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Liquid phase electron microscopy of biological specimens

Published online by Cambridge University Press:  10 September 2020

Diana B. Peckys ,
Elena Macías-Sánchez  and
Niels de Jonge
Diana B. Peckys
Affiliation:
Department of Biophysics, Saarland University, Germany; diana.peckys@uks.eu
Elena Macías-Sánchez
Affiliation:
Radboud University Medical Center, The Netherlands; elena.macias@radboudumc.nl
Niels de Jonge
Affiliation:
INM–Leibniz Institute for New Materials; and Department of Physics, Saarland University, Germany; Niels.deJonge@leibniz-inm.de
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Abstract

Liquid phase electron microscopy is a new analytical method that has opened up a rapidly emerging field of research during the past decade. This article discusses this new microscopy modality within the context of imaging eukaryotic cells, bacteria, proteins, viruses, and biomineralization processes. The obtained resolution is typically not a function of the instrument, rather it is limited by the available electron dose within the limit of radiation damage. Therefore, different types of samples are best imaged with different electron microscopy (EM) modalities. The obtained information differs from that acquired with conventional EM as well as cryo-electron microscopy. This article gives an overview of achievements thus far in this area and the unique information that has been obtained. A discussion on potential future developments in the field, and technological advancements required to reach those goals conclude the article.

Type
Liquid Phase Electron Microscopy
Information
MRS Bulletin , Volume 45 , Issue 9: Liquid Phase Electron Microscopy , September 2020 , pp. 754 - 760
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Copyright
Copyright © Materials Research Society 2020

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References

de Jonge, N., Ross, F.M., Nat. Nanotechnol. 6, 695 (2011).CrossRefGoogle Scholar
de Jonge, N., Peckys, D.B., Kremers, G.J., Piston, D.W., Proc. Natl. Acad. Sci. U.S.A. 106, 2159 (2009).CrossRefGoogle Scholar
Ross, F.M., Liquid Cell Electron Microscopy (Cambridge University Press, Cambridge, UK, 2017).Google Scholar
de Jonge, N., Houben, L., Dunin-Borkowski, R.E., Ross, F.M., Nat. Rev. Mater. 4, 61 (2019).CrossRefGoogle Scholar
Wu, H., Friedrich, H., Patterson, J.P., Sommerdijk, N., de Jonge, N., Adv. Mater. 32, 2001582 (2020).CrossRefGoogle Scholar
He, K., Shokuhfar, T., Shahbazian-Yassar, R., J. Phys. Condens. Matter 31, 103001 (2019).CrossRefGoogle Scholar
Parsons, D.F., Matricardi, V.R., Moretz, R.C., Turner, J.N., Adv. Biol. Med. Phys. 15, 161 (1974).CrossRefGoogle Scholar
Sugi, H., Akimoto, T., Sutoh, K., Chaen, S., Oishi, N., Suzuki, S., Proc. Natl. Acad. Sci. U.S.A. 94, 4378 (1997).CrossRefGoogle Scholar
Danilatos, G.D., in Advances in Electronics and Electron Physics (Academic Press, 1988), vol. 71, p. 109.Google Scholar
Stokes, D.L., Principles and Practice of Variable Pressure/Environmental Scanning Electron Microscopy (VP-ESEM) (Wiley, Chichester, UK, 2008).CrossRefGoogle Scholar
Bogner-Van De Moortele, A., Thollet, G., Basset, D., Jouneau, P.-H., Gauthier, C., Ultramicroscopy 104, 290 (2005).CrossRefGoogle Scholar
Peckys, D.B., Baudoin, J.P., Eder, M., Werner, U., de Jonge, N., Sci. Rep. 3, 2626 (2013).CrossRefGoogle Scholar
Thiberge, S., Nechushtan, A., Sprinzak, D., Gileadi, O., Behar, V., Zik, O., Chowers, Y., Michaeli, S., Schlessinger, J., Moses, E., Proc. Natl. Acad. Sci. U.S.A. 101, 3346 (2004).CrossRefGoogle Scholar
de Jonge, N., Peckys, D.B., Veith, G.M., Mick, S., Pennycook, S.J., Joy, C.S., Microsc. Microanal. 13 (Suppl. 2), 242 (2007).Google Scholar
Williamson, M.J., Tromp, R.M., Vereecken, P.M., Hull, R., Ross, F.M., Nat. Mater. 2, 532 (2003).CrossRefGoogle Scholar
Peckys, D.B., Veith, G.M., Joy, D.C., de Jonge, N., PLoS One 4, e8214 (2009).CrossRefGoogle Scholar
Nishiyama, H., Suga, M., Ogura, T., Maruyama, Y., Koizumi, M., Mio, K., Kitamura, S., Sato, C., J. Struct. Biol. 169, 438 (2010).CrossRefGoogle Scholar
Park, J., Park, H., Ercius, P., Pegoraro, A.F., Xu, C., Kim, J.W., Han, S.H., Weitz, D.A., Nano Lett. 15, 4737 (2015).CrossRefGoogle Scholar
Textor, M., de Jonge, N., Nano Lett. 18, 3313 (2018).CrossRefGoogle Scholar
Ghodsi, S.M., Megaridis, C.M., Shahbazian-Yassar, R., Shokuhfar, T., Small Methods 3, 1900026 (2019).CrossRefGoogle Scholar
Cho, H., Jones, M.R., Nguyen, S.C., Hauwiller, M.R., Zettl, A., Alivisatos, A.P., Nano Lett. 17, 414 (2017).CrossRefGoogle Scholar
Keskin, S., de Jonge, N., Nano Lett. 18, 7435 (2018).CrossRefGoogle Scholar
Dearnaley, W.J., Schleupner, B., Varano, A.C., Alden, N.A., Gonzalez, F., Casasanta, M.A., Scharf, B.E., Dukes, M.J., Kelly, D.F., Nano Lett. 19, 6734 (2019).CrossRefGoogle Scholar
Marchello, G., De Pace, C., Wilkinson, N., Ruiz-Perez, L., Battaglia, G., preprint, arXiv:1907.03348 (2019).Google Scholar
Masenelli-Varlot, K., Malchere, A., Ferreira, J., Heidari Mezerji, H., Bals, S., Messaoudi, C., Marco Garrido, S., Microsc. Microanal. 20, 366 (2014).CrossRefGoogle Scholar
de Jonge, N., Houben, L., Dunin-Borkowski, R.E., Ross, F.M., Nat. Rev. Mater. 4, 61 (2019).CrossRefGoogle Scholar
Woehl, T.J., Abellan, P., J. Microsc. 265, 135 (2017).CrossRefGoogle Scholar
Hoenger, A., Bouchet-Marquis, C., Adv. Protein Chem. Struct. Biol. 82, 67 (2011).CrossRefGoogle Scholar
Hermannsdörfer, J., Tinnemann, V., Peckys, D.B., de Jonge, N., Microsc. Microanal. 20, 656 (2016).CrossRefGoogle Scholar
Matricardi, V.R., Moretz, R.C., Parsons, D.F., Science 177, 268 (1972).CrossRefGoogle Scholar
Mirsaidov, U.M., Zheng, H., Casana, Y., Matsudaira, P., Biophys. J. 102, L15 (2012).CrossRefGoogle Scholar
Keskin, S., Besztejan, S., Kassier, G., Manz, S., Bucker, R., Riekeberg, S., Trieu, H.K., Rentmeister, A., Miller, R.J., J. Phys. Chem. Lett. 6, 4487 (2015).CrossRefGoogle Scholar
Wang, M., Park, C., Woehl, T., Microsc. Microanal. 25, 23 (2019).CrossRefGoogle Scholar
de Jonge, N., Ultramicroscopy 187, 113 (2018).CrossRefGoogle Scholar
Moser, T.H., Shokuhfar, T., Evans, J.E., Micron 117, 8 (2019).CrossRefGoogle Scholar
Baudoin, J.P., Jinschek, J.R., Boothroyd, C.B., Dunin-Borkowski, R.E., de Jonge, N., Microsc. Microanal. 19, 814 (2013).CrossRefGoogle 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).CrossRefGoogle Scholar
Elbaum, M., Wolf, S.G., Houben, L., MRS Bull. 41, 542 (2016).CrossRefGoogle Scholar
Peckys, D.B., Mazur, P., Gould, K.L., de Jonge, N., Biophys. J. 100, 2522 (2011).CrossRefGoogle Scholar
Dahmke, I.N., Verch, A., Hermannsdörfer, J., Peckys, D.B., Weatherup, R.S., Hofmann, S., de Jonge, N., ACS Nano 11, 11108 (2017).CrossRefGoogle Scholar
Evans, J.E., Jungjohann, K.L., Wong, P.C.K., Chiu, P.L., Dutrow, G.H., Arslan, I., Browning, N.D., Micron 43, 1085 (2012).CrossRefGoogle Scholar
Wang, C., Qiao, Q., Shokuhfar, T., Klie, R.F., Adv. Mater. 26, 3410 (2014).CrossRefGoogle Scholar
Dukes, M.J., Thomas, R., Damiano, J., Klein, K.L., Balasubramaniam, S., Kayandan, S., Riffle, J.S., Davis, R.M., McDonald, S.M., Kelly, D.F., Microsc. Microanal. 20, 338 (2014).Google Scholar
Wadell, C., Inagaki, S., Nakamura, T., Shi, J., Nakamura, Y., Sannomiya, T., ACS Nano 11, 1264 (2017).CrossRefGoogle Scholar
Yamazaki, T., Kimura, Y., Vekilov, P.G., Furukawa, E., Shirai, M., Matsumoto, H., Van Driessche, A.E.S., Tsukamoto, K., Proc. Natl. Acad. Sci. U.S.A. 114, 2154 (2017).CrossRefGoogle Scholar
Varano, A.C., Rahimi, A., Dukes, M.J., Poelzing, S., McDonald, S.M., Kelly, D.F., Chem. Commun. 51, 16176 (2015).CrossRefGoogle Scholar
Wang, H., Li, B., Kim, Y.J., Kwon, O.H., Granick, S., Proc. Natl. Acad. Sci. U.S.A. 117, 1283 (2020).CrossRefGoogle Scholar
Liu, K.L., Wu, C.C., Huang, Y.J., Peng, H.L., Chang, H.Y., Chang, P., Hsu, L., Yew, T.R., Lab Chip 8, 1915 (2008).CrossRefGoogle Scholar
Mohanty, N., Fahrenholtz, M., Nagaraja, A., Boyle, D., Berry, V., Nano Lett. 11, 1270 (2011).CrossRefGoogle Scholar
Prozorov, T., Almeida, T.P., Kovacs, A., Dunin-Borkowski, R.E., J. R. Soc. Interface 14, 20170464 (2017).CrossRefGoogle Scholar
Koo, K., Dae, K.S., Hahn, Y.K., Yuk, J.M., Nano Lett. 20, 4708 (2020).CrossRefGoogle Scholar
de Jonge, N., Peckys, D.B., ACS Nano 10, 9061 (2016).CrossRefGoogle Scholar
Reimer, L., Kohl, H., Transmission Electron Microscopy: Physics of Image Formation (Springer, New York, 2008).Google Scholar
Giepmans, B.N., Deerinck, T.J., Smarr, B.L., Jones, Y.Z., Ellisman, M.H., Nat. Methods 2, 743 (2005).CrossRefGoogle Scholar
Ando, T., Bhamidimarri, S.P., Brending, N., Colin-York, H., Collinson, L., de Jonge, N., de Pablo, P.J., Debroye, E., Eggeling, C., Franck, C., Fritzsche, M., Gerritsen, H., Giepmans, B.N.G., Grunewald, K., Hofkens, J., Hoogenboom, J.P., Janssen, K.P.F., Kaufman, R., Klumpermann, J., Kurniawan, N., Kusch, J., Liv, N., Parekh, V., Peckys, D.B., Rehfeldt, F., Reutens, D.C., Roeffaers, M.B.J., Salditt, T., Schaap, I.A.T., Schwarz, U.S., Verkade, P., Vogel, M.W., Wagner, R., Winterhalter, M., Yuan, H., Zifarelli, G., J. Phys. D Appl. Phys. 51, 443001 (2018).CrossRefGoogle Scholar
Maruyama, Y., Ebihara, T., Nishiyama, H., Suga, M., Sato, C., J. Struct. Biol. 180, 259 (2012).CrossRefGoogle Scholar
Peckys, D.B., de Jonge, N., Microsc. Microanal. 20, 189 (2014).CrossRefGoogle Scholar
Peckys, D.B., Hirsch, D., Gaiser, T., de Jonge, N., Mol. Med. 25, 42 (2019).CrossRefGoogle Scholar
Peckys, D.B., Stoerger, C., Latta, L., Wissenbach, U., Flockerzi, V., de Jonge, N., J. Struct. Biol. 199, 102 (2017).CrossRefGoogle Scholar
Alansary, D., Peckys, D.B., Niemeyer, B.A., de Jonge, N., J. Cell Sci. 133, 240358 (2020).CrossRefGoogle Scholar
Peckys, D.B., Korf, U., Wiemann, S., de Jonge, N., Mol. Biol. Cell 28, 3193 (2017).CrossRefGoogle Scholar
Yamazawa, T., Nakamura, N., Sato, M., Sato, C., Microsc. Res. Tech. 79, 1179 (2016).CrossRefGoogle Scholar
Memtily, N., Okada, T., Ebihara, T., Sato, M., Kurabayashi, A., Furihata, M., Suga, M., Nishiyama, H., Mio, K., Sato, C., Int. J. Oncol. 46, 1872 (2015).CrossRefGoogle Scholar
Nielsen, M.H., Aloni, S., De Yoreo, J.J., Science 345, 1158 (2014).CrossRefGoogle Scholar
Smeets, P.J., Cho, K.R., Kempen, R.G., Sommerdijk, N.A., De Yoreo, J.J., Nat. Mater. 14, 394 (2015).CrossRefGoogle Scholar
Liu, Z., Zhang, Z., Wang, Z., Jin, B., Li, D., Tao, J., Tang, R., De Yoreo, J.J., Proc. Natl. Acad. Sci. 117, 3397 (2020).CrossRefGoogle Scholar
Dey, A., Bomans, P.H., Muller, F.A., Will, J., Frederik, P.M., de With, G., Sommerdijk, N.A., Nat. Mater. 9, 1010 (2010).CrossRefGoogle Scholar
Wang, X.Y., Yang, J., Andrei, C.M., Soleymani, L., Grandfield, K., Commun. Chem. 1, 80 (2018).CrossRefGoogle Scholar
Sato, C., Yamazaki, D., Sato, M., Takeshima, H., Memtily, N., Hatano, Y., Tsukuba, T., Sakai, E., Sci. Rep. 9, 7352 (2019).CrossRefGoogle ScholarPubMed
Balzarotti, F., Eilers, Y., Gwosch, K.C., Gynna, A.H., Westphal, V., Stefani, F.D., Elf, J., Hell, S.W., Science 355, 606 (2017).CrossRefGoogle Scholar
Kourkoutis, L.F., Plitzko, J.M., Baumeister, W., Annu. Rev. Mater. Res. 42, 33 (2012).CrossRefGoogle Scholar
Lotze, J., Reinhardt, U., Seitz, O., Beck-Sickinger, A.G., Mol. Biosyst. 12, 1731 (2016).CrossRefGoogle Scholar
Murata, K., Wolf, M., Biochim. Biophys. Acta 1862, 324 (2018).CrossRefGoogle Scholar
van Deursen, P.M.G., Koning, R.I., Tudor, V., Moradi, M.-A., Patterson, J.P., Kros, A., Sommerdijk, N.A., Koster, A.J., Schneider, G.F., Adv. Funct. Mater. 30, 1904468 (2020).CrossRefGoogle Scholar
Danev, R., Glaeser, R.M., Nagayama, K., Ultramicroscopy 109, 312 (2009).CrossRefGoogle Scholar
Lazic, I., Bosch, E.G.T., Lazar, S., Ultramicroscopy 160, 265 (2016).CrossRefGoogle Scholar
Dahmen, T., Engstler, M., Pauly, C., Trampert, P., de Jonge, N., Mucklich, F., Slusallek, P., Sci. Rep. 6, 25350 (2016).CrossRefGoogle Scholar
Stevens, A., Yang, H., Carin, L., Arslan, I., Browning, N.D., Microscopy 63, 41 (2013).CrossRefGoogle Scholar
Beche, A., Goris, B., Freitag, B., Verbeeck, J., Appl. Phys. Lett. 108, 93103 (2016).CrossRefGoogle Scholar