Electron tomography of metaphase nucleolar organizer regions: Evidence for a twisted-loop organization

Molecular Biology of the Cell

Volumn 8, Issue 11, 1997, Pages 2199-2216

  Heliot, Laurent ^a   Kaplan, Hervé ^a   Lucas, Laurent ^a   Klein, Christophe ^a   Beorchia, Adrien ^a   Doco Fenzy, Martine ^a   Menager, Monique ^a   Thiry, Marc ^b   O'Donohue, Marie Françoise ^a   Ploton, Dominique ^a  

^a HÔPITAL MAISON BLANCHE   (France)

^b Institut Pitteurs   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA DIRECTED RNA POLYMERASE; PROTEIN;

ANIMAL CELL; ARTICLE; CHROMATIN; CHROMOSOME BAND; CHROMOSOME NOR; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; METAPHASE; MODEL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SILVER STAINING; TOMOGRAPHY;

ANIMALIA;

EID: 0030729070     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.8.11.2199     Document Type: Article

References (58)

1. Adolph, K.W., Kreisman, L.R., and Kuehn, R.L. (1986). Assembly of chromatin fibers into metaphase chromosomes analyzed by transmission electron microscopy and scanning electron microscopy. Biophys. J. 49, 221-231.
2. Babu, K.A., and Verma, R.S. (1985). Structural and functional aspects of nucleolar organizer regions (NORs) in human chromosomes. Int. Rev. Cytol. 94, 151-176.
3. Bahr, G.F., Boccia, J.A., and Engler, W.F. (1979). Reconstruction of a chromosome model from its projections. Ultramicroscopy 4, 45-53.
4. Beorchia, A., Heliot, L, Menager, M., Kaplan H., and Ploton, D. (1992). Applications of medium-voltage STEM for the 3-D study of organelles within very thick sections. J. Microsc. 170, 247-258.
5. Boy de la Tour, E., and Laemmli, U.K. (1988). The metaphase scaffold is helically folded: sister chromatids have predominantly opposite helical handedness. Cell 55, 937-944.
6. Brinkley, B.R., Ouspenski, I., and Zinkowski, R.P. (1992). Structure and molecular organization of the centromere-kinetochore complex. Trends Cell Biol. 2, 15-21.
7. Chan, E.K.L., Imai, H., Hamel, J.C., and Tan, E.M.. (1991). Human autoantibody to RNA polymerase I transcription factor hUBF. Molecular identity of nucleolus organizer region autoantigen NOR-90 and ribosomal RNA transcription upstream binding factor. J. Exp. Med. 174, 1239-1244.
8. Conconi, A., Widmer, R.M., Koller, T., and Sogo, J.M. (1989). Two different chromatin structures coexist in ribosomal RNA genes through out the cell cycle. Cell 57, 753-761.
9. Crowther, R.A., De Rosier, D.J., and Klug, A. (1970). The reconstruction of a three-dimensional structure from projections and its application to electron microscopy. Proc. R. Soc. Lond. Ser. A 317, 319-340.
10. Dupraw, E. (1966). Macromolecular organization of nuclei and chromosomes; a folded fiber model based on whole mount electron microscopy. Nature 206, 338-343.
11. Filipski, J., Leblanc, J., Youdale, T., Sikorska, M., and Walker, P.R. (1990). Periodicity of DNA folding in higher order chromatin structures. EMBO J. 9, 1319-1327.
12. Frank, J. (1992). Principles of electron tomography. In: Electron Tomography: Three Dimensional Imaging with the Transmission Electron Microscope, ed. J. Frank, New York: Plenum Press, 1-13.
13. Gilbert, N., Lucas, L., Klein, C., Menager, M., Bonnet, N., and Ploton, D. (1995). Three-dimensional co-location of RNA polymerase I and DNA during interphase and mitosis by confocal microscopy. J. Cell Sci. 108, 115-125.
14. Goodpasture, C., and Bloom, S.E. (1975). Visualization of nucleolar organizer regions in mammalian chromosomes using silver staining. Chromosoma 53, 37-50.
15. Gordon, R., Bender, R., and Herman, G.T. (1970). Algebraic reconstruction techniques (ART) for the three-dimensional electron microscopy and x-ray photography. J. Theor. Biol. 29, 471-481.
16. Haaf, T., Hayman, D.L., and Schmid, M. (1991). Quantitative determination of rDNA transcription units in vertebrate cells. Exp. Cell Res. 193, 78-86.
17. Hadjiolov, A.A. (1985). Ribosomal genes. In: The Nucleolus and Ribosome Biogenesis, ed. A.A. Hadjiolov, Wien, Austria: Springer-Verlag, 5-51.
18. Harrison, C.J., Britch, M., Allen, T.C., and Harris, R. (1981). Scanning electron microscopy of the G-banded human karyotype. Exp. Cell Res. 134, 141-153.
19. Hernandez-Verdun, D., and Derenzini, M. (1983). Non-nucleosomal configuration of chromatin in nucleolar organizer regions of metaphase chromosomes in situ. Eur. J. Cell Biol. 31, 360-365.
20. Holmquist, G.P. (1992). Chromosome bands: their chromatin flavors and their functional features. Am. J. Hum. Genet. 51, 17-37.
21. Howell, W.M. (1982). Selective staining of nucleolus organizer regions (NORs). In: The Cell Nucleus, Vol. XI, ed. H. Busch and L. Rothblum, New York: Academic Press, 89-142.
22. Lucas, L., Gilbert, N., Ploton, D., and Bonnet, N. (1996). Visualization of volume data in confocal microscopy: comparison and improvements of volume rendering methods. J. Microsc. 181, 238-252.
23. Manuelidis, L. (1990). A view of interphase chromosomes. Science 250, 1533-1540.
24. Marsden, M.P.F., and Laemmli, U.K. (1979). Metaphase chromosome structure: evidence for a radial loop model. Cell 17, 849-858.
25. Matsui, S., and Sandberg, A.A. (1985). Intranuclear compartmentalization of DNA-dependent RNA polymerases: association of RNA polymerase I with nucleolar organizing chromosomes. Chromosoma 92, 1-6.
26. McDowall, A.W., Smith, J.M., and Dubochet, J. (1986). Cryo-electron microscopy of vitrified chromosomes in situ. EMBO J. 5, 1393-1402.
27. McEwen, B.F. (1992). Three-dimensional reconstructions of organelles and cellular processes. In: Electron Tomography: Three-Dimensional Imaging with the Transmission Electron Microscope, ed. J. Franck, New York: Plenum Press, 281-311.
28. Monier, K., Usson, Y., Mongelard, Szepetowski, F.P., Robert-Nicoud, M., and Vourc'h, C. (1996). Metaphase and interphase mapping by FISH: improvement of chromosome banding and signal resolution in interphase nuclei by means of iterative deconvolution. Cytogenet. Cell Genet. 72, 200-204.
29. Ochs, R.L., and Press, R.I. (1992). Centromere auto antigens are associated with the nucleolus. Exp. Cell Res. 200, 339-350.
30. Paulson, J.R., and Laemmli, U.K. (1977). The structure of histone-depleted metaphase chromosomes. Cell 12, 817-828.
31. Ploton, D., Bobichon, H., and Adnet J.J. (1982). Ultrastructural localization of NOR in nucleoli of human breast cancer tissues using a one-step Ag-NOR staining method. Biol. Cell. 43, 229-232.
32. Ploton, D., Gilbert, N., Menager, M., Kaplan, H., and Adnet, J.J. (1994). Three-dimensional co-localization of nucleolar argyrophilic components and DNA in cell nuclei by confocal microscopy. The J. Histochem. Cytochem. 42, 137-148.
33. Ploton, D., Menager, M., Jeannesson, P., Beorchia, A., and Adnet, J.J. (1990). Localization of DNA and characterization of argyrophilic structures within nucleolar components during interphase and mitosis in leukemia cell lines. In: Nuclear Structure and Function, ed J.R. Harris and I.B. Zbarsky, New York: Plenum Press, 157-160.
34. Ploton, D., Menager, M., Jeannesson, P., Himber, G., Pigeon, F., and Adnet, J.J. (1986). Improvement in the staining and in the visualization of the argyrophilic proteins of the nucleolar organizer region at the optical level. Histochem. J. 18, 5-14.
35. Ploton, D., Thiry, M., Menager, M., Lepoint, A., Adnet, J.J., and Goessens, G. (1987). Behaviour of nucleolus during mitosis. A comparative ultrastructural study of various cancerous cell-lines using Ag-NOR staining procedure. Chromosoma 95, 95-107.
36. Poljak, L., and Kâs, E. (1995). Resolving the role of topoisomerase II in chromatin structure and function. Trends Cell Biol. 5, 348-354.
37. Rattner, J.B., and Lin, C.C. (1985). Radial loops and helical coils coexist in metaphase chromosomes. Cell 42, 291-296.
38. Robert-Fortel, I., Junera, H.R., Geraud., G., and Hernandez-Verdun, D. (1993). Three-dimensional organization of the ribosomal genes and Ag-NOR proteins during interphase and mitosis in Ptk1 cells studied by confocal microscopy. Chromosoma 102, 146-157.
39. Roussel, P., André, C., Comai, L., and Hernandez-Verdun, D. (1996). The rDNA transcription machinery is assembled during mitosis in active NORs and absent in inactive NORs. J. Cell Biol. 133, 235-246.
40. Roussel, P., and Hernandez-Verdun, D. (1994). Identification of Ag-NOR proteins, markers of proliferation related to ribosomal gene activity. Exp. Cell Res. 214, 465-472.
41. Saitoh, Y., and Laemmli, U.K. (1994). Metaphase chromosome structure : bands arise from a differential folding path of the highly AT-rich scaffold. Cell 76, 609-622.
42. Scheer, U., and Rose, K.M. (1984). Localization of RNA polymerase I in interphase cells and mitotic chromosomes by light and electron microscopic immunocytochemistry. Proc. Natl. Acad. Sci. USA 81, 1431-1435.
43. Sedat, J., and Manuelidis, L. (1977). A direct approach to the structure of eukaryotic chromosomes. J. Cell Biol. 42, 331-350.
44. Sibon, O.C.M., Cremers, F.F.M., Humbel, B.M., Boonstra, J., and Verkleij, A.J. (1995). Localization of nuclear RNA by pre and post embedding in situ hybridization using different gold probes. Histochem. J. 27, 35-45.
45. Sikorav, J.L., and Jannink, G. (1994). Kinetics of chromosome condensation in the presence of topoisomerases: a phantom chain model. Biophys. J. 66, 827-837.
46. Sumner, A.T. (1982). The nature and mechanisms of chromosome banding. Cancer Genet. Cytogenet. 6, 59-87.
47. Sumner, A.T. (1992). Classification and nomenclature of chromosome bands. In: Chromosome Banding, ed. A.T. Sumner, London: Unwin Hyman, 9-20.
48. Sumner, A.T. (1994). Functional aspects of the longitudinal differentiation of chromosomes. Eur. J. Histochem. 38, 91-109.
49. Thiry, M., and Goessens, G. (1996). The nucleolus during the cell cycle. In: Molecular Biology Intelligence Unit, ed. R.G. Landes Company, Location: Springer-Verlag.
50. Thiry, M., Ploton, D., Menager, M., and Goessens, G. (1993). Ultra-structural distribution of DNA within the nucleolus of various animal cell lines or tissues revealed by terminal deoxynucleotidyl transferase. Cell Tissue Res. 271, 33-45.
51. Turner, J.N., and Collins, D.N. (1990). Three-dimensional imaging at high resolution: high-voltage electron microscopy. J. Histotechnol. 13, 93-107.
52. Verma, R.S., and Babu, A. (1995). Human Chromosomes: Principles and Techniques, ed. R.S. Verma and A. Babu, New York: McGraw-Hill.
53. Warburton, D., and Henderson, A.S. (1979). Sequential silver staining and hybridization in situ on nucleolus organizing regions in human cells. Cytogenet. Cell Genet. 24, 168-175.
54. Weisenberger, D., and Scheer, U (1995). A possible mechanism for the inhibition of ribosomal RNA gene transcription during mitosis. J. Cell Biol. 129, 561-575.
55. Woodcock, C.L. (1992). The organization of chromosomes and chromatin. In: Electron Tomography: Three-Dimensional Imaging with the Transmission Electron Microscope, ed. J. Frank, New York: Plenum Press, 313-357.
56. Woodcock, C.L., and Horowitz, R.A. (1995). Chromatin organization re-viewed. Trends Cell Biol. 5, 272-277.
57. Yamada, E., and Ishikawa, H. (1981). Dense tissue and special stains. Methods Cell Biol. 22, 123-145.
58. Zatsepina, O.V., Voit, R., Grummt, I., Spring, H., Semenov, M.V., and Trendelenburg, M.F. (1993). The RNA polymerase I specific transcription initiation factor UBF is associated with transcriptionally active and inactive ribosomal genes. Chromosoma 102, 599-611.