113     Document Type: Article

References (65)

1. Bai X-C, McMullan G, Scheres SHW (2015) How cryo-EM is revolutionizing structural biology. Trends Biochem Sci 40(1):49-57.
2. Cheng Y, Grigorieff N, Penczek PA, Walz T (2015) A primer to single-particle cryoelectron microscopy. Cell 161(3):438-449.
3. Adrian M, Dubochet J, Lepault J, McDowall AW (1984) Cryo-electron microscopy of viruses. Nature 308(5954):32-36.
4. Dubochet J, et al. (1988) Cryo-electron microscopy of vitrified specimens. Q Rev Biophys 21(2):129-228.
5. Taylor KA, Glaeser RM (1976) Electron microscopy of frozen hydrated biological specimens. J Ultrastruct Res 55(3):448-456.
6. Frank J, Verschoor A, Boublik M (1981) Computer averaging of electron micrographs of 40S ribosomal subunits. Science 214(4527):1353-1355.
7. Penczek P, Radermacher M, Frank J (1992) Three-dimensional reconstruction of single particles embedded in ice. Ultramicroscopy 40(1):33-53.
8. Glaeser RM (2016) The resolution revolution: Recent advances in cryoEM. Methods in Enzymology, ed Crowther R (Academic, New York), Vol 579, pp 19-50.
9. Henderson R, et al. (1990) Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J Mol Biol 213(4):899-929.
10. Kühlbrandt W, Wang DN, Fujiyoshi Y (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367(6464):614-621.
11. Nogales E, Wolf SG, Downing KH (1998) Structure of the alpha beta tubulin dimer by electron crystallography. Nature 391(6663):199-203.
12. Gonen T, et al. (2005) Lipid-protein interactions in double-layered two-dimensional AQP0 crystals. Nature 438(7068):633-638.
13. Glaeser RM, et al. (2016) Factors that influence the formation and stability of thin, cryo-EM specimens. Biophys J 110(4):749-755.
14. McDowall AW, Dobro MJ, Melanson LA, Jensen GJ (2010) Cryo-EM part A: Sample preparation and data collection. Methods in Enzymology, ed Jensen GJ (Academic, New York), Vol 481, pp 63-82.
15. Taylor KA, Glaeser RM (2008) Retrospective on the early development of cryoelectron microscopy of macromolecules and a prospective on opportunities for the future. J Struct Biol 163(3):214-223.
16. Glaeser RM, Han B-G (2016) Opinion: Hazards faced by macromolecules when confined to thin aqueous films. Biophys Rep, 10.1007/s41048-016-0026-3.
17. Thompson RF, Walker M, Siebert CA, Muench SP, Ranson NA (2016) An introduction to sample preparation and imaging by cryo-electron microscopy for structural biology. Methods 100:3-15.
18. Stark H, Chari A (2016) Sample preparation of biological macromolecular assemblies for the determination of high-resolution structures by cryo-electron microscopy. Microscopy (Oxf) 65(1):23-34.
19. Douglas SM, et al. (2009) Self-assembly of DNA into nanoscale three-dimensional shapes. Nature 459(7245):414-418.
20. Dietz H, Douglas SM, Shih WM (2009) Folding DNA into twisted and curved nanoscale shapes. Science 325(5941):725-730.
21. Castro CE, et al. (2011) A primer to scaffolded DNA origami. Nat Methods 8(3):221-229.
22. Malo J, et al. (2005) Engineering a 2D protein-DNA crystal. Angew Chem Int Ed Engl 44(20):3057-3061.
23. Lane D, Levine A (2010) p53 research: The past thirty years and the next thirty years. Cold Spring Harb Perspect Biol 2(12):a000893.
24. Joerger AC, Fersht AR (2016) The p53 pathway: Origins, inactivation in cancer, and emerging therapeutic approaches. Annu Rev Biochem 85:375-404.
25. Joerger AC, Fersht AR (2008) Structural biology of the tumor suppressor p53. Annu Rev Biochem 77:557-582.
26. Cañadillas JMP, et al. (2006) Solution structure of p53 core domain: Structural basis for its instability. Proc Natl Acad Sci USA 103(7):2109-2114.
27. Wang Y, Rosengarth A, Luecke H (2007) Structure of the human p53 core domain in the absence of DNA. Acta Crystallogr D Biol Crystallogr 63(Pt 3):276-281.
28. Natan E, et al. (2011) Interaction of the p53 DNA-binding domain with its N-terminal extension modulates the stability of the p53 tetramer. J Mol Biol 409(3):358-368.
29. Cho Y, Gorina S, Jeffrey PD, Pavletich NP (1994) Crystal structure of a p53 tumor suppressor-DNA complex: Understanding tumorigenic mutations. Science 265(5170):346-355.
30. Jeffrey PD, Gorina S, Pavletich NP (1995) Crystal structure of the tetramerization domain of the p53 tumor suppressor at 1.7 angstroms. Science 267(5203):1498-1502.
31. Mittl PRE, Chène P, Grütter MG (1998) Crystallization and structure solution of p53(residues 326-356) by molecular replacement using an NMR model as template. Acta Crystallogr D Biol Crystallogr 54(Pt 1):86-89.
32. Clore GM, et al. (1995) Refined solution structure of the oligomerization domain of the tumour suppressor p53. Nat Struct Biol 2(4):321-333.
33. Lee W, et al. (1994) Solution structure of the tetrameric minimum transforming domain of p53. Nat Struct Biol 1(12):877-890.
34. Kitayner M, et al. (2010) Diversity in DNA recognition by p53 revealed by crystal structures with Hoogsteen base pairs. Nat Struct Mol Biol 17(4):423-429.
35. Chen Y, et al. (2013) Structure of p53 binding to the BAX response element reveals DNA unwinding and compression to accommodate base-pair insertion. Nucleic Acids Res 41(17):8368-8376.
36. Tidow H, et al. (2007) Quaternary structures of tumor suppressor p53 and a specific p53 DNA complex. Proc Natl Acad Sci USA 104(30):12324-12329.
37. Melero R, et al. (2011) Electron microscopy studies on the quaternary structure of p53 reveal different binding modes for p53 tetramers in complex with DNA. Proc Natl Acad Sci USA 108(2):557-562.
38. Okorokov AL, et al. (2006) The structure of p53 tumour suppressor protein reveals the basis for its functional plasticity. EMBO J 25(21):5191-5200.
39. Aramayo R, et al. (2011) Quaternary structure of the specific p53-DNA complex reveals the mechanism of p53 mutant dominance. Nucleic Acids Res 39(20):8960-8971.
40. Anderson ME, Woelker B, Reed M, Wang P, Tegtmeyer P (1997) Reciprocal interference between the sequence-specific core and nonspecific C-terminal DNA binding domains of p53: Implications for regulation. Mol Cell Biol 17(11):6255-6264.
41. Bai X-C, Martin TG, Scheres SHW, Dietz H (2012) Cryo-EM structure of a 3D DNAorigami object. Proc Natl Acad Sci USA 109(49):20012-20017.
42. Jensen GJ (2001) Alignment error envelopes for single particle analysis. J Struct Biol 133(2-3):143-155.
43. Scheres SHW (2015) Semi-automated selection of cryo-EM particles in RELION-1.3. J Struct Biol 189(2):114-122.
44. Scheres SHW (2012) RELION: Implementation of a Bayesian approach to cryo-EM structure determination. J Struct Biol 180(3):519-530.
45. Martin TG (2014) Functional synthetic DNA nanostructures. PhD dissertation (Technical University of Munich, Munich).
46. Fernández IS, et al. (2013) Molecular architecture of a eukaryotic translational initiation complex. Science 342(6160):1240585.
47. Danev R, Baumeister W (2016) Cryo-EM single particle analysis with the Volta phase plate. eLife 5:e13046.
48. Gerling T, Wagenbauer KF, Neuner AM, Dietz H (2015) Dynamic DNA devices and assemblies formed by shape-complementary, non-base pairing 3D components. Science 347(6229):1446-1452.
49. Shaw A, Benson E, Högberg B (2015) Purification of functionalized DNA origami nanostructures. ACS Nano 9(5):4968-4975.
50. Fairhead M, et al. (2014) SpyAvidin hubs enable precise and ultrastable orthogonal nanoassembly. J Am Chem Soc 136(35):12355-12363.
51. Veggiani G, Zakeri B, Howarth M (2014) Superglue from bacteria: Unbreakable bridges for protein nanotechnology. Trends Biotechnol 32(10):506-512.
52. Bayburt TH, Grinkova YV, Sligar SG (2002) Self-assembly of discoidal phospholipid bilayer nanoparticles with membrane scaffold proteins. Nano Lett 2(8):853-856.
53. Kocabey S, et al. (2015) Membrane-assisted growth of DNA origami nanostructure arrays. ACS Nano 9(4):3530-3539.
54. Kelly DF, Abeyrathne PD, Dukovski D, Walz T (2008) The Affinity Grid: A pre-fabricated EM grid for monolayer purification. J Mol Biol 382(2):423-433.
55. Walz T, Kelly DF, Dukovski D (2010) Cryo-EM part A: Sample preparation and data collection. Methods in Enzymology, ed Jensen GJ (Academic, New York), Vol 481, pp 83-107.
56. Yu G, et al. (2014) Single-step antibody-based affinity cryo-electron microscopy for imaging and structural analysis of macromolecular assemblies. J Struct Biol 187(1):1-9.
57. Yu G, Li K, Jiang W (2016) Antibody-based affinity cryo-EM grid. Methods 100:16-24.
58. Douglas SM, et al. (2009) Rapid prototyping of 3D DNA-origami shapes with cadnano. Nucleic Acids Res 37(15):5001-5006.
59. Douglas SM, Chou JJ, Shih WM (2007) DNA-nanotube-induced alignment of membrane proteins for NMR structure determination. Proc Natl Acad Sci USA 104(16):6644-6648.
60. Veprintsev DB, et al. (2006) Core domain interactions in full-length p53 in solution. Proc Natl Acad Sci USA 103(7):2115-2119.
61. Nikolova PV, Henckel J, Lane DP, Fersht AR (1998) Semirational design of active tumor suppressor p53 DNA binding domain with enhanced stability. Proc Natl Acad Sci USA 95(25):14675-14680.
62. Joerger AC, Allen MD, Fersht AR (2004) Crystal structure of a superstable mutant of human p53 core domain. Insights into the mechanism of rescuing oncogenic mutations. J Biol Chem 279(2):1291-1296.
63. Bharat TAM, Russo CJ, Löwe J, Passmore LA, Scheres SHW (2015) Advances in singleparticle electron cryomicroscopy structure determination applied to sub-tomogram averaging. Structure 23(9):1743-1753.
64. Li X, et al. (2013) Electron counting and beam-induced motion correction enable nearatomicresolution single-particle cryo-EM. Nat Methods 10(6):584-590.
65. Zhang K (2016) Gctf: Real-time CTF determination and correction. J Struct Biol 193(1):1-12.