Post-mitotic dynamics of pre-nucleolar bodies is driven by pre-rRNA processing

Journal of Cell Science

Volumn 125, Issue 19, 2012, Pages 4532-4542

  Carron, Coralie ^a,b   Balor, Stéphanie ^a,b   Delavoie, Franck ^a,b   Plisson Chastang, Célia ^a,b   Faubladier, Marlene ^a,b   Gleizes, Pierre Emmanuel ^a,b   ODonohue, Marie Francoise ^a,b  

^a UNIVERSITÉ PAUL SABATIER   (France)

^b CNRS   (France)

Author keywords

Homo sapiens; Mitosis; Pre nucleolar bodies; Pre ribosomal RNA processing; Ribosome biogenesis

Indexed keywords

RIBOSOME PROTEIN; RNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; CELL CYCLE G1 PHASE; CELL SIZE; CONTROLLED STUDY; ELECTRON TOMOGRAPHY; FLUORESCENCE IN SITU HYBRIDIZATION; HUMAN; HUMAN CELL; LOSS OF FUNCTION MUTATION; MITOSIS; NUCLEOLUS; NUCLEOTIDE SEQUENCE; PRE NUCLEOLAR BODY; PRIORITY JOURNAL; PROMETAPHASE; PROTEIN DOMAIN; PROTEIN EXPRESSION; RIBOSOME; RNA ANALYSIS; RNA PROCESSING; RNA STRUCTURE; TELOPHASE;

CELL NUCLEOLUS; ELECTRON MICROSCOPE TOMOGRAPHY; G1 PHASE; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HUMANS; MITOSIS; MODELS, BIOLOGICAL; RIBOSOMAL PROTEINS; RNA PRECURSORS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, SMALL INTERFERING; RNA, SMALL NUCLEOLAR;

HOMO SAPIENS;

EID: 84872181749     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.106419     Document Type: Article

References (53)

1. Angelier, N., Tramier, M., Louvet, E., Coppey-Moisan, M., Savino, T. M., De Mey, J. R. and Hernandez-Verdun, D. (2005). Tracking the interactions of rRNA processing proteins during nucleolar assembly in living cells. Mol. Biol. Cell 16, 2862-2871.
2. Azum-Gelade, M. C., Noaillac-Depeyre, J., Caizergues-Ferrer, M. and 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, 463-475.
3. Ben-Shem, A., Jenner, L., Yusupova, G. and Yusupov, M. (2010). Crystal structure of the eukaryotic ribosome. Science 330, 1203-1209.
4. Beven, A. F., Lee, R., Razaz, M., Leader, D. J., Brown, J. W. and Shaw, P. J. (1996). The organization of ribosomal RNA processing correlates with the distribution of nucleolar snRNAs. J. Cell Sci. 109, 1241-1251.
5. Borovjagin, A. V. and Gerbi, S. A. (2005). An evolutionary intra-molecular shift in the preferred U3 snoRNA binding site on pre-ribosomal RNA. Nucleic Acids Res. 33, 4995-5005.
6. Boulon, S., Westman, B. J., Hutten, S., Boisvert, F. M. and Lamond, A. I. (2010). The nucleolus under stress. Mol. Cell 40, 216-227.
7. Chan, E. K., 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. Chen, D., Dundr, M., Wang, C., Leung, A., Lamond, A., Misteli, T. and Huang, S. (2004). Condensed mitotic chromatin is accessible to transcription factors and chromatin structural proteins. J. Cell Biol. 168, 41-54.
9. DiMario, P. J. (2004). Cell and molecular biology of nucleolar assembly and disassembly. Int. Rev. Cytol. 239, 99-178.
10. Dousset, T., Wang, C., Verheggen, C., Chen, D., Hernandez-Verdun, D. and Huang, S. (2000). Initiation of nucleolar assembly is independent of RNA polymerase I transcription. Mol. Biol. Cell 11, 2705-2717.
11. Dundr, M. and Olson, M. O. (1998). Partially processed pre-rRNA is preserved in association with processing components in nucleolus-derived foci during mitosis. Mol. Biol. Cell 9, 2407-2422.
12. Dundr, M., Misteli, T. and Olson, M. O. (2000). The dynamics of postmitotic reassembly of the nucleolus. J. Cell Biol. 150, 433-446.
13. Eichler, D. C. and Craig, N. (1994). Processing of eukaryotic ribosomal RNA. Prog. Nucleic Acid Res. Mol. Biol. 49, 197-239.
14. Ellis, S. R. and Gleizes, P. E. (2011). Diamond Blackfan anemia: ribosomal proteins going rogue. Semin. Hematol. 48, 89-96.
15. Fan, H. and Penman, S. (1971). Regulation of synthesis and processing of nucleolar components in metaphase-arrested cells. J. Mol. Biol. 59, 27-42.
16. Fatica, A. and Tollervey, D. (2002). Making ribosomes. Curr. Opin. Cell Biol. 14, 313-318.
17. Fomproix, N. and Hernandez-Verdun, D. (1999). Effects of anti-PM-Scl 100 (Rrp6p exonuclease) antibodies on prenucleolar body dynamics at the end of mitosis. Exp. Cell Res. 251, 452-464.
18. Gebrane-Youne's, J., Fomproix, N. and Hernandez-Verdun, D. (1997). When rDNA transcription is arrested during mitosis, UBF is still associated with non-condensed rDNA. J. Cell Sci. 110, 2429-2440.
19. Hadjiolov, A. A. (1985). The nucleolus and ribosome biogenesis. In Cell Biology Monographs, Vol. 12 (ed. M. Alfert, W. Beermann, L. Goldstein, K. R. Porter and P. Sitte), 268 pp. Wien, Austria: Springer-Verlag.
20. Heix, J., Vente, A., Voit, R., Budde, A., Michaelidis, T. M. and 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, 7373-7381.
21. Henras, A. K., Soudet, J., Gerus, M., Lebaron, S., Caizergues-Ferrer, M., Mougin, A. and Henry, Y. (2008). The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell. Mol. Life Sci. 65, 2334-2359.
22. Jimenez-Garcia, L. F., Segura-Valdez, M. L., Ochs, R. L., Rothblum, L. I., Hannan, R. and Spector, D. L. (1994). Nucleologenesis: U3 snRNA-containing prenucleolar bodies move to sites of active pre-rRNA transcription after mitosis. Mol. Biol. Cell 5, 955-966.
23. Kremer, J. R., Mastronarde, D. N. and McIntosh, J. R. (1996). Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71-76.
24. Kressler, D., Hurt, E. and Bassler, J. (2010). Driving ribosome assembly. Biochim. Biophys. Acta 1803, 673-683.
25. Lamanna, A. C. and Karbstein, K. (2009). Nob1 binds the single-stranded cleavage site D at the 39-end of 18S rRNA with its PIN domain. Proc. Natl. Acad. Sci. USA 106, 14259-14264.
26. Lapik, Y. R., Fernandes, C. J., Lau, L. F. and Pestov, D. G. (2004). Physical and functional interaction between Pes1 and Bop1 in mammalian ribosome biogenesis. Mol. Cell 15, 17-29.
27. Leung, A. K., Gerlich, D., Miller, G., Lyon, C., Lam, Y. W., Lleres, D., Daigle, N., Zomerdijk, J., Ellenberg, J. and Lamond, A. I. (2004). Quantitative kinetic analysis of nucleolar breakdown and reassembly during mitosis in live human cells. J. Cell Biol. 166, 787-800.
28. Lindstrom,M. S. (2011). NPM1/B23: A multifunctional chaperone in ribosome biogenesis and chromatin remodeling. Biochem. Res. Int. 2011, doi:10.1155/2011/195209.
29. Louvet, E., Junera, H. R., Le Panse, S. and Hernandez-Verdun, D. (2005). Dynamics and compartmentation of the nucleolar processing machinery. Exp. Cell Res. 304, 457-470.
30. Mao, Y. S., Sunwoo, H., Zhang, B. and Spector, D. L. (2011). Direct visualization of the co-transcriptional assembly of a nuclear body by noncoding RNAs. Nat. Cell Biol. 13, 95-101.
31. Miyake, K., Utsugisawa, T., Flygare, J., Kiefer, T., Hamaguchi, I., Richter, J. and Karlsson, S. (2008). Ribosomal protein S19 deficiency leads to reduced proliferation and increased apoptosis but does not affect terminal erythroid differentiation in a cell line model of Diamond-Blackfan anemia. Stem Cells 26, 323-329.
32. Muro, E., Gebrane-Younis, J., Jobart-Malfait, A., Louvet, E., Roussel, P. and Hernandez-Verdun, D. (2010). The traffic of proteins between nucleolar organizer regions and prenucleolar bodies governs the assembly of the nucleolus at exit of mitosis. Nucleus 1, 202-211.
33. O'Donohue, M. F., Choesmel, V., Faubladier, M., Fichant, G. and Gleizes, P. E. (2010). Functional dichotomy of ribosomal proteins during the synthesis of mammalian 40S ribosomal subunits. J. Cell Biol. 190, 853-866.
34. Oakes, M., Aris, J. P., Brockenbrough, J. S., Wai, H., Vu, L. and Nomura, M. (1998). Mutational analysis of the structure and localization of the nucleolus in the yeast Saccharomyces cerevisiae. J. Cell Biol. 143, 23-34.
35. Perez-Fernandez, J., Roman, A., De Las Rivas, J., Bustelo, X. R. and Dosil, M. (2007). The 90S preribosome is a multimodular structure that is assembled through a hierarchical mechanism. Mol. Cell. Biol. 27, 5414-5429.
36. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C. and Ferrin, T. E. (2004). UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612.
37. Pinol-Roma, S. (1999). Association of nonribosomal nucleolar proteins in ribonucleoprotein complexes during interphase and mitosis. Mol. Biol. Cell 10, 77-90.
38. Pintilie, G. D., Zhang, J., Goddard, T. D., Chiu, W. and Gossard, D. C. (2010). Quantitative analysis of cryo-EM density map segmentation by watershed and scalespace filtering, and fitting of structures by alignment to regions. J. Struct. Biol. 170, 427-438.
39. Rouquette, J., Choesmel, V. and Gleizes, P. E. (2005). Nuclear export and cytoplasmic processing of precursors to the 40S ribosomal subunits in mammalian cells. EMBO J. 24, 2862-2872.
40. Roussel, P., Andre, C., Masson, C., Geraud, G. and Hernandez-Verdun, D. (1993). Localization of the RNA polymerase I transcription factor hUBF during the cell cycle. J. Cell Sci. 104, 327-337.
41. Roussel, P., Andre, 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.
42. Salic, A. and Mitchison, T. J. (2008). A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc. Natl. Acad. Sci. USA 105, 2415-2420.
43. Savino, T. M., Bastos, R., Jansen, E. and 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, 1889-1900.
44. Savino, T. M., Gebrane-Younes, J., De Mey, J., Sibarita, J. B. and Hernandez-Verdun, D. (2001). Nucleolar assembly of the rRNA processing machinery in living cells. J. Cell Biol. 153, 1097-1110.
45. Shevtsov, S. P. and Dundr, M. (2011). Nucleation of nuclear bodies by RNA. Nat. Cell Biol. 13, 167-173.
46. Sirri, V., Roussel, P. and Hernandez-Verdun, D. (1999). The mitotically phosphorylated form of the transcription termination factor TTF-1 is associated with the repressed rDNA transcription machinery. J. Cell Sci. 112, 3259-3268.
47. Srivastava, L., Lapik, Y. R., Wang, M. and Pestov, D. G. (2010). Mammalian DEAD box protein Ddx51 acts in 39 end maturation of 28S rRNA by promoting the release of U8 snoRNA. Mol. Cell. Biol. 30, 2947-2956.
48. Thomson, E. and Tollervey, D. (2010). The final step in 5.8S rRNA processing is cytoplasmic in Saccharomyces cerevisiae. Mol. Cell. Biol. 30, 976-984.
49. Trumtel, S., Leger-Silvestre, I., Gleizes, P. E., Teulieres, F. and Gas, N. (2000). Assembly and functional organization of the nucleolus: ultrastructural analysis of Saccharomyces cerevisiae mutants. Mol. Biol. Cell 11, 2175-2189.
50. van Heel, M., Harauz, G., Orlova, E. V., Schmidt, R. and Schatz, M. (1996). A new generation of the IMAGIC image processing system. J. Struct. Biol. 116, 17-24.
51. Wild, T., Horvath, P., Wyler, E., Widmann, B., Badertscher, L., Zemp, I., Kozak, K., Csucs, G., Lund, E. and Kutay, U. (2010). A protein inventory of human ribosome biogenesis reveals an essential function of exportin 5 in 60S subunit export. PLoS Biol. 8, e1000522.
52. 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.
53. Zemp, I., Wild, T., ODonohue, M. F., Wandrey, F., Widmann, B., Gleizes, P. E. and Kutay, U. (2009). Distinct cytoplasmic maturation steps of 40S ribosomal subunit precursors require hRio2. J. Cell Biol. 185, 1167-1180.