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Microcrystal electron diffraction methodology and applications

Published online by Cambridge University Press:  10 December 2019

Brent L. Nannenga
Affiliation:
School for Engineering Matter, Transport and Energy, Arizona State University, USA; brent.nannenga@asu.edu
Tamir Gonen
Affiliation:
Howard Hughes Medical Institute, Departments of Biological Chemistry and Physiology, University of California, Los Angeles, USA; tgonen@g.ucla.edu
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Abstract

Microcrystal electron diffraction (MicroED) is a cryo-electron microscopy technique that utilizes three-dimensional nano- and microcrystals for high-resolution structure determination. These extremely small crystals are several orders of magnitude smaller than what is used in conventional x-ray diffraction experiments. MicroED is capable of providing high-quality data from samples that would otherwise be considered useless for diffraction measurements. Since its initial implementation, MicroED has been used in the fields of structural biology, chemistry, and materials science. In this article, we provide an overview of the MicroED methodology as well as examples of how MicroED in cryo-electron microscopy has been used for structure determination of a variety of samples.

Type
Cryogenic Electron Microscopy in Materials Science
Copyright
Copyright © Materials Research Society 2019 

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References

Nannenga, B.L., Gonen, T., Nat. Methods 16, 369 (2019).10.1038/s41592-019-0395-xCrossRefGoogle Scholar
Jones, C.G., Martynowycz, M.W., Hattne, J., Fulton, T.J., Stoltz, B.M., Rodriguez, J.A., Nelson, H.M., Gonen, T., ACS Cent. Sci. 4, 1587 (2018).10.1021/acscentsci.8b00760CrossRefGoogle Scholar
Gruene, T., Wennmacher, J.T.C., Zaubitzer, C., Holstein, J.J., Heidler, J., Fecteau-Lefebvre, A., De Carlo, S., Muller, E., Goldie, K.N., Regeni, I., Li, T., Santiso-Quinones, G., Steinfeld, G., Handschin, S., van Genderen, E., van Bokhoven, J.A., Clever, G.H., Pantelic, R., Angew. Chem. Int. Ed. Engl. 57, 16313 (2018).CrossRefGoogle Scholar
Shi, D., Nannenga, B.L., de la Cruz, M.J., Liu, J., Sawtelle, S., Calero, G., Reyes, F.E., Hattne, J., Gonen, T., Nat. Protoc. 11, 895 (2016).10.1038/nprot.2016.046CrossRefGoogle Scholar
Nannenga, B.L., Shi, D., Leslie, A.G., Gonen, T., Nat. Methods 11, 927 (2014).10.1038/nmeth.3043CrossRefGoogle Scholar
Hattne, J., Shi, D., Glynn, C., Zee, C.T., Gallagher-Jones, M., Martynowycz, M.W., Rodriguez, J.A., Gonen, T., Structure 26, 759 (2018).10.1016/j.str.2018.03.021CrossRefGoogle Scholar
Leslie, A.G.W., Powell, H.R., Evolving Methods for Macromolecular Crystallography 245, 41, Read, R.J., Sussman, J.L., Eds. (Springer, Dordrecht, The Netherlands, 2007).10.1007/978-1-4020-6316-9_4CrossRefGoogle Scholar
Kabsch, W., Acta Crystallogr. D Biol. Crystallogr. 66, 125 (2010).10.1107/S0907444909047337CrossRefGoogle Scholar
Clabbers, M.T.B., Gruene, T., Parkhurst, J.M., Abrahams, J.P., Waterman, D.G., Acta Crystallogr. D Struct. Biol. 74, 506 (2018).10.1107/S2059798318007726CrossRefGoogle Scholar
Hattne, J., Reyes, F.E., Nannenga, B.L., Shi, D., de la Cruz, M.J., Leslie, A.G., Gonen, T., Acta Crystallogr. A Found. Adv. 71, 353 (2015).CrossRefGoogle Scholar
Martynowycz, M.W., Zhao, W., Hattne, J., Jensen, G.J., Gonen, T., Structure 27, 545 (2019).CrossRefGoogle Scholar
de la Cruz, M.J., Martynowycz, M.W., Hattne, J., Gonen, T., Ultramicroscopy 201, 77 (2019).10.1016/j.ultramic.2019.03.009CrossRefGoogle Scholar
Passmore, L.A., Russo, C.J., Methods Enzymol . 579, 51 (2016).10.1016/bs.mie.2016.04.011CrossRefGoogle Scholar
Lanza, A., Margheritis, E., Mugnaioli, E., Cappello, V., Garau, G., Gemmi, M., IUCrJ 6, 178 (2019).10.1107/S2052252518017657CrossRefGoogle Scholar
Zhou, H., Luo, F., Luo, Z., Li, D., Liu, C., Li, X., Anal. Chem. 91, 10996 (2019).10.1021/acs.analchem.9b01162CrossRefGoogle Scholar
van Genderen, E., Clabbers, M.T., Das, P.P., Stewart, A., Nederlof, I., Barentsen, K.C., Portillo, Q., Pannu, N.S., Nicolopoulos, S., Gruene, T., Abrahams, J.P., Acta Crystallogr. A Found. Adv. 72 (2), 236 (2016).CrossRefGoogle Scholar
Tinti, G., Frojdh, E., van Genderen, E., Gruene, T., Schmitt, B., de Winter, D.A.M., Weckhuysen, B.M., Abrahams, J.P., IUCrJ . 5 (2), 190 (2018).CrossRefGoogle Scholar
Hattne, J., Martynowycz, M.W., Penczek, P.A., Gonen, T., IUCrJ . 6 (5), 921 (2019).10.1107/S2052252519010583CrossRefGoogle Scholar
Mastronarde, D.N., J. Struct. Biol. 152, 36 (2005).10.1016/j.jsb.2005.07.007CrossRefGoogle Scholar
McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C., Read, R.J., J. Appl. Crystallogr. 40, 658 (2007).10.1107/S0021889807021206CrossRefGoogle Scholar
Vagin, A., Teplyakov, A., J. Appl. Crystallogr. 30, 1022 (1997).CrossRefGoogle Scholar
Sheldrick, G., Acta Crystallogr. A Found. Crystallogr. 64, 112 (2008).10.1107/S0108767307043930CrossRefGoogle Scholar
Afonine, P.V., Grosse-Kunstleve, R.W., Echols, N., Headd, J.J., Moriarty, N.W., Mustyakimov, M., Terwilliger, T.C., Urzhumtsev, A., Zwart, P.H., Adams, P.D., Acta Crystallogr. D Biol. Crystallogr. 68, 352 (2012).CrossRefGoogle Scholar
Murshudov, G.N., Vagin, A.A., Dodson, E.J., Acta Crystallogr. D Biol. Crystallogr. 53, 240 (1997).10.1107/S0907444996012255CrossRefGoogle Scholar
Sheldrick, G.M., Acta Crystallogr. C Struct. Chem. 71, 3 (2015).CrossRefGoogle Scholar
Hubschle, C.B., Sheldrick, G.M., Dittrich, B., J. Appl. Crystallogr. 44, 1281 (2011).CrossRefGoogle Scholar
Shi, D., Nannenga, B.L., Iadanza, M.G., Gonen, T., Elife 2, e01345 (2013).10.7554/eLife.01345CrossRefGoogle Scholar
Nannenga, B.L., Shi, D., Hattne, J., Reyes, F.E., Gonen, T., Elife 3, e03600 (2014).10.7554/eLife.03600CrossRefGoogle Scholar
Yonekura, K., Kato, K., Ogasawara, M., Tomita, M., Toyoshima, C., Proc. Natl. Acad. Sci. U.S.A. 112, 3368 (2015).CrossRefGoogle Scholar
Hattne, J., Shi, D., de la Cruz, M.J., Reyes, F.E., Gonen, T., J. Appl. Crystallogr. 49, 1029 (2016).10.1107/S1600576716007196CrossRefGoogle Scholar
Purdy, M.D., Shi, D., Chrustowicz, J., Hattne, J., Gonen, T., Yeager, M., Proc. Natl. Acad. Sci. U.S.A. 115, 13258 (2018).CrossRefGoogle Scholar
de la Cruz, M.J., Hattne, J., Shi, D., Seidler, P., Rodriguez, J., Reyes, F.E., Sawaya, M.R., Cascio, D., Weiss, S.C., Kim, S.K., Hinck, C.S., Hinck, A.P., Calero, G., Eisenberg, D., Gonen, T., Nat. Methods 14, 399 (2017).CrossRefGoogle Scholar
Xu, H., Lebrette, H., Clabbers, M.T.B., Zhao, J., Griese, J.J., Zou, X., Högbom, M., Sci. Adv. 5 (2019).Google Scholar
Liu, S., Gonen, T., Commun. Biol. 1, 38 (2018).CrossRefGoogle Scholar
Rodriguez, J.A., Eisenberg, D.S., Gonen, T., Curr. Opin. Struct. Biol. 46, 79 (2017).CrossRefGoogle Scholar
Nannenga, B.L., Gonen, T., Curr. Opin. Struct. Biol. 40, 128 (2016).10.1016/j.sbi.2016.09.007CrossRefGoogle Scholar
Seidler, P.M., Boyer, D.R., Rodriguez, J.A., Sawaya, M.R., Cascio, D., Murray, K., Gonen, T., Eisenberg, D.S., Nat. Chem. 10, 170 (2018).CrossRefGoogle Scholar
Krotee, P., Griner, S.L., Sawaya, M.R., Cascio, D., Rodriguez, J.A., Shi, D., Philipp, S., Murray, K., Saelices, L., Lee, J., Seidler, P., Glabe, C.G., Jiang, L., Gonen, T., Eisenberg, D.S., J. Biol. Chem. 293, 2888 (2018).10.1074/jbc.M117.806109CrossRefGoogle Scholar
Guenther, E.L., Ge, P., Trinh, H., Sawaya, M.R., Cascio, D., Boyer, D.R., Gonen, T., Zhou, Z.H., Eisenberg, D.S., Nat. Struct. Mol. Biol. 25, 311 (2018).CrossRefGoogle Scholar
Gallagher-Jones, M., Glynn, C., Boyer, D.R., Martynowycz, M.W., Hernandez, E., Miao, J., Zee, C.T., Novikova, I.V., Goldschmidt, L., McFarlane, H.T., Helguera, G.F., Evans, J.E., Sawaya, M.R., Cascio, D., Eisenberg, D.S., Gonen, T., Rodriguez, J.A., Nat. Struct. Mol. Biol. 25, 131 (2018).CrossRefGoogle Scholar
Krotee, P., Rodriguez, J.A., Sawaya, M.R., Cascio, D., Reyes, F.E., Shi, D., Hattne, J., Nannenga, B.L., Oskarsson, M.E., Philipp, S., Griner, S., Jiang, L., Glabe, C.G., Westermark, G.T., Gonen, T., Eisenberg, D.S., Elife 6, e19273 (2017).10.7554/eLife.19273CrossRefGoogle Scholar
Sawaya, M.R., Rodriguez, J., Cascio, D., Collazo, M.J., Shi, D., Reyes, F.E., Hattne, J., Gonen, T., Eisenberg, D.S., Proc. Natl. Acad. Sci. U.S.A. 133, 11232 (2016).10.1073/pnas.1606287113CrossRefGoogle Scholar
Vergara, S., Lukes, D.A., Martynowycz, M.W., Santiago, U., Plascencia-Villa, G., Weiss, S.C., de la Cruz, M.J., Black, D.M., Alvarez, M.M., Lopez-Lozano, X., Barnes, C.O., Lin, G., Weissker, H.C., Whetten, R.L., Gonen, T., Yacaman, M.J., Calero, G., J. Phys. Chem. Lett. 8, 5523 (2017).CrossRefGoogle Scholar
Wan, W., Sun, J.L., Su, J., Hovmoller, S., Zou, X.D., J. Appl. Crystallogr. 46, 1863 (2013).CrossRefGoogle Scholar
Mugnaioli, E., Gorelik, T., Kolb, U., Ultramicroscopy 109, 758 (2009).CrossRefGoogle Scholar
Denysenko, D., Grzywa, M., Tonigold, M., Streppel, B., Krkljus, I., Hirscher, M., Mugnaioli, E., Kolb, U., Hanss, J., Volkmer, D., Chemistry 17, 1837 (2011).CrossRefGoogle Scholar
Kolb, U., Mugnaioli, E., Gorelik, T.E., Cryst. Res. Technol. 46, 542 (2011).CrossRefGoogle Scholar
Mugnaioli, E., Andrusenko, I., Schuler, T., Loges, N., Dinnebier, R.E., Panthofer, M., Tremel, W., Kolb, U., Angew. Chem. Int. Ed. Engl. 51, 7041 (2012).CrossRefGoogle Scholar
Gemmi, M., Mugnaioli, E., Gorelik, T.E., Kolb, U., Palatinus, L., Boullay, P., Hovmöller, S., Abrahams, J.P., ACS Cent. Sci. 5, 1315 (2019).CrossRefGoogle Scholar
Ting, C.P., Funk, M.A., Halaby, S.L., Zhang, Z., Gonen, T., van der Donk, W.A., Science 365, 280 (2019).CrossRefGoogle Scholar
Zatsepin, N.A., Li, C., Colasurd, P., Nannenga, B.L., Curr. Opin. Struct. Biol. 58, 286 (2019).CrossRefGoogle Scholar
Nannenga, B.L., Gonen, T., Emerg. Top. Life Sci. 2, 1 (2018).Google Scholar
Rodriguez, J.A., Ivanova, M.I., Sawaya, M.R., Cascio, D., Reyes, F.E., Shi, D., Sangwan, S., Guenther, E.L., Johnson, L.M., Zhang, M., Jiang, L., Arbing, M.A., Nannenga, B.L., Hattne, J., Whitelegge, J., Brewster, A.S., Messerschmidt, M., Boutet, S., Sauter, N.K., Gonen, T., Eisenberg, D.S., Nature 525, 486 (2015).CrossRefGoogle Scholar
Guenther, E.L., Cao, Q., Trinh, H., Lu, J., Sawaya, M.R., Cascio, D., Boyer, D.R., Rodriguez, J.A., Hughes, M.P., Eisenberg, D.S., Nat. Struct. Mol. Biol. 25, 463 (2018).CrossRefGoogle Scholar