3D correlative light and electron microscopy of cultured cells using serial blockface scanning electron microscopy

Journal of Cell Science

Volumn 130, Issue 1, 2017, Pages 278-291

  Russell, Matthew R G ^a   Lerner, Thomas R ^a   Burden, Jemima J ^b   Nkwe, David O ^b,d   Pelchen Matthews, Annegret ^b   Domart, Marie Charlotte ^a   Durgan, Joanne ^c   Weston, Anne ^a   Jones, Martin L ^a   Peddie, Christopher J ^a   Carzaniga, Raffaella ^a   Florey, Oliver ^c   Marsh, Mark ^b   Gutierrez, Maximiliano G ^a   Collinson, Lucy M ^a  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c BABRAHAM INSTITUTE   (United Kingdom)

^d BOTSWANA INTERNATIONAL UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Botswana)

Author keywords

3D correlative light and electron microscopy; Autophagy; Entosis; HIV 1; Mycobacterium tuberculosis; Serial blockface SEM

Indexed keywords

ARTICLE; AUTOPHAGOSOME; CELL CULTURE MONITORING; CELL GROWTH; CELL ULTRASTRUCTURE; CELL VACUOLE; ENDOTHELIUM CELL; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMAGE ANALYSIS; IMAGE PROCESSING; LYMPH VESSEL ENDOTHELIUM; MACROPHAGE; MONOCYTE; MONOLAYER CULTURE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; THREE DIMENSIONAL CORRELATIVE LIGHT AND ELECTRON MICROSCOPY; THREE DIMENSIONAL IMAGING; TUBERCULOSIS; VIRUS RELEASE; CELL CULTURE; CELL SURVIVAL; CYTOLOGY; ENTOSIS; GROWTH, DEVELOPMENT AND AGING; HUMAN IMMUNODEFICIENCY VIRUS; INTRACELLULAR SPACE; MICROBIOLOGY; PROCEDURES; ULTRASTRUCTURE; VIROLOGY;

CELL SURVIVAL; CELLS, CULTURED; ENDOTHELIAL CELLS; ENTOSIS; HIV; HUMANS; IMAGING, THREE-DIMENSIONAL; INTRACELLULAR SPACE; MACROPHAGES; MICROSCOPY, ELECTRON, SCANNING; MONOCYTES; MYCOBACTERIUM TUBERCULOSIS;

EID: 85010197122     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.188433     Document Type: Article

References (50)

1. Armer, H. E. J., Mariggi, G., Png, K. M. Y., Genoud, C., Monteith, A. G., Bushby, A. J., Gerhardt, H. and Collinson, L. M. (2009). Imaging transient blood vessel fusion events in zebrafish by correlative volume electron microscopy. PLoS ONE 4, e7716.
2. Beckwith, M. S., Beckwith, K. S., Sikorski, P., Skogaker, N. T., Flo, T. H. and Halaas, O. (2015). Seeing a Mycobacterium-infected cell in Nanoscale 3D: correlative imaging by light microscopy and FIB/SEM tomography. PLoS ONE 10, e0134644.
3. Blazquez-Llorca, L., Hummel, E., Zimmerman, H., Zou, C., Burgold, S., Rietdorf, J. and Herms, J. (2015). Correlation of two-photon in vivo imaging and FIB/SEM microscopy. J. Microsc. 259, 129-136.
4. Bosch, C., Martinez, A., Masachs, N., Teixeira, C. M., Fernaud, I., Ulloa, F., Perez-Martinez, E., Lois, C., Comella, J. X., Defelipe, J. et al. (2015). FIB/SEM technology and high-throughput 3D reconstruction of dendritic spines and synapses in GFP-labeled adult-generated neurons. Front. Neuroanat. 9, 60.
5. Botelho, R. J., Teruel, M., Dierckman, R., Anderson, R., Wells, A., York, J. D., Meyer, T. and Grinstein, S. (2000). Localized biphasic changes in phosphatidylinositol-4, 5-bisphosphate at sites of phagocytosis. J. Cell Biol. 151, 1353-1368.
6. Bushby, A. J., Mariggi, G., Armer, H. E. J. and Collinson, L. M. (2012). Correlative light and volume electron microscopy: using focused ion beam scanning electron microscopy to image transient events in model organisms. Methods Cell Biol. 111, 357-382.
7. Collman, F., Buchanan, J., Phend, K. D., Micheva, K. D., Weinberg, R. J. and Smith, S. J. (2015). Mapping synapses by conjugate light-electron array tomography. J. Neurosci. 35, 5792-5807.
8. Cook, G. M., Berney, M., Gebhard, S., Heinemann, M., Cox, R. A., Danilchanka, O. and Niederweis, M. (2009). Physiology of mycobacteria. Adv. Microb. Physiol. 55, 81-182, 318-319.
9. Deerinck, T. J., Bushong, E., Thor, A. and Ellisman, M. H. (2010). NCMIR methods for 3D EM: A new protocol for preparation of biological specimens for serial block-face SEM. Microscopy [Online], 6-8. http://ncmir.ucsd.edu/sbfsemprotocol. pdf.
10. Deneka, M., Pelchen-Matthews, A., Byland, R., Ruiz-Mateos, E. and Marsh, M. (2007). In macrophages, HIV-1 assembles into an intracellular plasma membrane domain containing the tetraspanins CD81, CD9, and CD53. J. Cell Biol. 177, 329-341.
11. Denk, W. and Horstmann, H. (2004). Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol. 2, e329.
12. Farnia, P., Mohammad, R. M., Merza, M. A., Tabarsi, P., Zhavnerko, G. K., Ibrahim, T. A., Kuan, H. O., Ghanavei, J., Farnia, P., Ranjbar, R. et al. (2010). Growth and cell-division in extensive (XDR) and extremely drug resistant (XXDR) tuberculosis strains: transmission and atomic force observation. Int. J. Clin. Exp. Med. 3, 308-314.
13. Florey, O., Kim, S. E., Sandoval, C. P., Haynes, C. M. and Overholtzer, M. (2011). Autophagy machinery mediates macroendocytic processing and entotic cell death by targeting single membranes. Nat. Cell Biol. 13, 1335-1343.
14. Hayworth, K. J., Kasthuri, N., Schalek, R. and Lichtman, J. W. (2006). Automating the collection of ultrathin serial sections for large volume TEM reconstructions. Microsc. Microanal. 12, 86-87.
15. Heymann, J. A. W., Hayles, M., Gestmann, I., Giannuzzi, L. A., Lich, B. and Subramaniam, S. (2006). Site-specific 3D imaging of cells and tissues with a dual beam microscope. J. Struct. Biol. 155, 63-73.
16. Iudin, A., Korir, P. K., Salavert-Torres, J., Kleywegt, G. J. and Patwardhan, A. (2016). EMPIAR: a public archive for raw electron microscopy image data. Nat. Methods 13, 387-388.
17. Karreman, M. A., Mercier, L., Schieber, N. L., Solecki, G., Allio, G., Winkler, F., Ruthensteiner, B., Goetz, J. G. and Schwab, Y. (2016). Fast and precise targeting of single tumor cells in vivo by multimodal correlative microscopy. J. Cell Sci. 129, 444-456.
18. Kremer, J. R., Mastronarde, D. N. and Mcintosh, J. R. (1996). Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71-76.
19. Kremer, A., Lippens, S., Bartunkova, S., Asselbergh, B., Blanpain, C., Fendrych, M., Goossens, A., Holt, M., Janssens, S., Krols, M. et al. (2015). Developing 3D SEM in a broad biological context. J. Microsc. 259, 80-96.
20. Lerner, T. R., De Souza Carvalho-Wodarz, C., Repnik, U., Russell, M. R. G., Borel, S., Diedrich, C. R., Rohde, M., Wainwright, H., Collinson, L. M., Wilkinson, R. J. et al. (2016). Lymphatic endothelial cells are a replicative niche for Mycobacterium tuberculosis. J. Clin. Invest. 126, 1093-1108.
21. Limpens, R. W. A. L., Van Der Schaar, H. M., Kumar, D., Koster, A. J., Snijder, E. J., Van Kuppeveld, F. J. M. and Barcena, M. (2011). The transformation of enterovirus replication structures: a three-dimensional study of single-and doublemembrane compartments. MBio 2, e00166-11.
22. Lucas, M. S., Gunthert, M., Gasser, P., Lucas, F. and Wepf, R. (2012). Bridging microscopes: 3D correlative light and scanning electron microscopy of complex biological structures. Methods Cell Biol. 111, 325-356.
23. Lucas, M. S., Guenthert, M., Gasser, P., Lucas, F. and Wepf, R. (2014). Correlative 3D imaging: CLSM and FIB-SEM tomography using high-pressure frozen, freeze-substituted biological samples. Methods Mol. Biol. 1117, 593-616.
24. Maco, B., Holtmaat, A., Cantoni, M., Kreshuk, A., Straehle, C. N., Hamprecht, F. A. and Knott, G.W. (2013). Correlative in vivo 2 photon and focused ion beam scanning electron microscopy of cortical neurons. PLoS ONE 8, e57405.
25. Marsh, M., Theusner, K. and Pelchen-Matthews, A. (2009). HIV assembly and budding in macrophages. Biochem. Soc. Trans. 37, 185-189.
26. Micheva, K. D. and Smith, S. J. (2007). Array tomography: a new tool for imaging the molecular architecture and ultrastructure of neural circuits. Neuron 55, 25-36.
27. Mizushima, N., Ohsumi, Y. and Yoshimori, T. (2002). Autophagosome formation in mammalian cells. Cell Struct. Funct. 27, 421-429.
28. Mlcochova, P., Pelchen-Matthews, A. and Marsh, M. (2013). Organization and regulation of intracellular plasma membrane-connected HIV-1 assembly compartments in macrophages. BMC Biol. 11, 89.
29. Muller-Reichert, T. and Verkade, P. (2012). Introduction to correlative light and electron microscopy. Methods Cell Biol. 111, xvii-xxix.
30. Muller-Reichert, T. and Verkade, P. (2014). Preface. Correlative light and electron microscopy II. Methods Cell Biol. 124, xvii-xviii.
31. Murphy, G. E., Narayan, K., Lowekamp, B. C., Hartnell, L. M., Heymann, J. A.W., Fu, J. and Subramaniam, S. (2011). Correlative 3D imaging of whole mammalian cells with light and electron microscopy. J. Struct. Biol. 176, 268-278.
32. Nkwe, D. O., Pelchen-Matthews, A., Burden, J. J., Collinson, L. M. and Marsh, M. (2016). The intracellular plasma membrane-connected compartment in the assembly of HIV-1 in human macrophages. BMC Biol. 14, 50.
33. Oberti, D., Kirschmann, M. A. and Hahnloser, R. H. R. (2011). Projection neuron circuits resolved using correlative array tomography. Front. Neurosci. 5, 50.
34. Overholtzer, M. and Brugge, J. S. (2008). The cell biology of cell-in-cell structures. Nat. Rev. Mol. Cell Biol. 9, 796-809.
35. Overholtzer, M., Mailleux, A. A., Mouneimne, G., Normand, G., Schnitt, S. J., King, R. W., Cibas, E. S. and Brugge, J. S. (2007). A nonapoptotic cell death process, entosis, that occurs by cell-in-cell invasion. Cell 131, 966-979.
36. Peddie, C. J. and Collinson, L. M. (2014). Exploring the third dimension: volume electron microscopy comes of age. Micron 61, 9-19.
37. Pelchen-Matthews, A., Giese, S., Mlcochová, P., Turner, J. and Marsh, M. (2012). β2 integrin adhesion complexes maintain the integrity of HIV-1 assembly compartments in primary macrophages. Traffic 13, 273-291.
38. Pietzsch, T., Saalfeld, S., Preibisch, S. and Tomancak, P. (2015). BigDataViewer: visualization and processing for large image data sets. Nat. Methods 12, 481-483.
39. Polishchuk, R. S., Polishchuk, E. V., Marra, P., Alberti, S., Buccione, R., Luini, A. and Mironov, A. A. (2000). Correlative light-electron microscopy reveals the tubular-saccular ultrastructure of carriers operating between golgi apparatus and plasma membrane. J. Cell Biol. 148, 45-58.
40. Rappaport, J. and Volsky, D. J. (2015). Role of the macrophage in HIV-associated neurocognitive disorders and other comorbidities in patients on effective antiretroviral treatment. J. Neurovirol. 21, 235-241.
41. Royer, L. A., Weigert, M., Gunther, U., Maghelli, N., Jug, F., Sbalzarini, I. F. and Myers, E. W. (2015). ClearVolume: open-source live 3D visualization for lightsheet microscopy. Nat. Methods 12, 480-481.
42. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B. et al. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682.
43. Sewald, X., Ladinsky, M. S., Uchil, P. D., Beloor, J., Pi, R., Herrmann, C., Motamedi, N., Murooka, T. T., Brehm, M. A., Greiner, D. L. et al. (2015). Retroviruses use CD169-mediated trans-infection of permissive lymphocytes to establish infection. Science 350, 563-567.
44. Sharova, N., Swingler, C., Sharkey, M. and Stevenson, M. (2005). Macrophages archive HIV-1 virions for dissemination in trans. EMBO J. 24, 2481-2489.
45. Sprenkeler, E. G., Gresnigt, M. S. and Van De Veerdonk, F. L. (2016). LC3-associated phagocytosis: a crucial mechanism for antifungal host defence against Aspergillus fumigatus. Cell Microbiol. doi:10.1111/cmi.12616.
46. Sun, Q., Cibas, E. S., Huang, H., Hodgson, L. and Overholtzer, M. (2014). Induction of entosis by epithelial cadherin expression. Cell Res. 24, 1288-1298.
47. Tan, J. and Sattentau, Q. J. (2013). The HIV-1-containing macrophage compartment: a perfect cellular niche? Trends Microbiol. 21, 405-412.
48. Thaunat, O., Granja, A. G., Barral, P., Filby, A., Montaner, B., Collinson, L., Martinez-Martin, N., Harwood, N. E., Bruckbauer, A. and Batista, F. D. (2012). Asymmetric segregation of polarized antigen on B cell division shapes presentation capacity. Science 335, 475-479.
49. Wacker, I. and Schroeder, R. R. (2013). Array tomography. J. Microsc. 252, 93-99.
50. Welsch, S., Groot, F., Krausslich, H.-G., Keppler, O. T. and Sattentau, Q. J. (2011). Architecture and regulation of the HIV-1 assembly and holding compartment in macrophages. J. Virol. 85, 7922-7927.