Cryo-electron microscopy for structure analyses of membrane proteins in the lipid bilayer

Current Opinion in Structural Biology

Volumn 39, Issue , 2016, Pages 71-78

  Abe, Kazuhiro ^a,b   Fujiyoshi, Yoshinori ^a,b  

^a NAGOYA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN; HYDROGEN POTASSIUM ADENOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; PROTON PUMP;

BINDING SITE; COMPLEX FORMATION; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; CRYSTALLIZATION; CRYSTALLOGRAPHY; ELECTRON TOMOGRAPHY; HUMAN; HYDROGEN BOND; LIPID BILAYER; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTON TRANSPORT; REVIEW; STOICHIOMETRY; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY; CHEMISTRY; METABOLISM; PROCEDURES;

AQUAPORINS; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; LIPID BILAYERS; MEMBRANE PROTEINS;

EID: 84973860999     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2016.06.001     Document Type: Review

References (44)

1. Widdas W.F. Inability of diffusion to account for placental glucose transfer in the sheep and consideration of the kinetics of a possible carrier transfer. J Physiol 1952, 118:23-39.
2. Shi Y. A glimpse of structural biology through X-ray crystallography. Cell 2014, 159:995-1014.
3. Cheng Y. Single particle cryo-EM at crystallographic resolution. Cell 2015, 161:450-457.
4. Toyoshima C., Nakasako M., Nomura H., Ogawa H. Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 Å resolution. Nature 2000, 405:647-655.
5. Henderson R., Unwin P.N. Three-dimensional model of purple membrane obtained by electron microscopy. Nature 1975, 257:28-32.
6. Fujiyoshi Y., Unwin N. Electron crystallography of proteins in membranes. Curr Opin Struct Biol 2008, 18:587-592.
7. Oshima A., Tani K., Hiroaki Y., Fujiyoshi Y., Sosinsky G.E. Three-dimensional structure of a human connexin26 gap junction channel reveals a plug in the vestibule. Proc Natl Acad Sci U S A 2007, 104:10034-10039.
8. Lee G. How lipids affect the activities of integral membrane proteins. Biochim Biophys Acta 2004, 1666:62-87.
9. Mitsuoka K., Hirai T., Murata K., Miyazawa A., Kidera A., Kimura Y., Fujiyoshi Y. The structure of bacteriorhodopsin at 3.0 Å resolution based on electron crystallography: implication of the charge distribution. J Mol Biol 1999, 286:861-882.
10. Hite R.K., Li Z., Walz T. Principles of membrane protein interactions with annular lipids deduced from aquaporin-0 2D crystals. EMBO J 2010, 29:1652-1658.
11. Hite R.K., Gonen T., Harrison S.C., Walz T. Interaction of lipids with aquaporin-0 and other membrane proteins. Pflugers Arch 2008, 456:651-661.
12. Gonen T., Cheng Y., Sliz P., Hiroaki Y., Fujiyoshi Y., Harrison S.C., Walz T. Lipid-protein interactions in double-layered two-dimensional AQP0 crystals. Nature 2005, 438:633-638.
13. Tani K., Mitsuma T., Hiroaki Y., Kamegawa A., Nishikawa, Tanimura Y., Fujiyoshi Y. Mechanism of aquaporin-4's fast and highly selective water conduction and proton exclusion. J Mol Biol 2009, 389:694-706.
14. Ho J.D., Yeh R., Sandstrom A., Chormy I., Harries W.E.C., Robbins R.A., Miercke L.J.W., Stroud R.M. Crystal structure of human aquaporin 4 at 1.8 Å and its mechanism of conductance. Proc Natl Acad Sci U S A 2009, 106:7437-7442.
15. Tani K., Fujiyoshi Y. Water channel structures analysed by electron crystallography. Biochim Biophys Acta 2014, 1840:1605-1613.
16. Fujiyoshi Y. Development of the field of structural physiology. Proc Jpn Acad Ser B Phys Biol Sci 2015, 91:447-468.
17. Murata K., Mitsuoka K., Hirai T., Walz T., Agre P., Heymann J.B., Engel A., Fujiyoshi Y. Structural determinants of water permeation through aquaporin-1. Nature 2000, 407:599-605.
18. Sengupta D., Behera R.N., Smith J.C., Ullmann G.M. The α helix dipole: screened out?. Structure 2005, 13:849-855.
19. + conduction and selectivity. Science 1998, 280:69-77.
20. Payandeh J., Gamal El-Din T.M., Scheuer T., Zheng N., Catterall W.A. Crystal structure of a voltage-gated sodium channel in two potentially inactivated states. Nature 2012, 486:135-139.
21. Electron Crystallography of Biological Macromolecules 2007, Oxford Univ Press. R.M. Glaser, K. Downing, D. Derosier, W. Baumeister, J. Frank (Eds.).
22. Tsai C.J., Tani K., Irie K., Hiroaki Y., Shimomura T., McMillan D.G., Cook G.M., Schertler G.F.X., Fujiyoshi F., Li X.D. Two alternative conformations of a voltage-gated sodium channel. J Mol Biol 2013, 425:4074-4088.
23. +-ATPase prevents reverse reaction of the transport cycle. EMBO J 2009, 28:1637-1643.
24. +-ATPase with bound fluorinated phosphate analogs. J Struct Biol 2010, 170:60-68.
25. +-ATPase with an acid suppressant. Nat Commun 2011, 2:155.
26. +-ATPase with a single occupied cation-binding site. Proc Natl Acad Sci U S A 2012, 109:18401-18406.
27. +-ATPase reveals an important contribution of the A-M2 linker for the luminal gating. J Biol Chem 2014, 289:30590-30601.
28. Shin J.M., Munson K., Vagin O., Sachs G. The gastric HKATPase: structure, function, and inhibition. Pflugers Arch 2009, 457:609-622.
29. Dürr K.L., Abe K., Tavraz N.N., Friedrich T. E2P state stabilization by the N-terminal tail of the H,K-ATPase β-subunit is critical for efficient proton pumping under in vivo conditions. J Biol Chem 2009, 284:20147-20154.
30. +/ATP stoichiometry. J Biol Chem 1982, 257:6296-6299.
31. Shinoda T., Ogawa H., Cornelius F., Toyoshima C. Crystal structure of the sodium potassium pump at 2.4 Å resolution. Nature 2009, 459:446-450.
32. Tani K., Arthur C.P., Tamakoshi M., Yokoyama K., Mitsuoka K., Fujiyoshi Y., Gerle C. Visualization of two distinct states of disassembly in the bacterial V-ATPase from Thermus thermophiles. Microscopy (Tokyo) 2013, 62:467-474.
33. Shimada S., Shinzawa-Itoh K., Amano S., Akira Y., Miyazawa A., Tsukihara T., Tani K., Gerle C., Yoshikawa S. Three-dimensional structure of bovine heart NADH: ubiquinone oxidoreductase (complex I) by electron microscopy of a single negatively stained two-dimensional crystal. Microscopy (Tokyo) 2014, 63:167-174.
34. Jiko C., Davies K.M., Shinzawa-Itoh K., Tani K., Maeda S., Mills D.J., Tsukihara T., Fujiyoshi Y., Kühlbrandt W., Gerle C. Bovine F1Fo ATP synthase monomers bend the lipid bilayer in 2D membrane crystals. eLife 2015, 4:e06119.
35. Lučić V., Rigort A., Baumeister W. Cryo-electron tomography: the challenge of doing structural biology in situ. J Cell Biol 2013, 202:407-419.
36. Oda T., Yanagisawa H.A., Kamiya R., Kikkawa M. A molecular ruler determines the repeat length in eukaryotic cilia and flagella. Science 2014, 346:857-860.
37. Davies K.M., Anselmi C., Wittig I., Faraldo-Gomez J.D., Kuhlbrandt W. Structure of the yeast F1Fo-ATP synthase dimer and its role in shaping the mitochondrial cristae. Proc Natl Acad Sci U S A 2012, 109:13602-13607.
38. Allegretti M., Klusch N., Mills D.J., Vonck J., Kühlbrandt W., Davies K.M. Horizontal membrane-intrinsic α-helices in the stator a-subunit of an F-type ATP synthase. Nature 2015, 521:237-240.
39. Flank J. Generalized single-particle cryo-EM2016-a historical perspective. Microscopy (Tokyo) 2016, 65:3-8.
40. Li X., Mooney P., Zheng S., Booth C.R., Braunfeld M.B., Gubbens S., Agard D.A., Cheng Y. Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat Methods 2013, 10:584-590.
41. Fischer N., Konevega A.L., Wintermeyer W., Rodnina M.V., Stark H. Ribosome dynamics and tRNA movement by time-resolved electron cryomicroscopy. Nature 2010, 466:329-333.
42. Liao M., Cao E., Julius D., Cheng Y. Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature 2013, 504:107-112.
43. Efremov R.G., Leitner A., Aebersold R., Raunser S. Architecture and conformational switch mechanism of the ryanodine receptor. Nature 2015, 517:39-43.
44. Hauer F., Gerle C., Fischer N., Oshima A., Shinzawa-Itoh K., Shimada S., Yokoyama K., Fujiyoshi Y., Stark H. GraDeR: membrane protein complex preparation for single-particle cryo-EM. Structure 2015, 23:1769-1775.