Fol. Biol. 2010, 56, 97-109
https://doi.org/10.14712/fb2010056030097
Saccharomyces cerevisiae Nuclear and Nucleolar Antigen Preservation for Immunoelectron Microscopy
Veronika Mistríková1, Jan Bednár1,2
1Charles University in Prague, First Faculty of Medicine, Institute of Cellular Biology and Pathology, and Institute of Physiology, Academy of Sciences of the Czech Republic, Department of Cell Biology, Prague, Czech Republic
2CNRS/UJF, Laboratoire de Spectrométrie Physique, UMR 5588, BP87, St. Martin d’Hères, France
Received October 2009
Accepted January 2010
References
1. , S. M., Balduf, C., Hurt, E. (2001) The Nsp1p carboxyterminal domain is organized into functionally distinct coiled-coil regions required for assembly of nucleoporin subcomplexes and nucleocytoplasmic transport. Mol. Cell. Biol. 21, 7944-7955.
<https://doi.org/10.1128/MCB.21.23.7944-7955.2001>
2. , M., Shore, G. C. (1982) Immunocytochemical localization of mitochondrial proteins in the rat hepatocyte. J. Histochem. Cytochem. 30, 139-147.
<https://doi.org/10.1177/30.2.7061817>
3. , C., Walther, P. (2008) Freeze-substitution: the addition of water to polar solvents enhances the retention of structure and acts at temperatures around -60 degrees C. J. Microsc. 230, 268-277.
<https://doi.org/10.1111/j.1365-2818.2008.01984.x>
4. , E., Garavito, R. M., Villiger, W. (1982) Resin development for electron-microscopy and an analysis of embedding at low-temperature. J. Microsc. 126, 123-143.
<https://doi.org/10.1111/j.1365-2818.1982.tb00362.x>
5. , H. J., Rout, M. P., Giddings, T. H., Winey, M. (1998) Saccharomyces cerevisiae Ndc1p is a shared component of nuclear pore complexes and spindle pole bodies. J. Cell Biol. 143, 1789-1800.
<https://doi.org/10.1083/jcb.143.7.1789>
6. , M., Montanaro, L., Trere, D. (2009) What the nucleolus says to a tumour pathologist. Histopathology 54, 753-762.
<https://doi.org/10.1111/j.1365-2559.2008.03168.x>
7. , J. (2007) The physics of rapid cooling and its implications for cryoimmobilization of cells. Methods Cell Biol. 79, 7-21.
<https://doi.org/10.1016/S0091-679X(06)79001-X>
8. , M. L., Gas, N., Stevens, B. J. (1985) Immuno localization of the 100 K nucleolar protein in CHO cells. Biol. Cell 53, 99-109.
<https://doi.org/10.1111/j.1768-322X.1985.tb00359.x>
9. , B., Aris, J. P., Hurt, E. C., Pante, N., Aebi, U. (2000) Comparative spatial localization of protein-A-tagged and authentic yeast nuclear pore complex proteins by immunogold electron microscopy. J. Struct. Biol. 129, 295-305.
<https://doi.org/10.1006/jsbi.2000.4223>
10. , E., Zink, D. (2008) Nuclear architecture and gene regulation. Biochim. Biophys. Acta 1783, 2174-2184.
<https://doi.org/10.1016/j.bbamcr.2008.07.018>
11. , T. H. (2003) Freeze-substitution protocols for improved visualization of membranes in high-pressure frozen samples. J. Microsc. 212, 53-61.
<https://doi.org/10.1046/j.1365-2818.2003.01228.x>
12. , J., Mari, M., De Maziere, A., Reggiori, F. (2008) A cryosectioning procedure for the ultrastructural analysis and the immunogold labelling of yeast Saccharomyces cerevisiae. Traffic 9, 1060-1072.
<https://doi.org/10.1111/j.1600-0854.2008.00753.x>
13. , M. P., Girard, J. P., Zabetakis, D., Lapeyre, B., Melese, T., Caizergues-Ferrer, M. (1995) gar2 is a nucleolar protein from Schizosaccharomyces pombe required for 18S rRNA and 40S ribosomal subunit accumulation. Nucleic Acids Res. 23, 1912-1918.
<https://doi.org/10.1093/nar/23.11.1912>
14. , P., Netherton, C. L., Mueller, M., Wileman, T., Monaghan, P. (2007) Rapid freeze-substitution preserves membranes in high-pressure frozen tissue culture cells. J. Microsc. 226, 182-189.
<https://doi.org/10.1111/j.1365-2818.2007.01767.x>
15. , D. (2006) The nucleolus: a model for the organization of nuclear functions. Histochem. Cell Biol. 126, 135-148.
<https://doi.org/10.1007/s00418-006-0212-3>
16. , C., Cheeseman, I. M., Goode, B. L., McDonald, K. L., Barnes, G., Drubin, D. G. (1998) Saccharomyces cerevisiae Duo1p and Dam1p, novel proteins involved in mitotic spindle function. J. Cell Biol. 143, 1029-1040.
<https://doi.org/10.1083/jcb.143.4.1029>
17. , H., Mannweiler, K., Muller, M. (1994) Highpressure freezing of cell suspensions in cellulose capillary tubes. J. Microsc. 175, 34-43.
<https://doi.org/10.1111/j.1365-2818.1994.tb04785.x>
18. , B. M., Konomi, M., Takagi, T., Kamasawa, N., Ishijima, S. A., Osumi, M. (2001) In situ localization of beta-glucans in the cell wall of Schizosaccharomyces pombe. Yeast 18, 433-444.
<https://doi.org/10.1002/yea.694>
19. , J. V., Adams, A. E. (1984) Structural rearrangements of tubulin and actin during the cell cycle of the yeast Saccharomyces. J. Cell Biol. 98, 922-933.
<https://doi.org/10.1083/jcb.98.3.922>
20. , K., Inouye, M. (1992) Yeast NSR1 protein that has structural similarity to mammalian nucleolin is involved in pre-rRNA processing. J. Biol. Chem. 267, 16252-16258.
<https://doi.org/10.1016/S0021-9258(18)41993-X>
21. , W. C., Zabetakis, D., Melese, T. (1992) NSR1 is required for pre-rRNA processing and for the proper maintenance of steady-state levels of ribosomal subunits. Mol. Cell. Biol. 12, 3865-3871.
22. , I., Gulli, M. P., Noaillac-Depeyre, J., Faubladier, M., Sicard, H., Caizergues-Ferrer, M., Gas, N. (1997) Ultrastructural changes in the Schizosaccharomyces pombe nucleolus following the disruption of the gar2+ gene, which encodes a nucleolar protein structurally related to nucleolin. Chromosoma 105, 542-552.
<https://doi.org/10.1007/BF02510491>
23. , I., Trumtel, S., Noaillac-Depeyre, J., Gas, N. (1999) Functional compartmentalization of the nucleus in the budding yeast Saccharomyces cerevisiae. Chromosoma 108, 103-113.
<https://doi.org/10.1007/s004120050357>
24. , K. (1999) High-pressure freezing for preservation of high resolution fine structure and antigenicity for immunolabeling. Methods Mol. Biol. 117, 77-97.
<https://doi.org/10.1385/1-59259-678-9:77>
25. , K., Muller-Reichert, T. (2002) Cryomethods for thin section electron microscopy. Methods Enzymol. 351, 96-123.
<https://doi.org/10.1016/S0076-6879(02)51843-7>
26. , K. (2007) Cryopreparation methods for electron microscopy of selected model systems. Methods Cell Biol. 79, 23-56.
<https://doi.org/10.1016/S0091-679X(06)79002-1>
27. , K. L., Morphew, M., Verkade, P., Muller-Reichert, T. (2007) Recent advances in high-pressure freezing: equipmentand specimen-loading methods. Methods Mol. Biol. 369, 143-173.
<https://doi.org/10.1007/978-1-59745-294-6_8>
28. , T., Xue, Z. (1995) The nucleolus: an organelle formed by the act of building a ribosome. Curr. Opin. Cell Biol. 7, 319-324.
<https://doi.org/10.1016/0955-0674(95)80085-9>
29. Mosgoeller, W. (2004) Nucleolar ultrastructure in vertebrates. In: The Nucleolus, ed. Olson, M. O. J., pp 10-20, Eurekah. com and Kluwer Academic, New York, USA.
30. , J., Botstein, D. (2002) Immunoelectron microscopy of aldehyde-fixed yeast cells. Methods Enzymol. 351, 50-81.
<https://doi.org/10.1016/S0076-6879(02)51841-3>
31. , T., Sassoon, I., O’Toole, E., Romao, M., Ashford, A. J., Hyman, A. A., Antony, C. (2003) Analysis of the distribution of the kinetochore protein Ndc10p in Saccharomyces cerevisiae using 3-D modeling of mitotic spindles. Chromosoma 111, 417-428.
<https://doi.org/10.1007/s00412-002-0220-6>
32. , S. (2008) High pressure freezing and freeze substitution of Schizosaccharomyces pombe and Saccharomyces cerevisiae for TEM. Methods Cell Biol. 88, 3-17.
<https://doi.org/10.1016/S0091-679X(08)00401-9>
33. , D., Lopez-Iglesias, C. (1998) A comparison of cryoversus chemical fixation in the soil green algae Jaagiella. Tissue Cell 30, 368-376.
<https://doi.org/10.1016/S0040-8166(98)80050-5>
34. , J. R., Preston, R. A., Adams, A. E., Stearns, T., Drubin, D. G., Haarer, B. K., Jones, E. W. (1989) Fluorescence microscopy methods for yeast. Methods Cell Biol. 31, 357-435.
<https://doi.org/10.1016/S0091-679X(08)61620-9>
35. , H., Eifert, J., Wacheul, L., Thiry, M., Berger, A. C., Jakovljevic, J., Woolford, J. L., Jr., Corbett, A. H., Lafontaine, D. L., Terns, R. M., Terns, M. P. (2008) Identification of genes that function in the biogenesis and localization of small nucleolar RNAs in Saccharomyces cerevisiae. Mol. Cell. Biol. 28, 3686-3699.
<https://doi.org/10.1128/MCB.01115-07>
36. , C. (1994) Cryofixation, cryosubstitution, cryoembedding for ultrastructural, immunocytochemical and microanalytical studies. Micron 25, 63-99.
<https://doi.org/10.1016/0968-4328(94)90056-6>
37. , E. S. (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208-212.
<https://doi.org/10.1083/jcb.17.1.208>
38. , M., Kobori, H., Ishijima, S. A., Feng, Z. H., Hamada, K., Shimada, S., Osumi, M. (1996) Schizosaccharomyces pombe is more sensitive to pressure stress than Saccharomyces cerevisiae. Cell Struct. Funct. 21, 167-174.
<https://doi.org/10.1247/csf.21.167>
39. , T., Tollervey, D., Kern, H., Frank, R., Hurt, E. C. (1989) A yeast nucleolar protein related to mammalian fibrillarin is associated with small nucleolar RNA and is essential for viability. EMBO J. 8, 4015-4024.
<https://doi.org/10.1002/j.1460-2075.1989.tb08584.x>
40. Schwarz, H. Hohenberg, H., Humbel, B. M. (1993) Freezesubstitution in virus research: a preview. In: Immuno-gold Electron Microscopy in Virus Diagnosis and Research, eds. Hyatt A. D., Eaton, B. T., pp. 349-376, CRC Press, Inc., Boca Raton, Florida, USA.
41. , P., Doonan, J. (2005) The nucleolus. Playing by different rules? Cell Cycle 4, 102-105.
<https://doi.org/10.4161/cc.4.1.1467>
42. , H., Faubladier, M., Noaillac-Depeyre, J., LegerSilvestre, I., Gas, N., Caizergues-Ferrer, M. (1998) The role of the Schizosaccharomyces pombe gar2 protein in nucleolar structure and function depends on the concerted action of its highly charged N terminus and its RNA-binding domains. Mol. Biol. Cell. 9, 2011-2023.
<https://doi.org/10.1091/mbc.9.8.2011>
43. , V., Urcuqui-Inchima, S., Roussel, P., HernandezVerdun, D. (2008) Nucleolus: the fascinating nuclear body. Histochem. Cell Biol. 129, 13-31.
<https://doi.org/10.1007/s00418-007-0359-6>
44. , D. L., Ochs, R. L., Busch, H. (1984) Silver staining, immunofluorescence, and immunoelectron microscopic localization of nucleolar phosphoproteins B23 and C23. Chromosoma 90, 139-148.
<https://doi.org/10.1007/BF00292451>
45. , D., Humbel, B. M., Chiquet, M. (2008) Electron microscopy of high pressure frozen samples: bridging the gap between cellular ultrastructure and atomic resolution. Histochem. Cell Biol. 130, 877-889.
<https://doi.org/10.1007/s00418-008-0500-1>
46. , M., Lafontaine, D. L. (2005) Birth of a nucleolus: the evolution of nucleolar compartments. Trends Cell Biol. 15, 194-199.
<https://doi.org/10.1016/j.tcb.2005.02.007>
47. , D., Lehtonen, H., Carmo-Fonseca, M., Hurt, E. C. (1991) The small nucleolar RNP protein NOP1 (fibrillarin) is required for pre-rRNA processing in yeast. EMBO J. 10, 573-583.
<https://doi.org/10.1002/j.1460-2075.1991.tb07984.x>
48. , S., Leger-Silvestre, I., Gleizes, P. E., Teulieres, F., Gas, N. (2000) Assembly and functional organization of the nucleolus: ultrastructural analysis of Saccharomyces cerevisiae mutants. Mol. Biol. Cell 11, 2175-2189.
<https://doi.org/10.1091/mbc.11.6.2175>
49. , E., Posthuma, G., Zeuschner, D., Humbel, B. M., Slot, J. W. (2007) Immunogold labeling of cryosections from high-pressure frozen cells. Traffic 8, 471-485.
<https://doi.org/10.1111/j.1600-0854.2007.00552.x>
50. , E., Riezman, H. (1987) Immunolocalization of glyceraldehyde-3-phosphate dehydrogenase, hexokinase, and carboxypeptidase Y in yeast cells at the ultrastructural level. J. Histochem. Cytochem. 35, 327-333.
<https://doi.org/10.1177/35.3.3546482>
51. , D., Graber, W., Studer, D. (2008) Close-to-native ultrastructural preservation by high pressure freezing. Methods Cell Biol. 88, 151-164.
<https://doi.org/10.1016/S0091-679X(08)00409-3>
52. , M. L., Fakan, S., Villiger, W. (1991) Some applications of cryosubstitution in ultrastructural studies of the cell nucleus. Biol. Cell 72, 113-119.
<https://doi.org/10.1016/0248-4900(91)90085-2>
53. , M. L., Fakan, S. (1993) The study of the cell nucleus using cryofixation and cryosubstitution. Micron 24, 507-519.
<https://doi.org/10.1016/0968-4328(93)90027-X>
54. , P., Ziegler, A. (2002) Freeze substitution of highpressure frozen samples: the visibility of biological membranes is improved when the substitution medium contains water. J. Microsc. 208, 3-10.
<https://doi.org/10.1046/j.1365-2818.2002.01064.x>
55. , R. (2000) Transmission electron microscopy of yeast. Microsc. Res. Tech. 51, 496-510.
<https://doi.org/10.1002/1097-0029(20001215)51:6<496::AID-JEMT2>3.0.CO;2-9>
56. , C., Henry, P. A., Setya, A., Henry, M. F. (2003) In vivo analysis of nucleolar proteins modified by the yeast arginine methyltransferase Hmt1/Rmt1p. RNA 9, 746-759.
<https://doi.org/10.1261/rna.5020803>
57. , C., Melese, T. (1993) Multiple regions of NSR1 are sufficient for accumulation of a fusion protein within the nucleolus. J. Cell Biol. 123, 1081-1091.
<https://doi.org/10.1083/jcb.123.5.1081>
