Electron crystallography of ultrathin 3D protein crystals: Atomic model with charges

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

Volumn 112, Issue 11, 2015, Pages 3368-3373

  Yonekura, Koji ^a,b   Kato, Kazuyuki ^c   Ogasawara, Mitsuo ^b   Tomita, Masahiro ^b,c   Toyoshima, Chikashi ^b  

^a RIKEN SPring 8 Center   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c HITACHI HIGH TECHNOLOGIES CORPORATION   (Japan)

Author keywords

Ca2+ ATPase; Catalase; Coulomb potential; Electron crystallography; Protein crystal

Indexed keywords

ADENOSINE TRIPHOSPHATASE; AMINO ACID; CATALASE; HEME; ADENOSINE TRIPHOSPHATASE (CALCIUM);

ARTICLE; CRYSTAL; CRYSTAL STRUCTURE; CRYSTALLIZATION; CRYSTALLOGRAPHY; ELECTRON; ELECTRON CRYSTALLOGRAPHY; ELECTRON DIFFRACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; SYNCHROTRON; X RAY CRYSTALLOGRAPHY; ANIMAL; BOVINE; CHEMICAL STRUCTURE; CHEMISTRY; PROCEDURES; STATIC ELECTRICITY;

ANIMALS; CALCIUM-TRANSPORTING ATPASES; CATALASE; CATTLE; CRYSTALLOGRAPHY, X-RAY; ELECTRONS; MODELS, MOLECULAR; STATIC ELECTRICITY;

EID: 84925281992     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1500724112     Document Type: Article

References (34)

1. Henderson R (1995) The potential and limitations of neutrons, electrons and X-rays for atomic resolution microscopy of unstained biological molecules. Q Rev Biophys 28(2):171-193.
2. Gonen T, et al. (2005) Lipid-protein interactions in double-layered two-dimensional AQP0 crystals. Nature 438(7068):633-638.
3. 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.
4. Nannenga BL, Shi D, Leslie AGW, Gonen T (2014) High-resolution structure determination by continuous-rotation data collection in MicroED. Nat Methods 11(9):927-930.
5. Shi D, Nannenga BL, Iadanza MG, Gonen T (2013) Three-dimensional electron crystallography of protein microcrystals. eLife 2:e01345.
6. Mitsuoka K, et al. (1999) The structure of bacteriorhodopsin at 3.0 Å resolution based on electron crystallography: Implication of the charge distribution. J Mol Biol 286(3):861-882.
7. Toyoshima C, Nakasako M, Nomura H, Ogawa H (2000) Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 Å resolution. Nature 405(6787):647-655.
8. Taya S, Taniguchi Y, Nakazawa E, Usukura J (1996) Development of γ-type energy filtering TEM. J Electron Microsc (Tokyo) 45(4):307-313.
9. Toyoshima C, Ogawa H, Tani K (1998) Energy-filtering electron crystallography of proteins. Hitachi Instrument News, the 33rd Electron Microscopy Edition (Hitachi Ltd., Tokyo), pp 3-7.
10. Yonekura K, Maki-Yonekura S, Namba K (2002) Quantitative comparison of zero-loss and conventional electron diffraction from two-dimensional and thin three-dimensional protein crystals. Biophys J 82(5):2784-2797.
11. Dorset DL, Parsons DF (1975) Electron diffraction from single, fully-hydrated, ox-liver catalase microcrystals. Acta Crystallogr A 31(Pt 2):210-215.
12. Unwin PN (1975) Beef liver catalase structure: Interpretation of electron micrographs. J Mol Biol 98(1):235-242.
13. Foroughi LM, Kang Y-N, Matzger AJ (2011) Polymer-induced heteronucleation for protein single crystal growth: Structural elucidation of bovine liver catalase and concanavalin A forms. Cryst Growth Des 11(4):1294-1298.
14. Prince E, ed (2006) International Tables for Crystallography (Wiley, New York), Vol C, pp 263-281.
15. Hirai T, Mitsuoka K, Kidera A, Fujiyoshi Y (2007) Simulation of charge effects on density maps obtained by high-resolution electron crystallography. J Electron Microsc (Tokyo) 56(4):131-140.
16. Toyoshima C, Nomura H (2002) Structural changes in the calcium pump accompanying the dissociation of calcium. Nature 418(6898):605-611.
17. Toyoshima C, Mizutani T (2004) Crystal structure of the calcium pump with a bound ATP analogue. Nature 430(6999):529-535.
18. Toyoshima C, Nomura H, Tsuda T (2004) Lumenal gating mechanism revealed in calcium pump crystal structures with phosphate analogues. Nature 432(7015):361-368.
19. 2+-bound E1 state. Nature 495(7440):260-264.
20. 2+ pump. J Am Chem Soc 127(17):6150-6151.
21. Nannenga BL, Shi D, Hattne J, Reyes FE, Gonen T (2014) Structure of catalase determined by MicroED. eLife 3:e03600.
22. Chuang WJ, Johnson S, Van Wart HE (1988) Resonance Raman spectra of bovine liver catalase: Enhancement of proximal tyrosinate vibrations. J Inorg Biochem 34(3):201-219.
23. Reid TJ, 3rd, et al. (1981) Structure and heme environment of beef liver catalase at 2.5 Å resolution. Proc Natl Acad Sci USA 78(8):4767-4771.
24. Yano J, et al. (2005) X-ray damage to the Mn4Ca complex in single crystals of photosystem II: A case study for metalloprotein crystallography. Proc Natl Acad Sci USA 102(34):12047-12052.
25. 2 reduction site of fully oxidized cytochrome c oxidase could suppress the proton pump. Proc Natl Acad Sci USA 106(7):2165-2169.
26. Bartesaghi A, Matthies D, Banerjee S, Merk A, Subramaniam S (2014) Structure of β-galactosidase at 3.2-Å resolution obtained by cryoelectron microscopy. Proc Natl Acad Sci USA 111(32):11709-11714.
27. Rossmann MG (1979) Processing oscillation diffraction data for very large unit cells with an automatic convolution technique and profile fitting. J Appl Cryst 12(Pt 2):225-238.
28. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307-325.
29. McCoy AJ, Grosse-Kunstleve RW, Storoni LC, Read RJ (2005) Likelihood-enhanced fast translation functions. Acta Crystallogr D Biol Crystallogr 61(Pt 4):458-464.
30. Brünger AT, et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54(Pt 5):905-921.
31. Fabiola F, Bertram R, Korostelev A, Chapman MS (2002) An improved hydrogen bond potential: Impact on medium resolution protein structures. Protein Sci 11(6):1415-1423.
32. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53(Pt 3):240-255.
33. Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK: A program to check the stereochemical quality of protein structures. J Appl Cryst 26(Pt 2):283-291.
34. Cowtan K (1994) DM: An automated procedure for phase improvement by density modification. Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallography 31:34-38.