The traffic of proteins between nucleolar organizer regions and prenucleolar bodies governs the assembly of the nucleolus at exit of mitosis

Nucleus

Volumn 1, Issue 2, 2010, Pages

  Muro, Eleonora ^a,b   Gébrane Younès, Jeannine ^a,c   Jobart Malfait, Aude ^a   Louvet, Emilie ^a   Roussel, Pascal ^a   Hernandez Verdun, Danièle ^a  

^a INSTITUT JACQUES MONOD   (France)

^b Centre National de la Recherche Scientifique   (France)

^c SORBONNE UNIVERSITÉ   (France)

Author keywords

Cajal body; Cell cycle; CRM1; EM structure; Living cell; Nucleolus; Photoactivation; PNBs; Traffic

Indexed keywords

FIBRILLARIN; RIBOSOME DNA;

ARTICLE; BIOGENESIS; CELL COMPARTMENTALIZATION; CELL CYCLE G1 PHASE; CHROMOSOME NOR; COILED BODY; DNA TRANSCRIPTION; ELECTRON MICROSCOPY; FEMALE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INTERPHASE; MITOSIS; NUCLEOLUS; PHOTOACTIVATION; PROTEIN INTERACTION; RIBOSOME; TELOPHASE;

EID: 77957052031     PISSN: 19491034     EISSN: 19491042     Source Type: Journal    
DOI: 10.4161/nucl.11334     Document Type: Article

References (60)

1. Spector DL. Nuclear domains. J Cell Sci 2001; 114:2891-3.
2. Prasanth KV, Sacco-Bubulya PA, Prasanth SG, Spector DL. Sequential entry of components of the gene expression machinery into daughter nuclei. Mol Biol Cell 2003; 14:1043-57.
3. Bubulya PA, Prasanth KV, Deerinck TJ, Gerlich D, Beaudouin J, Ellisman MH, et al. Hypophosphorylated SR splicing factors transiently localize around active nucleolar organizing regions in telophase daughter nuclei. J Cell Biol 2004; 167:51-63.
4. Hernandez-Verdun D. The nucleolus: a model for the organization of nuclear functions. Histochem Cell Biol 2006; 126:135-48.
5. Gébrane-Younès J, Sirri V, Junéra HR, Roussel P, Hernandez-Verdun D. Nucleolus: An essential nuclear domain. In: Diekmann. PHaS, ed. Visions of the cell nucleus: ASP CA 2005; 120-35.
6. Raska I, Shaw PJ, Cmarko D. New insights into nucleolar architecture and activity. Int Rev Cytol 2006; 255:177-235.
7. Sirri V, Urcuqui-Inchima S, Roussel P, Hernandez- Verdun D. Nucleolus: the fascinating nuclear body. Histochem Cell Biol 2008; 129:13-31.
8. Boisvert FM, van Koningsbruggen S, Navascues J, Lamond AI. The multifunctional nucleolus. Nat Rev Mol Cell Biol 2007; 8:574-85.
9. Emmott E, Hiscox JA. Nucleolar targeting: the hub of the matter. EMBO Rep 2009; 10:231-8.
10. Hiscox JA. RNA viruses: hijacking the dynamic nucleolus. Nat Rev Microbiol 2007; 5:119-27.
11. Pederson T, Tsai RY. In search of nonribosomal nucleolar protein function and regulation. J Cell Biol 2009; 184:771-6.
12. Jimenez-Garcia LF, Segura-Valdez ML, Ochs RL, Rothblum LI, Hannan R, Spector DL. Nucleologenesis: U3 snRNA-containing prenucleolar bodies move to sites of active pre-rRNA transcription after mitosis. Mol Biol Cell 1994; 5:955-66.
13. Dundr M, Misteli T, Olson MO. The dynamics of postmitotic reassembly of the nucleolus. J Cell Biol 2000; 150:433-46.
14. Savino TM, Gebrane-Younes J, De Mey J, Sibarita JB, Hernandez-Verdun D. Nucleolar assembly of the rRNA processing machinery in living cells. J Cell Biol 2001; 153:1097-110.
15. Sirri V, Hernandez-Verdun D, Roussel P. Cyclindependent kinases govern formation and maintenance of the nucleolus. J Cell Biol 2002; 156:969-81.
16. Angelier N, Tramier M, Louvet E, Coppey-Moisan M, Savino TM, De Mey JR, et al. Tracking the Interactions of rRNA Processing Proteins during Nucleolar Assembly in Living Cells. Mol Biol Cell 2005; 16:2862-71.
17. Dimario PJ. Cell and molecular biology of nucleolar assembly and disassembly. Int Rev Cytol 2004; 239:99-178.
18. Phair RD, Misteli T. High mobility of proteins in the mammalian cell nucleus. Nature 2000; 404:604-9.
19. Carmo-Fonseca M, Platani M, Swedlow JR. Macromolecular mobility inside the cell nucleus. Trends Cell Biol 2002; 12:491-5.
20. Janicki SM, Spector DL. Nuclear choreography: interpretations from living cells. Curr Opin Cell Biol 2003; 15:149-57.
21. Dundr M, Hebert MD, Karpova TS, Stanek D, Xu H, Shpargel KB, et al. In vivo kinetics of Cajal body components. J Cell Biol 2004; 164:831-42.
22. Leung AK, Gerlich D, Miller G, Lyon C, Lam YW, Lleres D, et al. Quantitative kinetic analysis of nucleolar breakdown and reassembly during mitosis in live human cells. J Cell Biol 2004; 166:787-800.
23. Sleeman JE, Trinkle-Mulcahy L, Prescott AR, Ogg SC, Lamond AI. Cajal body proteins SMN and Coilin show differential dynamic behaviour in vivo. J Cell Sci 2003; 116:2039-50.
24. Trinkle-Mulcahy L, Sleeman JE, Lamond AI. Dynamic targeting of protein phosphatase 1 within the nuclei of living mammalian cells. J Cell Sci 2001; 114:4219-28.
25. Patterson GH, Lippincott-Schwartz J. A photoactivatable GFP for selective photolabeling of proteins and cells. Science 2002; 297:1873-7.
26. Fornerod M, Ohno M, Yoshida M, Mattaj IW. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 1997; 90:1051-60.
27. Boulon S, Verheggen C, Jady BE, Girard C, Pescia C, Paul C, et al. PHAX and CRM1 are required sequentially to transport U3 snoRNA to nucleoli. Mol Cell 2004; 16:777-87.
28. Sleeman J. A regulatory role for CRM1 in the multidirectional trafficking of splicing snRNPs in the mammalian nucleus. J Cell Sci 2007; 120:1540-50.
29. Dousset T, Wang C, Verheggen C, Chen D, Hernandez- Verdun D, Huang S. Initiation of nucleolar assembly is independent of RNA polmerase I transcription. Mol Biol Cell 2000; 11:2705-17.
30. Hernandez-Verdun D. Nucleolus: from structure to dynamics. Histochem Cell Biol 2006; 125:127-37.
31. Fomproix N, Gebrane-Younes J, Hernandez-Verdun D. Effects of anti-fibrillarin antibodies on building of functional nucleoli at the end of mitosis. J Cell Sci 1998; 111:359-72.
32. Roussel P, Andre C, Comai L, Hernandez-Verdun D. The rDNA transcription machinery is assembled during mitosis in active NORs and absent in inactive NORs. J Cell Biol 1996; 133:235-46.
33. Gébrane-Younès J, Fomproix N, Hernandez-Verdun D.When rDNA transcription is arrested during mitosis, UBF is still associated with non-condensed rDNA. J Cell Sci 1997; 110:2429-40.
34. Davis FM, Tsao TY, Fowler SK, Rao PN. Monoclonal antibodies to mitotic cells. Proc Natl Acad Sci USA 1983; 80:2926-30.
35. Skoufias DA, Indorato RL, Lacroix F, Panopoulos A, Margolis RL. Mitosis persists in the absence of Cdk1 activity when proteolysis or protein phosphatase activity is suppressed. J Cell Biol 2007; 179:671-85.
36. Clute P, Pines J. Temporal and spatial control of cyclin B1 destruction in metaphase. Nat Cell Biol 1999; 1:82-7.
37. Okuwaki M, Tsujimoto M, Nagata K. 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 2002; 13:2016-30.
38. Negi SS, Olson MO. Effects of interphase and mitotic phosphorylation on the mobility and location of nucleolar protein B23. J Cell Sci 2006; 119:3676-85.
39. Carvalho T, Almeida F, Calapez A, Lafarga M, Berciano MT, Carmo-Fonseca M. The spinal muscular atrophy disease gene product, SMN: A link between snRNP biogenesis and the Cajal (coiled) body. J Cell Biol 1999; 147:715-28.
40. Sleeman JE, Ajuh P, Lamond AI. snRNP protein expression enhances the formation of Cajal bodies containing p80-coilin and SMN. J Cell Sci 2001; 114:4407-19.
41. Hutten S, Kehlenbach RH. CRM1-mediated nuclear export: to the pore and beyond. Trends Cell Biol 2007; 17:193-201.
42. Ospina JK, Gonsalvez GB, Bednenko J, Darzynkiewicz E, Gerace L, Matera AG. Cross-talk between snurportin1 subdomains. Mol Biol Cell 2005; 16:4660-71.
43. Knauer SK, Bier C, Habtemichael N, Stauber RH. The Survivin-Crm1 interaction is essential for chromosome passenger complex localization and function. EMBO rep 2006; 7:1259-65.
44. Schneider DA, Michel A, Sikes ML, Vu L, Dodd JA, Salgia S, et al. Transcription elongation by RNA polymerase I is linked to efficient rRNA processing and ribosome assembly. Mol Cell 2007; 26:217-29.
45. Hadjiolov AA. The nucleolus and ribosome biogenesis. Wien, New-York: Springer-Verlag 1985.
46. Puvion-Dutilleul F, Puvion E, Bachellerie J-P. Early stages of pre-rRNA formation within the nucleolar ultrastructure of mouse cells studied by in situ hybridization with 5'ETS leader probe. Chromosoma 1997; 105:496-505.
47. Haaf T, Hayman DL, Schmid M. Quantitative determination of rDNA transcription units in vertebrate cells. Exp Cell Res 1991; 193:78-86.
48. Louvet E, Junera HR, Le Panse S, Hernandez-Verdun D. Dynamics and compartmentation of the nucleolar processing machinery. Exp Cell Res 2005; 304:457-70.
49. Colau G, Thiry M, Leduc V, Bordonne R, Lafontaine DL. The small nucle(ol)ar RNA cap trimethyltransferase is required for ribosome synthesis and intact nucleolar morphology. Mol Cell Biol 2004; 24:7976-86.
50. Hernandez-Verdun D, Bourgeois CA, Bouteille M. Simultaneous nucleologenesis in daughter cells during late telophase. Bio Cell 1980; 37:1-4.
51. Verheggen C, Le Panse S, Almouzni G, Hernandez- Verdun D. 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 1998; 142:1167-80.
52. Watkins NJ, Lemm I, Ingelfinger D, Schneider C, Hossbach M, Urlaub H, et al. Assembly and maturation of the U3 snoRNP in the nucleoplasm in a large dynamic multiprotein complex. Mol Cell 2004; 16:789-98.
53. Verheggen C, Lafontaine DL, Samarsky D, Mouaikel J, Blanchard JM, Bordonne R, et al. Mammalian and yeast U3 snoRNPs are matured in specific and related nuclear compartments. EMBO J 2002; 21:2736-45.
54. Reichow SL, Hamma T, Ferre-D'Amare AR, Varani G. The structure and function of small nucleolar ribonucleoproteins. Nucleic Acids Res 2007; 35:1452-64.
55. Gautier T, Robert-Nicoud M, Guilly MN, Hernandez- Verdun D. Relocation of nucleolar proteins around chromosomes at mitosis. A study by confocal laser scanning microscopy. J Cell Sci 1992; 102:729-37.
56. Lechertier T, Sirri V, Hernandez-Verdun D, Roussel P. A B23-interacting sequence as a tool to visualize protein interactions in a cellular context. J Cell Sci 2007; 120:265-75.
57. Moore GPM, Ringertz NR. Localization of DNAdependent RNA polymerase activities in fixed human fibroblasts by autoradiography. Exp Cell Res 1973; 76:223-8.
58. Louvet E, Tramier M, Angelier N, Hernandez- Verdun D. Time-lapse Microscopy and Fluorescence Resonance Energy Transfer to Analyze the Dynamics and Interactions of Nucleolar Proteins in Living Cells. Methods Mol Biol 2008; 463:123-35.
59. Deryusheva S, Gall JG. Dynamics of coilin in Cajal bodies of the Xenopus germinal vesicle. Proc Natl Acad Sci USA 2004; 101:4810-4.
60. Politz JC, Tuft RA, Pederson T. Diffusion-based transport of nascent ribosomes in the nucleus. Mol Biol Cell 2003; 14:4805-12.