Laboratory-based cryogenic soft x-ray tomography with correlative cryo-light and electron microscopy

Microscopy and Microanalysis

Volumn 19, Issue 1, 2013, Pages 22-29

  Carlson, David B ^a   Gelb, Jeff ^b   Palshin, Vadim ^b   Evans, James E ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b XRADIA INC   (United States)

^c PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

correlative microscopy; cryogenic soft X ray microscope; Key words compact light source; laboratory light source; X ray tomography

Indexed keywords

ARTICLE; CRYOELECTRON MICROSCOPY; ELECTRON PROBE MICROANALYSIS; ELECTRON TOMOGRAPHY; FLUORESCENCE MICROSCOPY; METHODOLOGY; SACCHAROMYCES CEREVISIAE; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPE TOMOGRAPHY; ELECTRON PROBE MICROANALYSIS; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; SACCHAROMYCES CEREVISIAE;

EID: 84873363420     PISSN: 14319276     EISSN: 14358115     Source Type: Journal    
DOI: 10.1017/S1431927612013827     Document Type: Article

References (37)

1. Adam, J.F., Moy, J.P. & Susini, J. (2005). Table-top water window transmission X-ray microscopy: Review of the key issues, and conceptual design of an instrument for biology. Rev Sci Instrum 76(9), 091301
2. Adrian, M.,Dubochet, J., Lepault, J.&McDowall,A.W. (1984). Cryo-electronmicroscopy of viruses. Nature 308(5954), 32-36
3. Al-Amoudi, A., Norlen, L.P. & Dubochet, J. (2004). Cryoelectron microscopy of vitreous sections of native biological cells and tissues. J Struct Biol 148(1), 131-135
4. Baker, L.A. & Rubinstein, J.L. (2010). Radiation damage in electron cryomicroscopy. Methods Enzymol 481, 371-388
5. Berglund, M., Rymell, L., Peuker, M., Wilhein, T. & Hertz, H.M. (2000).Compact water-window transmission X-ray microscopy. J Microsc 197(3), 268-273
6. Bertilson, M., von Hofsten, O., Vogt, U., Holmberg, A. & Hertz, H.M. (2009). High-resolution computed tomography with a compact soft X-ray microscope. Opt Express 17(13), 11057-11065
7. Carlson, D.B. & Evans, J.E. (2011). Low cost cryo-light microscopy stage fabrication for correlated light/electron microscopy. J Vis Exp 52, e2909
8. Chichon, F.J., Rodriguez, M.J., Pereiro, E., Chiappi, M., Perdiguero, B., Guttmann, P., Werner, S., Rehbein, S., Schneider, G., Esteban, M. & Carrascosa, J.L. (2012). Cryo X-ray nano-tomography of vaccinia virus infected cells. J Struct Biol 177(2), 202-211
9. Egerton, R.F., Li, P. & Malac, M. (2004). Radiation damage in the TEM and SEM. Micron 35(6), 399-409
10. Hagen, C., Guttmann, P., Klupp, B., Werner, S., Rehbein, S., Mettenleiter, T.C., Schneider, G. & Grunewald, K. (2012). Correlative VIS-fluorescence and soft X-ray cryo-microscopy/tomography of adherent cells. J Struct Biol 177(2), 193-201
11. Hanssen, E., Knoechel, C., Klonis, N., Abu-Bakar, N., Deed, S., LeGros, M., Larabell, C. & Tilley, L. (2011). Cryo transmission X-ray imaging of the malaria parasite, P. falciparum. J Struct Biol 173(1), 161-168
12. 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(2), 171-193
13. Hertz, H.M., von Hofsten, O., Bertilson, M., Vogt, U., Holmberg, A., Reinspach, J., Martz, D., Selin, M., Christakou, A.E., Jerlstrom-Hultqvist, J. & Svard, S. (2012). Laboratory cryo soft X-ray microscopy. J Struct Biol 177(2), 267-272
14. Horne, S.F., Silterra, J. & Holber, W. (2009). A compact soft X-ray microscope using an electrode-less Z-pinch source. J Phys Conf Ser 186, 12028
15. Howells, M.R., Beetz, T., Chapman, H.N., Cui, C., Holton, J.M., Jacobsen, C.J., Kirz, J., Lima, E., Marchesini, S., Miao, H., Sayre, D., Shapiro, D.A., Spence, J.C. & Starodub, D. (2009). An assessment of the resolution limitation due to radiation-damage in X-ray diffraction microscopy. J Electron Spectros Relat Phenomena 170(1-3), 4-12
16. Ingerman, E., Perkins, E.M., Marina, M., Mears, J.A., McCaffery, J.M., Hinshaw, J.E. & Nunnari, J. (2005). Dnm1 forms spirals that are structurally tailored to fit mitochondria. J Cell Biol 170(7), 1021-1027
17. Jacobsen, C., Kirz, J. & Williams, S. (1992). Resolution in soft X-ray microscopes. Ultramicroscopy 47, 55-79
18. Kirz, J., Jacobsen, C. & Howells, M. (1995). Soft X-ray microscopes and their biological applications. Q Rev Biophys 28(1), 33-130
19. Kneip, S.,McGuffey, C.,Martins, J.L.,Martins, S.F., Bellei, C., Chvykov, V., Dollar, F., Fonseca, R., Huntington, C., Kalintchenko, G., Maksimchuk, A., Mangles, S.P.D., Matsuoka, T., Nagel, S.R., Palmer, C.A.J., Schreiber, J., Ta Phuoc, K., Thomas, A.G.R., Yanovsky, V., Silva, L.O., Krushelnick, K. & Najmudin, Z. (2010). Bright spatially coherent synchrotron X-rays from a table-top source. Nat Phys 6, 980-983
20. Larabell, C.A. & Le Gros, M.A. (2004). X-ray tomography generates 3-D reconstructions of the yeast, saccharomyces cerevisiae, at 60-nm resolution. Mol Biol Cell 15(3), 957-962
21. Larabell, C.A. & Nugent, K.A. (2010). Imaging cellular architecture with X-rays. Curr Opin Struct Biol 20(5), 623-631
22. Le Gros, M.A., McDermott, G., Uchida, M., Knoechel, C.G. & Larabell, C.A. (2009). High-aperture cryogenic light microscopy. J Microsc 235(1), 1-8
23. Li, Z. & Jensen, G.J. (2009). Electron cryotomography: A new view into microbial ultrastructure. Curr Opin Microbiol 12(3), 333-340
24. McDermott, G., Le Gros, M.A., Knoechel, C.G., Uchida, M. & Larabell, C.A. (2009). Soft X-ray tomography and cryogenic light microscopy: The cool combination in cellular imaging. Trends Cell Biol 19(11), 587-595
25. Milne, J.L. & Subramaniam, S. (2009). Cryo-electron tomography of bacteria: Progress, challenges and future prospects. Nat Rev Microbiol 7(9), 666-675
26. Muller, W.G., Heymann, J.B., Nagashima, K., Guttmann, P., Werner, S., Rehbein, S., Schneider, G. & McNally, J.G. (2012). Towards an atlas of mammalian cell ultrastructure by cryo soft X-ray tomography. J Struct Biol 177(2), 179-192
27. Nelson, J., Huang, X., Steinbrener, J., Shapiro, D., Kirz, J., Marchesini, S., Neiman, A.M., Turner, J.J. & Jacobsen, C. (2010). High-resolution X-ray diffraction microscopy of specifically labeled yeast cells. Proc Natl Acad Sci USA 107(16), 7235-7239
28. Niemann, B., Rudolph, D. & Schmahl, G. (1976). X-ray microscopy with synchrotron radiation. Appl Optics 15(8), 1883-1884
29. Parkinson, D.Y., McDermott, G., Etkin, L.D., Le Gros, M.A. & Larabell, C.A. (2008). Quantitative 3-D imaging of eukaryotic cells using soft X-ray tomography. J Struct Biol 162(3), 380-386
30. Reimer, L. (1998). Scanning Electron Microscopy: Physics of Image Formation and Microanalysis. Heidelberg, Germany: Springer- Verlag
31. Sartori, A., Gatz, R., Beck, F., Rigort, A., Baumeister, W. & Plitzko, J.M. (2007). Correlative microscopy: Bridging the gap between fluorescence light microscopy and cryo-electron tomography. J Struct Biol 160(2), 135-145
32. Schmahl, G., Rudolph, D., Guttmann, P., Schneider, G., Thieme, J. & Niemann, B. (1995). Phase-contrast studies of biological specimens with the X-ray microscope at Bessy. Rev Sci Instrum 66(2), 1282-1286
33. Schneider, G., Guttmann, P., Heim, S., Rehbein, S.,Mueller, F., Nagashima, K., Heymann, J.B., Muller, W.G. & McNally, J.G. (2010). Three-dimensional cellular ultrastructure resolved by X-ray microscopy. Nat Methods 7(12), 985-987
34. Schneider, G., Guttmann, P., Rehbein, S., Werner, S. & Follath, R. (2012). Cryo X-ray microscope with flat sample geometry for correlative fluorescence and nanoscale tomographic imaging. J Struct Biol 177(2), 212-223
35. Schwartz, C.L., Sarbash, V.I., Ataullakhanov, F.I., McIntosh, J.R. & Nicastro, D. (2007). Cryo-fluorescence microscopy facilitates correlations between light and cryo-electron microscopy and reduces the rate of photobleaching. J Microsc 227(Pt 2), 98-109
36. Uchida, M., McDermott, G., Wetzler, M., Le Gros, M.A., Myllys, M., Knoechel, C., Barron, A.E. & Larabell, C.A. (2009). Soft X-ray tomography of phenotypic switching and the cellular response to antifungal peptoids in Candida albicans. Proc Natl Acad Sci USA 106(46), 19375-19380
37. Uchida, M., Sun, Y., McDermott, G., Knoechel, C., Le Gros, M.A., Parkinson, D., Drubin, D.G. & Larabell, C.A. (2011). Quantitative analysis of yeast internal architecture using soft X-ray tomography. Yeast 28(3), 227-236