The giant fibrillar center: A nucleolar structure enriched in upstream binding factor (UBF) that appears in transcriptionally more active sensory ganglia neurons

Journal of Structural Biology

Volumn 159, Issue 3, 2007, Pages 451-461

  Casafont, Iñigo ^a   Bengoechea, Rocio ^a   Navascués, Joaquín ^b   Pena, Emma ^a   Berciano, Maria T ^a   Lafarga, Miguel ^a  

^a CSIC   (Spain)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

5 Fluorouridine transcription assay; Cajal bodies; Giant fibrillar centers; Neuronal differentiation; Nucleolus; Sensory ganglia neurons; SUMO 1; UBF; Ubiquitin proteasome system

Indexed keywords

5' FLUOROURIDINE; DNA DIRECTED RNA POLYMERASE; DNA TOPOISOMERASE; FLUOROURIDINE; PROTEASOME; PROTEIN UBC9; SUMO 1 PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG; UPSTREAM BINDING FACTOR; UPSTREAM STIMULATORY FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELLULAR DISTRIBUTION; CONJUGATION; CONTROLLED STUDY; DENSITY; ELECTRON; FIBER; GENETIC TRANSCRIPTION; IMMUNOCYTOCHEMISTRY; MALE; NERVE CELL; NERVE CELL GROWTH; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN DOMAIN; RAT; RNA SYNTHESIS; SENSORY GANGLION;

ANIMALS; CELL DIFFERENTIATION; CELL NUCLEOLUS; GANGLIA, SENSORY; MALE; MICROSCOPY, IMMUNOELECTRON; NEURONS, AFFERENT; POL1 TRANSCRIPTION INITIATION COMPLEX PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; RATS; RATS, SPRAGUE-DAWLEY; RNA, RIBOSOMAL; SUMO-1 PROTEIN; TRANSCRIPTION, GENETIC; UBIQUITIN;

RATTUS;

EID: 34548359167     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2007.05.004     Document Type: Article

References (57)

1. Andersen J.S., Lam Y.W., Leung A.K.L., Ong S.E., Lyon C.E., Lamond A.I., and Mann M. Nucleolar proteasome dynamics. Nature 433 (2005) 77-83
2. Berciano, M.T., Novell, M., Villagra, N.T., Casafont, I., Bengoechea, R., Val-Bernal, J.F., Lafarga, M., in press. Cajal body number and nucleolar size correlate with the cell body mass in human sensory ganglia neurons, J. Struct. Biol. 158, 410-420.
3. Biggiogera M., Fakn S., Kaufmann S.H., Black A., Shaper J.H., and Busch H. Simultaneous immunoelectron microscopy visualization of proteinB23 and C23 ditribution in HeLa cell nucleolus. J. Histochem. Cytochem. 37 (1989) 1371-1374
4. Bohmann K., Ferreira J., and Lamond A.I. Mutational analysis of p80 coilin indicates a functional interaction between coiled bodies and the nucleolus. J. Cell Biol. 131 (1995) 817-831
5. Casafont I., Navascués J., Pena E., Lafarga M., and Berciano M.T. Nuclear organization and dynamics of transcription sites in rat sensory ganglia neurons detected by incorporation of 5′-fluorouridine into nascent RNA. Neuroscience 140 (2006) 453-462
6. Christensen M.O., Barthelmes H.U., Boege F., and Mielke C. The N-terminal domain anchors human topoisomerase I at fibrillar centers of nucleoli and nucleolar organizer region of miotic chromosomes. J. Biol. Chem. 277 (2002) 35932-35938
7. Derenzini M., Pasquinelli G., O'Donohue M., Ploton D., and Thiry M. Structural and functional organization of ribosomal genes within the mammalian cell nucleus. J. Histochem. Cytochem. 54 (2006) 131-145
8. Desterro J.M., Thomson J., and Hay R.T. Ubc9 conjugates SUMO but not ubiquitin. FEBS Lett. 417 (1997) 297-300
9. Desterro J.M., Keegan L.P., Jaffray E., Hay R.T., O'Connell M.A., and Carmo-Fonseca M. SUMO-1 modification alters ADAR1 editing activity. Mol. Biol. Cell 11 (2005) 5115-5126
10. Fields R.D. Volume transmission in activity-dependent regulation of myelinating glia. Neurochem. Int. 45 (2004) 503-509
11. Fulton B.P. Postnatal changes in conduction velocity and soma action potential parameters of rat dorsal root ganglion neurones. Neurosci. Lett. 73 (1987) 125-130
12. Gébrane-Younès J., Sirri V., Junéra H.R., Roussel P., and Hernandez-Verdun D. The nucleolus: an essential nuclear domain. In: Hemmerich P., and Diekmann S. (Eds). Vision of the Cell Nucleus (2005), Am. Sci. Publishers, Stevenson Ranch 120-135
13. Gong L., and Yeh E.T. Characterization of a family of nucleolar SUMO-specific proteases with preference for SUMO-2 or SUMO-3. J. Biol. Chem. 23 (2006) 15869-15877
14. Hay R.T. SUMO: a history of modification. Mol. Cell 18 (2005) 1-12
15. Hernandez-Verdun D. Nucleolus: from structure to dynamics. J. Histochem. Cell Biol. 125 (2006) 127-137
16. Harper A.A., and Lawson S.N. Electrical properties of rat dorsal root ganglion neurones with different peripheral nerve conduction velocities. J. Physiol. 359 (1985) 47-63
17. Hunt S.P., Mantyh P.W., and Priestley J.V. The organization of biochemically characterized sensory neurons. In: Scott S.A. (Ed). Sensory Neurons. Diversity, Development and Plasticity (1992), Oxford University Press, New York 60-76
18. Jordan P., Mannervik M., Tora L., and Carmo-Fonseca M. In vivo evidence that TATA-binding protein/SL1 colocalizes with UBF and RNA polymerase I when rRNA synthesis is either active or inactive. J. Cell Biol. 133 (1996) 225-234
19. Junera H.R., Masson C., Geraud G., Suja J., and Hernandez-Verdun D. Involvement of in situ conformation of ribosomal genes and selective distribution of upstream binding factor in rRNA transcription. Mol. Biol. Cell 1 (1997) 145-156
20. Koberna K., Malinsky K., Pliss A., Masata A., Vecerova M., Fialova M., Bednar J., and Raska I. Ribosomal genes in focus: new transcripts label the dense fibrillar components and form clusters indicative of "Christmas trees" in situ. J. Cell Biol. 157 (2002) 743-748
21. Lafarga M., Berciano M.T., Hervás J.P., and Villegas J. Nucleolar organization in granule cell neurons of the rat cerebellum. J. Neurocytol. 18 (1989) 19-26
22. Lafarga M., Andres M.A., Berciano M.T., and Maquiera E. Organization of nucleoli and nuclear bodies in osmotically stimulated supraoptic neurons of the rat. J. Comp. Neurol. 308 (1991) 329-339
23. Lafarga M., Berciano M.T., Pena E., Mayo I., Castaño J.G., Bohmann D., Rodrigues J.P., Tavanez J.P., and Carmo-Fonseca M. Clastosome: A subtype of nuclear body enriched in 19S and 20S proteasomes, ubiquitin, and protein substrates of proteasome. Mol. Biol. Cell 13 (2002) 2771-2782
24. Lam Y.W., Trinkle-Mulcahy L., and Lamond A.I. The nucleolus. J. Cell Sci. 118 (2005) 1335-1337
25. Lawson S.N. The postnatal development of large light and small dark neurons in mouse dorsal root ganglia: a statistical analysis of cell numbers and size. J. Neurocytol. 8 (1979) 275-294
26. Leppard J.B., and Champoux J.J. Human DNA topoisomerase I: relaxation, roles and damage control. Chromosoma 114 (2005) 75-85
27. Mais C., Wright J.E., Prieto J.L., Raggett S.L., and McStay B. UBF-binding site arrays form pseudo-NORs and sequester the RNA polymerase I transcription machinery. Genes Dev. 19 (2005) 50-64
28. McIlwain D.L. Nuclear and cell body size in spinal motor neurons. In: Rowland L.P. (Ed). Advances in Neurology. Amyotrophic Lateral Sclerosis and other Motor Neuron Diseases vol. 56 (1991), Raven press, New York 67-74
29. Meckhail K., Khacho M., Carrigan A., Hache R.R.J., Gunaratnam L., and Lee S. Regulation of ubiquitin ligase dynamics by the nucleolus. J. Cell Biol. 170 (2005) 733-744
30. Mengual E., Arizti P., Rodrigo J., Gimenez-Amaya J.M., and Castaño J.G. Immunohistochemical distribution and electron microscopic subcellular localization of the protasome in the rat CNS. J. Neurosci. 16 (1996) 6331-6341
31. Mirsky R., and Jessen K.R. Schwann cell development, differentiation and myelination. Curr. Opin. Neurobiol. 6 (1996) 89-96
32. Navascues J., Casafont I., Villagra N.T., Lafarga M., and Berciano M.T. Reorganization of nuclear compartments of type A neurons of trigeminal ganglia in response to inflammatory injury of peripheral nerve endings. J. Neurocytol. 33 (2004) 393-405
33. Olson M.O., and Dundr M. The moving parts of the nucleolus. Histochem. Cell Biol. 123 (2005) 203-216
34. O'Sullivan A.C., Sullivan G.J., and McStay B. UBF binding in vivo is not restricted to regulatory sequences within the vertebrate ribosomal DNA repeat. Mol. Cell Biol. 2 (2002) 657-668
35. Pannese, E., 1994. Neurocytology. Fine structure of Neurons, Nerve Processes, and Neuroglial Cells. Stuttgart, Georg Thieme Verlag.
36. Pébusque M.J., and Seïte R. 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 (1981) 85-94
37. Pébusque M.J., and Seïte R. Evidence of a circadian rhythm in nucleolar components of rat superior cervical ganglion neurons with particular reference to the fibrillar centers: An ultrastuctural and stereological analysis. J. Ultrastruct. Res. 77 (1981) 83-92
38. Pébusque M.J., Vio-Cigna M., Aldebert B., and Seite R. Circadian rhythm of nucleoli in rat superior cervical ganglion neurons: the two types of fibrillar centres and their quantitative relationship with the nucleolar organizing regions. J. Cell Sci. 74 (1985) 65-74
39. Pederson T. The plurifunctional nucleolus. Nucleic Acids Res. 26 (1998) 3871-3876
40. Pena E., Berciano M.T., Fernandez R., Ojeda J.L., and Lafarga M. 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 (2001) 250-263
41. Puvion-Dutilleul F., Mazan S., Nicoloso M., Pichard E., Bachellerie J.P., and Puvion E. Alterations of nucleolar ultrastructure and ribosome biogenesis by actinomycin D. Implications for U3 snRNP function. Eur. J. Cell Biol. 58 (1992) 149-162
42. Rambourg A., Clemont Y., and Beaudet A. Ultrastructural features of six types of neurons in rat dorsal root ganglia. J. Neurocytol. 12 (1983) 47-66
43. Raska I., Ochs R.L., and Michel L.S. Immunocytochemistry of the cell nucleus. Electr. Microsc. Rev. 3 (1990) 301-353
44. Raska I., Koberna K., Malinsky J., Fidlerova H., and Masata M. The nucleolus and transcription of ribosomal genes. Biol. Cell 96 (2004) 579-594
45. Raska I., Shaw P.J., and Cmarko D. New insights into nucleolar architecture and activity. Int. Rev. Cytol. 255 (2006) 177-235
46. Reimer G., Rose K., Scheer U., and Tan E.M. Autoantibody to RNA polymerase I in scleroderma sera. J. Clin. Invest. 79 (1987) 65-72
47. Roussel P., Andre C., Masson C., Geraud G., and Hernandez-Verdun D. Localization of the RNA polymerase I transcription factor hUBF during the cell cycle. J. Cell Sci. 2 (1993) 327-337
48. Sato S., Burgess S.B., and McIlwain D.L. Transcription and motoneuron size. J. Neurochem. 63 (1994) 1609-1615
49. Scheer U., and Rose K.M. Localization of RNA polymerase I in intrephase cells and mitotic chromosomes by light and electron mroscopy immunocytochemistry. Proc. Natl. Acad. Sci. USA 38 (1984) 1431-1435
50. Scherl A., Couté Y., Déon C., Callé A., Kindbeiter K., Sanchez J.C., Greco A., Hochstrasser D., and Diaz J.J. Functional proteomic analysis of human nucleolus. Mol. Biol. Cell. 13 (2002) 4100-4109
51. Schmidt E.E., and Schibler U. Cell size regulation, a mechanism that controls cellular RNA accumulation: consequences on regulation of the ubiquitous transcription factors Oct1 and NF-Y, and the liver-enriched transcription factor DBP. J. Cell. Biol. 128 (1995) 467-483
52. Schwarzacher H.G., and Wachtler F. The nucleolus. Anat. Embryol. 188 (1993) 515-536
53. Sobell H.M. Actinomycin and DNA transcription. Proc. Natl. Acad. Sci. USA 82 (1985) 1417-1421
54. Stavreva D.A., Kawasaki M., Dundr M., Koberna K., Muller W.G., Tsujimura-Takahashi T., Komatsu W., Hayano T., Isobe T., Raska I., Misteli T., Takahashi N., and McNally J.G. Potencial roles for ubiquitin and the proteasome during ribosome biogenesis. Mol. Cell Biol. 13 (2006) 5131-5145
55. Stefanovsky V., Langlois F., Gagnon-Kluger T., Rothblum L.I., and Moss T. Growth factor signaling regulates elongation of RNA polymerase I transcription in mammals via UBF phosphorylation and r-chromatin remodeling. Mol. Cell 21 (2006) 629-639
56. Teixeira M.T., Forstemann K., Gasser S.M., and Lingner J. Intracellular trafficking of yeast telomerase components. EMBO Rep. 3 (2002) 652-659
57. Wotherspoon G., and Priestly J.V. Expression of the 5-HT1B receptor by subtypes of rat trigeminal ganglion cells. Neuroscience 95 (1999) 465-471