Review
From Electron Crystallography to Single Particle CryoEM (Nobel Lecture)†
Richard Henderson,
Corresponding Author
Richard Henderson
MRC Laboratory of Molecular Biology, Francis Crick Avenue, Cambridge, CB2 0QH UK
Search for more papers by this authorRichard Henderson,
Corresponding Author
Richard Henderson
MRC Laboratory of Molecular Biology, Francis Crick Avenue, Cambridge, CB2 0QH UK
Search for more papers by this author†
Copyright© The Nobel Foundation 2017. We thank the Nobel Foundation, Stockholm, for permission to print this lecture.
Graphical Abstract
Pictures are a key to knowledge: The development of electron microscopy from its beginnings to modern single particle cryo-EM is described by R. Henderson in his Nobel lecture. Shown is the first projection structure at 7 Å resolution of the purple membrane from October 1974.
References
- 1B. W. Matthews, P. B. Sigler, R. Henderson, D. M. Blow, Nature 1967, 214, 652–656.
- 2T. A. Steitz, R. Henderson, D. M. Blow, J. Mol. Biol. 1969, 46, 337–348.
- 3R. Henderson, J. Mol. Biol. 1970, 54, 341–354.
- 4R. Henderson, J. H. Wang, Biochemistry 1972, 11, 4565–4569.
- 5D. Oesterhelt, W. Stoeckenius, Nat.-New Biol. 1971, 233, 149–152.
- 6A. E. Blaurock, W. Stoeckenius, Nat.-New Biol 1971, 233, 152–155.
- 7P. N. T. Unwin, R. Henderson, J. Mol. Biol. 1975, 94, 425–440.
- 8R. Henderson, P. N. T. Unwin, Nature 1975, 257, 28–32.
- 9R. Henderson, J. M. Baldwin, K. H. Downing, J. Lepault, F. Zemlin, Ultramicroscopy 1986, 19, 147–178.
- 10T. A. Ceska, R. Henderson, J. Mol. Biol. 1990, 213, 539–560.
- 11I. N. Tsygannik, J. M. Baldwin, Eur. Biophys. J. 1987, 14, 263–272.
- 12M. G. Rossmann, R. Henderson, Acta Crystallogr. Sect. A 1982, 38, 13–20.
- 13T. W. Jeng, W. Chiu, F. Zemlin, E. Zeitler, J. Mol. Biol. 1984, 175, 93–97.
- 14K. A. Taylor, R. M. Glaeser, Science 1974, 186, 1036–1037.
- 15K. A. Taylor, R. M. Glaeser, J. Ultrastruct. Res. 1976, 55, 448–456.
- 16R. M. Glaeser, J. Ultrastruct. Res. 1971, 36, 466–482.
- 17S. B. Hayward, R. M. Stroud, J. Mol. Biol. 1981, 151, 491–517.
- 18D. J. Smith, W. O. Saxton, M. A. O'Keefe, G. J. Wood, W. M. Stobbs, Ultramicroscopy 1983, 11, 263–281.
- 19F. Zemlin, Ultramicroscopy 1979, 4, 241–245.
- 20R. Henderson, J. M. Baldwin, 44th Annu. Proc. EMSA (Ed.: ), San Francisco Press, San Francisco, 1986, pp. 6–9.
- 21P. Bullough, R. Henderson, Ultramicroscopy 1987, 21, 223–229.
- 22K. H. Downing, Ultramicroscopy 1988, 24, 387–398.
- 23R. Henderson, C. Raeburn, G. Vigers, Ultramicroscopy 1991, 35, 45–53.
- 24R. Henderson, J. M. Baldwin, T. A. Ceska, F. Zemlin, E. Beckmann, K. H. Downing, J. Mol. Biol. 1990, 213, 899–929.
- 25W. Kühlbrandt, D. N. Wang, Y. Fujiyoshi, Nature 1994, 367, 614–621.
- 26E. Nogales, S. G. Wolf, K. H. Downing, Nature 1998, 391, 199–203.
- 27S. Subramaniam, M. Gerstein, D. Oesterhelt, R. Henderson, EMBO J. 1993, 12, 1–8.
- 28S. Subramaniam, M. Lindahl, P. Bullough, A. R. Faruqi, J. Tittor, D. Oesterhelt, L. Brown, J. Lanyi, R. Henderson, J. Mol. Biol. 1999, 287, 145–161.
- 29S. Subramaniam, R. Henderson, Nature 2000, 406, 653–657.
- 30N. Grigorieff, T. A. Ceska, K. H. Downing, J. M. Baldwin, R. Henderson, J. Mol. Biol. 1996, 259, 393–421.
- 31Y. Kimura, D. G. Vassylyev, A. Miyazawa, A. Kidera, M. Matsushima, K. Mitsuoka, K. Murata, T. Hirai, Y. Fujiyoshi, Nature 1997, 389, 206–211.
- 32E. PebayPeyroula, G. Rummel, J. P. Rosenbusch, E. M. Landau, Science 1997, 277, 1676–1681.
- 33H. Lücke, B. Schobert, H. T. Richter, J. P. Cartailler, J. K. Lanyi, J. Mol. Biol. 1999, 291, 899–911.
- 34J. Dubochet, J. J. Chang, R. Freeman, J. Lepault, A. W. McDowall, Ultramicroscopy 1982, 10, 55–61.
- 35J. Dubochet, J. Lepault, R. Freeman, J. A. Berriman, J. C. Homo, J. Microsc. 1982, 128, 219–237.
- 36J. Dubochet, M. Adrian, J. Teixeira, C. M. Alba, R. K. Kadiyala, D. R. Macfarlane, C. A. Angell, J. Phys. Chem. 1984, 88, 6727–6732.
- 37M. Adrian, J. Dubochet, J. Lepault, A. W. McDowall, Nature 1984, 308, 32–36.
- 38J. Dubochet, M. Adrian, J. J. Chang, J. C. Homo, J. Lepault, A. W. McDowall, P. Schultz, Q. Rev. Biophys. 1988, 21, 129–228.
- 39J. R. Bellare, H. T. Davis, L. E. Scriven, Y. Talmon, J. Electron Microsc. Tech. 1988, 10, 87–111.
- 40J. Frank, Ultramicroscopy 1975, 1, 159–162.
- 41J. Frank, L. Alali, Nature 1975, 256, 376–379.
- 42M. Van Heel, J. Frank, Ultramicroscopy 1981, 6, 187–194.
- 43J. Frank, M. vanHeel, J. Mol. Biol. 1982, 161, 134–137.
- 44M. Van Heel, Ultramicroscopy 1987, 21, 111–123.
- 45M. Radermacher, T. Wagenknecht, A. Verschoor, J. Frank, J. Microsc. 1987, 146, 113–136.
- 46J. Frank, P. Penczek, R. Grassucci, S. Srivastava, J. Cell Biol. 1991, 115, 597–605.
- 47I. S. Gabashvili, R. K. Agrawal, C. M. T. Spahn, R. A. Grassucci, D. I. Svergun, J. Frank, P. Penczek, Cell 2000, 100, 537–549.
- 48H. Hope, B. G. Nichols, Acta Crystallogr. Sect. B 1981, 37, 158–161.
- 49H. Hope, F. Frolow, K. Vonbohlen, I. Makowski, C. Kratky, Y. Halfon, H. Danz, P. Webster, K. S. Bartels, H. G. Wittmann, A. Yonath, Acta Crystallogr. Sect. B 1989, 45, 190–199.
- 50R. Henderson, Proc. R. Soc. B 1990, 241, 6–8.
- 51V. F. Sears, Neutron News 1992, 3, 26–37.
10.1080/10448639208218770 Google Scholar
- 52R. Henderson, Q. Rev. Biophys. 1995, 28, 171–193.
- 53B. Böttcher, S. A. Wynne, R. A. Crowther, Nature 1997, 386, 88–91.
- 54R. A. Crowther, N. A. Kiselev, B. Böttcher, J. A. Berriman, G. P. Borisova, V. Ose, P. Pumpens, Cell 1994, 77, 943–950.
- 55X. K. Yu, L. Jin, J. Jih, C. H. Shih, Z. H. Zhou, PLoS One 2013, 0069729.
- 56“Crystallography of Biological Macromolecules”: T. S. Baker, R. Henderson in International Tables for Crystallography, Vol. F. (Eds.: ), Kluwer, Dordrecht, 2001, Chap. 19.6, pp. 451–463; T. S. Baker, R. Henderson in International Tables for Crystallography, Vol. F. (Eds.: ), Kluwer, Dordrecht, 2001, Chap. 19.6, pp. 473–479.
- 57“Crystallography of Biological Macromolecules”: T. S. Baker, R. Henderson in International Tables for Crystallography, Vol. F, 2nd ed. (Eds.: ), Wiley, Chichester, 2012, Chap. 19.6, pp. 593–614.
10.1107/97809553602060000872 Google Scholar
- 58N. Grigorieff, R. Henderson, Ultramicroscopy 1995, 60, 295–309.
- 59N. Grigorieff, R. Henderson, Ultramicroscopy 1996, 65, 101–107.
- 60N. Grigorieff, E. Beckmann, F. Zemlin, J. Mol. Biol. 1995, 254, 404–415.
- 61N. Grigorieff, J. Mol. Biol. 1998, 277, 1033–1046.
- 62M. Van Heel, G. Harauz, E. V. Orlova, R. Schmidt, M. Schatz, J. Struct. Biol. 1996, 116, 17–24.
- 63J. Frank, M. Radermacher, P. Penczek, J. Zhu, Y. H. Li, M. Ladjadj, A. Leith, J. Struct. Biol. 1996, 116, 190–199.
- 64P. B. Rosenthal, L. J. Waddington, P. J. Hudson, J. Mol. Biol. 2003, 334, 721–731.
- 65J. L. S. Milne, D. Shi, P. B. Rosenthal, J. S. Sunshine, G. J. Domingo, X. W. Wu, B. R. Brooks, R. N. Perham, R. Henderson, S. Subramaniam, EMBO J. 2002, 21, 5587–5598.
- 66P. B. Rosenthal, R. Henderson, J. Mol. Biol. 2003, 333, 721–745.
- 67R. Henderson, R. M. Glaeser, Ultramicroscopy 1985, 16, 139–150.
- 68R. Henderson, Ultramicroscopy 1992, 46, 1–18.
- 69A. R. Faruqi, H. N. Andrews, R. Henderson, Nucl. Instrum. Methods Phys. Res. Sect. A 1995, 367, 408–412.
- 70A. R. Faruqi, R. Henderson, S. Subramaniam, Ultramicroscopy 1999, 75, 235–250.
- 71A. R. Faruqi, D. M. Cattermole, R. Henderson, B. Mikulec, C. Raeburn, Ultramicroscopy 2003, 94, 263–276.
- 72A. R. Faruqi, R. Henderson, M. Pryddetch, P. Allport, A. Evans, Nucl. Instrum. Methods Phys. Res. Sect. A 2005, 546, 170–175.
- 73M. Caccia, R. Campagnolo, C. Meroni, W. Kucewicz, G. Deptuch, A. Zalewska, R. Turchetta, 1999, arXiv:hep-ex/9910019v1.
- 74G. McMullan, S. Chen, R. Henderson, A. R. Faruqi, Ultramicroscopy 2009, 109, 1126–1143.
- 75G. McMullan, A. R. Faruqi, R. Henderson, N. Guerrini, R. Turchetta, A. Jacobs, G. van Hoften, Ultramicroscopy 2009, 109, 1144–1147.
- 76G. McMullan, A. T. Clark, R. Turchetta, A. R. Faruqi, Ultramicroscopy 2009, 109, 1411–1416.
- 77S. Kleinfelder, H. Bichsel, F. Bieser, H. S. Matis, G. Rai, F. Retiere, H. Weiman, E. Yamamoto, Proc. SPIE 2003, 4784, 208–217.
10.1117/12.450826 Google Scholar
- 78N. H. Xuong, A. C. Milazzo, P. LeBlanc, F. Duttweiler, J. Bouwer, S. Peltier, M. Ellisman, P. Denes, F. Bieser, H. S. Matis, H. Wieman, S. Kleinfelder, Proc. SPIE 2004, 5301, 242–249.
10.1117/12.526021 Google Scholar
- 79A. C. Milazzo, P. Leblanc, F. Duttweiler, L. Jin, J. C. Bouwer, S. Peltier, M. Ellisman, F. Bieser, H. S. Matis, H. Wieman, P. Denes, S. Kleinfelder, N. H. Xuong, Ultramicroscopy 2005, 104, 152–159.
- 80G. McMullan, A. R. Faruqi, D. Clare, R. Henderson, Ultramicroscopy 2014, 147, 156–163.
- 81A. F. Brilot, J. Z. Chen, A. C. Cheng, J. H. Pan, S. C. Harrison, C. S. Potter, B. Carragher, R. Henderson, N. Grigorieff, J. Struct. Biol. 2012, 177, 630–637.
- 82M. G. Campbell, A. C. Cheng, A. F. Brilot, A. Moeller, D. Lyumkis, D. Veesler, J. H. Pan, S. C. Harrison, C. S. Potter, B. Carragher, N. Grigorieff, Structure 2012, 20, 1823–1828.
- 83X.-C. Bai, I. S. Fernandez, G. McMullan, S. H. W. Scheres, eLife 2013, 00461.
- 84X. M. Li, P. Mooney, S. Zheng, C. R. Booth, M. B. Braunfeld, S. Gubbens, D. A. Agard, Y. F. Cheng, Nat. Methods 2013, 10, 584–590.
- 85S. H. W. Scheres, eLife 2014, 03665.
- 86K. R. Vinothkumar, G. McMullan, R. Henderson, Structure 2014, 22, 621–627.
- 87J. L. Rubinstein, M. A. Brubaker, J. Struct. Biol. 2015, 192, 188–195.
- 88T. Grant, N. Grigorieff, eLife 2015, 06980.
- 89S. H. W. Scheres, J. Struct. Biol. 2012, 180, 519–530.
- 90M. F. Liao, E. H. Cao, D. Julius, Y. F. Cheng, Nature 2013, 504, 107–112.
- 91A. Amunts, A. Brown, X.-C. Bai, J. L. Llacer, T. Hussain, P. Emsley, F. Long, G. Murshudov, S. H. W. Scheres, V. Ramakrishnan, Science 2014, 343, 1485–1489.
- 92M. Allegretti, D. J. Mills, G. McMullan, W. Kühlbrandt, J. Vonck, eLife 2014, 01963.
- 93W. Kühlbrandt, Science 2014, 343, 1443–1444.
- 94R. Henderson, S. X. Chen, J. Z. Chen, N. Grigorieff, L. A. Passmore, L. Ciccarelli, J. L. Rubinstein, R. A. Crowther, P. L. Stewart, P. B. Rosenthal, J. Mol. Biol. 2011, 413, 1028–1046.
- 95A. Bartesaghi, A. Merk, S. Banerjee, D. Matthies, X. W. Wu, J. L. S. Milne, S. Subramaniam, Science 2015, 348, 1147–1151.
- 96K. R. Vinothkumar, J. P. Zhu, J. Hirst, Nature 2014, 515, 80–84.
- 97J. P. Zhu, K. R. Vinothkumar, J. Hirst, Nature 2016, 536, 354–360.
- 98J. L. Rubinstein, J. E. Walker, R. Henderson, EMBO J. 2003, 22, 6182–6192.
- 99A. N. Zhou, A. Rohou, D. G. Schep, J. V. Bason, M. G. Montgomery, J. E. Walker, N. Grigorieff, J. L. Rubinstein, eLife 2015, 10180.
- 100H. Guo, S. A. Bueler, J. L. Rubinstein, Science 2017, 358, 936–940.
- 101R. Henderson, Arch. Biochem. Biophys. 2015, 581, 19–24.
- 102S. A. Müller, A. Engel, Micron 2001, 32, 21–31.
- 103G. McMullan, K. R. Vinothkumar, R. Henderson, Ultramicroscopy 2015, 158, 26–32.
- 104J. Brink, M. B. Sherman, J. Berriman, W. Chiu, Ultramicroscopy 1998, 72, 41–52.
- 105C. J. Russo, R. Henderson, Ultramicroscopy 2018, 187, 43–49.
- 106C. J. Russo, R. Henderson, Ultramicroscopy 2018, 187, 56–63.
- 107C. J. Russo, L. A. Passmore, Science 2014, 346, 1377–1380.
- 108J. A. Berriman, P. B. Rosenthal, Ultramicroscopy 2012, 116, 106–114.
- 109S. Q. Zheng, E. Palovcak, J.-P. Armache, K. A. Verba, Y. Cheng, D. A. Agard, Nat. Methods 2017, 14, 331–332.
- 110S. H. W. Scheres, H. X. Gao, M. Valle, G. T. Herman, P. P. B. Eggermont, J. Frank, J. M. Carazo, Nat. Methods 2007, 4, 27–29.
