Imaging Lipid Droplets by Electron Microscopy

Methods in Cell Biology

Volumn 116, Issue , 2013, Pages 227-251

  Fujimoto, Toyoshi ^a   Ohsaki, Yuki ^a   Suzuki, Michitaka ^a   Cheng, Jinglei ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Aldehyde; Cryoelectron microscopy; Electron microscopy; Freeze fracture; Freeze substitution; Immunoelectron microscopy; Lipid droplet; Osmium tetroxide; Quick freezing; Uranyl acetate

Indexed keywords

ALDEHYDE; FAT DROPLET; ORGANOMETALLIC COMPOUND; OSMIUM TETRAOXIDE; TRIACYLGLYCEROL; URANYL ACETATE;

ANIMAL; ARTICLE; CELL INCLUSION; CELL LINE; CHEMISTRY; CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPY; FREEZE DRYING; FREEZE-FRACTURE; FREEZE-SUBSTITUTION; HUMAN; IMMUNOELECTRON MICROSCOPY; METABOLISM; QUICK-FREEZING; ULTRASTRUCTURE;

ALDEHYDE; CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPY; FREEZE-FRACTURE; FREEZE-SUBSTITUTION; IMMUNOELECTRON MICROSCOPY; LIPID DROPLET; OSMIUM TETROXIDE; QUICK-FREEZING; URANYL ACETATE;

ALDEHYDES; ANIMALS; CELL LINE; CRYOELECTRON MICROSCOPY; FREEZE SUBSTITUTION; HUMANS; INCLUSION BODIES; ORGANOMETALLIC COMPOUNDS; OSMIUM TETROXIDE; TRIGLYCERIDES;

EID: 84884943296     PISSN: 0091679X     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-408051-5.00012-7     Document Type: Chapter

References (58)

1. Adams C.W., Abdulla Y.H., Bayliss O.B. Osmium tetroxide as a histochemical and histological reagent. Histochemie 1967, 9:68-77.
2. Adrian M., Dubochet J., Lepault J., McDowall A.W. Cryo-electron microscopy of viruses. Nature 1984, 308:32-36.
3. Al-Amoudi A., Chang J.J., Leforestier A., McDowall A., Salamin L.M., Norlen L.P., et al. Cryo-electron microscopy of vitreous sections. EMBO Journal 2004, 23:3583-3588.
4. Anchordoguy T.J., Rudolph A.S., Carpenter J.F., Crowe J.H. Modes of interaction of cryoprotectants with membrane phospholipids during freezing. Cryobiology 1987, 24:324-331.
5. Angermuller S., Fahimi H.D. Imidazole-buffered osmium tetroxide: An excellent stain for visualization of lipids in transmission electron microscopy. The Histochemical Journal 1982, 14:823-835.
6. Ariotti N., Murphy S., Hamilton N.A., Wu L., Green K., Schieber N.L., et al. Postlipolytic insulin-dependent remodeling of micro lipid droplets in adipocytes. Molecular Biology of the Cell 2012, 23:1826-1837.
7. Brasaemle D.L., Barber T., Kimmel A.R., Londos C. Post-translational regulation of perilipin expression. Stabilization by stored intracellular neutral lipids. The Journal of Biological Chemistry 1997, 272:9378-9387.
8. Cheng J., Fujita A., Ohsaki Y., Suzuki M., Shinohara Y., Fujimoto T. Quantitative electron microscopy shows uniform incorporation of triglycerides into existing lipid droplets. Histochemistry and Cell Biology 2009, 132:281-291.
9. Christian A.E., Haynes M.P., Phillips M.C., Rothblat G.H. Use of cyclodextrins for manipulating cellular cholesterol content. Journal of Lipid Research 1997, 38:2264-2272.
10. Dahl R., Staehelin L.A. High-pressure freezing for the preservation of biological structure: Theory and practice. Journal of Electron Microscopy Technique 1989, 13:165-174.
11. Elias P.M., Goerke J., Friend D.S., Brown B.E. Freeze-fracture identification of sterol-digitonin complexes in cell and liposome membranes. The Journal of Cell Biology 1978, 78:577-596.
12. Fairn G.D., Schieber N.L., Ariotti N., Murphy S., Kuerschner L., Webb R.I., et al. High-resolution mapping reveals topologically distinct cellular pools of phosphatidylserine. The Journal of Cell Biology 2011, 194:257-275.
13. Fujimoto K. Freeze-fracture replica electron microscopy combined with SDS digestion for cytochemical labeling of integral membrane proteins. Application to the immunogold labeling of intercellular junctional complexes. Journal of Cell Science 1995, 108(Pt 11):3443-3449.
14. Fujimoto T., Ohsaki Y., Cheng J., Suzuki M., Shinohara Y. Lipid droplets: A classic organelle with new outfits. Histochemistry and Cell Biology 2008, 130:263-279.
15. Fujita A., Cheng J., Fujimoto T. Quantitative electron microscopy for the nanoscale analysis of membrane lipid distribution. Nature Protocols 2010, 5:661-669.
16. Fujita A., Cheng J., Hirakawa M., Furukawa K., Kusunoki S., Fujimoto T. Gangliosides GM1 and GM3 in the living cell membrane form clusters susceptible to cholesterol depletion and chilling. Molecular Biology of the Cell 2007, 18:2112-2122.
17. Fujiyoshi Y., Kobayashi T., Ishizuka K., Uyeda N., Ishida Y., Harada Y. A new method for optimal-resolution electron microscopy of radiation-sensitive specimens. Ultramicroscopy 1980, 5:459-468.
18. Fukumoto S., Fujimoto T. Deformation of lipid droplets in fixed samples. Histochemistry and Cell Biology 2002, 118:423-428.
19. Ginsburg H., Wolosin J.M. Effects of uranyl ions on lipid bilayer membranes. Chemistry and Physics of Lipids 1979, 23:125-131.
20. Goldstein J.L., Basu S.K., Brown M.S. Receptor-mediated endocytosis of low-density lipoprotein in cultured cells. Methods in Enzymology 1983, 98:241-260.
21. Hagiwara A., Fukazawa Y., Deguchi-Tawarada M., Ohtsuka T., Shigemoto R. Differential distribution of release-related proteins in the hippocampal CA3 area as revealed by freeze-fracture replica labeling. The Journal of Comparative Neurology 2005, 489:195-216.
22. Hainfeld J.F. A small gold-conjugated antibody label: Improved resolution for electron microscopy. Science 1987, 236:450-453.
23. Hayat M.A. Immunogold-silver staining: Principles, methods, and application 1995, CRC Press, Boca Rayton.
24. Hayat M.A. Principles and techniques of electron microscopy: Biological applications 2000, Cambridge University Press, Cambridge. 4th ed.
25. Hayes T.L., Lindgren F.T., Gofman J.W. A quantitative determination of the osmium tetroxide-lipoprotein interaction. The Journal of Cell Biology 1963, 19:251-255.
26. Huang T.H., Blume A., Das Gupta S.K., Griffin R.G. Nuclear magnetic resonance and calorimetric study of the structure, dynamics, and phase behavior of uranyl ion/dipalmitoylphosphatidylcholine complexes. Biophysical Journal 1988, 54:173-179.
27. Jao C.Y., Roth M., Welti R., Salic A. Metabolic labeling and direct imaging of choline phospholipids in vivo. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:15332-15337.
28. Jimenez N., Vocking K., van Donselaar E.G., Humbel B.M., Post J.A., Verkleij A.J. Tannic acid-mediated osmium impregnation after freeze-substitution: A strategy to enhance membrane contrast for electron tomography. Journal of Structural Biology 2009, 166:103-106.
29. Karreman M.A., van Donselaar E.G., Gerritsen H.C., Verrips C.T., Verkleij A.J. VIS2FIX: A high-speed fixation method for immuno-electron microscopy. Traffic 2011, 12:806-814.
30. Kellner-Weibel G., McHendry-Rinde B., Haynes M.P., Adelman S. Evidence that newly synthesized esterified cholesterol is deposited in existing cytoplasmic lipid inclusions. Journal of Lipid Research 2001, 42:768-777.
31. Kuerschner L., Moessinger C., Thiele C. Imaging of lipid biosynthesis: How a neutral lipid enters lipid droplets. Traffic 2008, 9:338-352.
32. Liou W., Geuze H.J., Slot J.W. Improving structural integrity of cryosections for immunogold labeling. Histochemistry and Cell Biology 1996, 106:41-58.
33. McGookey D.J., Anderson R.G. Morphological characterization of the cholesteryl ester cycle in cultured mouse macrophage foam cells. The Journal of Cell Biology 1983, 97:1156-1168.
34. McIntosh R., Nicastro D., Mastronarde D. New views of cells in 3D: An introduction to electron tomography. Trends in Cell Biology 2005, 15:43-51.
35. Mobius W., Ohno-Iwashita Y., van Donselaar E.G., Oorschot V.M., Shimada Y., Fujimoto T., et al. Immunoelectron microscopic localization of cholesterol using biotinylated and non-cytolytic perfringolysin O. Journal of Histochemistry and Cytochemistry 2002, 50:43-55.
36. Nir I., Hall M.O. The ultrastructure of lipid-depleted rod photoreceptor membranes. The Journal of Cell Biology 1974, 63:587-598.
37. Ohsaki Y., Cheng J., Suzuki M., Fujita A., Fujimoto T. Lipid droplets are arrested in the ER membrane by tight binding of lipidated apolipoprotein B-100. Journal of Cell Science 2008, 121:2415-2422.
38. Ohsaki Y., Maeda T., Fujimoto T. Fixation and permeabilization protocol is critical for the immunolabeling of lipid droplet proteins. Histochemistry and Cell Biology 2005, 124:445-452.
39. Reynolds E.S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. The Journal of Cell Biology 1963, 17:208-212.
40. Rinia H.A., Burger K.N., Bonn M., Muller M. Quantitative label-free imaging of lipid composition and packing of individual cellular lipid droplets using multiplex CARS microscopy. Biophysical Journal 2008, 95:4908-4914.
41. Robenek H., Robenek M.J., Troyer D. PAT family proteins pervade lipid droplet cores. Journal of Lipid Research 2005, 46:1331-1338.
42. Roozemond R.C. The effect of fixation with formaldehyde and glutaraldehyde on the composition of phospholipids extractable from rat hypothalamus. Journal of Histochemistry and Cytochemistry 1969, 17:482-486.
43. Sawada H., Esaki M. Use of nanogold followed by silver enhancement and gold toning for preembedding immunolocalization in osmium-fixed, Epon-embedded tissues. Journal of Electron Microscopy 1994, 43:361-366.
44. Severs N.J. Freeze-fracture electron microscopy. Nature Protocols 2007, 2:547-576.
45. Shu X., Lev-Ram V., Deerinck T.J., Qi Y., Ramko E.B., Davidson M.W., et al. A genetically encoded tag for correlated light and electron microscopy of intact cells, tissues, and organisms. PLoS Biology 2011, 9:e1001041.
46. Slot J.W., Geuze H.J. Cryosectioning and immunolabeling. Nature Protocols 2007, 2:2480-2491.
47. Suzuki M., Ohsaki Y., Tatematsu T., Shinohara Y., Maeda T., Cheng J., et al. Translation inhibitors induce formation of cholesterol ester-rich lipid droplets. Plos One 2012, 7:e42379.
48. Suzuki M., Shinohara Y., Ohsaki Y., Fujimoto T. Lipid droplets: Size matters. Journal of Electron Microscopy 2011, 60(Suppl. 1):S101-S116.
49. Tahara Y., Fujiyoshi Y. A new method to measure bilayer thickness: Cryo-electron microscopy of frozen hydrated liposomes and image simulation. Micron 1994, 25:141-149.
50. Tanaka K.A., Suzuki K.G., Shirai Y.M., Shibutani S.T., Miyahara M.S., Tsuboi H., et al. Membrane molecules mobile even after chemical fixation. Nature Methods 2011, 7:865-866.
51. Tauchi-Sato K., Ozeki S., Houjou T., Taguchi R., Fujimoto T. The surface of lipid droplets is a phospholipid monolayer with a unique fatty acid composition. Journal of Biological Chemistry 2002, 277:44507-44512.
52. Tokuyasu K.T. A technique for ultracryotomy of cell suspensions and tissues. The Journal of Cell Biology 1973, 57:551-565.
53. van de Plas P., Leunissen J.L. Ultrasmall gold probes: Characteristics and use in immuno(cyto)chemical studies. Methods in Cell Biology 1993, 37:241-257.
54. van Donselaar E., Posthuma G., Zeuschner D., Humbel B.M., Slot J.W. Immunogold labeling of cryosections from high-pressure frozen cells. Traffic 2007, 8:471-485.
55. Vanhecke D., Graber W., Studer D. Close-to-native ultrastructural preservation by high pressure freezing. Methods in Cell Biology 2008, 88:151-164.
56. Walther P., Ziegler A. Freeze substitution of high-pressure frozen samples: The visibility of biological membranes is improved when the substitution medium contains water. Journal of Microscopy 2002, 208:3-10.
57. Westh P. Unilamellar DMPC vesicles in aqueous glycerol: Preferential interactions and thermochemistry. Biophysical Journal 2003, 84:341-349.
58. White D.L., Mazurkiewicz J.E., Barrnett R.J. A chemical mechanism for tissue staining by osmium tetroxide-ferrocyanide mixtures. Journal of Histochemistry and Cytochemistry 1979, 27:1084-1091.