Applied Microscopy

Korean Society of Microscopy (한국현미경학회)
권호 표지
DOI QR코드

DOI QR Code

Recent Advances in Electron Crystallography

  • Chung, Jeong Min (Department of Biochemistry, College of Natural Sciences, Kangwon National University) ;
  • Lee, Sangmin (Department of Biochemistry, College of Natural Sciences, Kangwon National University) ;
  • Jung, Hyun Suk (Department of Biochemistry, College of Natural Sciences, Kangwon National University)
  • Received : 2017.08.07
  • Accepted : 2017.09.08
  • Published : 2017.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Electron crystallography has been used as the one of powerful tool for studying the structure of biological macromolecules at high resolution which is sufficient to provide details of intramolecular and intermolecular interactions at near-atomic level. Previously it commonly uses two-dimensional crystals that are periodic arrangement of biological molecules, however recent studies reported a novel technical approach to electron crystallography of three-dimensional crystals, called micro electron-diffraction (MicroED) which involves placing the irregular and small sized protein crystals in a transmission electron microscope to determine the atomic structure. In here, we review the advances in electron crystallography techniques with several recent studies. Furthermore, we discuss the future direction of this structural approach.

Keywords

References

  1. Bendersky L A and Gayle F W (2001) Electron diffraction using transmission electron microscopy. J. Res. Natl. Inst. Stand. Technol. 106, 997-1012. https://doi.org/10.6028/jres.106.051
  2. Berman H M, Westbrook J, Feng Z, Gilliland G, Bhat T N, Weissig H, Shindyalov I N, and Bourne P E (2000) The protein data bank. Nucleic. Acids. Res. 28, 235-242. https://doi.org/10.1093/nar/28.1.235
  3. Bill R M, Henderson P J, Iwata S, Kunji E R, Michel H, Neutze R, Newstead S, Poolman B, Tate C G, and Vogel H (2011) Overcoming barriers to membrane protein structure determination. Nat. Biotechnol. 29, 335-340. https://doi.org/10.1038/nbt.1833
  4. Boutet S, Lomb L, Williams G J, Barends T R, Aquila A, Doak R B, Weierstall U, DePonte D P, Steinbrener J, Shoeman R L, Messerschmidt M, Barty A, White T A, Kassemeyer S, Kirian R A, Seibert M M, Montanez P A, Kenney C, Herbst R, Hart P, Pines J, Haller G, Gruner S M, Philipp H T, Tate M W, Hromalik M, Koerner L J, van Bakel N, Morse J, Ghonsalves W, Arnlund D, Bogan M J, Caleman C, Fromme R, Hampton C Y, Hunter M S, Johansson L C, Katona G, Kupitz C, Liang M, Martin A V, Nass K, Redecke L, Stellato F, Timneanu N, Wang D, Zatsepin N A, Schafer D, Defever J, Neutze R, Fromme P, Spence J C, Chapman H N, and Schlichting I (2012) Highresolution protein structure determination by serial femtosecond crystallography. Science 337, 362-364. https://doi.org/10.1126/science.1217737
  5. de la Cruz M J, Hattne J, Shi D, Seidler P, Rodriguez J, Reyes F E, Sawaya M R, Cascio D, Weiss S C, Kim S K, Hinck C S, Hinck A P, Calero G, Eisenberg D, and Gonen T (2017) Atomic-resolution structures from fragmented protein crystals with the cryoEM method MicroED. Nat. Methods 14, 399-402. https://doi.org/10.1038/nmeth.4178
  6. Ellis M J and Hebert H (2001) Structure analysis of soluble proteins using electron crystallography. Micron 32, 541-550. https://doi.org/10.1016/S0968-4328(00)00049-4
  7. Ganser-Pornillos B K, Cheng A, and Yeager M (2007) Structure of fulllength HIV-1 CA: a model for the mature capsid lattice. Cell 131, 70-79. https://doi.org/10.1016/j.cell.2007.08.018
  8. Gipson B, Zeng X, and Stahlberg H (2007) 2dx_merge: data management and merging for 2D crystal images. J. Struct. Biol. 160, 375-384. https://doi.org/10.1016/j.jsb.2007.09.011
  9. Glaeser R M (1971) Limitations to significant information in biological electron microscopy as a result of radiation damage. J. Ultrastruct. Res. 36, 466-482. https://doi.org/10.1016/S0022-5320(71)80118-1
  10. Gonen T, Cheng Y, Sliz P, Hiroaki Y, Fujiyoshi Y, Harrison S C, and Walz T (2005) Lipid-protein interactions in double-layered two-dimensional AQP0 crystals. Nature 438, 633-638. https://doi.org/10.1038/nature04321
  11. Henderson R (1975) The structure of the purple membrane from Halobacterium hallobium: analysis of the X-ray diffraction pattern. J. Mol. Biol. 93, 123-138. https://doi.org/10.1016/0022-2836(75)90123-0
  12. Henderson R, Baldwin J M, Ceska T A, Zemlin F, Beckmann E, and Downing K H (1990) Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J. Mol. Biol. 213, 899-929. https://doi.org/10.1016/S0022-2836(05)80271-2
  13. Henderson R and Unwin P N (1975) Three-dimensional model of purple membrane obtained by electron microscopy. Nature 257, 28-32. https://doi.org/10.1038/257028a0
  14. Kebbel F, Kurz M, Arheit M, Grutter M G, and Stahlberg H (2013) Structure and substrate-induced conformational changes of the secondary citrate/sodium symporter CitS revealed by electron crystallography. Structure 21, 1243-1250. https://doi.org/10.1016/j.str.2013.05.011
  15. Kimura Y, Vassylyev D G, Miyazawa A, Kidera A, Matsushima M, Mitsuoka K, Murata K, Hirai T, and Fujiyoshi Y (1997) Surface of bacteriorhodopsin revealed by high-resolution electron crystallography. Nature 389, 206-211. https://doi.org/10.1038/38323
  16. Kuhlbrandt W, Wang D N, and Fujiyoshi Y (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367, 614-621. https://doi.org/10.1038/367614a0
  17. Nannenga B L, Shi D, Hattne J, Reyes F E, and Gonen T (2014a) Structure of catalase determined by MicroED. Elife 3, e03600.
  18. Nannenga B L, Shi D, Leslie A G W, and Gonen T (2014b) High-resolution structure determination by continuous-rotation data collection in MicroED. Nat. Methods 11, 927-930. https://doi.org/10.1038/nmeth.3043
  19. Nass K, Foucar L, Barends T R, Hartmann E, Botha S, Shoeman R L, Doak R B, Alonso-Mori R, Aquila A, Bajt S, Barty A, Bean R, Beyerlein K R, Bublitz M, Drachmann N, Gregersen J, Jonsson H O, Kabsch W, Kassemeyer S, Koglin J E, Krumrey M, Mattle D, Messerschmidt M, Nissen P, Reinhard L, Sitsel O, Sokaras D, Williams G J, Hau-Riege S, Timneanu N, Caleman C, Chapman H N, Boutet S, and Schlichting I (2015) Indications of radiation damage in ferredoxin microcrystals using high-intensity X-FEL beams. J. Synchrotron. Radiat. 22, 225-238. https://doi.org/10.1107/S1600577515002349
  20. Oshima A, Tani K, Toloue M M, Hiroaki Y, Smock A, Inukai S, Cone A, Nicholson B J, Sosinsky G E, and Fujiyoshi Y (2011) Asymmetric configurations and N-terminal rearrangements in connexin26 gap junction channels. J. Mol. Biol. 405, 724-735. https://doi.org/10.1016/j.jmb.2010.10.032
  21. Paulino C, Wohlert D, Kapotova E, Yildiz O, and Kuhlbrandt W (2014) Structure and transport mechanism of the sodium/proton antiporter MjNhaP1. Elife 3, e03583.
  22. Pope C R and Unger V M (2012) Electron crystallography--the waking beauty of structural biology. Curr. Opin. Struct. Biol. 22, 514-519. https://doi.org/10.1016/j.sbi.2012.03.006
  23. Purdy J G, Flanagan J M, Ropson I J, Rennoll-Bankert K E, and Craven R C (2008) Critical role of conserved hydrophobic residues within the major homology region in mature retroviral capsid assembly. J. Virol 82, 5951-5961. https://doi.org/10.1128/JVI.00214-08
  24. Raunser S and Walz T (2009) Electron crystallography as a technique to study the structure on membrane proteins in a lipidic environment. Annu. Rev. Biophys. 38, 89-105. https://doi.org/10.1146/annurev.biophys.050708.133649
  25. Rodriguez J A, Ivanova M I, Sawaya M R, Cascio D, Reyes F E, Shi D, Sangwan S, Guenther E L, Johnson L M, Zhang M, Jiang L, Arbing M A, Nannenga B L, Hattne J, Whitelegge J, Brewster A S, Messerschmidt M, Boutet S, Sauter N K, Gonen T, and Eisenberg D S (2015) Structure of the toxic core of alpha-synuclein from invisible crystals. Nature 525, 486-490. https://doi.org/10.1038/nature15368
  26. Ruprecht J J, Mielke T, Vogel R, Villa C, and Schertler G F (2004) Electron crystallography reveals the structure of metarhodopsin I. EMBO J. 23, 3609-3620. https://doi.org/10.1038/sj.emboj.7600374
  27. Schenk A D, Castano-Diez D, Gipson B, Arheit M, Zeng X, and Stahlberg H (2010) 3D reconstruction from 2D crystal image and diffraction data. Methods. Enzymol. 482, 101-129.
  28. Scherer S, Arheit M, Kowal J, Zeng X, and Stahlberg H (2014) Single particle 3D reconstruction for 2D crystal images of membrane proteins. J. Struct. Biol. 185, 267-277. https://doi.org/10.1016/j.jsb.2013.12.011
  29. Shi D, Nannenga B L, Iadanza M G, and Gonen T (2013) Threedimensional electron crystallography of protein microcrystals. Elife 2, e01345.
  30. Wisedchaisri G and Gonen T (2011) Fragment-based phase extension for three-dimensional structure determination of membrane proteins by electron crystallography. Structure 19, 976-987. https://doi.org/10.1016/j.str.2011.04.008
  31. Wisedchaisri G, Reichow S L, and Gonen T (2011) Advances in structural and functional analysis of membrane proteins by electron crystallography. Structure 19, 1381-1393. https://doi.org/10.1016/j.str.2011.09.001
  32. Yonekura K, Kato K, Ogasawara M, Tomita M, and Toyoshima C (2015) Electron crystallography of ultrathin 3D protein crystals: atomic model with charges. Proc. Natl. Acad. Sci. U S A 112, 3368-3373. https://doi.org/10.1073/pnas.1500724112

Cited by

  1. Toward High-Resolution Cryo-Electron Microscopy: Technical Review on Microcrystal-Electron Diffraction vol.47, pp.4, 2017, https://doi.org/10.9729/AM.2017.47.4.223