Erratum: MicroED: A versatile cryoEM method for structure determination (Emerging Topics in Life Sciences (2018) 2 (1-8) DOI: 10.1042/ETLS20170082);MicroED: A versatile cryoEM method for structure determination

Emerging Topics in Life Sciences

Volumn 2, Issue 1, 2018, Pages 1-8

  Nannenga, Brent L ^a   Gonen, Tamir ^b,c  

^a Arizona State University   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85065168189     PISSN: 23978554     EISSN: 23978562     Source Type: Journal    
DOI: 10.1042/ETLS20170082C_COR     Document Type: Erratum

References (57)

1. Moraes, I., Evans, G., Sanchez-Weatherby, J., Newstead, S. and Stewart, P.D.S. (2014) Membrane protein structure determination - the next generation. Biochim. Biophys. Acta, Biomembranes 1838(Pt A), 78-87 https://doi.org/10.1016/j.bbamem.2013.07.010
2. Chapman, H.N., Fromme P., Barty A., White T.A., Kirian R.A., Aquila A. et al. (2011) Femtosecond X-ray protein nanocrystallography. Nature 470, 73-77 https://doi.org/10.1038/nature09750
3. Kang, Y., Zhou, X.E., Gao, X., He, Y., Liu, W., Ishchenko, A. et al. (2015) Crystal structure of rhodopsin bound to arrestin by femtosecond X-ray laser. Nature 523, 561-567 https://doi.org/10.1038/nature14656
4. Liu, W., Wacker, D., Gati, C., Han, G.W., James, D., Wang, D. et al. (2013) Serial femtosecond crystallography of G protein-coupled receptors. Science 342, 1521-1524 https://doi.org/10.1126/science.1244142
5. Tenboer, J., Basu, S., Zatsepin, N., Pande, K., Milathianaki, D., Frank, M. et al. (2014) Time-resolved serial crystallography captures high-resolution intermediates of photoactive yellow protein. Science 346, 1242-1246 https://doi.org/10.1126/science.1259357
6. Liu, S., Hattne, J., Reyes, F.E., Sanchez-Martinez, S., Jason de la Cruz, M., Shi, D. et al. (2017) Atomic resolution structure determination by the cryo-EM method MicroED. Protein Sci. 26, 8-15 https://doi.org/10.1002/pro.2989
7. Nannenga, B.L. and Gonen, T. (2014) Protein structure determination by MicroED. Curr. Opin. Struct. Biol. 27, 24-31 https://doi.org/10.1016/j.sbi. 2014.03.004
8. Nannenga, B.L. and Gonen, T. (2016) MicroED opens a new era for biological structure determination. Curr. Opin. Struct. Biol. 40, 128-135 https://doi. org/10.1016/j.sbi.2016.09.007
9. Rodriguez, J.A., Eisenberg, D.S. and Gonen, T. (2017) Taking the measure of MicroED. Curr. Opin. Struct. Biol. 46, 79-86 https://doi.org/10.1016/j. sbi.2017.06.004
10. Henderson, R. (1995) The potential and limitations of neutrons, electrons and X-rays for atomic resolution microscopy of unstained biological molecules. Q. Rev. Biophys. 28, 171-193 https://doi.org/10.1017/S003358350000305X
11. Martynowycz, M.W., Glynn, C., Miao, J., de la Cruz, M.J., Hattne, J., Shi, D. et al. (2017) MicroED structures from micrometer thick protein crystals. BioRxiv https://doi.org/10.1101/152504
12. Nannenga, B.L., Shi, D., Leslie, A.G.W. and Gonen, T. (2014) High-resolution structure determination by continuous-rotation data collection in MicroED. Nat. Methods 11, 927-930 https://doi.org/10.1038/nmeth.3043
13. Barnes, C.O., Kovaleva, E.G., Fu, X., Stevenson, H.P., Brewster, A.S., DePonte, D.P. et al. (2016) Assessment of microcrystal quality by transmission electron microscopy for efficient serial femtosecond crystallography. Arch. Biochem. Biophys. 602, 61-68 https://doi.org/10.1016/j.abb.2016.02.011
14. Stevenson, H.P., Makhov, A.M., Calero, M., Edwards, A.L., Zeldin, O.B., Mathews, I.I. et al. (2014) Use of transmission electron microscopy to identify nanocrystals of challenging protein targets. Proc. Natl Acad. Sci. U.S.A. 111, 8470-8475 https://doi.org/10.1073/pnas.1400240111
15. Stevenson, H.P., Lin, G., Barnes, C.O., Sutkeviciute, I., Krzysiak, T., Weiss, S.C. et al. (2016) Transmission electron microscopy for the evaluation and optimization of crystal growth. Acta Crystallogr., Sect. D: Struct. Biol. 72(Pt 5), 603-615 https://doi.org/10.1107/S2059798316001546
16. Wampler, R.D., Kissick, D.J., Dehen, C.J., Gualtieri, E.J., Grey, J.L., Wang, H.-F. et al. (2008) Selective detection of protein crystals by second harmonic microscopy. J. Am. Chem. Soc. 130, 14076-14077 https://doi.org/10.1021/ja805983b
17. de la Cruz, M.J., Hattne, J., Shi, D., Seidler, P., Rodriguez, J., Reyes, F.E. et al. (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
18. Shi, D., Nannenga, B.L., de la Cruz, M.J., Liu, J., Sawtelle, S., Calero, G. et al. (2016) The collection of MicroED data for macromolecular crystallography. Nat. Protoc. 11, 895-904 https://doi.org/10.1038/nprot.2016.046
19. Dubochet, J., Booy, F.P., Freeman, R., Jones, A.V. and Walter, C.A. (1981) Low temperature electron microscopy. Annu. Rev. Biophys. Bioeng. 10, 133-149 https://doi.org/10.1146/annurev.bb.10.060181.001025
20. Grassucci, R.A., Taylor, D.J. and Frank, J. (2007) Preparation of macromolecular complexes for cryo-electron microscopy. Nat. Protoc. 2, 3239-3246 https://doi.org/10.1038/nprot.2007.452
21. Mastronarde, D.N. (2005) Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152, 36-51 https://doi.org/10.1016/j.jsb.2005.07.007
22. Hattne, J., Reyes, F.E., Nannenga, B.L., Shi, D., de la Cruz, M.J., Leslie, A.G.W. et al. (2015) MicroED data collection and processing. Acta Crystallogr., Sect. A: Found. Adv. 71(Pt 4), 353-360 https://doi.org/10.1107/S2053273315010669
23. Arndt, U.W. and Wonacott, A.J. (1977) The Rotation Method in Crystallography: Data Collection From Macromolecular Crystals. North-Holland Pub. Co., sole distributors for the U.S.A. and Canada, Elsevier/North-Holland, Amsterdam, New York, NY. pp. xvii, 275p
24. Battye, T.G.G., Kontogiannis, L., Johnson, O., Powell, H.R. and Leslie, A.G.W. (2011) iMOSFLM: A new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr., Sect. D: Biol. Crystallogr. 67(Pt 4), 271-281 https://doi.org/10.1107/S0907444910048675
25. Leslie, A.G.W. and Powell, H.R. (2007) Processing diffraction data with mosflm. In Evolving Methods for Macromolecular Crystallography (Read, R.J. and Sussman, J.L., eds), vol. 245, NATO Science Series, Springer, Dordrecht https://doi.org/10.1007/978-1-4020-6316-9_4
26. Waterman, D.G., Winter, G., Parkhurst, J.M., Fuentes-Montero, L., Hattne, J., Brewster, A. et al. (2013) The DIALS framework for integration software. CCP4 Newsl. Protein Crystallogr. 49, 16-19
27. Kabsch, W. (2010) XDS. Acta Crystallogr., Sect. D: Biol. Crystallogr. 66(Pt 2), 125-132 https://doi.org/10.1107/S0907444909047337
28. Winn, M.D., Ballard, C.C., Cowtan, K.D., Dodson, E.J., Emsley, P., Evans, P.R. et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr., Sect. D: Biol. Crystallogr. 67, 235-242 https://doi.org/10.1107/S0907444910045749
29. Adams, P.D., Afonine, P.V., Bunkóczi, G., Chen, V.B., Davis, I.W., Echols, N. et al. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 213-221 https://doi.org/10.1107/S0907444909052925
30. Hattne, J., Shi, D., de la Cruz, M.J., Reyes, F.E. and Gonen, T. (2016) Modeling truncated pixel values of faint reflections in MicroED images. J. Appl. Crystallogr. 49(Pt 3), 1029-1034 https://doi.org/10.1107/S1600576716007196
31. Krotee, P., Rodriguez, J.A., Sawaya, M.R., Cascio, D., Reyes, F.E., Shi, D. et al. (2017) Atomic structures of fibrillar segments of hIAPP suggest tightly mated β-sheets are important for cytotoxicity. eLife 6, e12977 https://doi.org/10.7554/eLife.19273
32. Nannenga, B.L., Shi, D., Hattne, J., Reyes, F.E. and Gonen, T. (2014) Structure of catalase determined by MicroED. eLife 3, e03600 https://doi.org/10. 7554/eLife.03600
33. Sawaya, M.R., Rodriguez, J., Cascio, D., Collazo, M.J., Shi, D., Reyes, F.E. et al. (2016) Ab initio structure determination from prion nanocrystals at atomic resolution by MicroED. Proc. Natl Acad. Sci. U.S.A. 113, 11232-11236 https://doi.org/10.1073/pnas.1606287113
34. Shi, D., Nannenga, B.L., Iadanza, M.G. and Gonen, T. (2013) Three-dimensional electron crystallography of protein microcrystals. eLife 2, e01345 https://doi.org/10.7554/eLife.01345
35. Vergara, S., Lukes, D.A., Martynowycz, M.W., Santiago, U., Plascencia-Villa, G., Weiss, S.C. et al. (2017) MicroED structure of Au146(p-MBA)57 at subatomic resolution reveals a twinned FCC cluster. J. Phys. Chem. Lett. 8, 5523-5530 https://doi.org/10.1021/acs.jpclett.7b02621
36. Yonekura, K. and Maki-Yonekura, S. (2016) Refinement of cryo-EM structures using scattering factors of charged atoms. J. Appl. Crystallogr. 49, 1517-1523 https://doi.org/10.1107/S1600576716011274
37. Clabbers, M.T.B., van Genderen, E., Wan, W., Wiegers, E.L., Gruene, T. and Abrahams, J.P. (2017) Protein structure determination by electron diffraction using a single three-dimensional nanocrystal. Acta Crystallogr., Sect. D: Struct. Biol. 73(Pt 9), 738-748 https://doi.org/10.1107/S2059798317010348
38. Nederlof, I., van Genderen, E., Li, Y.-W. and Abrahams, J.P. (2013) A Medipix quantum area detector allows rotation electron diffraction data collection from submicrometre three-dimensional protein crystals. Acta Crystallogr., Sect. D: Biol. Crystallogr. 69(Pt 7), 1223-1230 https://doi.org/10.1107/S0907444913009700
39. Gonen, T. (2013) The collection of high-resolution electron diffraction data. Methods Mol. Biol. 955, 153-169 https://doi.org/10.1007/978-1-62703-176-9_9
40. 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
41. Sumner, J.B. and Dounce, A.L. (1937) Crystalline catalase. Science 85, 366-367 https://doi.org/10.1126/science.85.2206.366
42. Unwin, P.N.T. and Henderson, R. (1975) Molecular structure determination by electron microscopy of unstained crystalline specimens. J. Mol. Biol. 94, 425-440 https://doi.org/10.1016/0022-2836(75)90212-0
43. Unwin, P.N.T. (1975) Beef liver catalase structure: Interpretation of electron micrographs. J. Mol. Biol. 98, 235-242 https://doi.org/10.1016/S0022-2836(75)80111-2
44. Dorset, D.L. and Parsons, D.F. (1975) Electron diffraction from single, fully-hydrated, ox-liver catalase microcrystals. Acta Crystallogr., Sect. A 31, 210-215 https://doi.org/10.1107/S0567739475000423
45. Dorset, D.L. and Parsons, D.F. (1975) Thickness measurements of wet protein crystals in the electron microscope. J. Appl. Crystallogr. 8, 12-14 https://doi.org/10.1107/S0021889875009430
46. Matricar, V.R., Moretz, R.C. and Parsons, D.F. (1972) Electron diffraction of wet proteins: Catalase. Science 177, 268-270 https://doi.org/10.1126/science.177.4045.268
47. Rodriguez, J.A., Ivanova, M.I., Sawaya, M.R., Cascio, D., Reyes, F.E., Shi, D. et al. (2015) Structure of the toxic core of α-synuclein from invisible crystals. Nature 525, 486-490 https://doi.org/10.1038/nature15368
48. Gorelik, T.E., Stewart, A.A. and Kolb, U. (2011) Structure solution with automated electron diffraction tomography data: Different instrumental approaches. J. Microsc. 244, 325-331 https://doi.org/10.1111/j.1365-2818.2011.03550.x
49. Mugnaioli, E., Gorelik, T. and Kolb, U. (2009) 'Ab initio' structure solution from electron diffraction data obtained by a combination of automated diffraction tomography and precession technique. Ultramicroscopy 109, 758-765 https://doi.org/10.1016/j.ultramic.2009.01.011
50. van Genderen, E., Clabbers, M.T.B., Das, P.P., Stewart, A., Nederlof, I., Barentsen, K.C. et al. (2016) Ab initio structure determination of nanocrystals of organic pharmaceutical compounds by electron diffraction at room temperature using a Timepix quantum area direct electron detector. Acta Crystallogr., Sect. A: Found. Adv. 72(Pt 2), 236-242 https://doi.org/10.1107/S2053273315022500
51. Mugnaioli, E., Andrusenko, I., Schüler, T., Loges, N., Dinnebier, R.E., Panthöfer, M. et al. (2012) Ab initio structure determination of vaterite by automated electron diffraction. Angew. Chem. Int. Ed. 51, 7041-7045 https://doi.org/10.1002/anie.201200845
52. Baerlocher, C., Gramm, F., Massuger, L., McCusker, L.B., He, Z., Hovmoller, S. et al. (2007) Structure of the polycrystalline zeolite catalyst IM-5 solved by enhanced charge flipping. Science 315, 1113-1116 https://doi.org/10.1126/science.1137920
53. Martinez-Franco, R., Moliner, M., Yun, Y., Sun, J., Wan, W., Zou, X. et al. (2013) Synthesis of an extra-large molecular sieve using proton sponges as organic structure-directing agents. Proc. Natl Acad. Sci. U.S.A. 110, 3749-3754 https://doi.org/10.1073/pnas.1220733110
54. Sun, J.L., Bonneau, C., Cantín, Á., Corma, A., Díaz-Cabañas, M.J., Moliner, M. et al. (2009) The ITQ-37 mesoporous chiral zeolite. Nature 458, 1154-1157 https://doi.org/10.1038/nature07957
55. Zhang, Y.-B., Su, J., Furukawa, H., Yun, Y., Gándara, F., Duong, A. et al. (2013) Single-crystal structure of a covalent organic framework. J. Am. Chem. Soc. 135, 16336-16339 https://doi.org/10.1021/ja409033p
56. Wu, J.S. and Spence, J.C.H. (2003) Structure and bonding in α-copper phthalocyanine by electron diffraction. Acta Crystallogr., Sect. A: Found. Adv. 59(Pt 5), 495-505 https://doi.org/10.1107/S0108767303016866
57. Zuo, J.M., Kim, M., O'Keeffe, M. and Spence, J.C.H. (1999) Direct observation of d-orbital holes and Cu-Cu bonding in Cu2O. Nature 401, 49-52 https://doi.org/10.1038/43403 ©