24. Subramaniam S, Faruqi AR, Oesterhelt D,
Henderson R (1997) Electron diffraction studies of light-induced conformational changes in
the Leu-93 --> Ala bacteriorhodopsin mutant.
Proc Natl Acad Sci U S A 94(5):1767–1772
25. Fujiyoshi Y (1998) The structural study of
membrane proteins by electron crystallography. Adv Biophys 35:25–80
26. Subramaniam S, Henderson R (1999) Electron
crystallography of bacteriorhodopsin with millisecond time resolution. J Struct Biol 128
(1):19–25
27. Koning RI, Oostergetel GT, Brisson A (2003)
Preparation of flat carbon support films. Ultramicroscopy 94:183–191
28. Gyobu N, Tani K, Hiroaki Y, Kamegawa A,
Mitsuoka K, Fujiyoshi Y (2004) Improved
specimen preparation for cryo-electron microscopy using a symmetric carbon sandwich technique. J Struct Biol 146:325–333
29. Amos LA, Henderson R, Unwin PN (1982)
Three-dimensional structure determination by
electron microscopy of two-dimensional crystals. Prog Biophys Mol Biol 39(3):183–231
30. Grigorieff N, Ceska TA, Downing KH, Baldwin JM, Henderson R (1996) Electroncrystallographic refinement of the structure of
bacteriorhodopsin.
J
Mol
Biol
259
(3):393–421
31. Biyani N, Righetto RD, McLeod R, CaujolleBert D, Castano-Diez D, Goldie KN, Stahlberg H (2017) Focus: The interface between
data collection and data processing in cryoEM. J Struct Biol 198(2):124–133
32. Gonen T (2013) The collection of highresolution electron diffraction data. In: Electron crystallography of soluble and membrane
proteins. Humana Press, Totowa, NJ, pp
153–169
33. Suloway C, Pulokas J, Fellmann D, Cheng A,
Guerra F, Quispe J, Stagg S, Potter CS, Carragher B (2005) Automated molecular microscopy: the new Leginon system. J Struct Biol
151(1):41–60
34. Mastronarde DN (2005) Automated electron
microscope
tomography
using
robust
prediction of specimen movements. J Struct
Biol 152(1):36–51
35. Li X, Mooney P, Zheng S, Booth CR, Braunfeld MB, Gubbens S, Agard DA, Cheng Y
(2013) Electron counting and beam-induced
motion correction enable near-atomic-resolution single-particle cryo-EM. Nat Methods 10
(6):584–590
36. Zheng SQ, Palovcak E, Armache JP, Verba KA,
Cheng Y, Agard DA (2017) MotionCor2:
anisotropic correction of beam-induced
motion for improved cryo-electron microscopy. Nat Methods 14(4):331–332
37. Grant T, Grigorieff N (2015) Measuring the
optimal exposure for single particle cryo-EM
using a 2.6 A ˚ reconstruction of rotavirus VP6.
elife 4:e06980
38. Rohou A, Grigorieff N (2015) CTFFIND4:
Fast and accurate defocus estimation from electron micrographs. J Struct Biol 192
(2):216–221
39. Zhang K (2016) Gctf: Real-time CTF determination and correction. J Struct Biol 193(1):1–2
40. Crowther RA, Henderson R, Smith JM (1996)
MRC image processing programs. J Struct Biol
116(1):9–16
41. Walz T, H€ aner M, Wu XR, Henn C, Engel A,
Sun TT, Aebi U (1995) Towards the molecular
architecture of the asymmetric unit membrane
of the mammalian urinary bladder epithelium:
a closed “twisted ribbon” structure. J Mol Biol
248(5):887–900
42. Schmidt-Krey I, Kanaoka Y, Mills DJ,
Irikura D, Haase W, Lam BK, Austen KF, Ku ¨hlbrandt W (2004) Human leukotriene C4
synthase at 4.5 A ˚ resolution in projection.
Structure 12(11):2009–2014
43. Zhao G, Johnson MC, Schnell JR, Kanaoka Y,
Haase W, Irikura D, Lam BK, Schmidt-Krey I
(2010) Two-dimensional crystallization conditions of human leukotriene C4 synthase requiring adjustment of a particularly large
combination of specific parameters. J Struct
Biol 169(3):450–454
44. Gipson B, Zeng X, Zhang ZY, Stahlberg H
(2007) 2dx—user-friendly image processing
for 2D crystals. J Struct Biol 157(1):64–72
2D Electron Crystallography of Membrane Proteins
245
Henderson R (1997) Electron diffraction studies of light-induced conformational changes in
the Leu-93 --> Ala bacteriorhodopsin mutant.
Proc Natl Acad Sci U S A 94(5):1767–1772
25. Fujiyoshi Y (1998) The structural study of
membrane proteins by electron crystallography. Adv Biophys 35:25–80
26. Subramaniam S, Henderson R (1999) Electron
crystallography of bacteriorhodopsin with millisecond time resolution. J Struct Biol 128
(1):19–25
27. Koning RI, Oostergetel GT, Brisson A (2003)
Preparation of flat carbon support films. Ultramicroscopy 94:183–191
28. Gyobu N, Tani K, Hiroaki Y, Kamegawa A,
Mitsuoka K, Fujiyoshi Y (2004) Improved
specimen preparation for cryo-electron microscopy using a symmetric carbon sandwich technique. J Struct Biol 146:325–333
29. Amos LA, Henderson R, Unwin PN (1982)
Three-dimensional structure determination by
electron microscopy of two-dimensional crystals. Prog Biophys Mol Biol 39(3):183–231
30. Grigorieff N, Ceska TA, Downing KH, Baldwin JM, Henderson R (1996) Electroncrystallographic refinement of the structure of
bacteriorhodopsin.
J
Mol
Biol
259
(3):393–421
31. Biyani N, Righetto RD, McLeod R, CaujolleBert D, Castano-Diez D, Goldie KN, Stahlberg H (2017) Focus: The interface between
data collection and data processing in cryoEM. J Struct Biol 198(2):124–133
32. Gonen T (2013) The collection of highresolution electron diffraction data. In: Electron crystallography of soluble and membrane
proteins. Humana Press, Totowa, NJ, pp
153–169
33. Suloway C, Pulokas J, Fellmann D, Cheng A,
Guerra F, Quispe J, Stagg S, Potter CS, Carragher B (2005) Automated molecular microscopy: the new Leginon system. J Struct Biol
151(1):41–60
34. Mastronarde DN (2005) Automated electron
microscope
tomography
using
robust
prediction of specimen movements. J Struct
Biol 152(1):36–51
35. Li X, Mooney P, Zheng S, Booth CR, Braunfeld MB, Gubbens S, Agard DA, Cheng Y
(2013) Electron counting and beam-induced
motion correction enable near-atomic-resolution single-particle cryo-EM. Nat Methods 10
(6):584–590
36. Zheng SQ, Palovcak E, Armache JP, Verba KA,
Cheng Y, Agard DA (2017) MotionCor2:
anisotropic correction of beam-induced
motion for improved cryo-electron microscopy. Nat Methods 14(4):331–332
37. Grant T, Grigorieff N (2015) Measuring the
optimal exposure for single particle cryo-EM
using a 2.6 A ˚ reconstruction of rotavirus VP6.
elife 4:e06980
38. Rohou A, Grigorieff N (2015) CTFFIND4:
Fast and accurate defocus estimation from electron micrographs. J Struct Biol 192
(2):216–221
39. Zhang K (2016) Gctf: Real-time CTF determination and correction. J Struct Biol 193(1):1–2
40. Crowther RA, Henderson R, Smith JM (1996)
MRC image processing programs. J Struct Biol
116(1):9–16
41. Walz T, H€ aner M, Wu XR, Henn C, Engel A,
Sun TT, Aebi U (1995) Towards the molecular
architecture of the asymmetric unit membrane
of the mammalian urinary bladder epithelium:
a closed “twisted ribbon” structure. J Mol Biol
248(5):887–900
42. Schmidt-Krey I, Kanaoka Y, Mills DJ,
Irikura D, Haase W, Lam BK, Austen KF, Ku ¨hlbrandt W (2004) Human leukotriene C4
synthase at 4.5 A ˚ resolution in projection.
Structure 12(11):2009–2014
43. Zhao G, Johnson MC, Schnell JR, Kanaoka Y,
Haase W, Irikura D, Lam BK, Schmidt-Krey I
(2010) Two-dimensional crystallization conditions of human leukotriene C4 synthase requiring adjustment of a particularly large
combination of specific parameters. J Struct
Biol 169(3):450–454
44. Gipson B, Zeng X, Zhang ZY, Stahlberg H
(2007) 2dx—user-friendly image processing
for 2D crystals. J Struct Biol 157(1):64–72
2D Electron Crystallography of Membrane Proteins
245