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Cryo-scanning transmission electron tomography of biological cells

Published online by Cambridge University Press:  07 July 2016

Michael Elbaum ,
Sharon G. Wolf  and
Lothar Houben
Michael Elbaum
Affiliation:
Department of Materials and Interfaces, Weizmann Institute of Science, Israel; michael.elbaum@weizmann.ac.il
Sharon G. Wolf
Affiliation:
Department of Chemical Research Support, Weizmann Institute of Science, Israel; sharon.wolf@weizmann.ac.il
Lothar Houben
Affiliation:
Department of Chemical Research Support, Weizmann Institute of Science, Israel; lothar.houben@weizmann.ac.il
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Abstract

The electron microscope has made paramount contributions to understanding the structure of biological molecules, cells, and tissues. In general, the most faithful preservation of biological specimens and other soft-organic materials is achieved through cryogenic fixation. The embedding medium is the native aqueous environment itself, immobilized in vitrified form by rapid or pressurized cooling. Until recently, imaging of such vitrified thin specimens by electron cryo-microscopy has been nearly synonymous with wide-field transmission electron microscopy (TEM). Several new approaches have entered the cryo-microscopy field, including soft x-ray imaging, serial surface imaging using focused ion beam scanning electron microscopy, phase plates, and scanning TEM (STEM). In this article, we focus on the STEM method and its adaptation to biological cryo-microscopy. Cryogenic imaging of unstained specimens by STEM introduces specific challenges. Difficulties were long considered insurmountable, and the potential advantages were underappreciated. Future developments in experimental setup and detector technologies will allow for extension of the method to thicker specimens with improved resolution and analytic capabilities.

Keywords

scanning transmission electron microscopy (STEM)biologicalcellular
Type
Research Article
Information
MRS Bulletin , Volume 41 , Issue 7: Advanced Tomography Techniques for Materials Applications , July 2016 , pp. 542 - 548
Copyright
Copyright © Materials Research Society 2016 

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References

Frank, J., Electron Tomography: Methods for Three-Dimensional Visualization of Structures in the Cell (Springer, New York, 2008).Google Scholar
Gan, L., Jensen, G.J., Q. Rev. Biophys. 45, 27 (2012).Google Scholar
Micheva, K.D., Smith, S.J., Neuron 55, 25 (2007).Google Scholar
Wacker, I., Schroeder, R., J. Microsc. 252, 93 (2013).CrossRefGoogle Scholar
Denk, W., Horstmann, H., PLoS Biol. 2, e329 (2004).Google Scholar
Heymann, J.A.W., Shi, D., Kim, S., Bliss, D., Milne, J.L.S., Subramaniam, S., J. Struct. Biol. 166, 1 (2009).CrossRefGoogle Scholar
Weiner, A., Dahan-Pasternak, N., Shimoni, E., Shinder, V., von Huth, P., Elbaum, M., Dzikowski, R., Cell. Microbiol. 13, 967 (2011).Google Scholar
De Rosier, D.J., Klug, A., Nature 217, 130 (1968).CrossRefGoogle Scholar
Shu, X., Lev-Ram, V., Deerinck, T.J., Qi, Y., Ramko, E.B., Davidson, M.W., Jin, Y., Ellisman, M.H., Tsien, R.Y., PLoS Biol. 9, e1001041 (2011).Google Scholar
Diestra, E., Fontana, J., Guichard, P., Marco, S., Risco, C., J. Struct. Biol. 165, 157 (2009).CrossRefGoogle Scholar
Watanabe, S., Punge, A., Hollopeter, G., Willig, K.I., Hobson, R.J., Davis, M.W., Hell, S.W., Jorgensen, E.M., Nat. Methods 8, 80 (2011).Google Scholar
Zhang, P., Curr. Opin. Struct. Biol. 23, 763 (2013).CrossRefGoogle Scholar
Mellouk, N., Weiner, A., Aulner, N., Schmitt, C., Elbaum, M., Shorte, S.L., Danckaert, A., Enninga, J., Cell Host Microbe 16, 517 (2014).Google Scholar
Koster, J., Grünewald, K., Ultramicroscopy 143, 1 (2014).Google Scholar
Falls, H., Davis, H.T., Scriven, L.E., Talmon, Y., Biochim. Biophys. Acta Biomembr. 693, 364 (1982).Google Scholar
Lepault, J., Booy, F.P., Dubochet, J., J. Microsc. 129, 89 (1983).Google Scholar
Dahl, R., Staehelin, L.A., J. Electron Microsc. Tech. 13, 165 (1989).CrossRefGoogle Scholar
Medalia, O., Weber, I., Frangakis, A.S., Nicastro, D., Gerisch, G., Baumeister, W., Science 298, 1209 (2002).Google Scholar
Lučič, V., Rigort, A., Baumeister, W., J. Cell Biol. 202, 407 (2013).Google Scholar
Diebolder, A., Koster, A.J., Koning, R.I., J. Microsc. 248, 1 (2012).CrossRefGoogle Scholar
Kühlbrandt, W., eLife 3, e03678 (2014).Google Scholar
Al-Amoudi, A., Chang, J.-J., Leforestier, A., McDowall, A., Salamin, L.M., Norlén, L.P., Richter, K., Blanc, N.S., Studer, D., Dubochet, J., EMBO J. 23, 3583 (2004).CrossRefGoogle Scholar
Villa, E., Schaffer, M., Plitzko, J.M., Baumeister, W., Curr. Opin. Struct. Biol. 23, 771 (2013).Google Scholar
Hsieh, A., Schmelzer, T., Kishchenko, G., Wagenknecht, T., Marko, M., J. Struct. Biol. 185, 32 (2014).CrossRefGoogle Scholar
Li, X., Mooney, P., Zheng, S., Booth, C.R., Braunfeld, M.B., Gubbens, S., Agard, D.A., Cheng, Y., Nat. Methods 10, 584 (2013).Google Scholar
Bharat, T.A.M., Russo, C.J., Löwe, J., Passmore, L.A., Scheres, S.H.W., Structure 23, 1743 (2015).Google Scholar
Schneider, G., Guttmann, P., Heim, S., Rehbein, S., Mueller, F., Nagashima, K., Heymann, J.B., Müller, W.G., McNally, J.G., Nat. Methods 7, 985 (2010).Google Scholar
Kapishnikov, S., Weiner, A., Shimoni, E., Guttmann, P., Schneider, G., Dahan-Pasternak, N., Dzikowski, R., Leiserowitz, L., Elbaum, M., Proc. Natl. Acad. Sci. U.S.A. 109, 11188 (2012).CrossRefGoogle Scholar
Do, M., Isaacson, S.A., McDermott, G., Le Gros, M.A., Larabell, C.A., Arch. Biochem. Biophys. (2015), doi:10.1016/j.abb.2015.01.011.Google Scholar
Schertel, A., Snaidero, N., Han, H.-M., Ruhwedel, T., Laue, M., Grabenbauer, M., Möbius, W., J. Struct. Biol. 184, 355 (2013).Google Scholar
Vidavsky, N., Masic, A., Schertel, A., Weiner, S., Addadi, L., J. Struct. Biol. 192, 358 (2015).Google Scholar
Wolf, S.G., Houben, L., Elbaum, M., Nat. Methods 11, 423 (2014).CrossRefGoogle Scholar
Muller, A., Nat. Mater. 8, 263 (2009).Google Scholar
Krivanek, O.L., Chisholm, M.F., Nicolosi, V., Pennycook, T.J., Corbin, G.J., Dellby, N., Murfitt, M.F., Own, C.S., Szilagyi, Z.S., Oxley, M.P., Pantelides, S.T., Pennycook, S.J., Nature 464, 571 (2010).Google Scholar
Pennycook, S.J., Ultramicroscopy 123, 28 (2012).Google Scholar
Colliex, C., C. R. Phys. 15, 101 (2014).Google Scholar
Colliex, C., Gloter, A., March, K., Mory, C., Stéphan, O., Suenaga, K., Tencé, M., Ultramicroscopy 123, 80 (2012).Google Scholar
Wall, J.S., Hainfeld, J.F., Annu. Rev. Biophys. Biophys. Chem. 15, 355 (1986).Google Scholar
Engel, A., in Advances in Imaging and Electron Physics, Hawkes, P.W., Ed. (Elsevier, San Diego, 2009), vol. 159, pp. 357–386.Google Scholar
Trachtenberg, S., Leonard, K.R., Tichelaar, W., Ultramicroscopy 45, 307 (1992).Google Scholar
Carlemalm, E., Kellenberger, E., EMBO J. 1, 63 (1982).Google Scholar
Kellenberger, E., Carlemalm, E., Villiger, W., Wurtz, M., Mory, C., Colliex, C., Ann. N.Y. Acad. Sci. 483, 202 (1986).Google Scholar
Wu, J.S., Kim, A.M., Bleher, R., Myers, B.D., Marvin, R.G., Inada, H., Nakamura, K., Zhang, X.F., Roth, E., Li, S.Y., Woodruff, T.K., O’Halloran, T.V., Dravid, V.P., Ultramicroscopy 128, 24 (2013).Google Scholar
Klein, T., Buhr, E., Frase, C.G., in Advances in Imaging and Electron Physics, Hawkes, P.W., Ed. (Elsevier, San Diego, 2012), vol. 171, pp. 297–356.Google Scholar
Aronova, M.A., Leapman, R.D., MRS Bull. 37, 53 (2012).Google Scholar
Yakushevska, A.E., Lebbink, M.N., Geerts, W.J.C., Spek, L., van Donselaar, E.G., Jansen, K.A., Humbel, B.M., Post, J.A., Verkleij, A.J., Koster, A.J., J. Struct. Biol. 159, 381 (2007).Google Scholar
Aoyama, K., Takagi, T., Hirase, A., Miyazawa, A., Ultramicroscopy 109, 70 (2008).Google Scholar
Hohmann-Marriott, M.F., Sousa, A.A., Azari, A.A., Glushakova, S., Zhang, G., Zimmerberg, J., Leapman, R.D., Nat. Methods 6, 729 (2009).Google Scholar
Charuvi, D., Kiss, V., Nevo, R., Shimoni, E., Adam, Z., Reich, Z., Plant Cell 24, 1143–1157 (2012).Google Scholar
Mutsafi, Y., Shimoni, E., Shimon, A., Minsky, A., PLoS Pathog. 9, e1003367 (2013).Google Scholar
Tsabari, O., Nevo, R., Meir, S., Carrillo, L.R., Kramer, D.M., Reich, Z., Plant J. 81, 884 (2015).Google Scholar
Milrot, E., Mutsafi, Y., Fridmann-Sirkis, Y., Shimoni, E., Rechav, K., Gurnon, J.R., Van Etten, J.L., Minsky, A., Cell. Microbiol. 18, 3 (2016).Google Scholar
Boonrungsiman, S., Gentleman, E., Carzaniga, R., Evans, N.D., McComb, D.W., Porter, A.E., Stevens, M.M., Proc. Natl. Acad. Sci. U.S.A. 109, 14170 (2012).Google Scholar
Murata, K., Esaki, M., Ogura, T., Arai, S., Yamamoto, Y., Tanaka, N., Ultramicroscopy 146, 39 (2014).Google Scholar
Suarez, C., Andres, G., Kolovou, A., Hoppe, S., Salas, M.L., Walther, P., Krijnse-Locker, J., Cell. Microbiol. 17, 1683 (2015).CrossRefGoogle Scholar
Papanikou, E., Day, K.J., Ii, J.A., Glick, B.S., eLife 4, e13232 (2015).Google Scholar
Pokrovskaya, I.D., Aronova, M.A., Kamykowski, J.A., Prince, A.A., Hoyne, J.D., Calco, G.N., Kuo, B.C., He, Q., Leapman, R.D., Storrie, B., J. Thromb. Haemost. 14, 572 (2016).CrossRefGoogle Scholar
Kirchenbuechler, D., Mutsafi, Y., Horowitz, B., Levin-Zaidman, S., Fass, D., Wolf, S.G., Elbaum, M., AIMS Biophys. 2, 259 (2015).Google Scholar
Philippsen, A., Engel, H.-A., Engel, A., Ultramicroscopy 107, 202 (2007).Google Scholar
Zanetti, A., Riches, J.D., Fuller, S.D., Briggs, J.A.G., J. Struct. Biol. 168, 305 (2009).Google Scholar
Zernike, F., Science 121, 345 (1955).Google Scholar
Nagayama, K., J. Electron Microsc. (Tokyo) 60 (Suppl. 1), S43 (2011).Google Scholar
Glaeser, R.M., Rev. Sci. Instrum. 84, 111101 (2013).CrossRefGoogle Scholar
Danev, R., Buijsse, B., Khoshouei, M., Plitzko, J.M., Baumeister, W., Proc. Natl. Acad. Sci. U.S.A. 111, 15635 (2014).CrossRefGoogle Scholar
Mahamid, J., Pfeffer, S., Schaffer, M., Villa, E., Danev, R., Cuellar, L.K., Förster, F., Hyman, A.A., Plitzko, J.M., Baumeister, W., Science 351, 969 (2016).Google Scholar
Ophus, C., Ciston, J., Pierce, J., Harvey, T.R., Chess, J., McMorran, B.J., Czarnik, C., Rose, H.H., Ercius, P., Nat. Commun. 7, 10719 (2016).Google Scholar
Hyun, J.K., Ercius, P., Muller, D.A., Ultramicroscopy 109, 1 (2008).Google Scholar
Biskupek, J., Leschner, J., Walther, P., Kaiser, U., Ultramicroscopy 110, 1231 (2010).CrossRefGoogle Scholar
Rez, P., Ultramicroscopy 96, 117 (2003).Google Scholar
Rose, H., Ninth Int. Congr. Electron Microsc. Tor. III, 230–243 (1978).Google Scholar
Trepout, S., Messaoudi, C., Perrot, S., Bastin, P., Marco, S., Micron 77, 9 (2015).Google Scholar
Comolli, L.R., Downing, K.H., J. Struct. Biol. 152, 149 (2005).Google Scholar
Wolf, S.G., Rez, P., Elbaum, M., J. Microsc. 260, 227 (2015).Google Scholar
Seufferheld, M., Vieira, M.C.F., Ruiz, F.A., Rodrigues, C.O., Moreno, S.N.J., Docampo, R., J. Biol. Chem. 278, 29971 (2003).Google Scholar
Faas, F.G.A., Avramut, M.C., van den Berg, B.M., Mommaas, A.M., Koster, A.J., Ravelli, R.B.G., J. Cell Biol. 198, 457 (2012).Google Scholar
Gan, L., Ladinsky, M.S., Jensen, G.J., Chromosoma 122, 377 (2013).Google Scholar
Romero-Brey, I., Bartenschlager, R., Viruses 7, 6316 (2015).Google Scholar
Crewe, A.V., Wall, J., Langmore, J., Science 168, 1338 (1970).Google Scholar
Kirkland, E.J., in Advanced Computing in Electron Microscopy (Springer, New York), pp. 1–4.Google Scholar