Histochemistry and Cell Biology

, Volume 125, Issue 1–2, pp 127–137 | Cite as

Nucleolus: from structure to dynamics

  • Danièle Hernandez-VerdunEmail author


The nucleolus, a large nuclear domain, is the ribosome factory of the cells. Ribosomal RNAs are synthesized, processed and assembled with ribosomal proteins in the nucleolus, and the ribosome subunits are then transported to the cytoplasm. In this review, the structural organization of the nucleolus and the dynamics of the nucleolar proteins are discussed in an attempt to link both information. By electron microscopy, three main nucleolar components corresponding to different steps of ribosome biogenesis are identified and the nucleolar organization reflects its activity. Time-lapse videomicroscopy and fluorescent recovery after photobleaching (FRAP) demonstrate that mobility of GFP-tagged nucleolar proteins is slower in the nucleolus than in the nucleoplasm. Fluorescent recovery rates change with inhibition of transcription, decreased temperature and depletion of ATP, indicating that recovery is correlated with cell activity. At the exit of mitosis, the nucleolar processing machinery is first concentrated in prenucleolar bodies (PNBs). The dynamics of the PNBs suggests a steady state favoring residence of processing factors that are then released in a control- and time-dependent manner. Time-lapse analysis of fluorescence resonance energy transfer demonstrates that processing complexes are formed in PNBs. Finally, the nucleolus appears at the center of several trafficking pathways in the nucleus.


Nucleolus Organization Dynamics Assembly 



The authors thank Myriam Barre for help in photographic work and A. L. Haenni for critical reading of the paper. This work was supported in part by grants from the Centre National de la Recherche Scientifique and the Association pour la Recherche sur le Cancer (Contract 3303).

Supplementary material (351 kb)
Supplementary material



  1. Andersen JS, Lam YW, Leung AK, Ong SE, Lyon CE, Lamond AI, Mann M (2005) Nucleolar proteome dynamics. Nature 433:77–83PubMedCrossRefGoogle Scholar
  2. Angelier N, Tramier M, Louvet E, Coppey-Moisan M, Savino TM, De Mey JR, Hernandez-Verdun DD (2005) Tracking the interactions of rRNA processing proteins during nucleolar assembly in living cells. Mol Biol Cell 16:2862–2871PubMedCrossRefGoogle Scholar
  3. Azum-Gélade M-C, Noaillac-Depeyre J, Caizergues-Ferrer M, Gas N (1994) Cell cycle redistribution of U3 snRNA and fibrillarin. Presence in the cytoplasmic nucleolus remnant and in the prenucleolar bodies at telophase. J Cell Sci 107:463–475PubMedGoogle Scholar
  4. Bell P, Dabauvalle MC, Scheer U (1992) In vitro assembly of prenucleolar bodies in Xenopus egg extract. J Cell Biol 118:1297–1304PubMedCrossRefGoogle Scholar
  5. Bertrand E, Houser-Scott F, Kendall A, Singer RH, Engelke DR (1998) Nucleolar localization of early tRNA processing. Genes Dev 12:2463–2468PubMedGoogle Scholar
  6. Biggiogera M, Fakan S, Kaufmann SH, Black A, Shaper JH, Busch H (1989) Simultaneous immunoelectron microscopic visualization of protein B23 and C23 distribution in the HeLa cell nucleolus. J Histochem Cytochem 37:1371–1374PubMedGoogle Scholar
  7. Boulon S, Verheggen C, Jady BE, Girard C, Pescia C, Paul C, Ospina JK, Kiss T, Matera AG, Bordonne R, Bertrand E (2004) PHAX and CRM1 are required sequentially to transport U3 snoRNA to nucleoli. Mol Cell 16:777–787PubMedCrossRefGoogle Scholar
  8. Bubulya PA, Prasanth KV, Deerinck TJ, Gerlich D, Beaudouin J, Ellisman MH, Ellenberg J, Spector DL (2004) Hypophosphorylated SR splicing factors transiently localize around active nucleolar organizing regions in telophase daughter nuclei. J Cell Biol 167:51–63PubMedCrossRefGoogle Scholar
  9. Carmo-Fonseca M, Mendes-Soares L, Campos I (2000) To be or not to be in the nucleolus. Nat Cell Biol 2:107–112CrossRefGoogle Scholar
  10. Carmo-Fonseca M, Platani M, Swedlow JR (2002) Macromolecular mobility inside the cell nucleus. Trends Cell Biol 12:491–495PubMedCrossRefGoogle Scholar
  11. Chan PK, Qi Y, Amley J, Koller CA (1996) Quantitation of the nucleophosmin/B23-translocation using imaging analysis. Cancer Lett 100:191–197PubMedCrossRefGoogle Scholar
  12. Chen D, Huang S (2001) Nucleolar components involved in ribosome biogenesis cycle between the nucleolus and nucleoplasm in interphase cells. J Cell Biol 153:169–176PubMedCrossRefGoogle Scholar
  13. Clute P, Pines J (1999) Temporal and spatial control of cyclin B1 destruction in metaphase. Nat cell Biol 1:82–87PubMedCrossRefGoogle Scholar
  14. Cmarko D, Verschure PJ, Rothblum LI, Hernandez-Verdun D, Amalric F, van Driel R, Fakan S (2000) Ultrastructural analysis of nucleolar transcription in cells microinjected with 5-bromo-UTP. Histochem Cell Biol 113:181–187PubMedCrossRefGoogle Scholar
  15. Cockell MM, Gasser SM (1999) The nucleolus: nucleolar space for rent. Curr Biol 9:R575–R576PubMedCrossRefGoogle Scholar
  16. Colau G, Thiry M, Leduc V, Bordonne R, Lafontaine DL (2004) The small nucle(ol)ar RNA cap trimethyltransferase is required for ribosome synthesis and intact nucleolar morphology. Mol Cell Biol 24:7976–7986PubMedCrossRefGoogle Scholar
  17. David-Pfeuty T, Nouvian-Dooghe Y, Sirri V, Roussel P, Hernandez-Verdun D (2001) Common and reversible regulation of wild-type p53 function and of ribosomal biogenesis by protein kinases in human cells. Oncogene 20:5951–5963PubMedCrossRefGoogle Scholar
  18. Dousset T, Wang C, Verheggen C, Chen D, Hernandez-Verdun D, Huang S (2000) Initiation of nucleolar assembly is independent of RNA polmerase I transcription. Mol Biol Cell 11:2705–2717PubMedGoogle Scholar
  19. Dundr M, Olson MOJ (1998) Partially processed pre-rRNA is preserved in association with processing components in nucleolus derived foci during mitosis. Mol Biol Cell 9:2407–2422PubMedGoogle Scholar
  20. Dundr M, Misteli T, Olson MOJ (2000) The dynamics of postmitotic reassembly of the nucleolus. J Cell Biol 150:433–446PubMedCrossRefGoogle Scholar
  21. Dundr M, Hoffmann-Rohrer U, Hu Q, Grummt I, Rothblum LI, Phair RD, Misteli T (2002) A kinetic framework for a mammalian RNA polymerase in vivo. Science 298:1623–1626PubMedCrossRefGoogle Scholar
  22. Dundr M, Hebert MD, Karpova TS, Stanek D, Xu H, Shpargel KB, Meier UT, Neugebauer KM, Matera AG, Misteli T (2004) In vivo kinetics of Cajal body components. J Cell Biol 164:831–842PubMedCrossRefGoogle Scholar
  23. Emiliani V, Sanvitto D, Tramier M, Piolot T, Petrasek Z, Kemnitz K, Durieux C, Coppey-Moisan M (2003) Low-intensity two-dimensional imaging of fluorescence lifetimes in living cells. Appl Phys Lett 83:2471–2473CrossRefGoogle Scholar
  24. Fatica A, Tollervey D (2002) Making ribosomes. Curr Opin Cell Biol 14:313–318PubMedCrossRefGoogle Scholar
  25. Finch RA, Chan PK (1996) ATP depletion affects NPM translocation and exportation of rRNA from nuclei. Biochem Biophys Res Commun 222:553–558PubMedCrossRefGoogle Scholar
  26. Finch RA, Revankar GR, Chan PK (1993) Nucleolar localization of nucleophosmin/B23 requires GTP. J Biol Chem 268:5823–5827PubMedGoogle Scholar
  27. Fomproix N, Gébrane-Younès J, Hernandez-Verdun D (1998) Effects of anti-fibrillarin antibodies on building of functional nucleoli at the end of mitosis. J Cell Sci 111:359–372PubMedGoogle Scholar
  28. Fromont-Racine M, Senger B, Saveanu C, Fasiolo F (2003) Ribosome assembly in eukaryotes. Gene 313:17–42PubMedCrossRefGoogle Scholar
  29. Gall JG (2000) Cajal bodies: the first 100 years. Annu Rev Cell Dev Biol 16:273–300PubMedCrossRefGoogle Scholar
  30. Ganot P, Jady BE, Bortolin M-L, Darzacq X, Kiss T (1999) Nucleolar factors direct the 2′-O-ribose methylation and pseudouridylation of U6 spliceosomal RNA. Mol Cell Biol 19:6906–6917PubMedGoogle Scholar
  31. Gautier T, Dauphin-Villemant C, André C, Masson C, Arnoult J, Hernandez-Verdun D (1992a) Identification and characterization of a new set of nucleolar ribonucleoproteins which line the chromosomes during mitosis. Exp Cell Res 200:5–15PubMedCrossRefGoogle Scholar
  32. Gautier T, Masson C, Quintana C, Arnoult J, Hernandez-Verdun D (1992b) The ultrastructure of the chromosome periphery in human cells. An in situ study using cryomethods in electron microscopy. Chromosoma 101:502–510PubMedCrossRefGoogle Scholar
  33. Gautier T, Robert-Nicoud M, Guilly M-N, Hernandez-Verdun D (1992c) Relocation of nucleolar proteins around chromosomes at mitosis—a study by confocal laser scanning microscopy. J Cell Sci 102:729–737PubMedGoogle Scholar
  34. Gautier T, Fomproix N, Masson C, Azum-Gélade MC, Gas N, Hernandez-Verdun D (1994) Fate of specific nucleolar perichromosomal proteins during mitosis: cellular distribution and association with U3 snoRNA. Biol Cell 82:81–93PubMedCrossRefGoogle Scholar
  35. Gébrane-Younès J, Sirri V, Junéra HR, Roussel P, Hernandez-Verdun D (2005) Nucleolus: an essential nuclear domain. In: Diekmann PHaS (ed) Visions of the cell nucleus. ASP, CA, pp 120–135Google Scholar
  36. Ginisty H, Amalric F, Bouvet P (1998) Nucleolin functions in the first step of ribosomal RNA processing. EMBO J 17:1476–1486PubMedCrossRefGoogle Scholar
  37. Granick D (1975) Nucleolar necklaces in chick embryo fibroblast cells. II. Microscope observations of the effect of adenosine analogues on nucleolar necklace formation. J Cell Biol 65:418–427PubMedCrossRefGoogle Scholar
  38. Guarente L (2000) Sir2 links chromatin silencing, metabolism, and aging. Genes Dev 14:1021–1026PubMedGoogle Scholar
  39. Guillot PV, Martin S, Pombo A (2005) The organization of transcription in the nucleus of mammalian cells. In: Diekmann PHaS (eds) Visions of the cell nucleus. ASP, CA, pp 95–105Google Scholar
  40. Haaf T, Ward DC (1996) Inhibition of RNA polymerase II transcription causes chromatin decondensation, loss of nucleolar structure, and dispersion of chromosomal domains. Exp Cell Res 224:163–173PubMedCrossRefGoogle Scholar
  41. Haaf T, Hayman DL, Schmid M (1991) Quantitative determination of rDNA transcription units in vertebrate cells. Exp Cell Res 193:78–86PubMedCrossRefGoogle Scholar
  42. Hadjiolov AA (1985) The nucleolus and ribosome biogenesis. Springer, Berlin Heidelberg New York, pp 1–268Google Scholar
  43. Hadjiolova KV, Hadjiolov A, Bachelerie J-P (1995) Actinomycin D stimulates the transcription of rRNA minigenes transfected into mouse cells. Applications for the in vivo hypersensitivity of rRNA gene transcription. Eur J Biochem 228:605–615PubMedCrossRefGoogle Scholar
  44. Heix J, Vente A, Voit R, Budde A, Michaelidis TM, Grummt I (1998) Mitotic silencing of human rRNA synthesis: inactivation of the promoter selectivity factor SL1 by cdc2/cyclin B-mediated phosphorylation. EMBO J 17:7373–7381PubMedCrossRefGoogle Scholar
  45. Hernandez-Verdun D (2004) Behavior of the nucleolus during mitosis. Kluwer Academic, Dordrecht, pp 41–57Google Scholar
  46. Hernandez-Verdun D, Junéra HR (1995) The nucleolus. In: Principles of medical biology, cellular organels, vol 2. Jai Press, Greenwich, pp 73–92Google Scholar
  47. Hozak P, Novak JT, Smetana K (1989) Three-dimensional reconstructions of nucleolus-organizing regions in PHA-stimulated human lymphocytes. Biol Cell 66:225–233PubMedCrossRefGoogle Scholar
  48. Hozàk P, Cook PR, Schöfer C, Mosgöller W, Wachtler F (1994) Site of transcription of ribosomal RNA and intranucleolar structure in HeLa cells. J Cell Sci 107:639–648PubMedGoogle Scholar
  49. Isaac C, Yang Y, Meier T (1998) Nopp140 functions as a molecular link between the nucleolus and the coiled bodies. J Cell Biol 142:319–329PubMedCrossRefGoogle Scholar
  50. Janicki SM, Spector DL (2003) Nuclear choreography: interpretations from living cells. Curr Opin Cell Biol 15:149–157PubMedCrossRefGoogle Scholar
  51. Jarrous N, Wolenski D, Wesolowski D, Lee C, Altman S (1999) Localization in the nucleolus and coiled bodies of protein subunits of the ribonucleoprotein ribonuclease P. J Cell Biol 146:559–571PubMedCrossRefGoogle Scholar
  52. Jiménez-Garcia LF, Segura-Valdez MdL, Ochs RL, Rothblum LI, Hannan R, Spector DL (1994) Nucleologenesis: U3 snRNA-containing prenucleolar bodies move to sites of active pre-rRNA transcription after mitosis. Mol Biol Cell 5:955–966PubMedGoogle Scholar
  53. Junéra HR, Masson C, Géraud G, Hernandez-Verdun D (1995) The three-dimensional organization of ribosomal genes and the architecture of the nucleoli vary with G1, S and G2 phases. J Cell Sci 108:3427–3441PubMedGoogle Scholar
  54. Junéra HR, Masson C, Géraud G, Suja J, Hernandez-Verdun D (1997) Involvement of in situ conformation of ribosomal genes and selective distribution of UBF in rRNA transcription. Mol Biol Cell 8:145–156PubMedGoogle Scholar
  55. Le Panse S, Masson C, Héliot L, Chassery J-M, Junéra HR, Hernandez-Verdun D (1999) 3-D organization of single ribosomal transcription units after DRB inhibition of RNA polymerase II transcription. J Cell Sci 112:2145–2154Google Scholar
  56. Lippincott-Schwartz J, Snapp E, Kenworthy A (2001) Studying protein dynamics in living cells. Nat Rev Mol Cell Biol 2:444–456PubMedCrossRefGoogle Scholar
  57. Louvet E, Junera HR, Le Panse S, Hernandez-Verdun D (2005) Dynamics and compartmentation of the nucleolar processing machinery. Exp Cell Res 304:457–470PubMedCrossRefGoogle Scholar
  58. Matera AG (1999) Nuclear bodies: multifaceted subdomains of the interchromatin space. Trends Cell Biol 9:302–309PubMedCrossRefGoogle Scholar
  59. Mélèse T, Xue Z (1995) The nucleolus: an organelle formed by the act of building a ribosome. Curr Opin Cell Biol 7:319–324PubMedCrossRefGoogle Scholar
  60. Misteli T (2001) Protein dynamics: implications for nuclear architecture and gene expression. Science 291:843–847PubMedCrossRefGoogle Scholar
  61. Ochs RL, Lischwe MA, Shen E, Caroll RE, Busch H (1985a) Nucleologenesis: composition and fate of prenucleolar bodies. Chromosoma 92:330–336PubMedCrossRefGoogle Scholar
  62. Ochs RL, Lischwe MA, Spohn WH, Busch H (1985b) Fibrillarin: a new protein of the nucleolus identified by autoimmune sera. Biol Cell 54:123–134PubMedGoogle Scholar
  63. Okuwaki M, Tsujimoto M, Nagata K (2002) The RNA binding activity of a ribosome biogenesis factor, nucleophosmin/B23, is modulated by phosphorylation with a cell cycle-dependent kinase and by association with its subtype. Mol Biol Cell 13:2016–2030PubMedCrossRefGoogle Scholar
  64. Olson MO, Dundr M (2005) The moving parts of the nucleolus. Histochem Cell Biol 123:203–216PubMedCrossRefGoogle Scholar
  65. Olson MOJ, Dundr M, Szebeni A (2000) The nucleolus: an old factory with unexpected capabilities. Trends Cell Biol 10:189–196PubMedCrossRefGoogle Scholar
  66. Pébusque MJ, Seïte (1981) Electron microscopic studies of silver-stained proteins in nucleolar organizer regions: location in nucleoli of rat sympathetic neurons during light and dark periods. J Cell Sci 51:85–94PubMedGoogle Scholar
  67. Pederson T (1998) The plurifunctional nucleolus. Nucleic Acids Res 26:3871–3876PubMedCrossRefGoogle Scholar
  68. Pena E, Berciano MT, Fernandez R, Ojeda JL, Lafarga M (2001) Neuronal body size correlates with the number of nucleoli and Cajal bodies, and with the organization of the splicing machinery in rat trigeminal ganglion neurons. J Comp Neurol 430:250–263PubMedCrossRefGoogle Scholar
  69. Phair RD, Misteli T (2000) High mobility of proteins in the mammalian cell nucleus. Nature 404:604–609PubMedCrossRefGoogle Scholar
  70. Pinol-Roma S (1999) Association of nonribosomal nucleolar proteins in ribonucleoprotein complexes during interphase and mitosis. Mol Biol Cell 10:77–90PubMedGoogle Scholar
  71. Platani M, Golberg I, Swedlow JR, Lamond AI (2000) In vivo analysis of Cajal body movement, separation, and joining in live human cells. J Cell Biol 151:1561–1574PubMedCrossRefGoogle Scholar
  72. Politz JC, Yarovoi S, Kilroy SM, Gowda K, Zwieb C, Pederson T (2000) Signal recognition particle components in the nucleolus. Proc Natl Acad Sci USA 97:55–60PubMedCrossRefGoogle Scholar
  73. Politz JC, Lewandowski LB, Pederson T (2002) Signal recognition particle RNA localization within the nucleolus differs from the classical sites of ribosome synthesis. J Cell Biol 159:411–418PubMedCrossRefGoogle Scholar
  74. Puvion-Dutilleul F, Bachellerie J-P, Puvion E (1991) Nucleolar organization of HeLa cells as studied by in situ hybridization. Chromosoma 100:395–409PubMedCrossRefGoogle Scholar
  75. Puvion-Dutilleul F, Puvion E, Bachellerie J-P (1997) Early stages of pre-rRNA formation within the nucleolar ultrastructure of mouse cells studied by in situ hybridization with 5′ETS leader probe. Chromosoma 105:496–505PubMedGoogle Scholar
  76. Roix J, Misteli T (2002) Genomes, proteomes, and dynamic networks in the cell nucleus. Histochem Cell Biol 118:105–116PubMedGoogle Scholar
  77. Roussel P, André C, Comai L, Hernandez-Verdun D (1996) The rDNA transcription machinery is assembled during mitosis in active NORs and absent in inactive NORs. J Cell Biol 133:235–246PubMedCrossRefGoogle Scholar
  78. Rubbi CP, Milner J (2003) Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J 22:6068–6077PubMedCrossRefGoogle Scholar
  79. Savino TM, Bastos R, Jansen E, Hernandez-Verdun D (1999) The nucleolar antigen Nop52, the human homologue of the yeast ribosomal RNA processing RRP1, is recruited at late stages of nucleologenesis. J Cell Sci 112:1889–1900PubMedGoogle Scholar
  80. Savino TM, Gébrane-Younès J, De Mey J, Sibarita J-B, Hernandez-Verdun D (2001) Nucleolar assembly of the rRNA processing machinery in living cells. J Cell Biol 153:1097–1110PubMedCrossRefGoogle Scholar
  81. Scheer U, Benavente R (1990) Functional and dynamic aspects of the mammalian nucleolus. Bioessays 12:14–21PubMedCrossRefGoogle Scholar
  82. Scheer U, Hock R (1999) Structure and function of the nucleolus. Curr Opin Cell Biol 11:385–390PubMedCrossRefGoogle Scholar
  83. Scheer U, Rose KM (1984) Localisation of RNA polymerase I in interphase cells and mitotic chromosomes by light and electron microscopic immunocytochemistry. Proc Natl Acad Sci USA 81:1431–1435PubMedCrossRefGoogle Scholar
  84. Scheer U, Thiry M, Goessens G (1993) Structure, function and assembly of the nucleolus. Trends Cell Biol 3:236–241PubMedCrossRefGoogle Scholar
  85. Schul W, de Jong L, van Driel R (1998) Nuclear neighbours: the spatial and functional organization of genes and nuclear domains. J Cell Biochem 70:159–171PubMedCrossRefGoogle Scholar
  86. Shav-Tal Y, Blechman J, Darzacq X, Montagna C, Dye BT, Patton JG, Singer RH, Zipori D (2005) Dynamic sorting of nuclear components into distinct nucleolar caps during transcriptional inhibition. Mol Biol Cell 16:2395–2413PubMedCrossRefGoogle Scholar
  87. Shaw PJ, Jordan EG (1995) The nucleolus. Annu Rev Cell Dev Biol 11:93–121PubMedCrossRefGoogle Scholar
  88. Sirri V, Roussel P, Hernandez-Verdun D (2000) In vivo release of mitotic silencing of ribosomal gene transcription does not give rise to precursor ribosomal RNA processing. J Cell Biol 148:259–270PubMedCrossRefGoogle Scholar
  89. Sirri V, Hernandez-Verdun D, Roussel P (2002) Cyclin-dependent kinases govern formation and maintenance of the nucleolus. J Cell Biol 156:969–981PubMedCrossRefGoogle Scholar
  90. Sleeman JE, Lamond AI (1999) Newly assembled snRNPs associated with coiled bodies before speckles, suggesting a nuclear snRNP maturation pathway. Curr Biol 9:1065–1074PubMedCrossRefGoogle Scholar
  91. Snaar S, Wiesmeijer K, Jochemsen AG, Tanke HJ, Dirks RW (2000) Mutational analysis of fibrillarin and its mobility in living human cells. J Cell Biol 151:653–662PubMedCrossRefGoogle Scholar
  92. Sollner-Webb B, Tycowski KT, Steitz JA (1996) Ribosomal RNA processing in eukaryotes. In: Ribosomal RNA: structure, evolution, processing, and function in protein biosynthesis. CRC Press, New York, pp 469–490Google Scholar
  93. Spector DL (2001) Nuclear domains. J Cell Sci 114:2891–2893PubMedGoogle Scholar
  94. Strouboulis J, Wolffe AP (1996) Functional compartmentalization of the nucleus. J Cell Sci 109:1991–2000PubMedGoogle Scholar
  95. Thiry M, Goessens G (1996) The nucleolus during the cell cycle. Springer, Berlin Heidelberg New York, p 146Google Scholar
  96. Thiry M, Lafontaine DL (2005) Birth of a nucleolus: the evolution of nucleolar compartments. Trends Cell Biol 15:194–199PubMedCrossRefGoogle Scholar
  97. Tollervey D (1996) Transacting factors in ribosome synthesis. Exp Cell Res 229:226–232PubMedCrossRefGoogle Scholar
  98. Tsai RY, McKay RD (2005) A multistep, GTP-driven mechanism controlling the dynamic cycling of nucleostemin. J Cell Biol 168:179–184PubMedCrossRefGoogle Scholar
  99. Verheggen C, Le Panse S, Almouzni G, Hernandez-Verdun D (1998) Presence of pre-rRNAs before activation of polymerase I transcription in the building process of nucleoli during early development of Xenopus laevis. J Cell Biol 142:1167–1180PubMedCrossRefGoogle Scholar
  100. Visitin R, Amon A (2000) The nucleolus: the magician’s hat for cell cycle tricks. Curr Opin Cell Biol 12:372–377CrossRefGoogle Scholar
  101. Weisenberger D, Scheer U (1995) A possible mechanism for the inhibition of ribosomal RNA gene transcription during mitosis. J Cell Biol 129:561–575PubMedCrossRefGoogle Scholar
  102. Zatsepina OV, Todorov IT, Philipova RN, Krachmarov CP, Trendelenburg MF, Jordan EG (1997) Cell cycle-dependent translocations of a major nucleolar phosphoprotein, B23, and some characteristics of its variants. Eur J Cell Biol 73:58–70PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Nuclei and Cell Cycle, Institut Jacques Monod, CNRSUniversité Paris VI et Paris VIIParis, Cedex 05France

Personalised recommendations