Applied Microscopy

Korean Society of Microscopy (한국현미경학회)
권호 표지
DOI QR코드

DOI QR Code

The Nobel Prize in Chemistry 2017: High-Resolution Cryo-Electron Microscopy

  • Chung, Jae-Hee (Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST)) ;
  • Kim, Ho Min (Graduate School of Medical Science & Engineering, Korea Advanced Institute of Science and Technology (KAIST))
  • Received : 2017.11.15
  • Accepted : 2017.12.04
  • Published : 2017.12.30
Download PDF
⟨ Previous Next ⟩

Abstract

The 2017 Nobel Prize in Chemistry was awarded to the following three pioneers: Dr. Joachim Frank, Dr. Jacques Dubochet, and Dr. Richard Henderson. They all contributed to the development of a Cryo-electron microscopy (EM) technique for determining the high-resolution structures of biomolecules in solution, particularly without crystal and with much less amount of biomolecules than X-ray crystallography. In this brief commentary, we address the major advances made by these three Nobel laureates as well as the current status and future prospects of this Cryo-EM technique.

Keywords

References

  1. Adrian M, Dubochet J, Lepault J, and McDowall A W (1984) Cryo-electron microscopy of viruses. Nature 308, 32-36. https://doi.org/10.1038/308032a0
  2. Asano S, Engel B D, and Baumeister W (2016) In situ Cryo-electron tomography: a post-reductionist approach to structural biology. J. Mol. Biol. 428, 332-343. https://doi.org/10.1016/j.jmb.2015.09.030
  3. Bai X C, McMullan G, and Scheres S H (2015) How cryo-EM is revolutionizing structural biology. Trends Biochem. Sci. 40, 49-57. https://doi.org/10.1016/j.tibs.2014.10.005
  4. Beck M and Baumeister W (2016) Cryo-electron tomography: can it reveal the molecular sociology of cells in atomic detail? Trends Cell Biol. 26, 825-837. https://doi.org/10.1016/j.tcb.2016.08.006
  5. Beck M and Glavy J S (2014) Toward understanding the structure of the vertebrate nuclear pore complex. Nucleus 5, 119-123. https://doi.org/10.4161/nucl.28739
  6. Beck M, Lucic V, Forster F, Baumeister W, and Medalia O (2007) Snapshots of nuclear pore complexes in action captured by cryoelectron tomography. Nature 449, 611. https://doi.org/10.1038/nature06170
  7. Brenner S and Horne R W (1959) A negative staining method for high resolution electron microscopy of viruses. Biochim. Biophys. Acta 34, 103-110. https://doi.org/10.1016/0006-3002(59)90237-9
  8. Bui K H, von Appen A, DiGuilio A L, Ori A, Sparks L, Mackmull M T, Bock T, Hagen W, Andres-Pons A, Glavy J S, and Beck M (2013) Integrated structural analysis of the human nuclear pore complex scaffold. Cell 155, 1233-1243. https://doi.org/10.1016/j.cell.2013.10.055
  9. Danev R, Buijsse B, Khoshouei M, Plitzko J M, and Baumeister W (2014) Volta potential phase plate for in-focus phase contrast transmission electron microscopy. Proc. Natl. Acad. Sci. U S A 111, 15635-15640. https://doi.org/10.1073/pnas.1418377111
  10. de Boer P, Hoogenboom J P, and Giepmans B N G (2015) Correlated light and electron microscopy: ultrastructure lights up! Nat. Meth. 12, 503-513. https://doi.org/10.1038/nmeth.3400
  11. De Rosier D J and Klug A (1968) Reconstruction of three dimensional structures from electron micrographs. Nature 217, 130-134. https://doi.org/10.1038/217130a0
  12. Dodonova S O, Aderhold P, Kopp J, Ganeva I, Rohling S, Hagen W J H, Sinning I, Wieland F, and Briggs J A G (2017) 9A structure of the COPI coat reveals that the Arf1 GTPase occupies two contrasting molecular environments. Elife 6.
  13. Dodonova S O, Diestelkoetter-Bachert P, von Appen A, Hagen W J H, Beck R, Beck M, Wieland F, and Briggs J A G (2015) A structure of the COPI coat and the role of coat proteins in membrane vesicle assembly. Science 349, 195. https://doi.org/10.1126/science.aab1121
  14. Dubochet J, Adrian M, Chang J J, Homo J C, Lepault J, McDowall A W, and Schultz P (1988) Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 21, 129-228. https://doi.org/10.1017/S0033583500004297
  15. Dubochet J and McDowall A W (1981) Vitrification of pure water for electron microscopy. J. Microsc. 124, RP3-RP4.
  16. Frank J, Shimkin B, and Dowse H (1981) SPIDER - a modular software system for electron image processing. Ultramicroscopy 6, 343-358. https://doi.org/10.1016/S0304-3991(81)80221-5
  17. Frank J and van Heel M (1982) Correspondence analysis of aligned images of biological particles. J. Mol. Biol. 161, 134-137. https://doi.org/10.1016/0022-2836(82)90282-0
  18. Grigorieff N (2007) FREALIGN: high-resolution refinement of single particle structures. J. Struct. Biol. 157, 117-125. https://doi.org/10.1016/j.jsb.2006.05.004
  19. Hall C E, Jakus M A, and Schmitt F O (1945) The structure of certain muscle fibrils as revealed by the use of electron stains. J. Appl. Phys. 16, 459-465. https://doi.org/10.1063/1.1707615
  20. 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
  21. 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
  22. Huxley H E and Zubay G (1961) Preferential staining of nucleic acidcontaining structures for electron microscopy. J. Biophys. Biochem. Cytol. 11, 273-296. https://doi.org/10.1083/jcb.11.2.273
  23. Jeong H, Lee S G, Kweon H S, and Hyun J (2017) Facility for high resolution cryo-electron microscopy of biological macromolecules at Korea Basic Science Institute. Biodesign 5, 96-102.
  24. Li X, Mooney P, Zheng S, Booth C R, Braunfeld M B, Gubbens S, Agard D A, and Cheng Y (2013) Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat. Methods 10, 584-590. https://doi.org/10.1038/nmeth.2472
  25. Mattei S, Glass B, Hagen W J H, Krausslich H G, and Briggs J A G (2016) The structure and flexibility of conical HIV-1 capsids determined within intact virions. Science 354, 1434. https://doi.org/10.1126/science.aah4972
  26. Nickell S, Kofler C, Leis A P, and Baumeister W (2006) A visual approach to proteomics. Nat. Rev. Mol. Cell Biol. 7, 225. https://doi.org/10.1038/nrm1861
  27. Pfeffer S, Burbaum L, Unverdorben P, Pech M, Chen Y, Zimmermann R, Beckmann R, and Forster F (2015) Structure of the native Sec61 protein-conducting channel. Nat. Commun. 6, 1632-1643.
  28. Radermacher M, Wagenknecht T, Verschoor A, and Frank J (1986) A new 3-D reconstruction scheme applied to the 50S ribosomal subunit of E. coli. J. Microsc. 141, RP1-2. https://doi.org/10.1111/j.1365-2818.1986.tb02694.x
  29. Rigort A, Bauerlein F J B, Villa E, Eibauer M, Laugks T, Baumeister W, and Plitzko J M (2012) Focused ion beam micromachining of eukaryotic cells for cryoelectron tomography. Proc Natl. Acad. Sci. 109, 4449-4454. https://doi.org/10.1073/pnas.1201333109
  30. Scheres S H (2012) RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530. https://doi.org/10.1016/j.jsb.2012.09.006
  31. Scheres S H, Nunez-Ramirez R, Sorzano C O, Carazo J M, and Marabini R (2008) Image processing for electron microscopy single-particle analysis using XMIPP. Nat. Protoc. 3, 977-990. https://doi.org/10.1038/nprot.2008.62
  32. Schur F K M, Hagen W J H, Rumlova M, Ruml T, Muller B, Krausslich H G, and Briggs J A G (2014) Structure of the immature HIV-1 capsid in intact virus particles at 8.8 A resolution. Nature 517, 505.
  33. Schur F K M, Obr M, Hagen W J H, Wan W, Jakobi A J, Kirkpatrick J M, Sachse C, Krausslich H G, and Briggs J A G (2016) An atomic model of HIV-1 capsid-SP1 reveals structures regulating assembly and maturation. Science 353, 506. https://doi.org/10.1126/science.aaf9620
  34. Shaikh T R, Gao H, Baxter W T, Asturias F J, Boisset N, Leith A, and Frank J (2008) SPIDER image processing for single-particle reconstruction of biological macromolecules from electron micrographs. Nat. Protoc. 3, 1941-1974. https://doi.org/10.1038/nprot.2008.156
  35. Tang G, Peng L, Baldwin P R, Mann D S, Jiang W, Rees I, and Ludtke S J (2007) EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46. https://doi.org/10.1016/j.jsb.2006.05.009
  36. Taylor K A and Glaeser R M (1974) Electron diffraction of frozen, hydrated protein crystals. Science 186, 1036-1037. https://doi.org/10.1126/science.186.4168.1036
  37. van Heel M and Frank J (1981) Use of multivariate statistics in analysing the images of biological macromolecules. Ultramicroscopy 6, 187-194.
  38. van Heel M, Harauz G, Orlova E V, Schmidt R, and Schatz M (1996) A new generation of the IMAGIC image processing system. J. Struct. Biol. 116, 17-24. https://doi.org/10.1006/jsbi.1996.0004
  39. Villa E, Schaffer M, Plitzko J M, and Baumeister W (2013) Opening windows into the cell: focused-ion-beam milling for cryo-electron tomography. Curr. Opin. Struct. Biol. 23, 771-777. https://doi.org/10.1016/j.sbi.2013.08.006